Physical activity recommendations for adolescents with anorexia nervosa: An existing protocol based on physical activity risk

Mental Health and Physical Activity 7 (2014) 163e170

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Physical activity recommendations for adolescents with anorexia nervosa: An existing protocol based on physical activity risk Lisa Scott a, *, Sherry Van Blyderveen a, b, 1 a b

McMaster Children's Hospital, 1200 Main St W, Hamilton, ON, Canada L8N 3Z5 Department of Pediatrics, McMaster University, Hamilton, ON, Canada

a r t i c l e i n f o

a b s t r a c t

Article history: Received 31 March 2014 Received in revised form 2 September 2014 Accepted 2 September 2014 Available online 17 September 2014

Aim: There is a critical gap between the literature pertaining to physical activity (PA) in eating disorders and directives regarding the management of PA. There is evidence that managed PA in eating disorders is beneficial, as long as it accounts for compulsive exercise. The goal of this paper is to encourage future research to test the efficacy and safety of the existing protocol, leading to the development of clinical practice guidelines to optimize care. Method: A protocol developed for the purpose of individual prescription of PA for adolescents receiving inpatient treatment for AN is described. The protocol uses primary complications related to PA and AN to categorize an adolescents level of PA risk as high, moderate or low. The risk factors assessed include; vital sign instability, percentage of Ideal Body Weight and an evaluation of compulsive exercise. PA recommendations are implemented according to the level of PA risk. Two case studies are presented to illustrate the application of the protocol. Discussion: Critical limitations of the research to date regarding managed PA in eating disorders are numerous and a model of compulsive exercise has only recently been proposed, thus restricting the evaluation of existing research. The applicability of the protocol may be limited within Family Based Treatment in outpatient care, where the management of PA is the responsibility of the parents. Conclusion: Categorization of PA risk is assessed by the eating disorders team. A physical therapist should be considered for the implementation and management of the proposed PA recommendations according to the level of PA risk. © 2014 Elsevier Ltd. All rights reserved.

Keywords: Eating disorders Anorexia Recommendations Compulsive exercise Exercise guidelines Risk factors

1. Introduction Despite the fact that physical activity (PA) has historically been discouraged among patients receiving treatment for anorexia nervosa (AN), recent literature reviews suggest that the use of managed PA for patients with AN does not compromise weight gain, is not associated with eating pathology, and in fact is associated with positive physical and mental health outcomes (Moola, Gairdner, & Amara, 2013; Ng, Ng, & Wong, 2013). Whether or not managed PA, defined as the implementation and monitoring of PA recommendations, is permitted during inpatient treatment, and the amount of PA recommended, is frequently determined solely by

* Corresponding author. E-mail addresses: [email protected] (L. Scott), [email protected] (S. Van Blyderveen). 1 Present address; New Leaf Psychology Centre, Milton, ON 400 Main Street East, Suite 210, Milton, ON Canada L9T 4X5. http://dx.doi.org/10.1016/j.mhpa.2014.09.001 1755-2966/© 2014 Elsevier Ltd. All rights reserved.

weight criteria, with wide variability between pediatric treatment centers (Davies, Parekh, Etelapaa, Wood, & Jaffa, 2008). Although no clinical practice guidelines exist to direct the management of PA for patients with AN, the need for such guidelines with this population is highlighted in the literature (Bratland-Sanda et al., 2010a; Hausenblas, Cook, & Chittester, 2008; Hechler, Beumont, Marks, & Touyz, 2005; McCallum et al., 2006; Meyer, Taranis, & Touyz, 2008; Moola et al., 2013; Vancampfort et al., 2014; Zunker, Mitchell, & Wonderlich, 2011). There is a critical gap between the literature pertaining to PA in eating disorders and directives regarding the management of PA for patients with AN. The following existing protocol was developed for the purpose of individual prescription of PA for adolescents receiving inpatient treatment for AN in an acute care setting. It includes an assessment of PA risk and application of PA recommendations according to the determined level of PA risk. To the authors' knowledge, we are the first Canadian pediatric eating disorders centre to utilize a PA management tool for adolescents

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with AN. The objective of this publication is to generate research to test the efficacy and safety of the proposed PA risk categories and PA recommendations for adolescents with AN, with the hopes that such research will create the foundation for the future development of clinical practice guidelines. 1.1. Background AN is an eating disorder characterized by excessive dieting that results in low weight, a pathological fear of weight gain or becoming fat, and either distorted body image, a self-concept heavily influenced by weight and shape, or denial of the seriousness of low weight (American Psychiatric Association, 2013). AN can be further categorized into two subtypes, one that is characterized by dietary restriction and the second which is characterized by episodes of binge eating and/or purging (American Psychiatric Association, 2013). Given that the literature pertaining to the physical complications of AN often do not differentiate between the two subtypes of AN (Katzman, 2005; Yager et al., 2006), the existing protocol described in this paper can be applied to both AN subtypes, recognizing however that the AN- binge eating/purging subtype is understudied. Given the significant lack of evidence also related to PA and bulimia nervosa, this protocol was not designed for patients with bulimia nervosa. The onset of AN occurs most commonly in adolescence (Fairburn & Harrison, 2003; Favaro, Caregaro, Tenconi, Bosello, & Santonastaso, 2009), with a unique manifestation compared to adults. Adolescents may not necessarily present with weight loss, and may instead present with impaired linear growth (Katzman, 2005; Root & Powers, 1983; Workgroup for Classification of Eating Disorders in Children and Adolescents, 2007). Puberty may be delayed or interrupted (Steiner & Lock, 1998). Also, children and adolescents present with developmental differences in neurocognitive abilities compared to adults, thus impacting the emotional experience of eating disorders in adolescents compared to adults. For example, children and adolescents, describe and appreciate the meaning of their eating disorder behaviors and thoughts differently than adults (Workgroup for Classification of Eating Disorders in Children and Adolescents, 2007). The model of treatment recommended by the American Psychiatric Association (Yager et al., 2006) for youth with AN is Family Based Treatment for an Eating Disorder (FBT) (Lock & Le Grange, 2013). FBT is a form of outpatient treatment unique to youth where, during the initial phase, parents are empowered to take responsibility for changing the behaviors that maintain low weight, including diet and PA (Lock & Le Grange, 2013). Although in two randomized control trials, FBT has not been shown to be superior to individual treatment in regards to remission rates at discharge, FBT has been associated with more rapid recovery (Robin et al., 1999) and higher remission rates at 6 and 12 month follow-up among youth with AN (Lock et al., 2010). The nature of family involvement in FBT is unlike management of adult patients with AN, where treatment is typically directed at the individual. It is also of note that, with adolescents, their parents are the legal decision makers in their medical care. In order to be consistent with the FBT model, and the nature of treatment in adolescents, it is important to involve parents in the decision making process regarding PA for their child as they will be managing their child's PA once discharged from hospital. 1.2. Risks of unmanaged physical activity in anorexia nervosa Clinicians have traditionally had a negative view of exercise in eating disorders. Bed rest was the preferred management of PA during inpatient treatment, as exercise was conceptualized as a

symptom of the eating disorder (a strategy to manage weight) requiring intervention (Brumberg, 1988; Fairburn & Harrison, 2003; Shroff et al., 2006). Studies in support of this approach have found that young eating disorder patients who engaged in PA more frequently, for a longer duration and/or with greater intensity, had worse outcomes, such as longer inpatient treatment (Solenberger, 2001) and higher rates of relapse (Strober, Freeman, & Morrell, 1997), especially if they engaged in such PA within the first 3 months after discharge (Carter, Blackmore, Sutandar-Pinnock, & Woodside, 2004). Studies have also shown higher levels of PA to be associated with higher levels of eating disorder pathology (Solenberger, 2001) and greater drive for thinness among young adult eating disorder patients (Vansteelandt, Rijmen, Pieters, Probst, & Vanderlinden, 2007). 1.2.1. Compulsive exercise Exercise among those with eating disorders has historically been understood as a strategy to manage weight (Fairburn & Harrison, 2003; Shroff et al., 2006). However, a recent review of the literature has shown that exercise within the context of eating disorders is predicted by more than weight management goals (Meyer, Taranis, Goodwin, & Haycraft, 2011). Specifically, eating psychopathology, obsessive compulsiveness, affect regulation and perfectionism have each been correlated with exercise that is considered compulsive, and a model as to how these factors interact with one another to maintain compulsive exercise behaviors has been proposed (Meyer et al., 2011). Thus, compulsive exercise refers to exercise within the context of weight and/or shape concerns, which is both rigid and compulsive in nature, and has the goal of reducing feelings of guilt or other negative affect (Meyer et al., 2011). It is possible that the findings of earlier studies associated worse outcomes with PA that was frequent, of high intensity and/or long duration, were in fact as result of the PA being unmanaged and not due to such PA being compulsive in nature. It has been similarly argued that the duration and frequency of PA is less indicative of eating disorder pathology than the quality of such PA (Meyer & Taranis, 2011). It is this compulsive exercise that has been reported to be present in 44% (Shroff et al., 2006) to 78% (Davis, Kennedy, Ravelski, 1994) of patients with AN. Although compulsive exercise is a worrisome component of eating disorders psychopathology, deserving of significant consideration when recommending PA, it is possible that PA that is managed and not compulsive in nature could be associated with positive outcomes. 1.3. Benefits of managed physical activity in anorexia nervosa In contrast to the concerns regarding PA among patients with eating disorders, a meta-analyses of existing studies concluded that prescribed moderate PA has no adverse effects on body weight, Body Mass Index (BMI) or lean body mass (Ng et al., 2013). Similarly, a systematic review of the literature concluded that managed PA does not have an adverse effect on BMI or eating disorder symptoms (Moola et al., 2013). Individual studies have found managed PA among youth to be associated with improvements in eating disorder symptoms such as, decreased food preoccupation (Carei, Fyfe-Johnson, Breuner, & Brown, 2010), decreased negative exercise behaviors (Calogero & Pedrotty, 2007), a reduction in exercise dependence (Bratland-Sanda et al., 2010b), and a decrease in the importance of exercise for negative affect regulation (BratlandSanda et al., 2010b). Further, no adverse effects of managed PA have been found on the recovery of menstruation among youths with AN (Tokumura, Yoshiba, Tanaka, Nanri, & Watanabe, 2003). Managed PA has also resulted in improved physical health, including, beneficial changes in exercise capacity (Tokumura et al., 2003) and

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increased muscle strength (Chantler, Szabo, & Green, 2006). Further, a recent systematic review concluded that managed PA is beneficial in regards to quality of life, psychological well-being, and treatment compliance (Moola et al., 2013). The improved therapeutic relationship (Beumont, Arthur, Russell, & Touyz, 1994) and patient compliance (Taranis, Touyz, & Meyer, 2011; Touyz, Lennerts, & Arthur, 1993) associated with managed PA among patients receiving treatment for an eating disorder may be due to the fact that, allowing managed PA is more acceptable to patients struggling with eating disorders (Beumont et al, 1994; Touyz, Beumont, Glaun, Phillips, & Cowie, 1984). Critical limitations of the research regarding managed PA have been emphasized. Although Ng and colleagues included nine research studies for evaluation in their meta-analysis, they reported that their conclusions were limited due to the heterogeneity of the PA implemented (Ng et al., 2013). Other critical limitations of the research to date considering managed PA includes; short exercise interventions, small sample sizes, and limited follow-up (Hausenblas et al., 2008; Moola et al., 2013; Ng et al., 2013). A multitude of recommendations for the future direction of exercise interventions in the treatment of AN have been proposed, including, clarifying definitions and doses of exercise, as well as the specific exercise implemented (Moola et al., 2013), and incorporating PA interventions of longer duration and with longer-term follow-up (Zunker et al., 2011) through well designed randomized control trials (Moola et al., 2013; Vancampfort et al., 2014). 2. Categorization of physical activity risk The current evidence to support the continuance of managed PA while adolescents are being treated for AN does not explicitly address categories of risk associated with participating in PA. What criteria should be used to categorize an AN patient's risk of participating in PA? The existing protocol considers three criteria to determine a patient's risk level in regards to participating in PA. The primary complications related to PA and AN identified for this protocol are; vital sign instability, percentage of ideal body weight (IBW), and the evaluation of engagement in compulsive exercise. Other criteria which had been considered, but were excluded from the current protocol, include menstrual dysfunction, bone mineral density (BMD), and psychosocial risk factors, such as, parental efficacy in Family Based Treatment (FBT). Menstrual dysfunction was excluded as a risk factor in the protocol since the resumption of menses correlates closely with IBW, the percentage of weight expected for height and age. For example, 86% of youth presenting with secondary amenorrhea associated with an eating disorder resumed menses within 6 months of reaching 90% of their IBW (Golden, Jacobson, Schebendach, Hertz, & Shenker, 1997). Further, menstrual function was excluded as a possible risk factor as, amenorrhea is not applicable to male patients and adolescents typically present with irregular menstrual cycles during the first 2 years after menarche (Van Hooff et al., 1998).

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Low Bone Mineral Density (BMD) was another risk factor considered for inclusion in the protocol. Recent literature reviews demonstrate that in addition to the known contributors to decreased BMD, such as, poor nutritional intake, low IBW and estrogen levels; depression in adult populations can be also be a causal factor due to the exposure to selective serotonin reuptake inhibitors (Couturier, Sy, Johnson, & Findlay, 2013; Wu, Liu, Gallegos-Orozco, & Hentz, 2010). Bone mineral accrual critically occurs during adolescence (McKay, Bailey, Mirwald, Davison, & Faulkner, 1998) and has the potential to be an irreversible complication of AN (Katzman, 2005). Decreased BMD appears to be a risk for the majority of adolescent patients with AN, as most adolescent girls with AN are reported to have low BMD (Bachrach, Guido, Katzman, Litt, & Marcus, 1990; Morris et al., 2004). Therefore, modifying PA for fracture risk was included in the PA recommendations instead. Parental efficacy in FBT is a risk factor in the recovery and monitoring of PA among adolescents with AN. Although the Parents Versus Anorexia Scale (Rhodes, Baillie, Brown, & Madden, 2005) could be used to assess parental efficacy with FBT, no standardized measure of parents' ability to monitor PA exists. As FBT is an outpatient treatment model, it was not considered a relevant risk factor for managed PA in an inpatient setting. Future models of the categorization of PA risk in AN could consider these psychosocial factors and further extend the risk categories. Three risk factors are used by the protocol to identify whether an adolescent with AN is at high, moderate or low risk of participating in PA while being treated for AN. See Table 1. Explanations for the inclusion of these three chosen risk factors are as follows. 2.1. Vital sign instability As illustrated in Table 1, vital sign instability is the first risk factor one should consider. Cardiovascular complications have been reported in up to 80% of patients with AN (Cooke et al., 1994; De Simone et al., 1994; Goldberg, Comerci, & Feldman, 1988). The following potential cardiovascular complications in AN directly impact PA recommendations; loss of cardiac mass (De Simone et al., 1994), bradycardia, postural hypotension and/or postural tachycardia (McCallum et al., 2006; Yager et al., 2006). Since vital signs normalize at approximately 80% of IBW (Shamim, Golden, Arden, Filiberto, & Shenker, 2003), the presence of vital sign instability differentiates between an adolescent at high or moderate risk. Vital signs, including heart rate and orthostatic blood pressure can be efficiently and effectively measured by a nurse at the point of care. In AN patients, the use of routine echocardiograms or electrocardiography to evaluate PA risk is not routinely practiced, and is only anecdotally recommended for patients with cardiac dysfunction (McCallum et al., 2006). Electrocardiographic abnormalities are present in most adolescents with AN (Mont et al., 2003) and cardiovascular complications in AN are reversible in young adolescents after refeeding (Mont et al., 2003). Early research recommended the long-term follow-up of repeated exercise testing

Table 1 Categorization of physical activity risk in adolescents with anorexia nervosa. Risk

High

Moderate

Low

Vital sign instability Ideal body weight (%)

Yes Less than 80% IBW

No 90e100% IBW, demonstrating weight maintenance.

Evaluation of compulsive exercise (CE)

High CET score and significant previous and/or current features of CE.

No Between 80 and e90% IBW, demonstrating consistent weight restoration. Moderate CET score and moderate current and/or previous features of CE.

Low CET score and few current and/or previous features of CE.

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during recovery from AN, despite adolescents with AN being asymptomatic during progressive exercise testing of adolescents with AN (Nudel, Gootman, Nussbaum, & Shenker, 1984). Exercise testing involves a cardiovascular stress test using treadmill or bicycle exercise with electrocardiographic and blood pressure monitoring. Exercise testing is not routine clinical practice and this is supported by the evidence that adolescent patients with AN demonstrate normal myocardial performance with maximal exercise testing (Rowland, Koenigs, & Miller, 2003). 2.2. Percentage of ideal body weight Percentage of IBW for height is the second risk factor to consider. Weight restoration is primary to the management of the AN patient, with the goal of achieving and maintaining an IBW, which usually leads to substantial improvement in the patient's overall state (Fairburn & Harrison, 2003). Weight restoration is accomplished by increasing caloric intake by refeeding and decreasing caloric expenditure by restricting or moderating PA. Refeeding undernourished patients is achieved through oral feeding and/or nasogastric feeding with a caloric intake based on their IBW to maximize weight gain while preventing refeeding syndrome (Dickstein, Franco, Rome, & Auron, 2014). Weight restoration resulted in the reversal of most of the medical complications in a summary of clinical experience by Golden and Meyer (2003). Additionally, a normalization of vital signs occurs at an IBW of 80% (Shamim et al., 2003). At an IBW of 90%, aerobic exercise can be resumed (McCallum et al., 2006) in the absence of vital sign instability and features of compulsive exercise. Thus a patient with an IBW greater than 90% is categorized as having low risk, between 80 and 90% is categorized as moderate risk, and an IBW less than 80% is considered high risk. The AN patients' ability to demonstrate the maintenance of his/her IBW over a period of time improve outcomes (McCallum et al., 2006), and is therefore included as an additional requirement for an AN patient at low risk of participation in PA. 2.3. Evaluation of compulsive exercise An evaluation of compulsive exercise is the final risk factor to consider when determining risk for managed PA. Risk for engagement in compulsive exercise can be assessed through the clinical interview and the use of a self-report questionnaire. Consistent with the definition of compulsive exercise, the clinical interview should address weight and shape concerns, a compulsive and/or rigid approach to exercise in the past or present, and the use of exercise to manage affect, and perfectionistic tendencies. The Compulsive Exercise Test (CET) (Goodwin, Haycraft, Taranis, & Meyer, 2011; Goodwin, Haycraft, Willis, & Meyer, 2011) is used in conjunction with the interview of current and/or previous features of compulsive exercise. The CET is the only self-report measure which provides a multidimensional analysis of each of the core features of compulsive exercise, and is comprised of five subscales; avoidance and rule driven behavior, weight control exercise, mood improvement, lack of exercise enjoyment, and exercise rigidity (Goodwin, Haycraft, Taranis, et al., 2011; Goodwin, Haycraft, Willis, et al., 2011; Taranis & Meyer, 2011). The CET has demonstrated good reliability, as well as concurrent and convergent validity in both adult and adolescent samples (Goodwin, Haycraft, Taranis, et al., 2011; Taranis et al., 2011). The CET has also been shown to be a better predictor of eating disorder symptoms then either the Commitment to Exercise Scale (CES) (Davis, Kaptein, Kaplan, Olmsted, & Woodside, 1998) or the Obligatory Exercise Questionnaire (OEQ) (Pasman & Thompson, 1988; Taranis & Meyer, 2011). The CET is also preferred over measures of exercise frequency and

intensity, such as the Leisure Time Exercise Questionnaire (LTEQ) (Godin & Shephard, 1997), as such behavioral measures are not always associated with compulsive exercise attitudes (Ackard, Brehm, & Steffen, 2002; Adkins & Keel, 2005; Goodwin, Haycraft, & Meyer, 2012; Mond, Hay, Rodgers, Owen, & Beumont, 2004; Mond, Hay, Rodgers, & Owen, 2006). Although the CET is a comprehensive multidimensional measure of compulsive exercise, norms are presently unavailable to indicate clinically high, moderate and low CET scores. Thus, the CET score is currently formulated by the general impression of the CET score compared to other patients within the same clinical setting. 3. Application of categorization of physical activity risk Risk factors are viewed cumulatively; none of these risk factors alone is enough to categorize a patients' risk. Currently these three risk factors are not weighted, meaning each of the three risks is equally important. The most severe ranking in either of the three categories, identifies the patients' overall risk categorization. Additionally, since recovery from AN is rarely linear, the patient with AN may move between categorizes of risk upon reassessment throughout their treatment (Bulik, 2014). Many adolescents with AN will never be admitted to an inpatient program and will instead be managed only as an outpatient. To further the utility of the proposed recommendations, the existing inpatient protocol could be used by an outpatient eating disorders team. The outpatient care team would be capable of reassessing the categorization of PA risk, with knowledge of the three risk factors. A physician, nurse practitioner and/or nurse could evaluate vital signs and IBW and a psychiatrist, psychologist and/or social worker, could evaluate compulsive exercise through the clinical interview and CET score. 4. Application of physical activity recommendations The PA recommendations in this existing protocol have been utilized by a physical therapist. It is recommended that the implementation and management of the PA recommendations be performed by a health care professional with the knowledge of disease and the skills to apply therapeutic exercise programs or interventions. A physical therapist is one of the most qualified health care professional to perform this role. The addition of a physical therapist to the interdisciplinary eating disorders team for this purpose should be considered. There are only a handful of physical therapists who work in the area of eating disorders worldwide, but the scope of practice for physical therapists internationally encompasses the skills required to implement and manage the following PA recommendations according to the category assessed by the eating disorders team. (World Confederation for Physical Therapy, 2011, pp. 1e12) A recent systematic review of the effectiveness of physical therapy as conventional treatment for patients with eating disorders, similarly concluded there is added value for patients (Vancampfort et al., 2014). PA recommendations are prescribed according to the level of risk associated with participating in PA. See Table 2. The PA recommendations are based on the evidence available regarding the recovery of physical and mental health throughout weight restoration. 4.1. Physical activity recommendations for a patient with high risk The PA recommendations for a patient with high PA risk begin with bed rest. A patient with AN is restricted to lying in bed as a part of treatment. Getting out of bed to use the toilet or shower is permitted with supervision. This allows for close monitoring of vital signs on a cardiac monitor, as well as a reduction in PA for high

L. Scott, S. Van Blyderveen / Mental Health and Physical Activity 7 (2014) 163e170 Table 2 Physical activity recommendations for adolescents with anorexia nervosa. Risk

High

Moderate

Low

Bed rest Reduce PA Modify PA for fracture risk Supervised PA (low intensity, short duration) Normalize exercise behaviors Independent PA (low intensity, short duration) Aerobic PA (with required modifications to type) Potential return to training and competition

Yes Yes Yes Yes Yes No No No

No Yes Yes Yes Yes No No No

No No Yes No Yes Yes Yes Yes

risk patients, limiting caloric expenditure and reducing PA through behavioral monitoring of compulsive exercise. The modification of PA for fracture risk is applicable to patients at all levels of PA risk due to decreased bone mineral density (BMD) (Morris et al., 2004) and increased fracture risk (Vestergaard et al., 2003; Yager et al., 2006). The modifications required to PA for patients with decreased BMD are as follows; impact PA and moderate intensity resistance training are contraindicated (Golden, 2003; Kohrt, Bloomfield, Little, Nelson, & Yingling, 2004) until 21 months, on average, from weight restoration, due to the delay in an increase in BMD (Jagielska et al., 2001; Morris et al., 2004). The relationship between BMD and PA in adolescents with AN is not clear with respect to the intensity, frequency, and duration of PA that promotes an increase in BMD (Katzman, 2005). Once an adolescent with AN is weight restored, closely monitored weight bearing exercise can be considered (Katzman, 2005). The importance of supervised PA in AN patients should also be emphasized for patients at high PA risk due to the potential for cardiovascular complications (McCallum et al., 2006) and features of compulsive exercise. For patients at all levels of risk, an attempt is made to always normalize exercise behaviors. However, during weight restoration there are state alterations secondary to malnutrition (Kaye, Fudge, & Paulus, 2009) and impaired cognitive function (Jimerson & Wolfe, 2006). Therefore, the modeling and practice of behaviors is more valuable than education for a high risk patient. The recommended supervised PA should be of low intensity and short duration since high intensity and longer duration exercise during the first 3 months after discharge is significantly associated with the probability of relapse (Carter et al., 2004). 4.2. Physical activity recommendations for a patient with moderate risk The progression of PA recommendations for a patient with moderate PA risk mirrors that of the patient with low PA risk with the exception of bed rest not being required. A reduction of PA, modification of PA for fracture risk and supervised PA of low intensity and short duration are similarly recommended. 4.3. Physical activity recommendations for a patient with low risk A patient with low PA risk does not require bed rest, a reduction in PA or supervised PA. As previously stated, all patients, even those with low PA risk require modification of PA for fracture risk. This is the only risk category that permits independent PA of low intensity and short duration. Intensity and duration of PA must be managed due to changes in exercise capacity in AN, such as VO2max (maximal oxygen uptake) or maximal aerobic power, and muscle performance. A lower VO2max exists for 6 weeks during weight restoration (Rigaud et al., 1997), with changes occurring not until one year follow-up (Tokumura et al., 2003). Muscle atrophy in AN (McLoughlin et al., 1998) results in myopathy or decreased muscle

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strength (McLoughlin et al., 1998), decreased work capacity (Moodie & Salcedo, 1983) and decreased leg muscle performance (Rigaud et al., 1997). Muscle performance completely reversed with weight restoration (Rigaud et al., 1997). The type of aerobic PA prescribed for a patient with low PA risk, is modified, in order to reduce the risk associated with participation in certain types of sports and exercise environments (Powers, 1999). Sports that are aesthetically judged in which physical appearance influences performance evaluation, such as diving, figure skating, dance or gymnastics (Sundgot-Borgen, 1994; Sundgot-Borgen & Torstveit, 2004; Zucker, Womble, Williamson, & Perrin, 1999), have weight categories (Sundgot-Borgen & Torstveit, 2004), or emphasize aesthetics or leanness (Nattiv et al., 2007; Petrie, 1996), can lead to more frequent occurrences of eating disorders and may not be indicated for some patients (Nattiv et al., 2007). 4.3.1. Potential return to training and competition The resumption of training and competition must be approached with caution. Participation in training and competition may not be indicated or require modifications for some patients at low PA risk (Nattiv et al., 2007). Current practice does not automatically recommend abstinence from the return to training and competition (Littlefield, Zuercher, Daberkow, Hazel, & Woods, 2008). The possible risks associated with the type of sport in which a patient plans to return to, need to be considered (Littlefield et al., 2008). Additionally, participation in competition has entirely different cognitive, affective and physical demands, and certain aspects of the athletic environment may increase risk (Zucker et al., 1999), such as pressure from coaches and parents to perform (Taub & Blinde, 1992). It might be reasonable in future models to consider a separate assessment of the readiness of an adolescent patient with AN to return to sport. For adolescents with current and/or previous features of compulsive exercise, team sports and leisure activities, where accomplishment is more difficult to measure quantitatively are preferred over individual sports where performance can be measured. Team sports are also recommended over individual-based activities due to the social benefits that can be accrued from these activities. The importance of PA prescription for not only physical, but also mental health must be considered. Common co-morbitities associated with AN include; anxiety and depression (Fairburn & Harrison, 2003). In a systematic review of exercise and anxiety and depression amongst a general population of children and adolescents, a small reduction in depression and anxiety scores was reported (Larun, Nordheim, Ekeland, Hagen, & Heian, 2009). Unfortunately, the effect of exercise for youth with anxiety and depression, is unknown due to a paucity of research (Larun et al., 2009). 5. Clinical cases The following clinical cases demonstrate two typical adolescents with AN who presented to McMaster Children's Hospital Eating Disorder In-patient Program. Their cases illustrate the application of the categorization of PA risk and PA recommendations (see Tables 1 and 2) for an adolescent categorized with high PA risk and an adolescent categorized with low to moderate PA risk. 5.1. Patient with high physical activity risk Margot was a 16 year old female admitted to hospital with AN and bradycardia. She presented at 83% of her IBW for height and with secondary amenorrhea for 6e8 months. Co-morbidities included obsessive compulsive disorder and depression. Margot reported a long history of obsessive compulsive disorder (OCD) symptoms, starting at 10 years of age, as well as a five month

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escalation of her symptoms beginning with starting competitive running. During these 5 months, Margot reported her mood as low. She described having difficulty sleeping, frequent standing, decreased concentration, decreased appetite, and decreased interest in usual activities; such as, friends, school and sports. Margot had not attended school in two weeks. Her relevant past medical history revealed a right metatarsal stress fracture approximately 5 months prior to her hospital admission. Her recent PA included recreational soccer and hockey, as well as, school and community running clubs involving daily 10 km runs. Additionally, she would cycle 10 km, 4 times daily during the summer months. She performed a routine of sit-ups and push-ups and would walk daily sometimes with her family or dog. Within the last month, parents had not permitted Margot to run or cycle. Margot walked up to 2 h daily instead. She described good relationships with her two parents and two older siblings. Past PA included participation in elementary school volleyball, basketball, floor hockey and cross country. She reported her family had always been active together. On physical assessment she denied lightheadedness and dizziness, but did complain of coccyx pain from sitting in the bed. Her heart rate was 48 beats per minute (bpm). Her blood pressure lying was 106/67 and standing was 95/65. Physical exam revealed a bruise on left 2nd toe nail and very calloused feet. Range of motion and strength were within normal limits. Margot's CET score was 21.2/25 at the time of admission. Margot's affect appeared depressed and anxious; she was soft-spoken, but polite and co-operative, wellgroomed and maintained eye contact throughout assessment. Margot was observed to take all meals and snacks well with mom supervising on the ward. She was noted to sit at the edge of her bed to read the newspaper, reporting that while she found it easier to sit in hospital than at home, she still found it challenging. During her 13 day admission, Margot participated in twice weekly 30 min individual physiotherapy sessions of range of motion, stretching and deep breathing exercise in supine, prone, long sitting and 4 point positions with no adverse effects. Margot was compliant. Her Bone Mineral Density (BMD) completed 6 months later was normal. 5.2. Patient with low to moderate physical activity risk Genevieve was a 14 year old female with AN. She was referred to the McMaster Children's Hospital Eating Disorder Program for outpatient management approximately 9 months prior to her inpatient admission. Genevieve had longstanding issues with food and weight preoccupation, starting at 8 years of age when she was teased about her weight. Her initial physiotherapy assessment occurred during her inpatient admission for parental concerns regarding increased OCD behaviors. She presented at 88% of her IBW for height. Co-morbidities included, OCD and a general anxiety disorder. Genevieve reported her mood as a 6 or 7 out of 10. She described being more irritable, but denied having any difficulty sleeping or concentrating. Genevieve had two parents and an older sister. She reported feeling safe at home and getting along well with her family. Her resting heart rate was 59 bpm. Her blood pressure in lying was 103/62 and in standing was 103/72. Relevant past musculoskeletal history included a right calcaneus fracture at 5 years of age and a left distal radius fracture at 9 years of age. Her CET score was 2.8/25. BMD was normal. Genevieve's present PA included gymnastics for 1 h, 3 times a week. She previously participated in 15 min of cross-country running daily as required by the school during cross-country season and had attended 10 yoga sessions with her mom and sister. Genevieve's musculoskeletal assessment was unremarkable and she denied any dizziness or lightheadedness. Genevieve was pleasant and interactive throughout assessment. While an inpatient, Genevieve initially struggled with separation from her mom and with meal choices

that she perceived would result in her gaining too much weight. She participated in one 30 min physiotherapy session of yoga and relaxation. Genevieve participated well with no adverse effects and demonstrated a 0.8 kg (1.6%) weight gain over the course of a 7 day hospital admission. 5.3. Summary of clinical cases Margot presented with high PA risk despite an IBW of 83%, due to her vital sign instability, high CET score and significant previous and current features of compulsive exercise. PA recommendations included, bed rest and a reduction in PA. Also, supervised PA was prescribed during her inpatient admission. Genevieve presented with low to moderate PA risk, with no vital sign instability, an IBW of 88%, and a low CET score and few current or previous features of compulsive exercise. Genevieve was required to reduce her PA during her inpatient admission, but participated in supervised PA. Independent PA of low intensity and short duration would have been prescribed if she demonstrated consistent weight restoration and maintenance. 6. Limitations A variety of terms and definitions have existed to describe exercise in eating disorders. Terms such as; exercise addiction (Berczik et al., 2012; Lichtenstein, Larsen, Christiansen, Støving, & Bredahl, 2014; Terry, Szabo, & Griffiths, 2004), exercise dependence (Allegre, Souville, Therme, & Griffiths, 2006; Ogden, Veale, & Summers, 1997), excessive exercise (Davis, Brewer, & Ratusny, 1993), anorexia athletica (Sundgot-Borgen & Torstveit, 2004), obligatory exercise (Pasman & Thompson, 1988) and compulsive exercise (Taranis & Meyer, 2011). Since only recently has a clear definition and model of compulsive exercise been proposed, the evaluation of existing research and literature is limited (Meyer & Taranis, 2011). Also, as previously described, critical limitations of the research to date regarding managed PA in eating disorders are numerous. The applicability of the existing protocol may be limited within FBT in outpatient care, where the management of PA is the responsibility of the parents. How can PA recommendations made in an outpatient environment co-exist with FBT, when it is the parents, not the healthcare professionals, who are to make the decisions about PA? The recommendations described, while evidence-based and representative of best practices, are not clinical practice guidelines. According to the Appraisal of Guidelines for Research and Evaluation Instrument (AGREE II, 2009); stakeholder involvement from all relevant professional groups and rigor of development, including a systematic review and external review by clinical practitioners and researchers in the field, is recommended for development of clinical practice guidelines (Brouwers et al., 2009, pp. 1e56). Additionally, evaluation and implementation strategies were not developed for the PA recommendations provided in Table 2 for adolescents with AN (Brouwers et al., 2009, pp. 1e56). Addressing these limitations is necessary for future research to test the efficacy and safety of the existing protocol. 7. Conclusion It is unmanaged PA in eating disorders that is frequent, of high intensity and/or long duration that is associated with negative outcomes and higher levels of eating disorder psychopathology. In contrast, managed PA in the treatment of adolescents with AN is beneficial, as long as it accounts for the compulsive exercise. Previous or current features of compulsive exercise remain a worrisome component of eating disorder pathology and deserves

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significant attention during treatment. In the existing protocol, categorization of the level of PA risk includes an evaluation of compulsive exercise as one risk factor, as well as vital sign instability and percentage of IBW, which are assessed by the interdisciplinary eating disorders team. A physical therapist should be considered for the implementation and management of the proposed PA recommendations according to the level of PA risk. In order to optimize inpatient and outpatient management of PA for adolescents being treated for AN, the existing protocol of PA recommendations based on PA risk is available for use by clinical practitioners and researchers who are seeking to create clinical practice guidelines. References Ackard, D. M., Brehm, B. J., & Steffen, J. J. (2002). Exercise and eating disorders in college-aged women: profiling excessive exercisers. Eating Disorders, 10(1), 31e47. http://dx.doi.org/10.1080/106402602753573540. Adkins, E. C., & Keel, P. K. (2005). Does “excessive” or “compulsive” best describe exercise as a symptom of bulimia nervosa? The International Journal of Eating Disorders, 38(1), 24e29. http://dx.doi.org/10.1002/eat.20140. Allegre, B., Souville, M., Therme, P., & Griffiths, M. (2006). Definitions and measures of exercise dependence. Addiction Research & Theory, 14(6), 631e646. http:// dx.doi.org/10.1080/16066350600903302. American Psychiatric Association. (2013). Feeding and eating disorders, diagnostic and statistical manual of mental disorders (DSM-5). Bachrach, L. K., Guido, D., Katzman, D., Litt, I. F., & Marcus, R. (1990). Decreased bone density in adolescent girls with anorexia nervosa. Pediatrics, 86, 440.
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