Topic 7 assessment

Some resources have been attached and the link can also be used as a resource. Please follow all the instructions attached and the Rubric. 500-700 words

Resources:

https://www.nimh.nih.gov/health/topics/eating-disorders

https://zenodo.org/records/3471803

Eating Disorder Risks and Treatment Options – Rubric

Choose One Eating Disorder 2.75 points

Criteria Description

Paper describes the precursors, signs, and symptoms of the eating disorder a family

doctor, friend or family member would notice if an individual has developed the

chosen eating disorder.

5. Target 2.75 points

The poster expertly discusses the influence of the chosen eating disorder on

identity development, self-presentation, and self-esteem. The poster demonstrates

an exceptional understanding of the topic.

4. Acceptable 2.34 points

The poster clearly discusses the influence of the chosen eating disorder on identity

development, self-presentation, and self-esteem The poster demonstrates an

understanding that extends beyond the surface of the topic.

3. Approaching 2.06 points

The poster adequately discusses the influence of the chosen eating disorder on

identity development, self-presentation, and self-esteem. The poster demonstrates

a basic understanding of the topic.

2. Insufficient 1.79 points

The poster inadequately discusses the influence of the chosen eating disorder on

identity development, self-presentation, and self-esteem. The poster demonstrates

a poor understanding of the topic.

1. Unsatisfactory 0 points

The poster omits or incompletely discusses the influence of the chosen eating

disorder on identity development, self-presentation, and self-esteem. The poster

does not demonstrate understanding of the topic.

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https://www.gce.com/

Precursors, Signs, and Symptoms 11 points

Criteria Description

Highlight the key precursors, signs, and symptoms that individuals with this eating

disorder may exhibit. Use engaging visuals or icons to represent these symptoms,

making it easy to grasp the information at a glance.

5. Target 11 points

The poster expertly highlights the key precursors, signs, and symptoms that

individuals with this eating disorder may exhibit. The poster demonstrates an

exceptional understanding of the topic.

4. Acceptable 9.35 points

The poster clearly highlights the key precursors, signs, and symptoms that

individuals with this eating disorder may exhibit. The poster demonstrates an

understanding that extends beyond the surface of the topic.

3. Approaching 8.25 points

The poster adequately highlights the key precursors, signs, and symptoms that

individuals with this eating disorder may exhibit. The poster demonstrates a basic

understanding of the topic.

2. Insufficient 7.15 points

The poster inadequately highlights the key precursors, signs, and symptoms that

individuals with this eating disorder may exhibit. The poster demonstrates a poor

understanding of the topic.

1. Unsatisfactory 0 points

The poster omits or incompletely highlights the key precursors, signs, and

symptoms that individuals with this eating disorder may exhibit. The poster does

not demonstrate understanding of the topic.

https://www.gce.com/

Biopsychosocial Model Framework 11 points

Criteria Description

Explore the biopsychosocial model as the framework for understanding eating

disorders. Mention the biological, psychological, and social factors that contribute to

the development of the chosen eating disorder.

5. Target 11 points

The poster expertly explores the biopsychosocial model as the framework for

understanding eating disorders. Mentions the biological, psychological, and social

factors that contribute to the development of the chosen eating disorder. The

poster demonstrates an exceptional understanding of the topic.

4. Acceptable 9.35 points

The poster clearly explores the biopsychosocial model as the framework for

understanding eating disorders. Mentions the biological, psychological, and social

factors that contribute to the development of the chosen eating disorder. The

poster demonstrates an understanding that extends beyond the surface of the

topic.

3. Approaching 8.25 points

The poster adequately explores the biopsychosocial model as the framework for

understanding eating disorders. Mentions the biological, psychological, and social

factors that contribute to the development of the chosen eating disorder. The

poster demonstrates a basic understanding of the topic.

2. Insufficient 7.15 points

The poster inadequately explores the biopsychosocial model as the framework for

understanding eating disorders. Mentions the biological, psychological, and social

factors that contribute to the development of the chosen eating disorder. The

poster demonstrates a poor understanding of the topic.

1. Unsatisfactory 0 points

The poster omits or incompletely explores the biopsychosocial model as the

framework for understanding eating disorders. Mentions the biological,

psychological, and social factors that contribute to the development of the chosen

eating disorder. The poster does not demonstrate understanding of the topic.

https://www.gce.com/

Treatment Options 11 points

Criteria Description

Describe a concise list of treatment options that can be effective in managing the

chosen eating disorder. Include a brief description of each treatment.

5. Target 11 points

The poster expertly describes a concise list of treatment options that can be

effective in managing the chosen eating disorder. Include a brief description of each

treatment.

4. Acceptable 9.35 points

The poster clearly describes a concise list of treatment options that can be effective

in managing the chosen eating disorder. Include a brief description of each

treatment. The poster demonstrates an understanding that extends beyond the

surface of the topic.

3. Approaching 8.25 points

The poster adequately describes a concise list of treatment options that can be

effective in managing the chosen eating disorder. Include a brief description of each

treatment. The poster demonstrates a basic understanding of the topic.

2. Insufficient 7.15 points

The poster inadequately describes a concise list of treatment options that can be

effective in managing the chosen eating disorder. Include a brief description of each

treatment. The poster demonstrates a poor understanding of the topic.

1. Unsatisfactory 0 points

The poster omits or incompletely describes a concise list of treatment options that

can be effective in managing the chosen eating disorder. Include a brief description

of each treatment. The poster does not demonstrate understanding of the topic.

https://www.gce.com/

Visual Appeal 8.25 points

Criteria Description

Communicates reason for writing and demonstrates awareness of audience.

5. Target 8.25 points

Appropriate and thematic graphic elements are used to make visual connections

that contribute to the understanding of concepts, ideas, and relationships.

Differences in type size or color are used well and consistently. Elements commonly

found in social media websites/apps are present, attractive, used creatively, and

consistently contribute to an expert understanding of concepts, ideas, and

relationships.

4. Acceptable 7.01 points

Thematic graphic elements are used but not always in context. Visual connections

mostly contribute to the understanding of concepts, ideas, and relationships.

Differences in type size or color are used well and consistently. Elements commonly

found in social media websites/apps are present, show some creativity, and

consistently contribute to the understanding of concepts, ideas, and relationships.

3. Approaching 6.19 points

Minimal use of graphic elements is evident. Elements do not consistently contribute

to the understanding of concepts, ideas, and relationships. There is some variation

in type size, color, and layout. Elements commonly found in social media

websites/apps are present but do not consistently contribute to the understanding

of concepts, ideas, and relationships.

2. Insufficient 5.36 points

Color is garish and/or typographic variations are overused and legibility suffers.

Background interferes with readability. Understanding of concepts, ideas, and

relationships is limited. Elements commonly found in social media websites/apps

are limited and/or used unclearly.re is very little awareness of the intended

audience.

1. Unsatisfactory 0 points

There are few or no graphic elements. No variation in layout or typography is

evident. Elements commonly found in social media websites/apps are missing.

https://www.gce.com/

Presentation 5.5 points

Criteria Description

Advances position or purpose throughout writing; conclusion aligns to and evolves

from development.

5. Target 5.5 points

The poster is presented effectively and all of the required elements creatively

contribute to the presentation of the concepts.

4. Acceptable 4.68 points

The poster is presented effectively and contains all of the required elements.

3. Approaching 4.13 points

The poster contains minor inconsistencies that are not overly distracting.

Presentation contains a majority of the required elements.

2. Insufficient 3.58 points

The poster is ineffective, contains multiple inconsistencies, or is missing a few of the

required elements.

1. Unsatisfactory 0 points

The poster is incoherent, contains major inconsistencies, is not presented

effectively, or is missing a substantial amount of the required elements.

https://www.gce.com/

Mechanics of Writing 2.75 points

Criteria Description

Includes spelling, capitalization, punctuation, grammar, language use, sentence

structure, etc.

5. Target 2.75 points

No mechanical errors are present. Appropriate language choice and sentence

structure are used throughout.

4. Acceptable 2.34 points

Few mechanical errors are present. Suitable language choice and sentence

structure are used.

3. Approaching 2.06 points

Occasional mechanical errors are present. Language choice is generally

appropriate. Varied sentence structure is attempted.

2. Insufficient 1.79 points

Frequent and repetitive mechanical errors are present. Inconsistencies in language

choice or sentence structure are recurrent.

1. Unsatisfactory 0 points

Errors in grammar or syntax are pervasive and impede meaning. Incorrect language

choice or sentence structure errors are found throughout.

https://www.gce.com/

Format/Documentation 2.75 points

Criteria Description

Uses appropriate style, such as APA, MLA, etc., for college, subject, and level;

documents sources using citations, footnotes, references, bibliography, etc.,

appropriate to assignment and discipline.

5. Target 2.75 points

No errors in formatting or documentation are present.

4. Acceptable 2.34 points

Appropriate format and documentation are used with only minor errors.

3. Approaching 2.06 points

Appropriate format and documentation are used, although there are some obvious

errors.

2. Insufficient 1.79 points

Appropriate format is attempted, but some elements are missing. Frequent errors

in documentation of sources are evident.

1. Unsatisfactory 0 points

Appropriate format is not used. No documentation of sources is provided.

Total 55 points

https://www.gce.com/

Cognitive Behavioral Therapy for Bulimia Nervosa

Deborah R. Glasofer and Michael J. Devlin New York State Psychiatric Institute, New York, New York and Columbia University

Cognitive– behavioral therapy (CBT) is a first-line psychotherapeutic treatment for bulimia nervosa (BN). This article outlines three specific interventions—introducing and using the CBT model of BN, self-monitoring of eating and related experiences, and psychoeducation regarding various aspects of BN—representative of CBT overall but unique in their application to individuals with BN. The theoretical basis and supporting research relevant to each technique are highlighted. Clinical vignettes are provided to illustrate how these interventions might be integrated into the psychotherapy.

Keywords: cognitive–behavioral therapy, bulimia nervosa, eating disorders, self-monitoring, psycho- education

Cognitive– behavioral therapy (CBT) for bulimia nervosa (BN) was developed primarily by Fairburn and colleagues based on the principles of cognitive therapy (Beck, Rush, Shaw, & Emery, 1979), relapse prevention (Marlatt & Gordon, 1985), and established behavioral techniques such as stimulus control, selective reinforcement of desirable behaviors, and graded ex- posure. The initial manualized version (Fairburn, Marcus, & Wilson, 1993), used widely for 2 decades, has given way more recently to an elaborated version entitled enhanced CBT, or CBT-E, that may be delivered in a focused or broad form, the latter designed for patients with particular problems in the areas of self-esteem, perfectionism, or interpersonal functioning (Fairburn, 2008).

CBT for BN generally consists of 20 sessions delivered over 5–6 months with three distinct phases: (1) an initial phase (2 � /week sessions � 4 weeks) focused on rapid symptomatic im- provement; (2) a middle phase (1 � /week sessions � 12 weeks) tackling dietary beliefs and practices, including avoidance of “for- bidden” foods, as well as attitudes toward shape and weight that underlie the disorder; and (3) a final phase (1 � /1–2 weeks sessions � 4–8 weeks) that emphasizes continued improvement after termination and relapse prevention. Therapists using CBT for BN use many standard cognitive and behavioral techniques used for other psychological and behavioral disorders, such as cognitive restructuring, systematic problem-solving, stepwise engagement in anxiety-provoking activities, and development of self-efficacy through experimentation and debriefing. For the purposes of this article, we selected three interventions that we believe are repre- sentative of CBT overall but also illustrate some of the unique

features of CBT with this patient population. All three of these interventions—introducing and using the CBT model of BN, self- monitoring of eating and related experiences, and psychoeducation regarding various aspects of BN—are begun during the initial sessions of CBT but are carried throughout the treatment, existing in some form in every session. Patients who are successful in using CBT to treat their BN typically carry these interventions with them as they transition to the post-treatment phase of continued im- provement and long-term self-management. For each intervention, after the theoretical overview, fictionalized clinical vignettes based on the authors’ experience are provided to illustrate typical inter- actions within a session.

CBT Model

Theoretical Basis

The CBT model of BN emphasizes factors that perpetuate the illness, rather than those that account for the onset of the disorder. The central principle is that eating disorder symptoms are main- tained by the interaction between cognitive disturbances (e.g., preoccupation with shape, weight, and eating) and behavioral disturbances (e.g., rigid dietary rules, binge eating, purging) that impact eating and weight control (Fairburn, 2008; Fairburn et al., 1993).

The original CBT model for BN is illustrated in Fairburn and colleagues’ treatment manual (1993). The model may be devel- oped with the patient in diagram, or in narrative form, as used herein. An overreliance on control over shape, weight, and/or eating as the central or even sole determinant of self-worth, paired with social pressures to be thin and to eat sparingly, is theorized to be a conduit to the implementation of rigid dietary rules (Polivy & Herman, 1993). Dietary restriction predisposes individuals to ex- perience binge eating episodes, which are defined by a loss of control over eating and may be characterized by feelings of guilt associated with the violation of dietary rules. Inappropriate com- pensatory behaviors, such as self-induced vomiting, laxative mis- use, or overexercise, are relied on to counteract the effects of binge eating. These weight control behaviors instead promote subsequent

Deborah R. Glasofer and Michael J. Devlin, Division of Clinical Ther- apeutics, New York State Psychiatric Institute, New York, New York, and Department of Psychiatry, College of Physicians and Surgeons, Columbia University.

Correspondence concerning this article should be addressed to Deborah R. Glasofer, Columbia Center for Eating Disorders, New York State Psychiatric Institute, 1051 Riverside Drive, Unit 98, New York, NY 10032. E-mail: [email protected]

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mailto:[email protected]

http://dx.doi.org/10.1037/a0031939

binge eating, by disinhibiting further eating once the decision to purge is made, by disrupting normative satiety cues, or by creating distress after the fact that leads to further disinhibition. Moreover, episodes of binge eating and purging commonly result in a re- newed commitment to limit caloric intake, thus promoting a pat- tern of restriction and binge eating. The binge–purge cycle in turn causes distress and reinforces low self-esteem, increasing the like- lihood of continued cognitive distortions about shape and weight (Fairburn et al., 1993). An extended transdiagnostic CBT of eating disorders, including BN, also acknowledges that difficulty toler- ating negative mood states, problems in interpersonal relation- ships, underlying low self-esteem, and marked perfectionism are likely to perpetuate the cycle of illness in certain individuals (Fairburn, 2008).

After the general formulation of the eating disorder is explic- itly reviewed with the patient at the outset of treatment, the therapist and patient collaborate to adapt it as needed to better fit the individual’s narrative. It then becomes a central focus of treatment that is referred to throughout. Explicitly constructing a patient-specific CBT model serves to engage the patient, distance him or her from the problem, foster curiosity and understanding about the bidirectional relationship of symptoms, convey the idea that eating problems are complex but can be broken down into more manageable pieces, and provide a roadmap as to what will be focused on in therapy (and why) (Fairburn, Cooper, Shafran, & Wilson, 2008). It also serves as a platform to begin the process of psychoeducation. When reviewing the completed formulation, the therapist and patient can begin to discuss the centrality of dietary restraint in per- petuating aberrant eating behavior and the ineffectiveness of purging behaviors in controlling weight or quelling overconcern about shape and weight. This creates a rationale for targeting aspects of the illness that the patient may experience as ego- syntonic, such as dietary restriction and concern with shape and weight, as well as those that are more ego-dystonic, such as binge eating and purging. The model is also referred back to throughout treatment, as illustrated in the following vignette.

Clinical Vignette

Scene: CBT session number 10—patient is eating in a more regular pattern and is now discussing the rationale for beginning to include “forbidden foods” with the therapist.

Therapist: Now that you’ve been eating meals and snacks reg- ularly, how would you feel about doing some experiments with challenging foods, like pasta or ice cream.

Patient: But those are foods I used to binge on. Wouldn’t it be safer just to stay with the foods I’m comfortable with right now?

T: What is it that scares you about those foods? P: I’m afraid that either I would binge and purge or that I would

gain weight if I kept them down. T: Let’s take a look back at the CBT model that we created in

our very first session. Is there anything that you remember about that model that would be relevant to this challenge?

P: Well, I see here [looking at copy of personalized model of illness], and I remember that we talked about the link between rigid dietary rules and bingeing and purging.

T: Right. How do those things connect?

P: We said that such strict rules eventually catch up with me because I break them and then go to the other extreme and the bingeing feels even more out of control. We said that I need to learn how to have flexible guidelines for my eating instead of rigid rules.

T: Exactly. What would be a guideline? P: I guess it would be okay to eat pasta or ice cream if I only ate

a little. T: Right, and actually, eating a little on a regular basis helps

you not to overdo on any one occasion. P: But I’m really afraid that even with a little bit, I’d gain

weight. T: Can you see how that worry relates to the model? P: Yes. I see that being overly concerned with my weight is what

makes me think I need to have such rigid rules in the first place. T: Right. and the only way to counter that is to do the experi-

ment. Are you ready?

Supporting Research

Randomized controlled trials of a manualized CBT for BN that is based on this model support its overall efficacy in symptom reduction and show it to be superior to other short- term psychological treatments (Wilson, Fairburn, Agras, Walsh, & Kraemer, 2002) and to antidepressant medications (Wilson, Grilo, & Vitousek, 2007) for achieving abstinence from bulimic symptoms. Given the efficacy of the treatment, investigators have attempted to validate the underlying conceptual model. Whereas studies of individuals with and without BN more heavily favor self-esteem and overvaluation of shape and weight as key components of the formulation (Byrne & McLean, 2002; Schnitzler, von Ranson, & Wallace, 2012), prospective research with those meeting criteria for BN indicate that overvaluation of shape and weight predicts change in dietary restraint, which in turn predicts change in frequency of binge eating (Fairburn et al., 2003).

More recent studies have provided support for additional main- taining factors, including mood intolerance, core low self-esteem, and interpersonal problems (Tasca et al., 2011), negative affect (Stice, 2001), thin-ideal internalization, and impulsiveness (Schnit- zler et al., 2012). These findings support the potential utility of personalizing the original formulation with a patient to identify additional treatment targets (e.g., affect tolerance, shape/weight comparisons) that both help to maintain disordered eating and merit treatment in their own right.

Treatment studies have yielded data that further support the theoretical model. The reduction in dietary restraint achieved by CBT has been shown to partly mediate the intervention’s efficacy in eliminating binge eating and purging (Wilson et al., 2002). This is consistent with the CBT formulation’s emphasis on the role of rule-bound eating in perpetuating illness. The effects of CBT for BN are also evident in improvements in general psychopathology, including depressive symptoms, self-esteem, and social function- ing (Chen et al., 2003), thus supporting the inclusion of these constructs in the model of illness.

Taken together, extant data clearly support the CBT formulation of BN. The evidence base for the conceptualization and approach to treatment can help instill hope and provide a roadmap for recovery to individuals suffering from the bulimic cycle.

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538 GLASOFER AND DEVLIN

Self-Monitoring

Theoretical Basis

Self-monitoring refers to the routine collection of information related to target symptoms by a patient in his or her naturalistic environment. The purpose of self-monitoring is to enhance aware- ness of patterns and the occurrence of relevant behaviors, decrease the automaticity of actions, and provide a record that will be relevant to the development of incremental change toward treat- ment goals (Korotitsch & Nelson-Gray, 1999), including the pro- gressive reduction in anxiety that results when once-forbidden eating patterns become routine.

In CBT for BN, self-monitoring takes on a relatively standard- ized format. It consists of daily “real-time” recording of eating and purging behavior, thoughts, feelings, and relevant events (for sam- ple forms see p. 58, Fairburn, 2008). Patients are expected to monitor food intake, but are encouraged to do so in terms of approximation rather than in precise measurements (i.e., calories, grams) that might further promote restrictive or rule-bound eating (Wilson & Vitousek, 1999).

At the beginning of treatment, the records are used to further explicate the CBT model of illness as it plays out for the individual (e.g., adherence to particular dietary rules, emotional “triggers” for aberrant eating and purging, negative preoccupying thoughts about weight). Next, self-monitoring becomes a catalyst for change. The emphasis shifts to the patient’s eating habits, with the goal of behavior modification, including normalizing the eating pattern (i.e., three meals plus approximately two planned snacks daily) and enhancing the variety of foods eaten. Patient and therapist agree on appropriate “experiments” to challenge patients’ assumptions re- garding the consequences of more normal eating, thus undermin- ing food avoidance and systematically exposing patients to feared “forbidden foods” when feared uncontrolled weight gain is docu- mented not to occur.

Self-monitoring records can be also be used to capture prob- lematic behaviors, such as hypervigilant body-checking or ex- cessive exercise; document their emotional, cognitive, and be- havioral effects; and ultimately modify them. Finally, negative automatic thoughts and moods are addressed, particularly in relation to any lapses. Self-monitoring is discontinued toward the end of treatment, after an individual has experienced a significant period of abstinence from binge eating and purging while maintaining a regular eating pattern. However, it remains a central relapse prevention tool meant to be revisited as needed in anticipation of high-risk situations or in light of any lapses that occur.

Clinical Vignette

Scene: CBT session number 15—patient and therapist are re- viewing self-monitoring records and analyzing recent urges to binge eat and purge.

Patient: I’m glad we decided last time that I should continue to closely monitor my eating on weekends. This weekend was rough.

Therapist: How so? Let’s have a look at the records. P: Well, Saturday morning I was doing fine. I went out to

brunch with Dana. I had an omelet. Oh and that’s right, I wrote down here that I felt a little bad that she had a salad.

T: What about that made you feel bad? P: I guess I should know better at this point, but somehow I still

feel like if I’m not the healthiest eater at the table, then I’m being a pig or that I’m out of control.

T: Then what happened? P: Well, dinner was really a close call. I was pretty stressed out,

even before I started, so having a burger may not have been the best choice. If I’d been by myself, I’m pretty sure that I would have purged.

T: So having somebody with you really helped you. What else could we learn from this sequence of events?

P: I guess I didn’t realize, but my experience at brunch set me up for problems later on.

T: How might you have handled brunch differently? P: Maybe I could have checked in with myself and done a

thought record. T: Which thought would you have chosen? P: The thought that just because Dana ate a salad, that my

eating an omelet makes me a pig. Even just saying that makes me realize how irrational that is. I know that an omelet is fine and it doesn’t matter what Dana eats.

T: Great. Your self-monitoring really helped us to crack the case. Maybe the challenge for next time is to question your automatic thoughts in the moment. Let’s try that a little bit more together now, so you’ll be prepared.

Supporting Research

Findings from studies of self-monitoring in BN support the CBT formulation of the illness. The collective body of literature, for example, has demonstrated that aberrant eating episodes are typi- cally preceded by negative emotional states, and that those with BN experience more fluctuations in mood and negative affect than their healthy counterparts (Wilson & Vitousek, 1999). In addition, records of those with BN have yielded a fairly consistent pattern of late-day binge eating episodes that occur while alone and at home (Wilson & Vitousek, 1999).

Treatment outcome research has shown that when CBT for BN works, it works quickly, commonly achieving substantial thera- peutic effect within the first month of sessions (Wilson et al., 1999, 2002). The rapid impact on symptoms may, in part, be ascribed to the early introduction of self-monitoring (Wilson, 1999; Wilson & Vitousek, 1999). Dismantling studies evaluating the additive ef- fects of different components of CBT for BN suggest the effec- tiveness of self-monitoring depends on the therapeutic procedures used during the review of records (Agras, Schneider, Arnow, Raeburn, & Telch, 1989; Kirkley, Schneider, Agras, & Bachman, 1985). Using daily records as a platform for behavior change experiments is essential, comparing favorably with the use of nondirective and nonspecific review of self-monitoring, in effect- ing reduction in or abstinence from binge eating and purging (Agras et al., 1989).

Because the literature clearly favors self-monitoring as a cor- nerstone of CBT for BN, researchers have become interested in using advances in technology to enhance its use as a tool for behavior change (e.g., Rodgers et al., 2005; Shapiro et al., 2008, 2010). Preliminary data from feasibility research suggest that the use of text-messaging, for example, in the treatment of BN may enhance adherence to and accuracy of self-monitoring (Shapiro et

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539CBT FOR BN

al., 2010). Clinicians and patients may therefore want to think together about how to creatively approach self-monitoring (e.g., using applications on smartphones) so that it remains a viable aspect of treatment.

Psychoeducation

Theoretical Basis

Psychoeducation in CBT for BN covers topics including the deleterious effects of purging (and its ineffectiveness as a method of weight control), normative fluctuations in weight, healthy weight ranges (i.e., their derivation and significance from a med- ical perspective), energy regulation and weight change, and regular eating. Because individuals with eating disorders may be simulta- neously overinformed and misinformed in these areas (Fairburn et al., 2008), psychoeducation is a critical component of the treatment approach, and it is important that the clinician be well-versed.

The most common educational points made within a course of CBT for BN are: (1) 3,500 kcal in excess of what one needs to maintain his or her body weight are required to gain one additional pound; (2) weight typically fluctuates within an approximately five-pound range and thus weight trends are more important than fluctuations; (3) on average, self-induced vomiting removes 50% of what had been ingested; (4) laxatives cause dehydration, not weight loss; and (5) lapses in behavior are expected and do not indicate failure.

Psychoeducation regarding the risks of purging behaviors or the particulars of regular eating is provided in the form of informa- tional handouts assigned as take-home reading that is then re- viewed in session. Other topics are covered primarily during sessions, either as discrete agenda items or in relation to specific erroneous beliefs that may become apparent in the review of self-monitoring records.

Clinical Vignette

Scene: CBT session number 3—patient and therapist are re- viewing food records.

Therapist: So here again we see that the binge took place after you hadn’t eaten anything for several hours.

Patient: Yeah, I was really hungry and I started eating cookies, but I know that’s just going to make me gain weight, so I had to get rid of it.

T: And then it turned into a whole binge episode. P: Yeah, because once I had something as fattening as the

cookies, I knew I would get rid of everything, so I just let myself go. T: OK. Let’s look at that idea of “getting rid of everything.”

What do you know about what happens when you vomit after a large binge?

P: Well, I know it’s bad for my stomach and it makes my throat hurt but it’s the only way to get rid of the calories. I’m sure I don’t get everything up, if that’s what you mean, but I get most of it.

T: What percentage of the calories do you think you get rid of when you vomit?

P: I think about 90%. I usually rinse a couple of times with water, and vomit as much as I can.

T: That’s what most people think, but the reality might surprise you. Scientists carried out studies some years ago in which people

who had BN binged and vomited in a laboratory. The scientists analyzed what came up in order to determine its caloric content, which they can do very precisely. It turns out that the amount that came back up was quite variable, but averaged out to about half.

P: Well maybe, but I keep vomiting until I see the first foods that I ate come up.

T: Actually, the participants in the study were doing the same things that you do, like checking for the first foods or rinsing to try to get all the food out. It turns out that it’s just not possible to get rid of all the food—your body begins to move the food out of the stomach and digesting it as soon as you start eating.

P: Wow, you mean that with all the food I binge on, I’m keeping half of it? That’s really scary.

T: That’s part of why this is a behavior that does not really help people control their weight. But there’s also some good news. If you’re keeping down half of the calories in your binges and maintaining your weight, that means that you will maintain your weight on a higher number of calories than you thought. So if you stop binge eating and purging, you have a lot of calories to redistribute into regular planned meals and snacks. That’s why most people don’t gain weight when they stop their bulimia and begin to eat regularly. If you are willing to start to do this experiment, I bet that’s what we will see for you too. But I know it’s scary until you experience it for yourself.

Supporting Research

To date, no studies have been done to look at specific effects of the psychoeducational components of CBT for BN. How- ever, psychoeducation has frequently been conceptualized as a necessary, but not sufficient, element of psychotherapeutic in- tervention for a variety of psychiatric illnesses (Colom & Lam, 2005; Colom & Vieta, 2004; Segredou et al., 2012; Xia, Mer- inder, & Belgamwar, 2011), including eating disorders (Davis, Olmsted, Rockert, Marques, & Dolhanty, 1997; Geist, Hei- nmaa, Stephens, Davis, & Katzman, 2000). In the treatment of BN, providing education on the aforementioned topics is criti- cal in engaging and empowering the patient in the other essen- tial aspects of the therapy, such as a regular eating pattern and increased variability in food choices, and enhancing his or her ability to challenge cognitive distortions.

Notably, all of the information provided to patients is well- grounded in biology and human physiology. At times, research that specifically supports a particular educational point may be profitably shared with the patient. For example, the study of Kaye, Weltzin, Hsu, McConaha, and Bolton (1993) regarding the inefficiency of self-induced vomiting is often eye-opening for patients who believe that they are getting rid of all calories in a binge meal and therefore maintain their weight on low daily intake. In addition, there are data to support the normative fluctuations of weight over time in those maintaining a stable weight (Fairburn, 2008, pp. 63– 65). This can help patients understand the rationale for not interpreting a single weight reading as a meaningful trend.

Conclusion

As is hopefully now evident, CBT offers an approach that is conducive to the targeting of the symptoms of BN. Its focus on the

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540 GLASOFER AND DEVLIN

here and now, enhanced awareness of behavioral patterns and related cognitions, problem-solving, and between-session behav- ioral experiments afford individuals with BN tools to carry for- ward into recovery after the formal psychotherapy has ended. To date, data suggest that 30% to 50% of individuals who receive CBT for BN are fully abstinent from binge eating and purging behaviors by conclusion of the treatment (Wilson et al., 2007). The effects of CBT for BN are evident not only in improvements in binge eating and purging, but also for general psychopathology, including depressive symptoms, self-esteem, and social function- ing (e.g., Chen et al., 2003). Moreover, improvement is often sustained at 1-year follow-up (Wilson et al., 2007).

However, although a large majority of patients improve sub- stantially with a time-limited course of CBT, a significant number do not achieve binge–purge remission (Wilson et al., 2007). Thus, medication treatment and other forms of psychotherapy such as interpersonal therapy or dialectical behavior therapy have addi- tionally been found effective and may be appropriate for some patients. Self-help and guided self-help forms of CBT for BN have also been developed and are helpful for some (Wilson & Zandberg, 2012). Unfortunately, few factors that predict differential response to particular treatments have been identified. Until these factors are clarified, CBT remains a first-line treatment for individuals with BN.

References

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Chen, E., Touyz, S. W., Beumont, P. J., Fairburn, C. G., Griffiths, R., Butow, P., . . . Basten, C. (2003). Comparison of group and individual cognitive-behavioral therapy for patients with bulimia nervosa. Interna- tional Journal of Eating Disorders, 33, 241–254; discussion 255–246.

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Colom, F., & Vieta, E. (2004). Improving the outcome of bipolar disorder through non-pharmacological strategies: The role of psychoeducation. Bipolar Disorders, 6, 480–486. doi:10.1111/j.1399-5618.2004.00136.x

Davis, R., Olmsted, M., Rockert, W., Marques, T., & Dolhanty, J. (1997). Group psychoeducation for bulimia nervosa with and without additional psychotherapy process sessions. International Journal of Eating Disor- ders, 22, 25–34. doi:10.1002/(SICI)1098-108X(199707)22:1�25::AID- EAT3�3.0.CO;2-4

Fairburn, C. G. (2008). Cognitive behavior therapy and eating disorders. New York: Guilford Press.

Fairburn, C. G., Cooper, Z., Shafran, R., & Wilson, G. T. (2008). Eating disorders: A transdiagnostic protocol. In D. H. Barlow (Ed.), Clinical handbook of psychological disorders: A step-by-step treatment manual (4th ed., pp. 578–614). New York: Guilford Press.

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Marlatt, G. A., & Gordon, J. R. (1985). Relapse prevention: Maintenance strategies in the treatment of addictive behaviors. New York: Guilford Press.

Polivy, J., & Herman, C. P. (1993). Etiology of binge eating: Psychological mechanisms. In C. G. Fairburn & G. T. Wilson (Eds.), Binge eating: Nature, assessment and treatment (pp. 173–205). New York: Guilford Press.

Rodgers, A., Corbett, T., Bramley, D., Riddell, T., Wills, M., Lin, R. B., & Jones, M. (2005). Do u smoke after txt? Results of a randomised trial of smoking cessation using mobile phone text messaging. Tobacco Con- trol, 14, 255–261. doi:10.1136/tc.2005.011577

Schnitzler, C. E., von Ranson, K. M., & Wallace, L. M. (2012). Adding thin-ideal internalization and impulsiveness to the cognitive-behavioral model of bulimic symptoms. Eating Behaviors, 13, 219–225. doi: 10.1016/j.eatbeh.2012.02.007

Segredou, I., Xenitidis, K., Panagiotopoulou, M., Bochtsou, V., Antonia- dou, O., & Livaditis, M. (2012). Group psychosocial interventions for adults with schizophrenia and bipolar illness: The evidence base in the light of publications between 1986 and 2006. International Journal of Social Psychiatry, 58, 229–238. doi:10.1177/0020764010390429

Shapiro, J. R., Bauer, S., Andrews, E., Pisetsky, E., Bulik-Sullivan, B., Hamer, R. M., & Bulik, C. M. (2010). Mobile therapy: Use of text- messaging in the treatment of bulimia nervosa. International Journal of Eating Disorders, 43, 513–519. doi:10.1002/eat.20744

Shapiro, J. R., Bauer, S., Hamer, R. M., Kordy, H., Ward, D., & Bulik, C. M. (2008). Use of text messaging for monitoring sugar-sweetened beverages, physical activity, and screen time in children: A pilot study. Journal of Nutrition, Education, and Behavior, 40, 385–391. doi: 10.1016/j.jneb.2007.09.014

Stice, E. (2001). A prospective test of the dual-pathway model of bulimic pathology: Mediating effects of dieting and negative affect. Journal of Abnormal Psychology, 110, 124–135. doi:10.1037/0021-843X.110.1 .124

Tasca, G. A., Presniak, M. D., Demidenko, N., Balfour, L., Krysanski, V., Trinneer, A., & Bissada, H. (2011). Testing a maintenance model for eating disorders in a sample seeking treatment at a tertiary care center: A structural equation modeling approach. Comprehensive Psychiatry, 52, 678–687. doi:10.1016/j.comppsych.2010.12.010

Wilson, G. T. (1999). Rapid response to cognitive behavior therapy. Clinical Psychology: Science and Practice, 6, 289–292. doi:10.1093/ clipsy/6.3.289

Wilson, G. T., Fairburn, C. C., Agras, W. S., Walsh, B. T., & Kraemer, H. (2002). Cognitive-behavioral therapy for bulimia nervosa: Time course and mechanisms of change. Journal of Consulting and Clinical Psychol- ogy, 70, 267–274. doi:10.1037/0022-006X.70.2.267

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541CBT FOR BN

http://dx.doi.org/10.1037/0022-006X.57.2.215

http://dx.doi.org/10.1002/eat.10002%20

http://dx.doi.org/10.1016/j.eurpsy.2005.06.002%20

http://dx.doi.org/10.1111/j.1399-5618.2004.00136.x

http://dx.doi.org/10.1002/%28SICI%291098-108X%28199707%2922:1%3C25::AID-EAT3%3E3.0.CO%3B2-4%20

http://dx.doi.org/10.1037/0022-006X.71.1.103%20

http://dx.doi.org/10.1037/0022-006X.53.1.43

http://dx.doi.org/10.1037/1040-3590.11.4.415%20

http://dx.doi.org/10.1136/tc.2005.011577

http://dx.doi.org/10.1016/j.eatbeh.2012.02.007%20

http://dx.doi.org/10.1177/0020764010390429

http://dx.doi.org/10.1002/eat.20744%20

http://dx.doi.org/10.1016/j.jneb.2007.09.014

http://dx.doi.org/10.1037/0021-843X.110.1.124%20

http://dx.doi.org/10.1016/j.comppsych.2010.12.010

http://dx.doi.org/10.1093/clipsy/6.3.289%20

http://dx.doi.org/10.1037/0022-006X.70.2.267

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Wilson, G. T., & Zandberg, L. J. (2012). Cognitive-behavioral guided self-help for eating disorders: Effectiveness and scalability. Clinical Psychology Review, 32, 343–357. doi:10.1016/j.cpr.2012.03.001

Xia, J., Merinder, L. B., & Belgamwar, M. R. (2011). Psychoeducation for schizophrenia. Cochrane Database System Reviews, CD002831.

Received January 4, 2013 Revision received January 9, 2013

Accepted January 10, 2013 �

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http://dx.doi.org/10.1037/0003-066X.62.3.199%20

http://dx.doi.org/10.1037/0022-006X.67.4.451

http://dx.doi.org/10.1037/1040-3590.11.4.480%20

http://dx.doi.org/10.1016/j.cpr.2012.03.001

Cognitive Behavioral Therapy for Bulimia Nervosa

CBT Model

Theoretical Basis
Clinical Vignette
Supporting Research

Self-Monitoring

Theoretical Basis
Clinical Vignette
Supporting Research

Psychoeducation

Theoretical Basis
Clinical Vignette
Supporting Research

Conclusion
References

Bariatric Times • December 2016 • Supplement C C9

C ustomized care, sometimes called precision

medicine, attempts to help create specific

treatments geared to the needs of an

individual patient and this model is extremely

relevant for obesity treatment. It also allows for

the patient and clinician to intensify treatment as

needed or to change it as the patient proceeds

along the continuum of care. It allows for care to

be more or less intensive at different phases of the

patient’s journey.

There are four main domains of treatment. The

least invasive of these is an intensive lifestyle

intervention (ILI). The following can be added to

ILI: anti-obesity pharmacological therapy (second

domain), intermediate procedures (third domain),

and finally bariatric surgery (fourth domain). All

domains involve ILI, which must always be

considered the foundation, and then medications,

intermediate procedures, and bariatric surgery

may be added. Healthcare professionals involved

include the primary care physician (PCP) and

integrated health support at first, followed by

obesity specialists, and finally, in the fourth

domain, a bariatric surgeon.

INTeNSIve lIFeSTyle INTerveNTION

Intensive lifestyle intervention (ILI) is the

cornerstone of all obesity care.18 It includes a

comprehensive program of nutrition (diet),

physical activity (exercise), a psychosocial

component, sleep, and stress reduction.19 Each of

these components can be individualized for each

patient. For example, nutrition must include

caloric reduction and appropriate nutrition, but

the exact diet and special needs for the patient will

play a role and allow for the plan to be customized

as needed. For example, some patients may have

certain food allergies, need a gluten-free diet,

prefer vegetarian meals, or enjoy certain types of

foods. Patients may have physiologies that

respond better to some diet plans than others. For

example, some patients may do well on low-

carbohydrate diets while others feel lethargic on

the same diet. Special needs for individuals may

also be accommodated with meal replacements for

some patients or the use of artificial sweeteners for

others. In short, the “one size fits all” approach to

diet and nutrition is neither realistic nor effective.

The same approach applies to the patient’s

physical activities. There is a wide range of

physical exercises available including some that

are gravity-mediated and may be easier for

patients with obesity. Patients with obesity or

those with mobility issues may benefit more from

water exercises, others may experience more

benefits from vigorous strength training, while

others may need recumbent type activities to

accommodate their limited movement.

Psychosocial interventions, sleep hygiene, and

stress reduction also can be individualized to best

meet an individual patient’s needs and be most

effective.20 A sleep history may be useful for

treating patients with obesity, including not just

the presence or absence of obstructive sleep apnea

(OSA), but also sleep volume and quality. Poor

sleep habits may change hormonal levels,

Insights into the Patient Population with Obesity: Assessment and Treatment

customizing obesity treatments Deborah Bade Horn, DO, MFOMA

President, Obesity Medicine Association; Medical Director, Clinical Assistant Professor, Center for Obesity Medicine and Metabolic Performance, UT McGovern Medical School, Houston, Texas

C10 Bariatric Times • December 2016 • Supplement C

predisposing patients to fat storage, and elevating

their risk of comorbid conditions such as

diabetes.21

Once the basic ILI plan is crafted, the patient can

use this to begin the treatment. For some patients,

however, this level of intervention is insufficient,

and the next layer must be added.

IlI + ANTI-OBeSITy MeDICATIONS Anti-obesity medications (AOM) when added to

ILI represent the second domain for obesity

treatment. AOM should be used after ILI and

before intermediate procedures. AOM should be

considered in patients with a BMI >30kg/m2 or in

those with a BMI >27kg/m2 with comorbid

conditions. Before selecting pharmacotherapeutic

options, the prescriber should consider how well

the patient did using just ILI alone, how much

weight was lost, and how quickly it was lost.

There are a number of AOM available with unique

mechanisms of action.22 Prescribing choices should

be guided first by understanding contraindications

of AOMs and then by understanding the patient’s

symptoms, such as overriding persistent hunger,

specific or very strong food cravings, or a

tendency toward emotional eating. In some cases,

AOMs may help address the patient’s

comorbidities or provide additional benefits.

Patient monitoring over the course of therapy

can help confirm whether or not the prescribed

AOM is effective and if the patient is experiencing

side effects or tolerability issues. By monitoring at

around three months, it should be possible to

determine if reasonable weight loss goals have

been met and if the patient is tolerating the

medicine well.

It may benefit the patient to escalate from ILI

alone to ILI plus AOM sooner in the patient’s

continuum of care rather than later. With a large

and robust armamentarium of AOMs, there are

more options for early intervention. In many

primary care clinics, escalation to AOMs may

happen only slowly, if at all. It may be erroneously

believed that AOMs should only be considered for

the most extreme cases of obesity. In fact, AOM

treatment is prescribed to only about one percent

of patients with obesity, which indicates many

patients who would benefit from it are not

receiving it.22

IlI + INTerMeDIATe PrOCeDureS The third domain adds another layer:

intermediate procedures such as gastric balloons,

gastric emptying systems, or an electrical

stimulation system. These are not considered

surgical procedures, but rather represent

temporary devices intended to be used for a

specific but not indefinite period of time. These

procedures should always supplement an

underlying ILI foundational program and often

with AOM pharmacotherapy. There are many

considerations with this domain including

tolerability issues (not all patients can tolerate

these systems) and efficacy.23

Gastric Baloon. Gastric balloon systems are

appropriate for patients with a BMI ≥ 30kg/m2.

The gastric balloon is placed in the patient

endoscopically although in the future, it may be

possible for the patient to simply swallow the

balloon. It occupies space within the stomach

which stimulates the hormones that provide the

patient with the sensation of fullness and

satiety.24,25

Gastric emptying System. A gastric emptying

system is appropriate for patients over age 22 with

a BMI in the range of 35 to 55kg/m2. This system

requires surgical placement that uses an internal

tubing system, a port or valve in the skin, and an

external pump to remove substances out of the

stomach.26 The device is activated by the patient,

who affixes a tube to the port to empty the

stomach. To be effective, the system must be used

within 30 minutes of taking in a meal. The gastric

emptying system can remove about 30 percent of

the caloric content of the meal.

electrical Stimulation System. An electrical

stimulation system should be used in patients

either with a BMI in the range of 35 to 39kg/m2

with one comorbid condition or a BMI ≥ 40kg/m2.

The concept of an electrical stimulation system is

that nerve activation can blunt signals of hunger

and encourage signals of satiety.27

Insights into the Patient Population with Obesity: Assessment and Treatment

Bariatric Times • December 2016 • Supplement C C11

IlI + BArIATrIC SurGery

The most invasive form of intervention is

bariatric surgery—gastric band, gastric sleeve, or

gastric bypass.28 This intervention should always

rely on ILI as the foundation and it should be used

in patients who have tried or may still be utilizing

AOM pharmacotherapy. The main criteria for

bariatric surgery is that the patient have a BMI

>40kg/m2 or a BMI >35kg/m2 with comorbidities.

The gastric band is surgically placed to go

around the stomach, which restricts the stomach

space and thus limits food intake. The gastric band

may be considered the least invasive of the

bariatric surgeries. The gastric sleeve removes part

of the stomach but it does not re-route any of the

bowel system. The most invasive procedure is

gastric bypass which both removes a portion of the

stomach and re-routes the bowel system.

The role of AOM with bariatric surgery is

evolving. Some patients need even more signal

interruptions to be successful with weight loss

than are available with bariatric surgery alone.

Some of the new medications may work well to

provide bariatric surgery patients with this added

support.

Bariatric surgery is not utilized as much as is

indicated. Early intervention can be particularly

helpful for patients with type 2 diabetes mellitus

as it may have a beneficial effect on the course of

the disease. In fact, it may be helpful to think of

bariatric procedures as metabolic surgeries rather

than obesity surgeries. PCPs should be aware of

the important role of bariatric surgery and when it

is indicated—which may be at lower BMI values

than many expect. Many patients under the care of

a PCP might be appropriate candidates for

bariatric surgery, but are not being informed about

this option. It is not necessary for the PCP to

understand the nuances of the individual

procedures or to provide highly specific

recommendations to the patient. A bariatric

surgeon can be consulted and help advise the

patient.

FuTure DIreCTIONS IN weIGHT lOSS

AND weIGHT CONTrOl

The heritability of an individual’s BMI has been

estimated to be about 40 to 70 percent,29 which

roughly translates to the fact that about half of the

differences in body weight can be traced to

genetics and the other half to environment. The

issue of genetics poses questions but may also

offer future answers to better obesity management.

Genetic variations have been associated with the

relative success of ILI efforts, bariatric surgery

effectiveness, and the variations in the

macronutrient composition of diet. Genetics may

also help clinicians prescribe the most effective

weight loss strategies and therapies for an

individual patient.

It is now thought that areas of genomic

influence/customized care, such as control of

energy expenditure, appetite control and food

intake, and adipogenesis and lipid metabolism,

may be key components to weight loss.30 How the

body takes in energy and stores it varies by

individuals and this information may be useful in

finding the best weight loss strategies for the

patient.

In addition to genetics or genomics, epigenetics

should be considered in that these describe the

interactions between the patient’s environmental

factors and his or her genes. Epigenetics can allow

clinicians to find the best individualized and

customized care regimen. For example, physical

activity and high-fat diets may alter DNA

methylation, which, in turn, may affect the energy

homeostasis in skeletal muscles and adipose

tissue. Muscle tissue sends very specific signals to

adipose tissue. Thus, specific physical activity

plans can change the messaging of muscle to

adipose tissue and, in that way, encourage weight

loss.31

Epigenetics has opened up new ways of

clinically understanding weight loss, weight gain,

and weight maintenance, the latter being a

particularly challenging aspect of weight control.32

By understanding the genes that regulate energy, it

may be possible to find a more sustainable

approach to weight loss and weigh maintenance.

There are currently consumer tests available that

Insights into the Patient Population with Obesity: Assessment and Treatment

C12 Bariatric Times • December 2016 • Supplement C

look at genetics and epigenetics, but work is

ongoing to better understand how these will

impact clinical practice.

The gut microbiome is another important part of

individualized/customized care. The microbiome

in the gut changes compositionally and

functionally with external and internal influences.

It is believed that the gut mechanisms have a

direct effect on obesity by modulating energy

balance and by regulating inflammation. In fact,

the gut microbiome may be considered an

epigenetic regulator, mediating through “back

signaling” how the environment and genetics

interact.32

Inflammation and obesity are closely associated.

Many diseases, particularly those with an

inflammatory component, have an association

with obesity. Understanding the connection

between obesity and inflammation may help guide

future treatment of obesity. For example, glycogen

accumulation in adipose tissue may be a key

feature in inflammation-associated metabolic

stress syndromes of obesity.33

A number of genes, including the FTO gene,

have been identified as potential risk factors for

obesity. The question arises as to how patients

might respond upon learning that they had this

potential risk factor—would it change their

behavior? Patients who learned that they had the

genotype that put them at risk for obesity and who

also at the same time got information about weight

management strategies, were more likely to accept

treatment than those who did not get this genetic

information.34,35 When patients knew they had the

FTO genotype, they were more likely to

contemplate or take action about their weight than

patients who did not have this genetic

information. This propensity for action was more

pronounced if the patient already had overweight

or obesity; those who got genetic information and

already had overweight or obesity were more

ready for change than those with genetic

information but at normal weight. Readiness to

change behavior occurs on a continuum—from

pre-contemplation to contemplation to taking

steps and then finally to maintaining the changes.

In this study, FTO genotype information and the

patient’s overweight or obesity status made them

more ready to change, but in terms of actually

taking steps, the groups had similar rates. In other

words, genetic information and current weight

caused the patient to contemplate change but not

necessarily to implement it. This intriguing study

has caused clinicians to consider what might be

the next steps to causing change, such as

identifying resources to help the patient lose

weight, actionable education, self-monitoring of

obesity-related variables, and progress evaluation.

In particular, a risk scoring system that allows

patients to evaluate, monitor, and understand their

individual risks with obesity may be helpful.

Insights into the Patient Population with Obesity: Assessment and Treatment

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cells

Review

Physical Exercise and Selective Autophagy: Benefit and Risk on Cardiovascular Health

Ne N. Wu 1,2,† , Haili Tian 3,†, Peijie Chen 3, Dan Wang 4, Jun Ren 1,2,* and Yingmei Zhang 1,2,* 1 Department of Cardiology, Zhongshan Hospital, Fudan University, Shanghai 200032, China;

[email protected] 2 Shanghai Institute of Cardiovascular Diseases, Department of Cardiology, Zhongshan Hospital,

Fudan University, Shanghai 200032, China 3 School of Kinesiology, Shanghai University of Sport, Shanghai 200438, China; [email protected] (H.T.);

[email protected] (P.C.) 4 School of Physical Education and Sport Training, Shanghai University of Sport, Shanghai 200438, China;

[email protected] * Correspondence: [email protected] (J.R.); [email protected] (Y.Z.) † These authors contributed equally to this paper.

Received: 20 October 2019; Accepted: 13 November 2019; Published: 14 November 2019 ��

Abstract: Physical exercise promotes cardiorespiratory fitness, and is considered the mainstream of non-pharmacological therapies along with lifestyle modification for various chronic diseases, in particular cardiovascular diseases. Physical exercise may positively affect various cardiovascular risk factors including body weight, blood pressure, insulin sensitivity, lipid and glucose metabolism, heart function, endothelial function, and body fat composition. With the ever-rising prevalence of obesity and other types of metabolic diseases, as well as sedentary lifestyle, regular exercise of moderate intensity has been indicated to benefit cardiovascular health and reduce overall disease mortality. Exercise offers a wide cadre of favorable responses in the cardiovascular system such as improved dynamics of the cardiovascular system, reduced prevalence of coronary heart diseases and cardiomyopathies, enhanced cardiac reserve capacity, and autonomic regulation. Ample clinical and experimental evidence has indicated an emerging role for autophagy, a conservative catabolism process to degrade and recycle cellular organelles and nutrients, in exercise training-offered cardiovascular benefits. Regular physical exercise as a unique form of physiological stress is capable of triggering adaptation while autophagy in particular selective autophagy seems to be permissive to such cardiovascular adaptation. Here in this mini-review, we will summarize the role for autophagy in particular mitochondrial selective autophagy namely mitophagy in the benefit versus risk of physical exercise on cardiovascular function.

Keywords: cardiovascular; physical exercise; autophagy; selective autophagy; benefit; risk

1. Introduction

Regular physical exercise is a part of healthy lifestyle, with multiple cross-sectional studies consolidating reduced overall risk of cardiovascular diseases and cardiac events associated with habitual or leisure physical exercises [1,2]. Ample evidence has indicated a much better survival rate following a cardiovascular event in those who are physically active in comparison with more sedentary individuals, and the beneficial impact of physical exercise on heart failure is also described [1,3–5]. Regular physical exercise is now becoming a non-pharmacological remedy to lower cardiovascular morbidity and mortality courtesy of the exercise-induced cardiovascular benefit [6,7]. Such maneuver drastically improves the overall cardiovascular survival despite the poor success for current pharmaceutical

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therapeutics against cardiovascular diseases. More evidence has favored a close dose–response correlation between exercise duration and/or intensity and overall cardiovascular benefit [8–10]. Although the precise nature of physical activity in cardiovascular regulation and disease prevention remains poorly defined, low-, moderate-, and vigorous-intensity exercise have all exhibited some degrees of health benefit [1,11,12]. Moreover, it has been reported that intense/extreme exercise may also be detrimental to human hearts [1,8]. Here the term ‘exercise’ is mainly used to reflect regular aerobic or endurance exercise, unless otherwise stated.

To-date, a number of theories at the cellular and molecular levels have been postulated towards exercise-offered cardiovascular benefits including increased insulin sensitivity, reduced oxidative stress and adiposity, fiber transformation toward oxidative myofibers, and increased mitochondrial content/function [1,12,13]. More recently, there is a growing concern of physiological adaptation and induction of autophagy, a conserved evolutionary process responsible for the degradation of multiple cellular components [1,14–16]. Under stress conditions such as starvation and increased physical activity, autophagy is usually turned on to recycle long-lived or damaged cellular organelles and proteins for the resynthesis of new organelles and ATP. Particular recognition and degradation of damaged or superfluous organelles may also be achieved by a special form of autophagy—selective autophagy [17,18]. Recently, a growing body of literature has recognized the pivotal role of mitophagy—selective autophagy of mitochondria, in conditions with energy stresses, such as starvation, obesity and physical exercise [19,20]. In the heart, timely removal of dysregulated (long-lived or damaged) mitochondria is essential to cardiac homeostasis, while excessive or pathological mitophagy is deemed harmful to the organism [21–26]. Interestingly, previous studies indicated that not only does exercise transiently induce cardioprotective mitophagy, but also helps to sustain a proper level of mitophagy over time [15,27]. Thus, mitophagy might be instrumental to a better understanding of how exercise impacts the overall organismal health. In this mini-review, we will highlight the essential role of mitophagy in exercise-induced effects on cardiovascular system.

2. Contemporary Theory behind Exercise-Induced Cardiovascular Benefit

Physical exercise of sufficient intensity and duration improves cardiovascular performance and cardiac reserve in healthy individuals [28]. For example, a 3–5 day short-term endurance training may elicit cardioprotection against ischemia–reperfusion insult, although molecular mechanisms behind physical exercise-induced cardioprotection remain elusive. In-depth analysis was carried out by Luan and associates in an effort to recapitulate beneficial effects of various types of exercise on 26 forms of chronic diseases, including cardiovascular diseases. These authors have concluded that long-term aerobic or home-based exercise seems to benefit patients with coronary artery diseases the most, while high-intensity interval training (HIIT) significantly enhances cardiac performance in patients with chronic heart failure [12]. These notions are supported by more studies focusing on exercise, cardiovascular function, and structure, which will be discussed in detail below.

2.1. Exercise-Induced Functional and Structural Changes

At the tissue level, exercise-induced cardiovascular benefits can be divided into two broad types: Functional responses to higher energy demand during exercise and chronic adaptations in the long run. The latter is thought to be a predominant feature of sustained exercise (i.e., structured, well-planned, and repetitive physical activity). This section will begin with cardiac changes induced by short-term exercise. Then we will discuss chronic responses of physical exercise, mainly focusing on three themes—metabolic flexibility, cardiac remodeling, and angiogenesis (shown in Figure 1).

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Figure 1. Schematic of mitochondrial adaptations in response to exercise and how it contributes to cardioprotection.

2.2. Acute Alterations in Cardiac Function during Exercise

With exercise, hearts will experience physiological adaptations including increased cardiac output (CO) and peripheral perfusion to cope up with dramatically increased musculoskeletal and pulmonary requirements [29–31]. The higher CO results from a concerted effort from increased heart rate (HR), stroke volume (SV), and/or cardiac contractile capacity [29,32]. In addition, exercise may stimulate autonomic function to promote cardiac function. Cardiac chronotropic and inotropic responses to sympathetic system (β-adrenergic response) may be facilitated by exercise along with stimulation of intrinsic myogenic tone [13]. Ample evidence has depicted a rather minor role for parasympathetic system in the tonic control of myocardial function, with norepinephrine from sympathetic nerve fibers being the predominant myocardial regulator in response to exercise [33]. Norepinephrine binds with β1 receptor to turn on G protein and adenylate cyclase. In consequence, cAMP is accumulated in the cytosolic space leading to elevated intracellular Ca2+ levels and higher cardiac contractility [34], which may also be arrhythmogenic and harmful if it is excessive.

2.3. Metabolic Flexibility

Metabolic flexibility refers to the ability of an organism to adapt changes in metabolic demand [35]. Physical exercise significantly increases energy expenditure and demand. Previous findings have identified a link between exercise and improved fatty acid and/or glucose oxidation [36–38]. During exercise, changes in mechanical stretch, catecholamines and circulating substrates (such as free fatty acids) impact cardiac metabolism. Glucose catabolism is transiently suppressed during exercise and is then elevated above the un-trained state after recovery [39]. In this regard, these metabolic changes are not only transient responses to physical activity but also adaptations that prepare the organism for the next bout of activity [40]. This is possibly achieved through autophagy and other cellular catabolic processes to elevate metabolism capacity [40]. Exercise also appears to improve insulin signaling. Exercise is known to promote insulin sensitivity and benefit glucose and energy homeostasis given that insulin signaling is vital for GLUT-4 and hemodynamic function [41]. Preserved glucose uptake has been documented in insulin-resistant muscle following exercise [42]. These events would promote glucose utilization and energy production in the heart. Mounting evidence has suggested that exercise may improve cardiovascular function through indirect actions on lipid and insulin profiles [11,43]. In addition, non-target GC-MS metabolomics analysis of rat

Figure 1. Schematic of mitochondrial adaptations in response to exercise and how it contributes to cardioprotection.

2.2. Acute Alterations in Cardiac Function during Exercise

2.3. Metabolic Flexibility

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2.4. Chronic Adaptations in Heart and Vasculature

Cardiac hypertrophy is thought to be a part of the adaptive remodeling process [5,45,46]. The heart mass, especially those within the ventricular wall (eccentric hypertrophy), rises physiologically as a result of sustained changes in metabolic and remodeling pathways in the heart [47]. Unlike hypertrophy observed in pathological conditions, such as hypertension, this cardiac hypertrophy is characterized by a mild increase in ventricular volume accompanied with reserved or increased myocardial function due to cardiomyocyte growth in size. In addition, this physiological hypertrophy displays none of the features of adverse cardiac remodeling, such as cardiac fibrosis and necrosis [48]. More recent studies have demonstrated distinct signaling molecules mediating cardiac hypertrophy in both physiological and pathological states [49], while how exercise exerts disparate induction of hypertension remains unclear. Induction of IGF-1/IRS-PI3K-Akt pathway is deemed to mediate physiological hypertrophy, which regulates several transcriptional factors [1].

In addition, intermittent hemodynamic stimuli induced by exercise also enhances vascular structure (i.e., increased angiogenesis) and function, which contribute to the increased cardiac output (CO) and lessened atherosclerosis [4]. Exercise training is probably the most sufficient way to improve endothelial function. Based on a systematic review and meta-analysis, a reduction in blood pressure was noted in patients of stroke or transient ischemic attack following exercise training [50]. Complex factors, such as shear stress and alternations in plasma profiles precipitate the activation or restoration of endothelial pathways during exercise [51]. Exercise-induced circulating catecholamines could act on β-3 adrenergic receptors (B3AR) to increase endothelial nitric oxide synthase (eNOS), which augments the bioavailability of NO (nitric oxide), an essential molecule responsible for vasodilation and anti-atherosclerosis effects [52–55]. More recent evidence suggested that rhythmic handgrip exercise promoted increased eNOS phosphorylation, NO generation, and O2

− production, along with improved autophagy markers including Beclin1, microtubule-associated proteins 1A/1B light chain 3B (LC3B), autophagy-related gene 3 (Atg3), and lysosomal-associated membrane protein 2A (LAMP2) as well as decreased levels of p62 in endothelial cells from human radial artery [56]. These findings denote a close tie between eNOS/NO signal cascade and autophagy in exercise-induced regulation on endothelial function.

2.5. Cellular and Molecular Alternations Induced by Exercise

At the cellular level, findings have indicated that physiological hypertrophy is accompanied with the induction of several mechanisms that promote cellular survive, including protein quality control, cell growth protein synthesis, antioxidant generation, autophagy-lysosomal system, and mitochondrial adaptation [1]. In a recent randomized controlled trial, endurance training and interval training (but not resistance training) were found to promote telomerase activity and telomere length, essential markers for cellular senescence, regenerative capacity, and healthy aging [57]. Moreover, physical exercise appears to exert a favorable effect on aging-related cardiometabolic stress through mediating autophagy [58].

Among these mechanisms mentioned above, emerging findings have consolidated a critical role for mitochondria in exercise-offered cardiovascular benefit. Mitochondrial remodeling is a vital determinant in exercise-dependent adaptations. Metabolic changes induced by exercise may influence mitochondrial function, dynamics and turnover, leading to robust mitochondrial network and enhanced metabolic flexibility. It has been shown that the transcription factor EB (TFEB) translocated to myonuclei during exercise and regulated mitochondrial biogenesis and glucose uptake, therefore acting as a major mediator for metabolic flexibility [59]. During exercise, there is a significant increase of mitochondrial biogenesis. Catabolic process through mitophagy is required to confer materials for synthesis and remove dysfunctional organelles that otherwise might result in cellular death. Thus, it is probable that the cardioprotective effects of exercise are strongly associated with mitophagy.

To further discern the upstream pathways in exercise-induced mitochondrial biogenesis and mitophagy, a number of studies were performed which have greatly enriched our knowledge of the

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impact of exercise on mitochondrial integrity [15,27,60–63]. For example, it was demonstrated that exercise-induced phosphorylation of an important energy sensor protein kinase AMPK (protein kinase AMP-activated catalytic subunit alpha 1) and AMPK-dependent ULK1 (unc-51 like autophagy activating kinase 1) phosphorylation is required to target lysosome to mitochondria [64]. Previous studies have recognized a rather pivotal role for transcriptional coactivator peroxisome proliferator-activated receptor-γ coactivator-1α (PGC-1α) in mediating exercise-induced responses on mitochondria. PGC-1α is capable of interacting with several nuclear transcription factors, such as peroxisome-proliferator activated receptor β (PPARβ) and estrogen-related receptor (ERR) to increase mitochondrial biogenesis and to improve mitochondrial energy metabolism [65,66]. Exercise restores mitophagy in high-fat high-fructose-treated liver in a PCG-1α-dependent manner [67], while deletion of PCG-1α compromises the flourishing of mitochondria following exercise [68]. However, Kang and Ji established an overexpression model of PCG-1α via in vivo transfection and found that PCG-1α overexpression drastically suppressed the levels of FoxO1/3 and mitophagy in immobilization-remobilization muscles [69]. Furthermore, the IGF-1/PI3K/Akt cascade implicates in chronic cardiac adaptations following exercise through regulating diverse cellular functions, such as cell growth, glucose metabolism and mitochondrial turnover [1,48]. Akt inhibits the transcription factor C/EBPβand then frees certain serum response factors (SRF) to bind target gene promotor, which orchestrates the maintenance of healthy mitochondrial network and contributes to cardiac hypertrophy [1,48]. Collectively, these studies have delineated general mechanism underlying exercise-induced mitophagy (shown in Figure 2), while more questions remain to be answered.

3. Risk of Exercise for Cardiovascular Function

Regular exercise provides benefit to cardiovascular function [70], while much uncertainty still exists with regards to the impact of strenuous exercise. To date, most studies assumed that whether exercise is salutary largely depends on the frequency, intensity, and duration of exercise [71]. High levels of physical exercise well beyond the recommended levels are tied with higher mortality risks in patients with preexisting cardiovascular diseases. Nevertheless, how much exercise is optimal to exert cardiovascular benefit remains unclear and equally controversial [72,73]. Recent studies have suggested a U-or J-shaped curve which reflects the association between exercise level and health outcomes [74,75]. Substantial evidence has shown that moderate levels of exercise are associated with a reduction in cardiovascular risks [47,76,77]. While too much exercise may be detrimental and is associated with increased risk of cardiovascular mortality [47,75]. Reports in endurance runners demonstrated that marathoners who completed at least 25 marathons in more than 25 years normally possess more severe coronary artery calcification and calcified coronary plaque [78]. A recent survey denoted that individuals who maintain a very high level of physical activity have likely higher odds of developing coronary artery calcification, especially in white American males [79]. Similarly, a large prospective cohort finding from Armstrong and colleagues involving 1,000,000+ women suggesting that strenuous daily physical activity may impose much higher risks of coronary heart disease [74]. Not surprisingly, we should take special precaution in weighing the overall benefit versus risk when advising individuals with regards to the physical exercise engagement. A number of unfavorable cardiovascular events may occur following intensive or excessive physical exercise. For example, exercise is known to precipitate angina pectoris, myocardial infarction, arrhythmias, and sudden death in those individuals with pre-existing coronary artery diseases [1,8,80].

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cellular death. Thus, it is probable that the cardioprotective effects of exercise are strongly associated with mitophagy.

To further discern the upstream pathways in exercise-induced mitochondrial biogenesis and mitophagy, a number of studies were performed which have greatly enriched our knowledge of the impact of exercise on mitochondrial integrity [15,27,60–63]. For example, it was demonstrated that exercise-induced phosphorylation of an important energy sensor protein kinase AMPK (protein kinase AMP-activated catalytic subunit alpha 1) and AMPK-dependent ULK1 (unc-51 like autophagy activating kinase 1) phosphorylation is required to target lysosome to mitochondria [64]. Previous studies have recognized a rather pivotal role for transcriptional coactivator peroxisome proliferator- activated receptor-γ coactivator-1α (PGC-1α) in mediating exercise-induced responses on mitochondria. PGC-1α is capable of interacting with several nuclear transcription factors, such as peroxisome-proliferator activated receptor β (PPARβ) and estrogen-related receptor (ERR) to increase mitochondrial biogenesis and to improve mitochondrial energy metabolism [65,66]. Exercise restores mitophagy in high-fat high-fructose-treated liver in a PCG-1α-dependent manner [67], while deletion of PCG-1α compromises the flourishing of mitochondria following exercise [68]. However, Kang and Ji established an overexpression model of PCG-1α via in vivo transfection and found that PCG-1α overexpression drastically suppressed the levels of FoxO1/3 and mitophagy in immobilization-remobilization muscles [69]. Furthermore, the IGF-1/PI3K/Akt cascade implicates in chronic cardiac adaptations following exercise through regulating diverse cellular functions, such as cell growth, glucose metabolism and mitochondrial turnover [1,48]. Akt inhibits the transcription factor C/EBPβand then frees certain serum response factors (SRF) to bind target gene promotor, which orchestrates the maintenance of healthy mitochondrial network and contributes to cardiac hypertrophy [1,48]. Collectively, these studies have delineated general mechanism underlying exercise-induced mitophagy (shown in Figure 2), while more questions remain to be answered.

Figure 2. Mechanism and signaling pathways involved in mitochondrial adaptation in heart following exercise. Acute exercise augments mitophagy depending on the phosphorylation of AMPK (protein kinase AMP-activated catalytic subunit alpha 1) and ULK1 (unc-51 like autophagy activating kinase 1). AMPK could be activated by exercise-related increase of AMP/ATP ratio, sympathetic activation and other signaling. Mitophagy removes dysfunctional mitochondria and reduces reactive oxygen species (ROS). AMPK also promotes mitochondrial biogenesis through regulating PGC-1a. Regular exercise mainly activates the IGF1-PI3K-Akt pathway, which targets several transcription factors in nucleus and contributes to cell growth, cellular survival, metabolic homeostasis, and mitochondrial maintenance. Abbreviations: AMPK, AMP-activated kinase; Sirt1, Sirtuin 1; PGC-1a, peroxisome proliferator activated receptor gamma co-activator 1a; IGF-1, insulin-like growth factor-1; PI3K, phosphoinositide-3 kinase; Akt, serine/threonine-protein kinase; C/EBPβ, CCAAT/enhancer binding protein b; Cited4, cbp/p300- interacting transactivator with Glu/Asp-rich carboxy-terminal domain 4; SRF, serum response factor.

There are emerging data denoting that sustained intense exercise may lead to adverse electrical and structural remodeling in the heart [81]. Moreover, plasma catecholamine responsiveness may be inappropriately affected by exercise which is manifested as chronotropic incompetence and lower plasma epinephrine response to exercise probably as a result of abnormal sympathoadrenal and autonomic function. Sustained exposure of catecholamine may trigger downregulation of β-adrenergic receptors (desensitization), resulting in loss of adenylate cyclase responsiveness and cardiac contraction during exercise. The β-adrenergic receptor-adenylate cyclase signaling cascade is essential to the maintenance of myocardial homeostasis [82]. A loss in either quantity or sensitivity of β-adrenergic receptors should disengage myocardium to sympathetic innervation (through norepinephrine) during physical exercise. Likewise, modification of β-adrenergic receptor-linked adenylate cyclase may also decrease adenylate cyclase activity and exercise capacitance. Therefore, decreased (or sometimes unchanged) myocardial contractile function during exercise fails to cope with the need from cardiopulmonary system for blood and oxygen for a homeostatic condition. Other than decreased left ventricular contraction, compromised diastolic function was also noted during exercise [83]. Although a number of mechanisms have been put forward, loss of myocardial function at rest and during exercise

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seems to be associated with myocardial alterations including myosin isozyme switch (V1 to V3) and phosphorylation of cardiac inhibitory protein TnI [34].

In contrast, this scenario may not hold true in healthy individuals. High levels of strenuous or vigorous exercise seem to have little effects on overall mortality in healthy individuals although intensive training may compromise the health benefits associated with regular moderate physical activity [72]. Greater emphasis should be made on how a well-functioning organism or individual combats the risks of exercise. Mounting efforts have illustrated exercise, especially intense or prolonged exercise, may cause oxidative stress and subsequent damage in myocytes [80]. Oxidative stress, energy requirement, and mitochondria are closely linked [20,84]. Therefore, we may propose that mitochondrial quality control is indispensable for beneficial adaptations induced by exercise. Oxidative stress could activate mitophagy to cope with mitochondrial dysfunction. Earlier studies have demonstrated a strong association between protective mitophagy and exercise, which we will elaborate in the next section.

4. Mitophagy and Exercise

Mitophagy is initiated when damaged mitochondria are labeled for degradation [20]. The major fission protein Drp1 (dynamin related protein 1) is translocated to depolarized mitochondrial membrane and segregates the damaged components from the rest of the healthy mitochondria [20,85]. Then, PINK1 (PTEN induced kinase 1) accumulates on compromised mitochondria and recruits E3 ubiquitin-protein ligase Parkin, which ubiquitinates a branch of proteins on outer mitochondrial membrane (OMM) [20,86]. Certain autophagy receptors, such as NDP52 (CALCOCO2, Ca2+ binding and coiled-coil domain 2) and optineurin then tether mitochondria to autophagosomes, which subsequently fuse with lysosomes for lysosomal degradation. It is noted that PINK1 would recruit autophagy receptors at a low rate independent of Parkin [87]. In addition to the PINK1/Parkin signaling cascade, several OMM-localized mediators, including NIX (NIP3-like protein X), BNIP3 (BCL2 interacting protein 3), FUNDC1, and cardiolipin could target mitochondria to autophagosome through binding to LC3 (microtubule associated protein 1 light chain 3α) on phagophores in response to developmental signals or hypoxia [88,89]. However, it should be noted that chronic hypoxia may overtly upregulate the level of housekeeper proteins. Thus, data normalized against these housekeeping proteins, such as GAPDH, actin and tubulin should be handled with special caution when heart tissue is exposed to hypoxia [90].

Exercise-induced mitophagy might slightly differ from the conventional pathways. It has been demonstrated that Parkin is indispensable for exercise-induced mitophagy initiation. Exercise stimulates mitophagy flux courtesy of increased recruitment of Parkin to mitochondria, despite that Parkin knockout did not impact basal mitophagy [91]. Examination conducted by Drake and colleagues found enhanced mitophagy levels in the absence of discernable PINK1 accumulation in skeletal muscles following exercise, while HeLa cells treated with carbonyl cyanide m-chlorophenyl hydrazone (CCCP) displayed overtly elevated PINK1 [92]. The relationship between exercise and mitophagy has been extensively studied, mainly using skeletal muscle or myocytes. Given the critical role of mitochondria in cardiomyocyte energy production and function [20], there has been an increasing interest in exercise-induced mitophagy in heart. In this section, we will introduce recent studies (last 5 years) on how exercise regulates mitophagy.

4.1. Exercise as a Treatment or Prevention to Diseases: The Role of Mitophagy

First, a mainstream of research has focused on revealing the close tie between exercise and temporarily enhanced mitophagy. It was indicated that Beclin1, LC3, and BNIP3 were remarkably upregulated in rat myocardium during acute exercise and were then slowly declined to baseline 48 h later [93]. Likewise, PINK1, Parkin, Ubiquitin, p62, and LC3 were overtly elevated in rat skeletal muscles after downhill treadmill running for 90 min with the upregulation lasting for more than 24 h [94]. It is noteworthy that shear stress has emerged as a modulator of autophagy during exercise. It was reported that 1 h of rhythmic handgrip exercise initiated autophagy, NO generation and O2

−

production in humans due to the elevated shear stress [56]. In an earlier study, it was determined that

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inhibition of autophagy prevented NO production and enhanced ROS formation [95]. Thus, autophagy plays a critical role in NO bioavailability and redox homeostasis in endothelial cells. In addition to acute exercise, Ju and coworkers observed remarkable activation of autophagy flux and mitochondrial dynamics (both fusion and fission) in mice following sustained (8-week) swimming training. Moreover, when treated with colchicine, a blocker for autophagosomal degradation, BNIP3 was found increased while exercise-induced mitochondrial biogenesis was greatly diminished, indicating a possible role of mitophagy in mitochondrial content or biogenesis following exercise [96].

To date, studies have recognized a protective role of mitophagy during exercise. Mitophagy flux presumably protects the heart from exercise-induced risk. It is possible that mitophagy was stimulated by exercise-related activation of inflammation and accumulation of ROS, while upregulated mitophagy could remove ROS and eliminate inflammation, thus reducing mitochondrial injuries [93]. Figure 1 shows the possible schematic of how exercise exerts cardioprotective effects through modulating mitochondria homeostasis. Moreover, exercise shows promise as a safe and inexpensive way to treat multiple diseases, including cardiovascular diseases. There is an increasing emphasis on mitophagy in exercise treatment. Short-duration exercise regimen has been recommended for cardiac rehabilitation after stable myocardial infarction based on the favorable response of short-duration exercise (15-min swimming training per day, 5 times per week for 8 weeks) on cardiac function in mice. It has been suggested that increased SIRT3 as well as PINK1/Parkin was responsible for this [62]. Moreover, it was suggested that long-term (8 weeks) exercise coupled with caloric restriction prior to isoproterenol injection may prevent heart failure more efficiently than either therapy alone possibly through stimulation of autophagy [97]. Despite few data available on the role of mitophagy in resistance exercise, it was indicated that resistance exercise may attenuate muscle atrophy through elevated mitophagy and biogenesis in rats [98].

It is speculated that autophagy is required during caloric restriction and physical exertion for survival, and is repressed in nutrient-rich conditions [99]. However, human beings are no longer forced to be engaged in frequent physical activity in modern life, with the development of science and technology. Moreover, there is a rising concern that both sedentary behavior and caloric abundance are major contributors to a range of chronic diseases, including insulin resistance, obesity, diabetes mellitus, cardiovascular diseases, and various forms of cancer [100–104], while regular physical exercise helps to prevent these chronic diseases [105,106]. Moreover, metabolic diseases are among the major independent risk factors of cardiovascular diseases. Hopefully, physical exercise would promote cardiovascular health through primary and secondary prevention. Therefore, a number of investigators have sought to determine the salutary effects of exercise concurrent with low-quality diet. In particular, the contribution of autophagy or mitophagy has drawn close attention recently. Markers of mitophagy, autophagy, and mitochondrial dynamics were assessed in high-fat diet treated mice which were also engaged in either voluntary physical activity (VPA) or endurance training (ET). Researchers found that both VPA and ET rescued the high-fat-related increase of apoptosis and decrease of autophagy and mitochondrial biogenesis in mouse livers, leading to protection against nonalcoholic steatohepatitis. In particular, only ET reverted mitophagy and reduced mPTP opening [107]. Likewise, Rosa and colleagues detected an increase of autophagy (LC3-II/I ratio, p62) in mouse livers following a 4-week voluntary wheel running in both Western diet and normal diet groups, while Western diet suppressed BNIP3 levels by 30% compared to normal diet group. These authors proposed that increased autophagy may protect the liver from excessive lipid accumulation [108]. In addition, Tarpey found a remarkable increase of mitophagy in skeletal muscle biopsies from male runners after endurance training. However, they found no difference in mitophagy between fasting conditions and 4 h after high-fat diet intake, indicating that mitophagy may not be the dominant contributor to the exercise-induced protective metabolic flexibility against high fat diet intake [109]. One can argue that 4 h of high-fat diet intake is too short to impose any metabolic abnormality. To this end, these inconsistent findings are slightly biased, given the complexity of exercise and diet.

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4.2. Mitophagy is Attenuated Due to Improved Mitochondrial Pool after Sustained Exercise Training

Mitophagy triggered by regular exercise precipitates the accumulation of healthy mitochondria as well as improved mitochondrial function. Therefore, mitophagy is believed to be maintained at an optimal (perhaps a low) level as a result of the long-term exercise training. Muscle biopsy obtained from human subjects showed increased LC3I, BNIP3, and Parkin levels 2 h following moderate cycling training. Interestingly, an increased capacity for mitophagy was also observed following an 8-week training [3]. Chen and coworkers further noted that sustained endurance training drastically attenuated exercise-induced mitophagy due to the overall improvement of mitochondrial quality [91]. Likewise, a study examining mitophagy between young and aged rat muscles revealed upregulated mitophagy in the aged group, while chronic contractile activity (CCA) limited mitophagy and improved mitochondrial stabilization [110]. In the same vein, another independent study also documented decreased mitophagy after a 5-day CCA. They further detected increased lysosome biogenesis regulator TFEB and LAMP1, indicating improved lysosomal degradation capacity [111]. Li and associates found that exhaustive exercise following exercise preconditioning displayed an unchanged LC3-II/LC3-I ratio. They further determined the levels of autophagy in different phases. Exhaustive exercise (EE) showed reduced LC3-II/LC3-I ratio, while exercise preconditioning (EP) transiently activated autophagy (especially at 2 h after EP) and attenuated EE-induced myocardial injury, which indicated preserved basal autophagy might underlie EP-offered benefit [112]. Besides endurance exercise, a study conducted by Estebanez and colleagues depicted that 8-week resistance exercise training prevented activation of mitophagy in peripheral blood mononuclear cells from otherwise healthy elderly individuals [113].

Ample studies have focused on the long-term effects of exercise on diseases as summarized nicely in recent reviews [1,3,100]. It is assumed that improved mitochondrial quality after exercise confers better cardiac performance and restrains pathological activation of mitophagy in response to acute stresses. Several attempts have been made to clarify whether exercise preconditioning imposes protective effects under acute cardiac stress. It has been shown that late exercise preconditioning protected the heart from exhaustive exercise-caused injuries through increasing Parkin-mediated mitophagy [114]. It was further suggested that exercise preconditioning augmented mitophagy via H2O2 oxidative stress-induced activation of PI3K [115]. Consistent with this view, it was found that earlier aerobic exercise complemented by a natural herb Rhodiola sacra protected the cardiac and skeletal muscles in exhaustive exercise through enhanced mitophagy [116]. Moreover, it has been demonstrated that exercise preconditioning may also exert protection against doxorubicin-induced cardiotoxicity [117]. Marques and team suggested that endurance exercise training before or during sub-chronic doxorubicin treatment prohibited doxorubicin-induced mitophagy, mPTP opening and apoptosis [118]. However, in contrast to finding from Marques, Lee argued that endurance exercise training prior to doxorubicin-treatment turned on protective mitophagy and suppressed NADPH oxidase 2 (NOX2) to protect against doxorubicin-induced cardiotoxicity [119].

Arrhythmia, especially fibrillation serves as a hallmark of cardiac injury and contributes to high cardiac mortality. Although a tight correlation between mitophagy and ischemic injury has been extensively described [120], whether mitophagy/autophagy participates in myocardial arrhythmia remains somewhat elusive. Lekli and associates thoroughly examined the occurrence of autophagy as an adaptive response to arrhythmogenesis, which might improve myocardial recovery through offsetting proteotoxic stress [121]. These authors suggested that intervention targeting autophagy should be taken with the precaution since excessive autophagy may be detrimental. A more recent study showed complex alternations of autophagy-associated proteins (decreased p62 and gradually reduced LC3BII/LC3BI) in ventricular fibrillation [122]. Thus, the association between arrhythmia and autophagy is unclear and further studies should be warranted. Isoproterenol is an extensively employed non-selective β-adrenergic agonist. It was suggested that at small dose of isoproterenol, autophagy may cope with the toxic arrhythmic effect of isoproterenol [123]. It is anticipated that non-invasive interventions such as exercise might be the countermeasure to arrhythmogenesis.

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4.3. Compromised Mitophagy Response under Certain Pathological Conditions

It is possible that aging or certain metabolic diseases, such as obesity and diabetes, might compromise the regulation of mitophagy during exercise (shown in Figure 1) [58,124]. To examine whether mitophagy response induced by exercise vary in pathological states, a number of studies have been carried out. It has been shown that mitophagy flux stimulated by exercise was attenuated with age, resulting in mitochondrial deficiency during exercise in aging muscles [91]. Lipidated LC3II, the gold-standard indicator of autophagosome content, was upregulated 48 h following resistance exercise in untrained young but not older men [125]. The unfolded protein response (UPR) is another important adaptive reaction to exercise. Transcriptomic analysis revealed that the activation of UPR was attenuated in older healthy women and men compared to young adults following a single bout of exercise. Furthermore, the coordination between UPR and p53/p21 axis of autophagy was less evident in older [126]. In another independent study, an aging-induced significant decline of mitochondrial quality control proteins, such as Lon, could be partly rescued by exercise training [127]. Likewise, despite the increase of mitochondrial complex II, there was no noticeable change in BNIP3, MUL1, and LC3 II/I ratio in muscle biopsies of type 2 diabetic patients following a 3-month endurance training [128]. Nonetheless, contradictory findings are observed in human and rodent studies. A study tested mitophagy in mouse and human skeletal muscles. The results showed an aging-associated decline of PCG-1α and an increase of BNIP3 and LC3 II in mice, which was ameliorated by lifelong exercise training. However, markers of mitophagy and apoptosis were altered slightly during human aging, while lifelong exercise training upregulated BNIP3 [129]. It has been reported that a bout of unaccustomed resistance exercise for knee extensors transiently reduced the overall expression of mitochondrial proteins except for PCG-1α with no apparent change of mitophagy (VDAC, PINK1/Parkin) in both young and age candidates [130].

Sex difference exists in cardiovascular function [131,132]. Likewise, sex difference has also been noted in cardiac responses to exercise in individuals with cardiovascular diseases. Despite a similar exercise capacity, female heart failure patients with preserved ejection fraction (HFpEF) exhibited greater cardiac and extracardiac deficits, including worse biventricular systolic reserve, diastolic reserve, and peripheral O2 extraction [133]. A number of scenarios have been postulated for the sex difference in exercise-induced cardiovascular responses. For example, sex steroid hormones and their receptors exist in mitochondria from skeletal muscles, which may contribute to sex differences in cardiac performance in response to exercise. It was suggested that estrogen receptor binding attenuates the reduction in mitochondrial size and thus inhibits apoptosis. Other mechanisms in sex difference in exercise response may encompass activation of PI3K/AKT pathway and extracellular signal-regulated kinase 1/2 (ERK 1/2), which are also important regulators in exercise-induced mitophagy. Lack of estrogen and disruption of estrogen receptors might explain, in part, the reduced mitochondrial density and muscle mass in postmenopausal women [134]. Nonetheless, whether autophagy directly participates in these sex-related differences in exercise response remains unclear.

Moreover, studies have cast doubts on exercise-induced mitophagy. Unlike previous studies, Schwalm and colleagues provided evidence that mitophagy remained unchanged during and early (1 h) after acute high-density (70% VO2peak) endurance exercise in human skeletal muscles, whereas proteins and mRNA markers for mitochondrial fission and mitophagy (Drp1, Fis1, BNIP3) were more expressed in the fed state than the fasted state [135]. For some reason, a study including 11 participants examined gene expression of human muscles after exercise and argued that PINK1 and PARK2 mRNA were transiently decreased 3 h after 60-min cycling and returned to baseline 6 h later. These investigators also noticed that PCG-1α was elevated after exercise but was gradually decreased (albeit not below the baseline level) 6 h later [136]. In addition, a recent study also showed reduced mitochondrial mass and impaired respiratory function along with exercise-induced mitophagy induction in rat soleus muscles. However, the sample size was relatively small and the mitochondrial defect may also be attributed to lack of mitophagolysosome degradation [94]. Taken together, further research is needed to clarify the transient changes of mitophagy in health and diseases during and after exercise as well as how it impacts cellular health.

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5. Conclusions

Given the ever-growing public concern on cardiometabolic diseases, there is an urgent need to hunt for effective preventive regimen, from pharmacological and non-pharmacological perspectives [137–140]. Given that physical inactivity is a well-known independent risk factor for all-cause mortality, regular physical exercise may offer profound health benefits in many aspects including cardiac performance, exercise tolerance, endothelial function, inflammatory response, insulin sensitivity, autonomic regulation, and blood pressure control along with glucose and lipid metabolism, adiposity, and psychosocial parameters [57,140]. Considering that exercise may impose both benefit and risk to human health, only modest or moderate exercise (less resistant type), is recommended to achieve a cardiovascular benefit. It is well perceived that regular moderate exercise may serve as an essential measure for the prevention and management of chronic diseases, including obesity, diabetes mellitus, atherosclerosis, and coronary artery disease [141,142]. Long-term exercise instigates physiological cardiac hypertrophy with preserved pump function. In this regard, a better understanding of the cellular and molecular mechanisms behind cardiac responses to exercise (physiology or pathological) should offer potential novel therapies against various cardiac anomalies. Given the critical role of mitochondria in the maintenance of cardiac homeostasis, mitochondrial quality control in particular mitophagy should be vital for cardiac health. In view of all that has been discussed in our review, we may propose that endurance exercise training protects cardiovascular system from acute stress possibly through maintaining homeostatic mitophagy. However, what we have learned about exercise-induced mitophagy is essentially based upon experimental studies and mainly skeletal muscles. There is a current paucity of well-controlled studies describing how exercise impacts cardiovascular function through regulation of mitophagy. To unveil the benefit versus risk for physical exercise on cardiovascular function, future studies should examine various types of exercise on autophagy and selective autophagy levels in an effort to provide insights into novel therapeutic avenues for the management of cardiovascular diseases. These findings will help us to evaluate the potential of mitophagy as a target for cardioprotection.

Author Contributions: N.N.W., H.T. and J.R. drafted the manuscript, P.C., D.W. and Y.Z. edited the manuscript.

Funding: Work conducted in our lab was supported in part by the Natural Science Foundation of China (NSFC 81570225, 91749128 and 81770261), Science and Technology Innovation Project of the Chinese Academy of Medical Sciences (Health and Longevity Pilot Special Project 2019-RC-HL-021). HT received support in part from the Chinese Postdoctoral Science Foundation (2019M651553).

Acknowledgments: The authors received support in part from the Natural Science Foundation of China, Chinese Academy of Medical Sciences and Chinese Postdoctoral Science Foundation.

Conflicts of Interest: The authors declare no conflict of interest.

Ethical Approval and Consent to Participate: Work conducted in our laboratories has been approved by the institutional ethics committee at the Zhongshan Hospital Fudan University (Shanghai). No human studies were involved.

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Introduction
Contemporary Theory behind Exercise-Induced Cardiovascular Benefit

Exercise-Induced Functional and Structural Changes
Acute Alterations in Cardiac Function during Exercise
Metabolic Flexibility
Chronic Adaptations in Heart and Vasculature
Cellular and Molecular Alternations Induced by Exercise

Risk of Exercise for Cardiovascular Function
Mitophagy and Exercise

Exercise as a Treatment or Prevention to Diseases: The Role of Mitophagy
Mitophagy is Attenuated Due to Improved Mitochondrial Pool after Sustained Exercise Training
Compromised Mitophagy Response under Certain Pathological Conditions

Conclusions
References

Turning the Corner: A Comparison of Collegiate Athletes’ and Non-Athletes’

Turning Points in Eating Disorder Recovery

Jessyca N. Arthur-Cameselle Western Washington University

Molly Curcio William James College

The purpose of this qualitative study was to identify turning points in eating disorder recovery in collegiate female athletes compared to non-athletes. The sample included 12 varsity athletes and 17 non-athlete college students who previously met criteria for Anorexia Nervosa (AN; n = 17); Bulimia Nervosa (BN; n = 3); Binge Eating Disorder (n = 1); or both AN and BN (n = 8). Participants completed individual interviews and responses were analyzed inductively. There was some commonality in the athletes’ and non-athletes’ experiences. For exam- ple, the most frequent turning point for both groups was Insight/Self Realization. Regarding the next three most frequent turning points, athletes reported Sport Performance, Confrontation, and Support/Concern from Others, whereas non- athletes reported Professional Treatment, Hitting a Low, and Support/Concern from Others. This study contributes to the sparse literature on competitive athletes’ recovery. Results indicated that athletes’ turning points differed from non-athletes; therefore, findings are discussed concerning athlete-specific treatment recommen- dations and suggestions for coaches.

Keywords: anorexia, bulimia, motivation, sport, tipping point

It is evident that competitive athletes experience clinical eating disorders (EDs). Out of the broader athlete population, research has demonstrated fairly consistently that female athletes are at higher risk for EDs and disordered eating than male athletes (e.g., Giel et al., 2016) and that athletes who compete in weight- sensitive sports are at higher risk than those from ballgame sports (e.g., Krentz & Warschburger, 2011). There are no known studies that report athlete-specific treat- ment and recovery rate data; however, literature reviews on general ED popula- tions indicate that treatment is only effective for roughly 50 to 70% of individuals with EDs (e.g., Keel & Brown, 2010). For those with Anorexia Nervosa (AN),

Arthur-Cameselle is with the Health and Human Development Department, Western Washington University, Bellingham, WA. Curcio is with the Clinical Psychology Department, William James College, Newton, MA. Address author correspondence to Jessyca N. Arthur-Cameselle at Jessyca. [email protected].

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https://doi.org/10.1123/jcsp.2018-0030

mailto:[email protected]

there may even be strong reluctance to recover (Nordbø et al., 2012), yet it is clear that motivation and readiness for change predicts success in ED treatment (Clausen, Lubeck, & Jones, 2013). Thus, researchers have sought to better under- stand what motivates women to recover and why some are able to begin recovery.

Due to the complex and personal nature of ED recovery, qualitative methods are well suited to explore the topic. Indeed, there is now a large body of qualitative studies on the emotional, personal, and social experiences of (non-athlete) women who have recovered (e.g., Linville, Brown, Sturm, & McDougal, 2012). Though many studies have explored the process and course of recovery, far fewer have focused specifically on the initial motivation to begin recovery. This initial period in the recovery process is referred to in the literature as a turning point or tipping point, described as the “point at which the illness trajectory is interrupted” (Fogarty & Ramjan, 2017, p. 2) so that “the balance finally tipped in favor of pursuing recovery as opposed to continuing with the illness” (Dawson, Rhodes, & Touyz, 2014, p. 499).

Previous qualitative studies on non-athlete female samples have provided information about turning or tipping points as part of broader studies on the entire recovery journey. For example, through interviews with 48 women (average age 27.6) with a variety of EDs, Pettersen and Rosenvinge (2002) found that motiva- tion to recover was most often due to “the desire for a better life” (p. 65) in addition to experiencing negative consequences from the ED. Similarly, Redenbach and Lawler (2003) reported that their five participants (ages 24–51) initiated recovery following physical or medical complications, the desire for an improved life, self- determination, and self-acceptance. Also through interviews, D’Abundo and Chally (2004) found that their 17 participants’ (ages 17–46) ED symptoms esca- lated until the disorder controlled their lives and compromised their health, which was followed by acceptance of each of the following: the ED, others, and spiri- tuality. The nine participants (ages 19–48) in Lamoureux and Bottorff’s (2005) study also began recovery after acknowledging the dangers of AN. Likewise, Nilsson and Hägglöf (2006) reported that all of their 58 recovered participants (median age 30) could identify a turning point, which included negative medical consequences from the ED, new insights, or unexpected life events like a death of a friend. Overall, these studies indicate that participants often turn to recovery after a realization that the ED had compromised their quality of life.

More recent studies have revealed similar findings. For example, for 14 women (ages 23–26) who had recovered from Bulimia Nervosa (BN), turning points included self-realizations, opening up to others, hitting a low, and experienc- ing negative physical and social consequences (Lindgren, Enmark, Bohman, & Lundstrom, 2015). The researchers noted that for most participants, “a crisis or turning point was important to taking the first step” (Lindgren et al., 2015, p. 866). Similar turning points were reported by eight women (ages 31–64) who recovered fromAN, which included feeling exhausted, gaining insight into the function of the disorder, feeling more understood, and newfound agency (Dawson et al., 2014). Moreover, Linville et al. (2012) reported that, in their sample of 22 participants (ages 23–55) with a variety of EDs, recovery was sparked by a desire to repair key relationships. Finally, in narrative-discursive interviews with 14 recovered women (ages 19–49), Moulding (2016) found that participants’ turning points included finding a new sense of belonging, gaining insight into consequences of the

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disorder, becoming self-reliant, and cultivating a new identity. Taken together, these studies indicate that turning points are common, if not somewhat universal, in the recovery journey and that they consistently include internal shifts, acknowl- edging negative consequences of EDs, relationship changes, hitting a personal low, and increased self-reliance.

Only a few published qualitative studies have focused solely on turning points, providing more in-depth information about this early stage of recovery. Matusek and Knudson (2009) used co-constructed performance texts to explore the turning points of eight women, though they published only three participants’ accounts (ages 24–57). All three participants described involvement in some kind of larger cause, such as community events, political movements, or spiritual outlets; in addition, participants described internal turning points that occurred almost simultaneously, such as increased self-agency. The authors stated that treat- ment was not critical to participants’ recovery and instead suggested that starting recovery required holistic healing, with attention to community and spiritual connections, not only physical and emotional health (Matusek & Knudson, 2009). Activism or spiritualty reportedly moved participants’ focus away from internal self-criticism, providing a new sense of identity and a commitment to a larger purpose, which allowed them to leave the ED behind. Next, through analysis of 31 autobiographies by authors who had recovered from AN (ages 18–57), Hay and Cho (2013) found that all texts referenced a turning point, including increased self-regard, positive treatment experiences, new or improved relationships, as well as finding personal meaning in hobbies or activities unrelated to AN. Improved self-esteem was key to turning participants toward recovery, which was often a result of self-reflection that did not involve treatment. Like Matusek and Knudson (2009), Hay and Cho (2013) suggested that engaging with spirituality, as well as hobbies that encouraged participants to spend energy on things other than AN, tipped the balance to recovery. Most recently, Fogarty and Ramjan (2017) asked 67 women with AN (average age 25.11 years), via open-ended surveys, to “describe the turning point (or light bulb moment)” (p. 6) in their recovery. Common themes in the responses were: realization of the health consequences from AN, a loss or potential loss of life experiences, or the desire to be healthy for a specific purpose (e.g., becoming a mother). The authors stated that the women needed to lose something personally important before they were truly motivated to recover, yet that loss came in variety of forms depending upon the individual. Based on these more in-depth studies, turning points appear to be comprised of a mix of internal and external experiences, which regularly include a reprioritization of values that is not necessarily connected to experience in professional treatment. These studies also highlight that turning points are complex, demonstrating the importance of qualitative studies that capture rich data on multifaceted influences on recovery.

Though the above studies provide an understanding of turning points for non- athletes, there are few studies that examine any aspect of athletes’ ED recovery or treatment (e.g., Plateau, Arcelus, Leung, & Meyer, 2017) and only two studies, to our knowledge, that reference athletes’ turning points. First, for a male athlete with Bulimia, a serious injury that required him to leave competitive sport was the “key transition” that led to his recovery; specifically, leaving sport afforded him more free time to cope with life stressors (Papathomas & Lavallee, 2006, p. 165). In another qualitative investigation, Arthur-Cameselle and Quatromoni (2014a)

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interviewed 16 female collegiate athletes who had recovered from clinical EDs, inquiring about factors that initiated, assisted, and hindered their recovery. The most commonly reported factor that initiated recovery was negative consequences from the ED. Other turning points included an intervention, wanting a better quality of life, confiding in others, and improved self-esteem. Although these two studies provide some insight into athletes’ experiences, turning points were not the primary focus of either study; thus, very few participant quotes were included and implications of the turning point findings were not elaborated upon. Therefore, athletes’ turning points have not been explored thoroughly enough to understand their experiences or inform practitioners’ work.

At present, there are no published studies that have directly compared the turning points of athletes to those of non-athletes; yet, there are several reasons to expect that athletes may have unique experiences. First, past research indicates that athletes are a unique ED subgroup in that they experience sport-specific weight pressures including revealing uniforms, coach criticism, and team weigh- ins (e.g., Reel, SooHoo, Petrie, Greenleaf, & Carter, 2010). In addition, athletes have reported several sport-specific triggers for disordered eating and clinical EDs, including performance pressure, sport injuries, and changes in coaches (e.g., Arthur-Cameselle, Sossin, & Quatromoni, 2017; Papathomas & Lavallee, 2006, 2014; Sundgot-Borgen, 1994). Although non-athletes certainly experience pressures that contribute to EDs, such as academic pressure, they do not use their bodies for competition like athletes, which may differentially influence athletes’ food choices and eating behaviors. Based on evidence that socio-cultural factors influence EDs (e.g., Matusek & Knudson, 2009; Papathomas & Lavallee, 2014), it is also possible that athletes’ turning points, due to their interactions with coaches, teammates, and competitors within the social world of sport, may differ from non- athletes. Therefore, past non-athlete findings should not be assumed to apply to athletes. Given that motivation for recovery predicts treatment outcomes (Clausen et al., 2013), more precise knowledge of what tips athletes toward recovery could help to design more effective interventions for athletes. Moreover, it is of clinical interest to determine how athletes are able to achieve recovery while still within the competitive sport environment, with its sport-specific weight pressures and triggers. Of course, such information cannot be gleaned from past studies on non-athletes.

In addition, there is a need for turning point research on younger samples. As indicated above, most studies on turning points have utilized samples with a very wide variety in age, regularly including women between 30 to 50 years old, who arguably have much different life circumstances than typical competitive athlete samples, who are more likely to be in their teens and twenties. As such, it is unclear if insights from these studies are relevant for competitive college-aged athletes. Again, because social worlds influence turning points (e.g.,Matusek&Knudson, 2009)more homogeneous samples in terms of age and social environment are needed.

Finally, there is a need for research on clinical-level EDs in athletes. Although there are many studies on the efficacy of ED prevention programs for athletes (see Bar, Cassin, & Dionne, 2016 for a review) as well as in-depth analyses of dis- ordered eating in athletes (e.g., Papathomas & Lavallee, 2010, 2014), there is still relatively little information on athletes’ recovery from clinical EDs. Therefore, studies are needed that directly compare the recovery experiences of athletes with clinical EDs to a group of non-athletes who are similar in terms of other key

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demographics such as age, education level, and experience with treatment. If sub- group differences exist, such information could inform athletes’ clinical ED treatment as well as coach education programs.

In sum, there is a need for research on athletes’ turning point experiences, particularly since they report sport-specific ED onset triggers. Researchers have called for more in-depth understanding of the personal experiences of athletes with EDs (e.g., Papathomas & Lavallee, 2014). Yet, there remains a dearth of research on athletes’ turning points and relatively few studies on any aspect of recovery in athletes with clinical EDs. There is also a lack of research on turning points in young adults. Therefore, the purpose of this qualitative study was to identify turning points that initiated recovery from clinical EDs in a sample of collegiate female athletes compared to a group of non-athlete college student peers, to determine if any subgroup differences were evident. The inclusion criteria required that all participants were female college students, over 18 years old, who had experienced a clinical level ED for six or more months, had attended professional treatment, and had experienced at least three months of recovery. The focus of this study was on women because they more frequently experience EDs than men (American Psychiatric Association [APA], 2013) and because there is a more much substantial body of previous research on female non-athletes’ tipping points. Thus, a focus on women in the current study allowed for a richer comparison of findings from this study to past research, which could help to elucidate any sport-specific findings in the current results.

Method

Participants

The sample included 29 women (12 varsity collegiate student-athletes, 17 non- athletes) who attended colleges on the east coast of the United States. They were, on average, 20.1 years old (athletes’ mean = 20.5 years; non-athletes’mean = 19.8 years) and identified as White (n = 28) or Hispanic/White (n = 1). Athletes com- peted in varsity sports at the Division I (n = 10) or Division III (n = 2) levels of the National Collegiate Athletic Association (NCAA) in track& field and cross-country (n = 4), track & field only (n = 4), basketball (n = 1), crew (n = 1), soccer (n = 1), or tennis (n = 1). Participants previously met Diagnostic and Statistical Manual of Mental Disorders (DSM-5; APA, 2013) criteria for Anorexia (AN), Bulimia (BN), or Binge Eating Disorder (BED) and all had attended professional treatment. The athletes previously experienced AN (n = 8, 66.7%), BN (n = 2, 16.7%), or AN fol- lowed by BN (n = 2, 16.7%); the non-athletes previously met criteria for AN (n = 9, 53%), BN (n = 1, 6%), BED (n = 1, 6%), or AN followed byBN (n = 6, 35%). At the time of the interview, all participants were in a self-defined period of “recovery” and also no longer met DSM-5 criteria for any ED. On average, the athletes’ recovery period was 10.4 months long and non-athletes’ recovery was 14.4 months long.

Procedure

Participants were recruited for a two-part interview study. They were initially located through fliers posted on college campuses on the East Coast of the United

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States as well as emails to athletic directors. All procedures received institutional ethical approval and participants provided informed consent. The first author, a licensed psychologist, conducted all interviews and confirmed by way of diag- nostic questions that participants previously had met DSM-5 criteria (APA, 2013) for an ED and that they no longer met criteria for any ED. They then responded to questions for a study regarding the onset of EDs (Arthur-Cameselle et al., 2017). All participants who completed the portion of the interview related to ED onset continued to respond to questions for the current investigation on turning points. Therefore, the researcher had already established rapport and had an understanding of the circumstances associated with the onset of each participant’s ED before exploring turning points.

For this study, the interview was semi-structured and began with open-ended questions about the duration and details of the participants’ symptoms. After describing their ED history, most participants spontaneously began talking about what initially motivated their recovery. If they spontaneously discussed a turning point, the interviewer encouraged elaboration and followed-up with neutral probes for additional details and reflection. The first follow-up probe was, “What do you think helped you to begin recovery at that time?” and after participants had appeared to finish responding they were asked, “Were there any other things that contributed to your recovery starting at that time?” If participants finished dis- cussing symptoms without talking about turning points, the interviewer asked them to describe any turning points, which were defined using the description from Dawson et al. (2014, p. 499). The interviewer used the same follow-up probes with all participants. Otherwise, the interviewer allowed participants to tell their stories at their own pace and interjected only for points of clarification.

Interviews ranged from 29 to 44 minutes for this portion of the research (64 to 78 minutes total for both segments). Each interview was recorded and transcribed verbatim; only filler words such as “um” and “like” were removed. All partici- pants were offered their interview transcript and were asked to report any inac- curacies; none requested changes. Despite claims that there may be limited utility in sending participants their transcripts to enhance data analysis (Thomas, 2017), we believed it demonstrated respect for participants and displayed our commitment to informed consent. Past researchers have sent transcripts for similar reasons (Thomas, 2017).

Data Analysis

We used the inductive coding protocol outlined in Consensual Qualitative Research (CQR) for analysis (Hill et al., 2005; Hill, Thompson, Williams, 1997), which is recommended for research on psychological experiences. The research team included the primary author, who is a licensed psychologist and professor, as well as two senior undergraduate student researchers (one man, one woman) who had completed coursework in abnormal psychology, sport psychology, and re- search methods. The primary author trained them in CQR and the team completed practice coding on sample data prior to this analysis. In line with CQR protocol, we set inclusion criteria at the outset of the study, did not begin analysis until all interviews were complete, did not use a theory to frame the analysis, and made all coding decisions by consensus.

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Each member of the research team inductively coded responses individually. We then met to discuss coding decisions. When the research team has undergrad- uate coders, Hill et al. (1997) suggest taking steps to minimize power differentials; therefore, we used a rotation system so that for each new segment, a different researcher began the discussion and shared their coding decisions. After discus- sion, we achieved consensus before assigning a final code. Our initial analysis resulted in 53 turning point codes. We used the constant comparison method (Strauss & Corbin, 1998) to condense the codes to 11 themes that we then grouped into four superordinate categories (see Table 1). As is typical in CQR, we reported the frequency of each coded theme.

Trustworthiness

We attempted to enhance the trustworthiness of the analysis throughout the study. First, there were no interview questions about the role of sport or being an “athlete.” In addition, participants were not aware that the analysis included a comparison of athletes to non-athletes. Therefore, the interviewer did not prime the athletes to discuss the influence of the sport environment. Moreover, the same non- leading follow-up probes were used for all participants. Next, we used low infer- ence coding to stay as close to participants’ words as possible. Finally, there was evidence of data saturation in both subgroups, indicating adequate sample size.

Results

All participants described multiple turning points. Broadly, all themes were classified as either an Internal or External turning point. Those categories were

Table 1 Themes to Describe Participants’ Turning Points Toward Eating Disorder Recovery

Superordinate Themes Related Sub-Themes

Internal/Autonomous Shifts Insight/Self Realization (A = 92%, NA = 82%)

Diet/Exercise Changes (A = 0%, NA = 29%)

Internal/Acknowledging Consequences

Hit a Low (A = 33%, NA = 41%)

Sport Performance (A = 50%, NA = 12%)

Medical Consequences (A = 25%, NA = 12%)

External/Direct Influences Others’ Support/Concern (A = 50%, NA = 41%)

Treatment (A = 17%, NA = 65%)

Intervention (A = 50%, NA = 24%)

ED Role Model (A = 0%, NA = 24%)

External/Indirect Influences Environment Change (A = 17%, NA = 24%)

Relationship Changes (A = 0%, NA = 12%)

Note. The percentage of participants who reported each theme is reported for athletes (A) and non- athletes (NA). The percentages for each subgroup total to over 100% because each participant’s narrative included at least two themes.

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further delineated into four superordinate themes, with 11 related sub-themes (see Table 1). The frequency that each theme was mentioned by athlete (A) and non- athlete (NA) participants is included for comparison.

Internal Turning Points: Autonomous Shifts

Nearly all participants’ narratives included the role that their own autonomous, self-determined shifts played in initiating recovery. In fact, the most frequently identified theme across all participants’ transcripts was the fact that a new Insight or Self-Realization (A = 92%, NA = 82%) about the role of the ED in their life, their sense of identity, or their priorities acted as a turning point. A non-athlete (p#11) recalled the distinct moment she committed to recovery:

I’m looking around my room and I have posters of these gorgeous women and I had tacked to my wall all of my favorite little exercise things that I had ripped out of Cosmo and I was just like, “I hate this. This isn’t fair.” : : : I just got mad at society for making women feel this way. And it was just this decision that for all of womanhood, I need to beat this : : : and I remember that I refused to let [the ED] win from that moment forward.

Three non-athletes reported that they had a realization that they would rather put their energy into causes like animal rights and veganism instead of an ED. As such, becoming a vegan helped them to adopt a new, healthier identity that they were proud of. For example:

I wanted to be a good advertisement for vegans. Because you are not going to promote veganism if you are like a sickly, tiny, little waif. You want to be healthy and strong so that people can see like, ‘Ok vegans can be healthy.’ (p#8)

Athletes also shared insights about reformed identity and a shift in their priorities that sparked recovery. A Division III runner who had restricted her food intake for a prolonged period in an effort to enhance her performance, explained that a turning point was realizing that:

I definitely didn’t want to be a person with an eating disorder : : : that’s not part of my identity : : : I started to really realize that I’m a really great person : : : There was just this moment of realizing that I’m not going to be running competitively for the rest of my life. To make choices that were, that are gonna really affect me, suddenly didn’t make sense anymore : : : I always will love running and I always will do it : : : I just realized that there’s nothing real at stake for me to be putting my whole body through it. (p #23)

The other autonomous shift for some non-athletes was making Diet or Exercise Changes (A = 0%, NA 29%). Self-determined changes like reduced calorie counting after becoming a vegan and varying one’s exercise routine to include activities other than running (e.g., weight training) served as turning points. For Participant #4, a diet change was key to starting recovery:

[After eating] milk and dairy products I would either throw up, get diarrhea, get nauseous and bloated : : : So, associated with the lactose in my diet, I was

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getting very bloated, which made me look bigger, which made me want to not eat. As soon as [I] cut lactose out : : : the bloating went down and I wasn’t having problems anymore : : :That was a turning point.

Internal Turning Points: Acknowledging Negative Consequences

For almost all participants, acknowledging the negative consequences from their ED was a crucial turning point; however, those consequences took various forms. More than a third of participants were not motivated to recover until they psy- chologically Hit a Low (A = 33%, NA = 41%). Responses in this theme included descriptions of depression, loneliness, or a sense of lost identity, which reached a point that was intolerable. A Division I tennis player (p#25) explained:

I was so, so unhappy. I just I thought a lot about running away. I thought a lot about hurting myself. I think that I realized one day that it was not going down a good path and so I told my mom. I was like, “I need to get help. I’m really scared of what I’m going to do to myself : : : .and I want to get better.” : : : bulimia was not working for me anymore.

A non-athlete similarly noted:

It was the first day of the New Year, and I remember turning to my mom and saying “I’m through with this : : : I cannot have this eating disorder anymore. It’s fucking up my life and I hate it.”And it was that point, exactly pivotal, like 360, I turned it around. (p#6)

In addition to awareness of negative psychological experiences, acknowledg- ing physical consequences also stimulated recovery. For example, reduced Sport Performance (A = 50%, NA = 12%) acted as a motivator. Two participants, who were not college athletes, said that their reduced performance in high school dance (p#1) or crew (p#21) motivated recovery, whereas half of the college athlete participants, from both the Division I (n = 5) and Division III (n = 1) levels, noted that concern about their sport performance in college was a turning point. A Division I soccer player (p#26) who had anorexia said, “I lost confidence and I played really small too.” Acknowledging that her reduced performance was due to being underweight and underfed was the critical turning point for her. She said, “It was just the harshest realization that probably saved my life : : : . I want to be strong” (p#26). A Division I distance runner (p#15) shared a comparable turning point after she was unable to compete due to AN, “I wanted to eat, to be stronger, to be able to run again.” A Division I track and field athlete similarly said:

I had no energy : : : I was always a power athlete, and I had no power. I could only do about 6 jumps in a training session, when I was used to doing over 30. And it was that moment that I just went, ‘no. I can’t do this [ED] any- more. I want to get back to where I was’ : : :That was definitely the turning point. (p#13)

A Division I basketball player described a key turning point in her recovery:

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I had a meeting with all four of my [college] coaches and we talked about my performance : : : and how disappointed they were and what a big impact I could have on the program : : : I hadn’t put two and two together that my performance had declined and my performance was directly correlated to my eating disorder. (p#20)

Finally, for some, it was negative Medical Consequences (A = 25%, NA = 12%) of the ED that acted as a tipping point. Being “cold all the time” (p#6, NA) due to weight loss and susceptibility to colds were most common. A Division I track and field athlete also shared:

I also got really sick to the point where : : : I got up to go to the bathroom and I almost passed out from dehydration and then my mom rushed me to the hospital : : : that was the main factor in me being like, ‘Ok. Maybe you should start eating more.’ (p#19)

External Factors: Direct Social Influences

Participants’ interpersonal relationships and interactions with others often included direct discussions about ED symptoms. For both subgroups, Others’ Support and Concern (A = 50%, NA = 41%) operated as a turning point. Participant #10, a non- athlete, noted that, “feeling that love and support [from my peers] is something that I don’t really feel like I got a lot of when I was younger, and I think that I really responded well to that.” Another shared her turning point:

The main thing that made me stop was my family and my friends, seeing my dad cry, seeing mymom cry : : : I loved these people too much, even if I didn’t love myself. I needed to suck it up because I couldn’t do it to them anymore. (p#16, NA).

Although all participants had attended treatment for their ED, Professional Treatment (A = 17%, NA = 65%) was only reported as a turning point for some. Non-athletes more commonly stated that they were not able to make progress toward recovery until they sought treatment or that, despite not being initially motivated or able to reduce ED behavior when they began treatment, a particular provider helped them to interrupt the ED cycle. For example, one non-athlete said, “the day I started treatment and got a plan of what to eat and became—started to become more healthy, that was the beginning of my recovery” (p#12). Another explained:

The point at which binging and purging started to not happen anymore was almost immediately after I started family therapy : : : It really amazed me, because it’s just talking. Talking to my mom candidly about emotions fixed things almost immediately. (p#18)

Although some participants sought treatment or began recovery on their own, others reported that a confrontation or Intervention (A = 50%, NA = 24%) from family, friends, or a coach was key to stimulating recovery. Interventions operated as either a wake-up call about the severity of their ED behavior or the intervention included an ultimatum, such as not being allowed to compete, which motivated

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participants to start treatment or recover. Several athletes were particularly influenced by interventions from their college coaches. One shared, “My coach just literally sat me down one day and he said, “Do you want to be back where you were [with elite sport performance]?” And I said, “yes.” And he said, “You won’t be unless you start eating” (p#13, Div. I, track and field). A Division I rower had not made any attempt to recover until:

[My coach] called me out on it, and we had multiple talks and he pointed out, “you’re losing weight. Your scores are going down. You take things too seriously. Maybe you need to see a therapist.” : : : all of this made me question what I was doing. (p# 28)

A final direct social influence was guidance, support, and a sense of universality provided byEDRecovered RoleModels (A = 0%,NA = 24%), whowerementioned only by non-athletes. Participant #2 said, “I started talking to my cousin : : : I had someone that was almost like a sister telling me that she had the same problem and I listened.” Joining Overeaters Anonymous was a turning point for Participant #5, who said it “changed my life : : : . It was never as bad because : : : I was able to be around other people that talked about food in the ways that I behaved.”

External Factors: Indirect Influences

A final superordinate theme was used for external events that indirectly became turning points. Some participants’ recovery was, in part, spurred by Environmental Changes (A = 17%, NA = 24%), such as moving out of their parents’ house or having a shared bathroom in college. For example, a Division I tennis player said that recovery began when, “I moved out of my house : : : I definitely could not get better in that environment” (p#25). A non-athlete who recovered from bulimia stated, “I didn’t really feel comfortable purging in [the suite bathroom] because someone might walk in” (p#21). Finally, for two non-athletes, romantic Relation- ship Changes (A = 0%, NA = 12%) stimulated recovery. Although their romantic partner did not directly discuss the ED, the relationship still offered a turning point. A non-athlete shared, “I started dating somebody and I wanted to be healthy enough to be in a relationship” (#14).

Subgroup Comparison of Turning Points

There were some commonalities in the subgroups’ themes. Both groups most commonly cited Insight/Self-Realization (A = 92%, NA = 82%) as a turning point and reported a relatively similar frequency of Others’ Support/Concern (A = 50%, NA = 41%) as well as Hitting a Low (A = 33%, NA = 41%). There were also several sub-group differences. Athletes were more than four times as likely to report that they initiated recovery because of desire to improve Sport Performance (A = 50%, NA = 12%) and twice as likely to cite an Intervention (A = 50%, NA = 24%) as a turning point. For non-athletes, it was much more common that Professional Treatment (A = 17%, NA = 65%) ignited recovery. In addition, there were three themes that were only present in non-athletes’ narratives, including: Diet/Exercise Changes (A = 0%, NA = 29%), EDRole Models (A = 0%, NA = 24%), and Relationship Changes (A = 0%, NA = 12%).

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Discussion

This study compared athletes’ and non-athletes’ turning points in the ED recovery journey. For clinicians who work with clients who are not motivated to recover or are not yet able to reduce ED behaviors, knowledge of turning points and what motivates change is critical in order to facilitate early recovery, especially given that longer duration of symptoms is related to worse long-term outcomes (Fichter, Quadflieg, & Hedlund, 2006; Reas, Williamson, Martin, & Zucker, 2000). The results of this study are novel in two ways. First, the findings shed light on young women’s experiences with turning points, as most studies have been conducted on older samples. Second, this is the first study to offer an in-depth analysis of athletes’ turning points in recovery.

In the overall sample, qualitative analysis of participants’ narratives yielded many similar themes to past non-athlete research, which has identified internal turning points like experiencing negative consequences from the ED (D’Abundo& Chally, 2004; Fogarty & Ramjan, 2017; Lamoureux & Bottorff, 2005; Lindgren et al., 2015; Moulding, 2016; Nilsson & Hägglöf, 2006; Pettersen & Rosenvinge, 2002; Redenbach & Lawler, 2003), hitting a low (Lindgren et al., 2015) as well as new insight or self-realizations, particularly about one’s identity or priorities (Dawson et al., 2014; Hay & Cho, 2013; Lindgren et al., 2015; Matusek & Knudson, 2009; Moulding, 2016; Nilsson &Hägglöf, 2006; Redenbach & Lawler, 2003). An external turning point from past studies that also appeared in the current results was the role of support or connection to others (D’Abundo & Chally, 2004; Dawson et al., 2014; Hay & Cho, 2013; Lindgren et al., 2015; Linville et al., 2012; Matusek & Knudson, 2009; Moulding, 2016). Some non-athletes in the current study also described shifting their identity to someone who spends their energy on animal rights and veganism, rather than an ED, which was similar to the identity changes described by Matusek and Knudson’s (2009) participants. However, contrary to past reports, participants in our study did not describe external turning points related to religion and spirituality (D’Abundo & Chally, 2004; Matusek & Knudson, 2009) or life events like the death of a friend (Nilsson & Hägglöf, 2006). It is possible that some of these differences are explained by the fact that many participants in previous studies were in their forties and fifties and therefore may have had quite different life experiences than our college-aged participants. Overall, our results align with past research on non-athletes in that turning points were not exclusively internal or external in nature; rather, several internal and external factors coalesced to tip the balance toward recovery.

Findings from the current study appear to be quite similar to results of the only other published studies that have referenced athletes’ turning points. Like Arthur- Cameselle and Quatromoni’s (2014a) participants, athletes in the current study reported that negative consequences of the ED, interventions, or a change in thinking were key turning points. Such similarities in findings indicate that these experiences for female athletes are somewhat consistent. However, the current study provided a more comprehensive analysis. For example, though Arthur- Cameselle and Quatromoni (2014a) indicated that negative consequences acted as a turning point, the current investigation further clarified that for athletes, reduced Sport Performance was the most common negative consequence (50%), as compared to Hitting a Low (33%) psychologically or general Medical

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Consequences (25%). In addition, perhaps because of more in-depth questioning, athletes in the current study were more likely to discuss key Self-Realizations (92%) that sparked recovery. Reprioritization of values, namely reclaiming their role as a strong and capable athlete, appeared critical for many athletes in this study to successfully begin recovery. Female athletes with disordered eating in past studies have similarly described internal conflict over the discrepancy between their disordered self and their athletic self (Papathomas & Lavallee, 2010). For half of the current athletes, acknowledging such discrepancy led to reclaiming their athletic identity through recovery. Reduced sport performance as a result of ED related behavior or weight loss appears to be a sport-specific form of loss, which supports Fogarty and Ramjan’s (2017) claim that personal loss may operate as a crucial turning point. In contrast to our finding on the importance of sport in sparking recovery, the male athlete in Papathomas and Lavallee’s (2006) case study indicated that leaving sport due to injury helped him to begin recovery, as he was better able to manage stress without the added pressures of sport. Given these differing reports, further investigations are needed to understand the role of athletic identity in ED recovery.

This study offers something novel to the literature on turning points in that our methodology allowed for a direct comparison of collegiate athletes’ and non- athlete college students’ experiences. Past research on athletes’ experiences with the onset of clinical EDs (Arthur-Cameselle et al., 2017) and recovery (Arthur- Cameselle & Quatromoni, 2014a, 2014b) have suggested that athletes may be a unique ED subgroup. The current study’s results align with such claims in that key subgroup differences emerged in athletes and non-athletes’ turning points. For example, after Insight/Self-Realization, non-athletes’ most frequent turning point was Treatment (65%) whereas athletes reported Sport Performance (50%), and Intervention (50%). Both of these factors, which were reported by athletes at both the Division I and III levels, included sport-specific elements. For example, all but one of the athletes’ Interventions was initiated by a coach. In addition, reflections about the key influence of caring coaches were also included under the Support/ Concern theme. These findings align with past research on the helpful role coaches can play related to athletes’ EDs (Sherman, Dehass, Thompson, & Wilfert, 2005). Unfortunately, non-athlete college students may not have someone who is in a similar position to intervene. It is important to note that the athletes were not prompted to discuss sport or being an athlete and were unaware of the study’s non- athlete comparison group, yet their narratives still contained a high frequency of sport-related themes; this suggests that athletes’ turning points meaningfully differ from non-athletes.

Given that all participants had attended treatment as per inclusion criteria, it is noteworthy that non-athletes (65%) were far more likely to have a turning point as a result of Treatment than athletes (17%). Similarly, ED Role Models were not influential for athletes (0%), yet 24% of non-athletes mentioned them. Perhaps these differences can be explained by findings from a recent study in which athletes reported that ED treatment programs were ineffective because their needs were different from their non-athlete peers and the staff did not address sport-specific ED triggers (Plateau et al., 2017). Based on this finding, in combination with our results, athlete-specific ED treatment may be most effective, particularly for group modalities.

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Moreover, the current results indicate that, because EDs threaten something that athletes highly value (i.e., sport performance), athletes may have intrinsic motivation for recovery and experience turning points prior to entering treatment, compared to non-athlete peers who were much more likely to report that they had a turning point while engaging in treatment. Although non-athletes in previous studies have mentioned that academic or work consequences from EDs were turning points (e.g., Lindgren et al., 2015), such effects were only reported by one non-athlete in the current study, who noted that feeling lightheaded from her AN made it hard to focus in class. Since shifts in identity appear key as turning points (Matusek & Knudson, 2009; Moulding, 2016), athletes may have an easier time transitioning their focus away from the ED, because they can shift back to the identity of being an “athlete” when they begin recovery.

Limitations

Though this study contributes to the small body of work on athletes’ recovery from EDs, several limitations were evident. First, we used convenience sampling, which could make our results vulnerable to volunteer bias. Also, there was an uneven sample size between the two subgroups. However, there was evidence of data saturation in both groups, thus indicating that the sample size was adequate. The smaller athlete sample is explained by the fact that the inclusion criteria were stringent; athlete participants had to be a varsity level collegiate athlete who had experienced a clinical ED, engaged in professional treatment, and had achieved a period of recovery. Based on the specificity of these criteria, the sample size of 12 can actually be viewed as a strength. In addition, our overall sample of 29 was also larger than many past studies on tipping points in non-athletes and we had a higher degree of homogeneity in participant experiences (particularly in age) than many past studies. However, the various ED diagnoses in our sample is an area of het- erogeneity that is a limitation. Although several previous studies on tipping points have used mixed ED samples (D’Abundo & Chally, 2004; Linville et al., 2012; Matusek & Knudson, 2009; Moulding, 2016; Pettersen & Rosenvinge, 2002), it would be preferable to focus on one disorder. We chose not to analyze the data broken down by ED diagnosis because eight participants (27.6% of the sample) had met criteria for two different eating disorders. Past studies indicate that people with AN often later meet criteria for BN (Keel & Brown, 2010), as has been the case in samples from previous studies on turning points (Moulding, 2016; Redenbach & Lawler, 2003). Finally, although all participants were in a period of recovery during their interviews, it is unknown if they will maintain long-term recovery.

Clinical Implications

The results of this study offer insight for practitioners who treat athletes with EDs. First, the current findings support past claims that athletes are a unique ED population (Arthur-Cameselle et al., 2017) in that their turning point patterns were in many ways distinct from the non-athlete comparison group. Next, it was evident that in order to turn the corner and actively pursue recovery, participants had to hit a threshold of internal frustration over the consequences of their ED while simultaneously having a supportive external environment. Specifically,

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internal motivation to recapture physical health and reclaim a more stable identity was nearly universal. For those who have not yet had a turning point, the results of this study indicate that Motivational Interviewing techniques (Miller & Rollnick, 1991) may be useful to help athletes to articulate the way that their ED affects their performance, which was a key motivator for our athlete participants. Indeed, past research indicates that motivation for change is predictive of ED treatment success (e.g., Clausen et al., 2013), thus raising motivation is critical. For clinicians and researchers who want to formally assess clients’ readiness for recovery, a recent study found that participants’ scores on the Eating Disorder Readiness Ruler (ED-RR), which assesses readiness for change, predicted decreases in ED symp- toms over time in treatment (St-Hilaire, Axelrod, Geller, Azanek-Antunes, & Steiger, 2017). A tool like the ED-RR, which appears to be appropriate for clients with AN or BN (St-Hilaire et al., 2017), could help clinicians to determine when to focus primarily on building motivation for change and when there may be suf- ficient client readiness to begin strategies to reduce maladaptive eating and exercise behaviors.

The results of this study indicate that athletes in need of treatment should be referred to a provider who is knowledgeable of the sport environment or to an athlete-specific ED group or inpatient treatment center (for those who require intensive care), given that sport performance was so often a turning point for recovery. This recommendation is supported by past evidence that participation in competitive sport is connected to the onset of EDs (Arthur-Cameselle et al., 2017; Sundgot-Borgen, 1994) and that athletes have been dissatisfied with treatment that does not acknowledge their athlete identity (Plateau et al., 2017). As such, athletes may benefit fromAcceptance and Commitment Therapy (ACT; Hayes, Strosahl, & Wilson, 1999), which encourages clients to identify personal values and refocus energy toward achieving goals that are in their control. This recommendation is supported by studies that have shown that ACT had slightly more positive effects than treatment as usual in a residential ED program (Juarascio et al., 2013a) and was more effective than standard cognitive behavioral therapy (CBT) in a ran- domized control trial (Juarascio, Forman, & Herbert, 2010). Researchers noted that ACT might be particularly effective for EDs, compared to CBT, because it more directly addresses motivational issues (Juarascio et al., 2010). Juarascio et al. (2013b) published group session outlines, which may be of use to practitioners who want to incorporate ACT into treatment. However, it should be noted that there are not yet studies on ACT in athlete samples.

Additionally, the results of this study highlight the critical role coaches can play in supporting athletes with EDs. As such, athletic departments should provide more training on the signs of EDs, particularly since past educational programs have effectively increased coaches’ knowledge on the topic (e.g., Martinsen, Sherman, Thompson, & Sundgot-Borgen, 2015). Clinical providers are encour- aged to build relationships with coaches and should offer resources to help coaches better understand EDs. For example, Selby and Reel’s (2011) guide for coaches offers ideas of how to interact with an athlete with a suspected ED, including the suggestion to avoid using the term “eating disorder”with them and to instead focus on concerns like the athlete not having “as much energy” as they used to (p. 107). The results of the current study certainly support this suggestion. Specifically, participants responded positively when coaches brought reduced performance to

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their attention. Notably, none of the athletes mentioned that their low body weight or appearance motivated their recovery. Thus, coaches’ comments about appear- ance or weight loss may be less effective than performance focused comments.

Conclusions and Future Directions

This is the first study to explore athletes’ turning points in ED recovery in com- parison to a non-athlete sample. The presence of sport-specific turning points, including sport performance and coach interventions, provides credence to past claims that athletes have unique ED recovery experiences (Arthur-Cameselle & Quatromoni, 2014a). Overall, the results suggest that although many internal, autonomous shifts help to tip the balance toward recovery, relationships are also critical. Thus, treatment providers and coaches can help athletes turn the corner to recovery.

Several important questions about athletes’ ED recovery remain. First, it would be useful to conduct studies that focus either on athletes with one ED diagnosis or competitors from one category of sport, such as weight-sensitive sports, to determine if differences emerge based on these demographic groups. Additionally, the extant literature includes relatively few studies on male athletes’ ED experiences. Knowledge of turning points could also be expanded by tracking athletes over time to determine if particular turning points, for example internal/ self-determined as compared to external/relationship, are associated with sustained recovery or are instead associated with relapse. In addition, since athlete parti- cipants in this study were motivated to recover because of reduced sport perfor- mance, it is important to determine how ED recovery is affected after retirement from sport. Retired collegiate swimmers with disordered eating reported that it took them a substantial amount of time to adjust to new caloric needs after their sport career was over (Cooper & Winter, 2017) and an elite female basketball player reported that her disordered eating worsened after leaving sport (Papathomas & Lavallee, 2014). Female athletes who recover from clinical level EDs may face similar challenges in retirement, but their experiences have not yet been explored. Finally, it would be of utility to interview coaches who have confronted athletes with EDs to better understand what leads to a successful intervention, as coaches are in a key position to help athletes with EDs tip the balance toward recovery.

Acknowledgments

We would like to acknowledge the work of Michael Alcaraz for his role as a member of the data coding team for this study.

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Diet Pill and Laxative Use for Weight Control and Subsequent Incident Eating Disorder in US Young Women: 2001–2016

Jordan A. Levinson, BA, Vishnudas Sarda, MBBS, MPH, Kendrin Sonneville, RD, ScD, Jerel P. Calzo, PhD, MPH, Suman Ambwani, PhD, and S. Bryn Austin, ScD

Objectives. To investigate the prospective association of diet pill and laxative use for

weight control with subsequent first eating disorder diagnosis in young women.

Methods.We used longitudinal data from 10058 US women spanning 2001 through

2016. We used multivariable logistic regression models, adjusting for age, race/

ethnicity, and overweight status to estimate the association between weight-control

behaviors and subsequent eating disorder diagnosis.

Results. Among those who had not previously received an eating disorder diagnosis,

women who reported diet pill (adjusted odds ratio [AOR] = 5.6; 95% confidence interval

[CI] = 3.0, 10.5) or laxative (AOR=6.0; 95% CI = 4.2, 8.7) use for weight control had higher

odds of receiving a subsequent first eating disorder diagnosis within 1 to 3 years than

those who did not report using these products.

Conclusions.Useof diet pills or laxatives forweight loss canbedangerous andmaybe a

warning sign that warrants counseling and evaluation for the presence of or risk of

developing an eating disorder.

Public Health Implications. Policymakers and public health professionals should

develop and evaluate policy initiatives to reduce or prohibit access to diet pills and

laxatives abused for weight control. (Am J Public Health. 2020;110:109–111. doi:

10.2105/AJPH.2019.305390)

Research shows that unhealthy weight- control behaviors, including use of diet

pills and laxatives for weight control, can put individuals at risk for the development of eating disorders.1 Use of over-the-counter diet pills or laxatives is not recommended by health care providers as a healthy way to manage weight and can have severe health consequences.2 Despite these risks, use of these products for weight control persists in people of all genders, ages, races/ethnicities, and socioeconomic statuses.3,4 An estimated 15%3 of adults report lifetime use of diet pills for weight control. Lifetime use of laxatives for weight control among adults is estimated at 5%5 and from 15%5 to 62% in those with eating disorders.2

Although use of diet pills and laxatives for weight control is common in people with eating disorders,2,6 the prospective association of use of these products and subsequent

diagnosis with an eating disorder is not known. Use of these products could indicate an incipient eating disorder or the presence of a full, yet undiagnosed eating disorder. Alternatively, a causal relationship may exist, as using diet pills and laxatives for weight control could serve as a “gateway” behavior to escalating weight-control practices,7 dysregulate normal digestive functioning leading to more disordered eating,8 and exacerbate emotion dysregu- lation through dependence on unhealthy

and ineffective coping (i.e., diet pill and laxative use).9

We examined whether use of these products for weight control predicts sub- sequent clinical diagnosis with an eating disorder among young women who have not previously received an eating disorder di- agnosis. We hypothesized that those who reported past-year use of diet pills or laxatives for weight control would be more likely than would those who did not to receive a first diagnosis of an eating disorder on the next wave of data collection (1–3 years later).

METHODS We examined diet pill use, laxative use for

weight control, and eating disorder diagnosis using longitudinal data fromyoungwomen in the US-based Growing Up Today Study (GUTS), which enrolled children, aged 9 to 15 years in 2 stages: GUTS1 baseline in 1996 (n = 16 882) and GUTS2 baseline in 2004 (n = 10 442). Our analysis included GUTS1 and GUTS2 participants who provided data both on past-year use of these products and eating disorder diagnosis from 2001 to 2016. Participants were asked about their use of diet pills (In the past year, did you use diet pills to lose weight or to keep from gaining weight?) and laxatives (In the past year, did you take laxatives to lose weight or keep from gaining

ABOUT THE AUTHORS Jordan A. Levinson, Vishnudas Sarda, and S. Bryn Austin are with the Division of Adolescent and Young Adult Medicine, Boston Children’s Hospital, Boston, MA. Kendrin Sonneville is with the Department of Nutritional Sciences, School of Public Health, University of Michigan, Ann Arbor. Jerel P. Calzo is with the Division of Health Promotion and Behavioral Science, School of Public Health, SanDiego StateUniversity, SanDiego, CA. SumanAmbwani is with theDepartment of Psychology, Dickinson College, Carlisle, PA.

Correspondence should be sent to Jordan A. Levinson, BA, 11000 Weyburn Dr. #821, Los Angeles, CA 90024 (e-mail: [email protected]). Reprints can be ordered at http://www.ajph.org by clicking the “Reprints” link.

This article was accepted September 13, 2019. doi: 10.2105/AJPH.2019.305390

January 2020, Vol 110, No. 1 AJPH Levinson et al. Peer Reviewed Research 109

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mailto:[email protected]

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weight?) for weight control (coded as binary: “yes” if any past-year use; “no” if no past-year use). Surveys were administered annually or sometimes biennially.

We assessed eating disorder diagnosis on 10 waves. Four waves of surveys assessed diet pill use and 10waves assessed laxative use. To assess eating disorder diagnosis, partici- pants were asked if a doctor, nurse, or other health care provider had ever told them they had an eating disorder, such as anorexia nervosa or bulimia nervosa (coded as binary: yes/no). We excluded respondents if they reported being told they had an eating dis- order before or on the same wave that they first reported diet pill or laxative use, and we also excluded them from subsequent analysis once they reported being told they have an eating disorder.

We conducted multivariable logistic re- gression modeling with 7564 responses from 6977 participants for diet pill use and 40 305 responses from 10 058 participants for laxative use to estimate the prospective association of past-year diet pill or laxative use for weight control with subsequent first report of an eating disorder diagnosis by a health care provider in the next wave of data collection, which could occur 1 to 3 years after the wave reporting product use. We did not consider first report of eating disorder diagnosis that occurred more than 1 consecutive wave from reported diet pill or laxative use as associated with product use. Models controlled for age, race/ethnicity, and overweight status at the time of response to the eating disorder di- agnosis item, and generalized estimating equations accounted for repeated measures and sibling clusters. We conducted the sta- tistical analyses using SAS version 9.2 (SAS Institute, Cary, NC).

RESULTS We conducted analyses with data from

10 058 women, ranging from 14 to 36 years old, over the observation period from 2001 to 2016. Among 7564 responses included in diet pill analyses, 1.8% of these reporting diet pill use in the past year, compared with 1.0% of those not reporting diet pill use in the past year, subsequently reported a first eating disorder diagnosis from a health care provider in the next wave of data collection. Those

who used diet pills had more than 5 times higher adjusted odds (adjusted odds ratio [AOR]=5.6; 95% confidence interval [CI]= 3.0, 10.5) of receiving an eating disorder diagnosis from a health care provider within 1 to 3 years than those who did not. Among 40 305 responses included in the laxative use analyses, 4.2% of those reporting laxative use for weight control in the past year, compared with 0.8% of those not reporting past-year laxative use for weight control, subsequently reported an eating disorder di- agnosis from a health care provider in the next survey wave of data collection. The appen- dix contains more information (available as a supplement to the online version of this article at http://www.ajph.org). Those who re- ported laxative use for weight control had 6 times higher adjusted odds (AOR=6.0; 95% CI= 4.2, 8.7) of receiving an eating disorder diagnosis from a health care pro- vider within 1 to 3 years than those who did not (Table 1).

DISCUSSION Use of diet pills and laxatives for weight

management can have deleterious effects.2 In addition to the known risks associated with use of these products for weight control, we found that use of these products can precede first eating disorder diagnosis. Although the prospective association between unhealthy

weight-control behaviors and eating disorder symptoms has been previously docu- mented,1,2 to our knowledge, this study is the first to estimate the prospective association of use of diet pills or laxatives for weight control and subsequent first diagnosis with an eating disorder. It is plausible that use of these productsmay increase the likelihood of eating disorder onset by contributing to behavioral dysregulation of eating,7 physiological dys- regulation of digestion,8 or psychological dysregulation.9

Our study has several limitations. Many people with eating disorders are never di- agnosed by a health care provider, leading to many missed cases of eating disorders. Re- latedly, we controlled for race/ethnicity and overweight status because of well- documented diagnostic bias leading to underdetection of eating disorders in people of color and those at higher weights,10

but residual confounding may still have af- fected our results. Future research should investigate possible pathways through which diet pill and laxative use might potentiate vulnerability to eating disorders. In addition, family members, clinicians, coaches, and others who work with young people should be aware that any use of diet pills or laxatives for weight control can be dangerous.2 Re- peated use of these products is a warning sign that warrants counseling and evaluation for the presence or risk of developing an eating disorder.

TABLE 1—Prospective AdjustedOdds Ratios (AORs) and 95%Confidence Intervals (95%CIs) of Adolescent and Young Adult Women Receiving a New Eating Disorder Diagnosis From a Health Care Provider 1–3 Years After Reporting Diet Pill or Laxative Use for Weight Control: Growing Up Today Study Cohort, United States, 2001–2016

Incident Eating Disorder Diagnosis Total Responsesa Responses Reporting Eating Disorder Diagnosis,a No. (%) AORb (95% CI)

Diet pill model

Diet pill use, noc 6 469 63 (1.0) 1 (Ref)

Diet pill use, yesc 1 095 20 (1.8) 5.58 (2.97, 10.49)

Laxative model

Laxative use, nod 39 289 293 (0.8) 1 (Ref)

Laxative use, yesd 1 016 43 (4.2) 6.03 (4.18, 8.69)

Note. Study size was n = 10058 participants. aRepeated measures responses from participants in prospective cohort over multiple survey waves. bMultivariable models control for age, race/ethnicity, and overweight status. Models estimate odds of new eating disorder diagnosis associated with report of diet pill or laxative use for weight control on previous survey wave. cData on diet pill use collected in 4 waves of the survey. dData on laxative use collected in 10 waves of the survey.

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PUBLIC HEALTH IMPLICATIONS Results of this study suggest that use of diet

pills and laxatives for weight control is pre- dictive of later diagnosis of an eating disorder. Given the myriad health risks of these products well documented in the literature,2

combined with our evidence that their use may be prospectively associated with eating disorder diagnosis, public health professionals, policymakers, and community advocates should pursue remedies to reduce access to and use of these products, such as a tax11 on these products as well as legislation to ban the sale of diet pills to minors.12

CONTRIBUTORS J. A. Levinson prepared the article. V. Sarda performed analyses. K. Sonneville, J. P. Calzo, and S. Ambwani conceptualized the study and prepared the article. S. B. Austin conceptualized the study, created the database, performed analyses, and prepared the article. All authors interpreted results.

ACKNOWLEDGMENTS S. B. Austin is supported by the Ellen Feldberg Gordon Fund for Eating Disorders Research and theMaternal and Child Health Bureau, Health Resources and Services Administration, US Department of Health and Human Services (training grants T71-MC-00009 and T76-MC- 00001). S. Ambwani is supported by a Faculty Sabbatical Grant from the Research and Development Committee, Dickinson College.

CONFLICTS OF INTEREST The authors have no conflicts of interest.

HUMAN PARTICIPANT PROTECTION This study was approved by the Brigham and Women’s Hospital human subjects committee.

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2. Roerig JL, Steffen KJ, Mitchell JE, Zunker C. Laxative abuse: epidemiology, diagnosis and management. Drugs. 2010;70(12):1487–1503.

3. Blanck HM, Serdula MK, Gillespie C, et al. Use of nonprescription dietary supplements for weight loss is common among Americans. J Am Diet Assoc. 2007; 107(3):441–447.

4. Neumark-Sztainer D, Croll J, Story M, Hannan PJ, French SA, Perry C. Ethnic/racial differences in weight-related concerns and behaviors among adolescent girls and boys: findings from Project EAT. J Psychosom Res. 2002;53(5):963–974.

5. Neims DM,McNeill J, Giles TR, Todd F. Incidence of laxative abuse in community and bulimic populations: a descriptive review. Int J Eat Disord. 1995;17(3):211–228.

6. Steffen KJ, Mitchell JE, le Grange D, et al. A preva- lence study and description of alli use by patients with eating disorders. Int J Eat Disord. 2010;43(5):472–479.

7. Neumark-Sztainer D, Wall MM, Eisenberg ME, Story M.Obesity and eating disorders in older adolescents: does early dieting make things better or worse? J Adolesc Health. 2005;36(2):152–153.

8. Mitchell JE, Boutacoff LI. Laxative abuse complicating bulimia: medical and treatment implications. Int J Eat Disord. 1986;5(2):325–334.

9.Wonderlich SA, Lavender JM. Emotion regulation and eating disorders. In: Brownell KD, Walsh BT, eds. Eating Disorders and Obesity: A Comprehensive Handbook. New York, NY: Guilford Press; 2017:260–264.

10. Sonneville KR, Lipson SK. Disparities in eating disorder diagnosis and treatment according to weight status, race/ethnicity, socioeconomic background, and sex among college students. Int J Eat Disord. 2018;51(6): 518–526.

11. Austin SB, Liu SH, Tefft N. Could a tax on unhealthy products sold for weight loss reduce consumer use? A novel estimation of potential taxation effects. Prev Med. 2018;114:39–46.

12. Pomeranz JL, Taylor LM, Austin SB. Over-the- counter and out-of-control: legal strategies to protect youths from abusing products for weight control. Am J Public Health. 2013;103(2):220–225.

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