Indira Nathan, PhD, BSc (Hons), SRD Christine Norton, PhD, MA, RN Wladyslawa Czuber-Dochan, MSc, PGPD, RN, RNT Alastair Forbes, MD, FRCP, FHEA
Exercise in Individuals With Inflammatory Bowel Disease ABSTRACT There is increasing evidence that exercise may improve symptoms in individuals with inflammatory bowel disease (IBD). This study aims to explore issues that clinicians may need to consider when giving advice on exercise to such individuals. Limited existing evidence suggests that low to moderate physical activity may improve symptoms without any adverse effects in individuals with IBD. This is largely supported by the findings of the current case series of “exercising” individuals with IBD who reported that low- to moderate-intensity exercise (most commonly walking) had a positive effect on their mood, fatigue, weight maintenance, and osteoporosis. Overexertion was reported as a potential problem. Scant advice regarding exercise had been given by their healthcare professionals according to participants. The current literature and findings of this small case series suggest that exercise is likely to be beneficial and safe for individuals with IBD. However, more research is required on which recommendations for exercise could be based.
T
here is some supportive evidence that exercise is beneficial for individuals with inflammatory bowel disease (IBD) (Martin, 2011). However, people with IBD experience considerable barriers to exercise, including the unpredictReceived April 28, 2012; accepted August 2, 2012. About the authors: Indira Nathan, PhD, BSc (Hons), SRD, is Research Associate, Centre for Gastroenterology and Nutrition, University College London, London, England. Christine Norton, PhD, MA, RN, is Florence Nightingale Professor of Clinical Nursing Research, King's College London, Florence Nightingale School of Nursing and Midwifery, London, England. Wladyslawa Czuber-Dochan, MSc, PGPD, RN, RNT, is PhD Research Fellow, King’s College London, Florence Nightingale School of Nursing and Midwifery, London, England. Alastair Forbes, MD, FRCP, FHEA, is Professor of Gastroenterology and Clinical Nutrition, University College London and University College London Hospital, Department of Gastroenterology, London, England. Supplemental digital content is available for this article. Direct URL citations appear in the printed text and is provided in the HTML and PDF versions of this article on the journal’s Web site (http://www .gastroenterologynursing.com). This study has received funding from the Big Lottery Fund and is commissioned by Crohn's and Colitis UK. The authors declare no conflict of interest. Correspondence to: Indira Nathan, PhD, BSc (Hons), SRD, Centre for Gastroenterology and Nutrition, Rockefeller Building, University College London, Gower St., London WC1 6BT, England (i.shanmuganathan@ ucl.ac.uk). DOI: 10.1097/SGA.0000000000000005
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able fluctuating nature of the disease and its symptoms such as pain, fatigue, and fear of fecal incontinence. There are currently no evidence-based guidelines for this group of patients that take such factors into consideration. Development of a practical physical activity protocol that can be recommended in routine clinical practice is a research priority (Chey & Rai, 2011). This article, by means of a literature review supplemented with qualitative data from a small case series, aims to explore the issues to be considered by clinicians when advising patients with IBD to increase exercise.
Methods Literature Review A selective review of evidence on exercise for IBD up to November 2011 (MEDLINE, EMBASE, CINAHL, and Cochrane data bases) was initiated. The search for articles on IBD was based on the search strategy used by the National Health Service (2011) evidence gastroenterology and liver disease specialist project team for the annual evidence update on IBD. This was combined for exercise using the following search terms: “exercise,” “exercise therapy,” and “exercise tolerance.”
Case Series Participants were a sample of convenience who were interviewed during pilot work for a larger study 437
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screening IBD clinic attenders who might benefit from increasing exercise. These were people who were already reporting regular exercise. A sample of adults with IBD who reported themselves as “exercising” (n = 11) were purposively selected and interviewed regarding their exercise history prior to diagnosis, current exercise activity levels, and any benefits and difficulties experienced. They were also asked to recall any advice received about exercise from healthcare professionals since their first diagnosis, what information they would find helpful, and what advice they would give other IBD patients wishing to start exercising. Current activity levels were determined using the Godin Leisure-Time Exercise Questionnaire (GLTEQ), and a Leisure Score Index was calculated (Godin & Shephard, 1985). The GLTEQ has four questions that measure self-reported leisure time exercise habits. The first three items measure weekly frequencies of “strenuous,” “moderate,” and “light” activities for periods of 15 minutes or more. These items are multiplied by 9, 5, and 3, respectively, and then summed to give the Leisure Score Index. The fourth item assesses frequency of weekly leisure time activities of sufficient intensity to “work up a sweat.” There is a choice of three responses: “never,” “sometimes,” or “often.”
Findings Literature Review Current Guidelines for Exercise for IBD Current guidelines provide only scant guidance on exercise for individuals with IBD. There are general guidelines for IBD patients in relation to osteoporosis that address exercise. These British Society of Gastroenterology guidelines state that it is difficult to make precise recommendations for exercise in relation to bone health; however, they advise that at least minimal activity should be encouraged and that active sports should give additional benefit (Scott, Gaywood, & Scott, 2000). Recent UK nationwide guidelines for exercise in the general population include reference to vigorous activity and resistance exercise (UK Department of Health, 2011). The suitability for this in individuals with IBD is unknown. This expert panel recommended that the United Kingdom as a priority “should establish a process to develop physical activity guidelines for adults, children, and young people with noncommunicable disease.”
Potential Benefits of Exercise Studies of exercise in individuals with IBD have reported that exercise is well tolerated (D’Inca et al., 1999;
Loudon, Corroll, Butcher, Rawsthorne, & Bernstein, 1999; Ng, Millard, Lebrun, & Howard, 2007). A small study (n = 6) found that males with Crohn disease were able to cycle for 1 hour at 60% of oxygen consumption with no adverse effect (D’Inca et al., 1999). A 12-week walking program elicited psychological benefits (Loudon et al., 1999); however, this was a small uncontrolled pilot study (n = 12). Improvements in quality of life were found in patients with Crohn disease following a 3-month low-grade walking program that required walking three times a week at 60% of maximum heart rate (Ng, Millard, Lebrun, & Howard, 2006). The patients were in remission or with mild disease activity and included a control group (n = 16) and an exercise group (n = 16). There is some limited evidence from randomized controlled trials that exercise improves the symptoms of irritable bowel syndrome (IBS) (Daley et al., 2008; Johannesson, Simren, Strid, Bajor, & Sadik, 2011). This suggests that increasing exercise may be beneficial for individuals with IBD who also report IBS-type symptoms. It has been suggested that low to moderate activity is safe (Martin, 2011; Packer, 2010) and in general individuals with IBD should benefit from (Narula & Fedorak, 2008) and increase exercise (Cosnes, 2010; Martin, 2011; McGowan, Jones, Long, & Barritt, 2012). The benefits of exercise have been recognized in cancer survivors: recent guidelines on exercise for cancer survivors indicate that advice to rest is unhelpful and that in general, all patients with cancer should undertake physical activity, individually tailored depending on their ability (Schmitz et al., 2010). However, it is unclear whether, and to what extent, this advice can be extrapolated to individuals with IBD. Exercise may help prevent comorbidities in IBD patients; for example, exercise is recommended for the general population to reduce the risk of colon cancer (Sellar & Courneya, 2011). It has been estimated using a modeling approach that 5.3% of cases of colon cancer diagnoses in the United Kingdom in 2010 were due to suboptimal levels of activity in 2000 (Parkin, 2011). It has also been suggested that the effect of inactivity may be greater in women (de Vries et al., 2010). The effect of exercise on the risk of colon cancer in patients with IBD has not been studied but could be of particular importance as a preventative factor in this higher risk group. However, it is not known whether exercise would have any effect on cancer risk in IBD. The UK Department of Health guidelines recommend resistance training for the general population (UK Department of Health, 2011). This type of exercise may particularly benefit the IBD population in whom corticosteroid use and intermittent periods of
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inactivity as a result of active disease may impair muscle mass (Fletcher et al., 1996; Jahnsen, Falch, Mowinckel, & Aadland, 2003) and bone health (Scott et al., 2000; Valentini et al., 2008). Similarly, sarcopenia (involuntary loss of muscle mass) is common in IBD patients and it has been suggested that physical activity may help improve muscle mass and function (Schneider et al., 2008). A program of resistance training for patients with short bowel syndrome was reported to increase lean body mass. An increase in energy intake of approximately 15% was also reported, so resistance exercise may provide a useful therapy for improving nutritional status (Araujo, Suen, Marchini, & Vannucchi, 2008). Studies in animal models have suggested a possible impact of exercise on the immune system (Cook, 2011). It has been documented that for the patient with IBD, exercise may reduce disease activity (Packer, 2010). However, research in this area is at an early stage and limited evidence exists to draw any final conclusions.
Potential Harms of Exercise It has been suggested that clinicians may be reluctant to prescribe exercise because of the fear of symptom exacerbation (Ng et al., 2007); however, there are no studies in IBD patients to support this concern. Although anecdotal evidence suggests that some patients with IBD successfully compete in high-level competitive sport and endurance events (e.g., marathon running and rowing), there is a dearth of information regarding the impact on health. When considering high-intensity exercise, extrapolation of results from endurance athletes supports the need for a cautious approach for the IBD patient. For the healthy athlete, marathon runners’ diarrhea is well recognized and common (Sullivan & Wong, 1992). This is something that individuals with IBD would particularly want to avoid. In a small study (n = 12) of endurance athletes, all complaining of gastrointestinal symptoms (commonly abdominal cramps and the urge to defecate), gastric ischemia was found in all athletes exercising at maximal intensity and in 50% at submaximal exercise (ter Steege, Geelkerken, Huisman, & Kolkman, 2012). It is unclear why only some individuals present with gastrointestinal symptoms during high-intensity exercise. Successful management of symptoms was achieved by reducing exercise intensity for a few months, then gradually increasing this to resume previous levels. For patients with IBD, there have been reports of reduced exercise capacity in children (Ploeger et al., 2011) and reduced muscle strength in adults (Wiroth et al., 2005). Following bowel surgery, there is some evidence that exercise capacity is reduced in VOLUME 36 | NUMBER 6 | NOVEMBER/DECEMBER 2013
proportion to the length of bowel resected (Brevinge et al., 1995).
Case Series The majority of interviewees had Crohn disease (n = 10). One patient had ulcerative colitis and three of 11 patients had a stoma (six females and five males). A summary of the data is presented in Supplemental Digital Content Table 1 (available at: http://links.lww.com/GNJ/A24).
Types of Exercise The GLTEQ indicated that exercise was predominantly of low intensity (6 of 11 patients), with only 3 of 11 individuals reporting “often” doing exercise of intensity to “work up a sweat.” Aerobic exercise was the most common type of exercise undertaken (11/11 patients). There was some interest in resistance exercise; a small number of the patients were doing resistance exercise regularly (2 of 11 patients). A high proportion reported a history of previous involvement in sport (7 of 11 patients). Walking was the most common type of exercise (8 of 11 patients). Other activities included water-skiing (1 of 11 patients) competitive football (2 of 11 patients), running (1 of 11 patients), swimming (3 of 11 patients), cycling (3 of 11 patients), Wii Fit (1 of 11 patients), karate (1 of 11 patients), and yoga (2 of 11 patients). There was little gym-based exercise (1 of 11 patients). One individual was particularly dissatisfied with gymbased exercise: “Gyms are obsessed with weight reduction and can’t advise for people trying to gain or maintain a healthy weight.” Another patient reported that she struggled and then gave up a morning exercise class, as on a regular basis, her diarrhea was worst at this time.
Benefit of Exercise Benefits reported frequently included improvement in mood and a “feel good factor” (seven of 11 patients). Individuals described feeling “run down” if they did not exercise. Exercise was reported to help with fatigue (4 of 11 patients). Individuals said that exercise made them feel “fatigued but energized,” and helped with “lethargy” and “tiredness.” The effect of exercise was a “good kind of tiredness.” Exercise “increased appetite” and “helped with weight gain” (1 of 11 patients). Wanting to lose weight was also a reason for exercising (2 of 11 patients). Exercise as a prevention or treatment for osteoporosis was reported (2 of 11 patients). One patient who had received advice from a physical therapist regarding resistance exercise at home followed this advice and on a regular basis made use of 439
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tins of food to provide a measured weight, also using her wall for press-ups. Those who were members of clubs or groups enjoyed the social interaction and valued the camaraderie. The fact that “other members understand” their IBD was important.
Problems Encountered Patients described overexerting themselves (three of 11 patients) and suffering the next day with a feeling described as being “wiped out.” One man did report “nearly drowning” when trying to swim soon after a flare-up believing that swimming “is good for you.”
Current Exercise Patients reported that they determine their own amount, type, and intensity of exercise. When asked how they determine how much exercise to do, the replies included “as much as I could do” and “keep going until I run out of energy.” One person used a heart-rate monitor and struggled to keep the heart rate in what they calculated as their “training zone.”
Advice Received by Patients Six patients reported having received no advice from healthcare professionals regarding exercise (6 of 11 patients). Advice received included minimal reference to health benefits or how this might be achieved. Patients had repeatedly been advised to limit exercise in the abdominal area after surgery (3 of 11 patients), but then following recovery, and in fact years after this, no further advice had been given. The only advice received by one patient was to rest. There was also uncertainty about advice for resistance exercise (two of seven patients), the use of weights, and what encompassed “weight bearing” exercise. Three of the patients had a stoma and had varied experiences and amounts of information given regarding swimming and other aspects of daily living. Encouragingly, one lady reported “invaluable help” from a stoma nurse regarding clothing and all aspects of managing daily activities; she swam routinely. Others had received less advice (two of three patients with a stoma), particularly with regard to swimming and swimwear and this was having an impact on physical activity undertaken; for example, “I just didn’t go in the sea.”
Patient-Suggested Recommendations for Exercise All 11 exercising patients felt that exercise was beneficial and that “both children and adults with IBD should be encouraged to exercise.” Those who had negative experiences of exercise as a result of “trying to do too much” specifically recommended a step-bystep approach to increasing exercise. Patients frequently
reported adopting a strategy of adjusting activity level depending on how they felt (five of 11 patients). In the clinical setting, patients welcomed the opportunity to talk about their experience of exercise and were keen to offer information that might assist nonexercising IBD patients. It was suggested that “it would be good if the hospital offered an exercise class for people with mobility difficulties.”
Discussion Specific considerations for the appropriate level of activity for patients with “mild,” “moderate,” and “active” IBD have not been addressed in the literature. A population-based study of Canadians living with Crohn disease and ulcerative colitis found that only one in four individuals were engaged in sufficient selfreported leisure time physical activity to achieve likely health benefits (Mack, Wilson, Gilmore, & Gunnell, 2011). The most common activities reported were walking and gardening with a notable lack of involvement in “structured” physical activity. A significantly lower proportion of the population with Crohn disease (17.9%) and ulcerative colitis (21%) were classified as physically “active” compared with the control population who did not report IBD (24.1%); however, no measure of disease activity was given. Current practice suggests that during active disease, IBD patients have a reduced capacity for exercise and self-limit their activity; however, there is no evidence to suggest that total rest is advisable. With respect to exercise when IBD is in remission, the evidence is similarly sparse. There is minimal information about exercise capacity and effect of increasing activity on fitness levels and health status. Anemia is common in IBD (Lomer, 2011), and it has been reported that anemia reduces exercise capacity (Haas & Brownlie, 2001). There is no evidence to show whether optimizing the iron status of patients with IBD improves exercise capacity. There are few intervention studies of exercise in IBD patients (D’Inca et al., 1999; Loudon et al., 1999; Ng et al., 2007). Overall, there is little evidence to indicate that exercise is risky for patients with IBD. Experiences of our small sample of “exercising” IBD patients suggest that if they take care to avoid overexerting themselves and exercise at their own level, exercise is safe.
Conclusions The reviewed literature highlights the need for further research in exercise and IBD and the need for standardized reporting of exercise programs to enable evaluation and implementation of research results. If guidelines are to be evidence-based, there is a need for rapid expansion of research in this area. This lack of evidence contributes to the cautious approach taken by
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healthcare professionals. Patients with IBD should not miss out on what has been described recently as “the indisputable” benefits of exercise in relation to treatment and prevention of disease (Khan, Weiler, & Blair, 2011); neither should inactivity in this patient group contribute to an increased prevalence of obesity and osteoporosis. However, barriers to exercise in the IBD population have not been studied. The present nonspecific and ad hoc advice regarding physical activities is unlikely to alter the status quo for the sedentary IBD population. According to our interviewees, healthcare professionals are giving vague advice regarding exercise and there is confusion among both clinicians and patients as to what is appropriate. To enable patients to vary exercise levels according to their disease activity, effects of medication, and severity of symptoms, there is a need to test individually prescribed exercise for the patient with IBD. ✪
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Haas, J. D., & Brownlie, T. T. (2001). Iron deficiency and reduced work capacity: A critical review of the research to determine a causal relationship. Journal of Nutrition, 131(2S–2), 676S– 688S; Discussion 688S–690S. Jahnsen, J., Falch, J. A., Mowinckel, P., & Aadland, E. (2003). Body composition in patients with inflammatory bowel disease: A population-based study. American Journal of Gastroenterology, 98(7), 1556–1562. Johannesson, E., Simren, M., Strid, H., Bajor, A., & Sadik, R. (2011). Physical activity improves symptoms in irritable bowel syndrome: A randomized controlled trial. American Journal of Gastroenterology, 106(5), 915–922. Khan, K. M., Weiler, R., & Blair, S. N. (2011). Prescribing exercise in primary care. British Medical Journal, 343, d4141. doi: 10.1136/bmj.d4141. Lomer, M. C. E. (2011). Dietary and nutritional considerations for inflammatory bowel disease. Proceedings of the Nutrition Society, 70(3), 329–335. Loudon, C. P., Corroll, V., Butcher, J., Rawsthorne, P., & Bernstein, C. N. (1999). The effects of physical exercise on patients with Crohn’s disease. American Journal of Gastroenterology, 94(3), 697–703. Mack, D. E., Wilson, P. M., Gilmore, J. C., & Gunnell, K. E. (2011). Leisure-time physical activity in Canadians living with Crohn disease and ulcerative colitis: Population-based estimates. Gastroenterology Nursing, 34(4), 288–294. Martin, D. (2011). Benefits and risks of exercise on the gastrointestinal system. Southern Medical Journal, 104(12), 831–837. McGowan, C. E., Jones, P., Long, M. D., & Barritt, A. S. (2012). Changing shape of disease: Nonalcoholic fatty liver disease in Crohn’s disease—A case series and review of the literature. Inflammatory Bowel Diseases, 18(1), 49–54. doi:10.1002/ ibd.21669. Narula, N., & Fedorak, R. N. (2008). Exercise and inflammatory bowel disease. Canadian Journal of Gastroenterology, 22(5), 497–504. National Health Service. (2011). NHS evidence and liver diseases specialist collection project team: Annual evidence update on inflammatory bowel disease. Retrieved February 7, 2012, from http://arms.evidence.nhs.uk/resources/hub/36890/attachment Ng, V., Millard, W., Lebrun, C., & Howard, J. (2006). Exercise and Crohn’s disease: Speculations on potential benefits. Canadian Journal of Gastroenterology, 20(10), 657–660. Ng, V., Millard, W., Lebrun, C., & Howard, J. (2007). Low-intensity exercise improves quality of life in patients with Crohn’s disease. Clinical Journal of Sport Medicine, 17(5), 384–388. Packer, N. (2010). Does physical activity affect quality of life, disease symptoms and immune measures in patients with inflammatory bowel disease? A systematic review. Journal of Sports Medicine and Physical Fitness, 50(1), 1–18. Parkin, D. M. (2011). Cancers attributable to inadequate physical exercise in the UK in 2010. British Journal of Cancer, 105(S2), S38–S41. Ploeger, H. E., Takken, T., Wilk, B., Issenman, R. M., Sears, R., Suri, S., & Timmons, B. W. (2011). Exercise capacity in pediatric patients with inflammatory bowel disease [Comparative Study]. Journal of Pediatrics, 158(5), 814–819. Schmitz, K., Courneya, K., Matthews, C., Demark Wahnefried, W., Galvo, D., Pinto, B., … Schwartz, A. (2010). American College of Sports Medicine roundtable on exercise guidelines for cancer
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survivors. Medicine and Science in Sports and Exercise, 42(7), 1409–1426. Schneider, S. M., Al-Jaouni, R., Filippi, J., Wiroth, J.-B., Zeanandin, G., Arab, K., & Hebuterne, X. (2008). Sarcopenia is prevalent in patients with Crohn’s disease in clinical remission. Inflammatory Bowel Diseases, 14(11), 1562–1568. Scott, E. M., Gaywood, I., & Scott, B. B. (2000). Guidelines for osteoporosis in coeliac disease and inflammatory bowel disease: British Society of Gastroenterology. Gut, 46(Suppl. 1), i1–i8. Sellar, C., & Courneya, K. (2011). Physical activity and gastrointestinal cancer survivorship. Recent Results in Cancer Research, 186, 237–253. Sullivan, S. N., & Wong, C. (1992). Runners’ diarrhea: Different patterns and associated factors. Journal of Clinical Gastroenterology, 14(2), 101–104. ter Steege, R. W., Geelkerken, R. H., Huisman, A. B., & Kolkman, J. J. (2012). Abdominal symptoms during physical exercise and
the role of gastrointestinal ischaemia: A study in 12 symptomatic athletes. British Journal of Sports Medicine, 46(13), 931–935. doi:10.1136/bjsports-2011-090277. UK Department of Health. (2011). Start active, stay active: a report on physical activity from the four home countries’ chief medical officers. Retrieved January 24, 2012, from http://www.dh.gov .uk/prod_consum_dh/groups/dh_digitalassets/documents/ digitalasset/dh_128210.pdf Valentini, L., Schaper, L., Buning, C., Hengstermann, S., Koernicke, T., Tillinger, W., … Lochs, H. (2008). Malnutrition and impaired muscle strength in patients with Crohn’s disease and ulcerative colitis in remission. Nutrition, 24(7/8), 694–702. Wiroth, J.-B., Filippi, J., Schneider, S. M., Al-Jaouni, R., Horvais, N., Gavarry, O., … Hebuterne, X. (2005). Muscle performance in patients with Crohn’s disease in clinical remission. Inflammatory Bowel Diseases, 11(3), 296–303.
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Exercise in Individuals With Inflammatory Bowel Disease ABSTRACT There is increasing evidence that exercise may improve symptoms in individuals with inflammatory bowel disease (IBD). This study aims to explore issues that clinicians may need to consider when giving advice on exercise to such individuals. Limited existing evidence suggests that low to moderate physical activity may improve symptoms without any adverse effects in individuals with IBD. This is largely supported by the findings of the current case series of “exercising” individuals with IBD who reported that low- to moderate-intensity exercise (most commonly walking) had a positive effect on their mood, fatigue, weight maintenance, and osteoporosis. Overexertion was reported as a potential problem. Scant advice regarding exercise had been given by their healthcare professionals according to participants. The current literature and findings of this small case series suggest that exercise is likely to be beneficial and safe for individuals with IBD. However, more research is required on which recommendations for exercise could be based.
T
here is some supportive evidence that exercise is beneficial for individuals with inflammatory bowel disease (IBD) (Martin, 2011). However, people with IBD experience considerable barriers to exercise, including the unpredictReceived April 28, 2012; accepted August 2, 2012. About the authors: Indira Nathan, PhD, BSc (Hons), SRD, is Research Associate, Centre for Gastroenterology and Nutrition, University College London, London, England. Christine Norton, PhD, MA, RN, is Florence Nightingale Professor of Clinical Nursing Research, King's College London, Florence Nightingale School of Nursing and Midwifery, London, England. Wladyslawa Czuber-Dochan, MSc, PGPD, RN, RNT, is PhD Research Fellow, King’s College London, Florence Nightingale School of Nursing and Midwifery, London, England. Alastair Forbes, MD, FRCP, FHEA, is Professor of Gastroenterology and Clinical Nutrition, University College London and University College London Hospital, Department of Gastroenterology, London, England. Supplemental digital content is available for this article. Direct URL citations appear in the printed text and is provided in the HTML and PDF versions of this article on the journal’s Web site (http://www .gastroenterologynursing.com). This study has received funding from the Big Lottery Fund and is commissioned by Crohn's and Colitis UK. The authors declare no conflict of interest. Correspondence to: Indira Nathan, PhD, BSc (Hons), SRD, Centre for Gastroenterology and Nutrition, Rockefeller Building, University College London, Gower St., London WC1 6BT, England (i.shanmuganathan@ ucl.ac.uk). DOI: 10.1097/SGA.0000000000000005
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able fluctuating nature of the disease and its symptoms such as pain, fatigue, and fear of fecal incontinence. There are currently no evidence-based guidelines for this group of patients that take such factors into consideration. Development of a practical physical activity protocol that can be recommended in routine clinical practice is a research priority (Chey & Rai, 2011). This article, by means of a literature review supplemented with qualitative data from a small case series, aims to explore the issues to be considered by clinicians when advising patients with IBD to increase exercise.
Methods Literature Review A selective review of evidence on exercise for IBD up to November 2011 (MEDLINE, EMBASE, CINAHL, and Cochrane data bases) was initiated. The search for articles on IBD was based on the search strategy used by the National Health Service (2011) evidence gastroenterology and liver disease specialist project team for the annual evidence update on IBD. This was combined for exercise using the following search terms: “exercise,” “exercise therapy,” and “exercise tolerance.”
Case Series Participants were a sample of convenience who were interviewed during pilot work for a larger study 437
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screening IBD clinic attenders who might benefit from increasing exercise. These were people who were already reporting regular exercise. A sample of adults with IBD who reported themselves as “exercising” (n = 11) were purposively selected and interviewed regarding their exercise history prior to diagnosis, current exercise activity levels, and any benefits and difficulties experienced. They were also asked to recall any advice received about exercise from healthcare professionals since their first diagnosis, what information they would find helpful, and what advice they would give other IBD patients wishing to start exercising. Current activity levels were determined using the Godin Leisure-Time Exercise Questionnaire (GLTEQ), and a Leisure Score Index was calculated (Godin & Shephard, 1985). The GLTEQ has four questions that measure self-reported leisure time exercise habits. The first three items measure weekly frequencies of “strenuous,” “moderate,” and “light” activities for periods of 15 minutes or more. These items are multiplied by 9, 5, and 3, respectively, and then summed to give the Leisure Score Index. The fourth item assesses frequency of weekly leisure time activities of sufficient intensity to “work up a sweat.” There is a choice of three responses: “never,” “sometimes,” or “often.”
Findings Literature Review Current Guidelines for Exercise for IBD Current guidelines provide only scant guidance on exercise for individuals with IBD. There are general guidelines for IBD patients in relation to osteoporosis that address exercise. These British Society of Gastroenterology guidelines state that it is difficult to make precise recommendations for exercise in relation to bone health; however, they advise that at least minimal activity should be encouraged and that active sports should give additional benefit (Scott, Gaywood, & Scott, 2000). Recent UK nationwide guidelines for exercise in the general population include reference to vigorous activity and resistance exercise (UK Department of Health, 2011). The suitability for this in individuals with IBD is unknown. This expert panel recommended that the United Kingdom as a priority “should establish a process to develop physical activity guidelines for adults, children, and young people with noncommunicable disease.”
Potential Benefits of Exercise Studies of exercise in individuals with IBD have reported that exercise is well tolerated (D’Inca et al., 1999;
Loudon, Corroll, Butcher, Rawsthorne, & Bernstein, 1999; Ng, Millard, Lebrun, & Howard, 2007). A small study (n = 6) found that males with Crohn disease were able to cycle for 1 hour at 60% of oxygen consumption with no adverse effect (D’Inca et al., 1999). A 12-week walking program elicited psychological benefits (Loudon et al., 1999); however, this was a small uncontrolled pilot study (n = 12). Improvements in quality of life were found in patients with Crohn disease following a 3-month low-grade walking program that required walking three times a week at 60% of maximum heart rate (Ng, Millard, Lebrun, & Howard, 2006). The patients were in remission or with mild disease activity and included a control group (n = 16) and an exercise group (n = 16). There is some limited evidence from randomized controlled trials that exercise improves the symptoms of irritable bowel syndrome (IBS) (Daley et al., 2008; Johannesson, Simren, Strid, Bajor, & Sadik, 2011). This suggests that increasing exercise may be beneficial for individuals with IBD who also report IBS-type symptoms. It has been suggested that low to moderate activity is safe (Martin, 2011; Packer, 2010) and in general individuals with IBD should benefit from (Narula & Fedorak, 2008) and increase exercise (Cosnes, 2010; Martin, 2011; McGowan, Jones, Long, & Barritt, 2012). The benefits of exercise have been recognized in cancer survivors: recent guidelines on exercise for cancer survivors indicate that advice to rest is unhelpful and that in general, all patients with cancer should undertake physical activity, individually tailored depending on their ability (Schmitz et al., 2010). However, it is unclear whether, and to what extent, this advice can be extrapolated to individuals with IBD. Exercise may help prevent comorbidities in IBD patients; for example, exercise is recommended for the general population to reduce the risk of colon cancer (Sellar & Courneya, 2011). It has been estimated using a modeling approach that 5.3% of cases of colon cancer diagnoses in the United Kingdom in 2010 were due to suboptimal levels of activity in 2000 (Parkin, 2011). It has also been suggested that the effect of inactivity may be greater in women (de Vries et al., 2010). The effect of exercise on the risk of colon cancer in patients with IBD has not been studied but could be of particular importance as a preventative factor in this higher risk group. However, it is not known whether exercise would have any effect on cancer risk in IBD. The UK Department of Health guidelines recommend resistance training for the general population (UK Department of Health, 2011). This type of exercise may particularly benefit the IBD population in whom corticosteroid use and intermittent periods of
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inactivity as a result of active disease may impair muscle mass (Fletcher et al., 1996; Jahnsen, Falch, Mowinckel, & Aadland, 2003) and bone health (Scott et al., 2000; Valentini et al., 2008). Similarly, sarcopenia (involuntary loss of muscle mass) is common in IBD patients and it has been suggested that physical activity may help improve muscle mass and function (Schneider et al., 2008). A program of resistance training for patients with short bowel syndrome was reported to increase lean body mass. An increase in energy intake of approximately 15% was also reported, so resistance exercise may provide a useful therapy for improving nutritional status (Araujo, Suen, Marchini, & Vannucchi, 2008). Studies in animal models have suggested a possible impact of exercise on the immune system (Cook, 2011). It has been documented that for the patient with IBD, exercise may reduce disease activity (Packer, 2010). However, research in this area is at an early stage and limited evidence exists to draw any final conclusions.
Potential Harms of Exercise It has been suggested that clinicians may be reluctant to prescribe exercise because of the fear of symptom exacerbation (Ng et al., 2007); however, there are no studies in IBD patients to support this concern. Although anecdotal evidence suggests that some patients with IBD successfully compete in high-level competitive sport and endurance events (e.g., marathon running and rowing), there is a dearth of information regarding the impact on health. When considering high-intensity exercise, extrapolation of results from endurance athletes supports the need for a cautious approach for the IBD patient. For the healthy athlete, marathon runners’ diarrhea is well recognized and common (Sullivan & Wong, 1992). This is something that individuals with IBD would particularly want to avoid. In a small study (n = 12) of endurance athletes, all complaining of gastrointestinal symptoms (commonly abdominal cramps and the urge to defecate), gastric ischemia was found in all athletes exercising at maximal intensity and in 50% at submaximal exercise (ter Steege, Geelkerken, Huisman, & Kolkman, 2012). It is unclear why only some individuals present with gastrointestinal symptoms during high-intensity exercise. Successful management of symptoms was achieved by reducing exercise intensity for a few months, then gradually increasing this to resume previous levels. For patients with IBD, there have been reports of reduced exercise capacity in children (Ploeger et al., 2011) and reduced muscle strength in adults (Wiroth et al., 2005). Following bowel surgery, there is some evidence that exercise capacity is reduced in VOLUME 36 | NUMBER 6 | NOVEMBER/DECEMBER 2013
proportion to the length of bowel resected (Brevinge et al., 1995).
Case Series The majority of interviewees had Crohn disease (n = 10). One patient had ulcerative colitis and three of 11 patients had a stoma (six females and five males). A summary of the data is presented in Supplemental Digital Content Table 1 (available at: http://links.lww.com/GNJ/A24).
Types of Exercise The GLTEQ indicated that exercise was predominantly of low intensity (6 of 11 patients), with only 3 of 11 individuals reporting “often” doing exercise of intensity to “work up a sweat.” Aerobic exercise was the most common type of exercise undertaken (11/11 patients). There was some interest in resistance exercise; a small number of the patients were doing resistance exercise regularly (2 of 11 patients). A high proportion reported a history of previous involvement in sport (7 of 11 patients). Walking was the most common type of exercise (8 of 11 patients). Other activities included water-skiing (1 of 11 patients) competitive football (2 of 11 patients), running (1 of 11 patients), swimming (3 of 11 patients), cycling (3 of 11 patients), Wii Fit (1 of 11 patients), karate (1 of 11 patients), and yoga (2 of 11 patients). There was little gym-based exercise (1 of 11 patients). One individual was particularly dissatisfied with gymbased exercise: “Gyms are obsessed with weight reduction and can’t advise for people trying to gain or maintain a healthy weight.” Another patient reported that she struggled and then gave up a morning exercise class, as on a regular basis, her diarrhea was worst at this time.
Benefit of Exercise Benefits reported frequently included improvement in mood and a “feel good factor” (seven of 11 patients). Individuals described feeling “run down” if they did not exercise. Exercise was reported to help with fatigue (4 of 11 patients). Individuals said that exercise made them feel “fatigued but energized,” and helped with “lethargy” and “tiredness.” The effect of exercise was a “good kind of tiredness.” Exercise “increased appetite” and “helped with weight gain” (1 of 11 patients). Wanting to lose weight was also a reason for exercising (2 of 11 patients). Exercise as a prevention or treatment for osteoporosis was reported (2 of 11 patients). One patient who had received advice from a physical therapist regarding resistance exercise at home followed this advice and on a regular basis made use of 439
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tins of food to provide a measured weight, also using her wall for press-ups. Those who were members of clubs or groups enjoyed the social interaction and valued the camaraderie. The fact that “other members understand” their IBD was important.
Problems Encountered Patients described overexerting themselves (three of 11 patients) and suffering the next day with a feeling described as being “wiped out.” One man did report “nearly drowning” when trying to swim soon after a flare-up believing that swimming “is good for you.”
Current Exercise Patients reported that they determine their own amount, type, and intensity of exercise. When asked how they determine how much exercise to do, the replies included “as much as I could do” and “keep going until I run out of energy.” One person used a heart-rate monitor and struggled to keep the heart rate in what they calculated as their “training zone.”
Advice Received by Patients Six patients reported having received no advice from healthcare professionals regarding exercise (6 of 11 patients). Advice received included minimal reference to health benefits or how this might be achieved. Patients had repeatedly been advised to limit exercise in the abdominal area after surgery (3 of 11 patients), but then following recovery, and in fact years after this, no further advice had been given. The only advice received by one patient was to rest. There was also uncertainty about advice for resistance exercise (two of seven patients), the use of weights, and what encompassed “weight bearing” exercise. Three of the patients had a stoma and had varied experiences and amounts of information given regarding swimming and other aspects of daily living. Encouragingly, one lady reported “invaluable help” from a stoma nurse regarding clothing and all aspects of managing daily activities; she swam routinely. Others had received less advice (two of three patients with a stoma), particularly with regard to swimming and swimwear and this was having an impact on physical activity undertaken; for example, “I just didn’t go in the sea.”
Patient-Suggested Recommendations for Exercise All 11 exercising patients felt that exercise was beneficial and that “both children and adults with IBD should be encouraged to exercise.” Those who had negative experiences of exercise as a result of “trying to do too much” specifically recommended a step-bystep approach to increasing exercise. Patients frequently
reported adopting a strategy of adjusting activity level depending on how they felt (five of 11 patients). In the clinical setting, patients welcomed the opportunity to talk about their experience of exercise and were keen to offer information that might assist nonexercising IBD patients. It was suggested that “it would be good if the hospital offered an exercise class for people with mobility difficulties.”
Discussion Specific considerations for the appropriate level of activity for patients with “mild,” “moderate,” and “active” IBD have not been addressed in the literature. A population-based study of Canadians living with Crohn disease and ulcerative colitis found that only one in four individuals were engaged in sufficient selfreported leisure time physical activity to achieve likely health benefits (Mack, Wilson, Gilmore, & Gunnell, 2011). The most common activities reported were walking and gardening with a notable lack of involvement in “structured” physical activity. A significantly lower proportion of the population with Crohn disease (17.9%) and ulcerative colitis (21%) were classified as physically “active” compared with the control population who did not report IBD (24.1%); however, no measure of disease activity was given. Current practice suggests that during active disease, IBD patients have a reduced capacity for exercise and self-limit their activity; however, there is no evidence to suggest that total rest is advisable. With respect to exercise when IBD is in remission, the evidence is similarly sparse. There is minimal information about exercise capacity and effect of increasing activity on fitness levels and health status. Anemia is common in IBD (Lomer, 2011), and it has been reported that anemia reduces exercise capacity (Haas & Brownlie, 2001). There is no evidence to show whether optimizing the iron status of patients with IBD improves exercise capacity. There are few intervention studies of exercise in IBD patients (D’Inca et al., 1999; Loudon et al., 1999; Ng et al., 2007). Overall, there is little evidence to indicate that exercise is risky for patients with IBD. Experiences of our small sample of “exercising” IBD patients suggest that if they take care to avoid overexerting themselves and exercise at their own level, exercise is safe.
Conclusions The reviewed literature highlights the need for further research in exercise and IBD and the need for standardized reporting of exercise programs to enable evaluation and implementation of research results. If guidelines are to be evidence-based, there is a need for rapid expansion of research in this area. This lack of evidence contributes to the cautious approach taken by
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healthcare professionals. Patients with IBD should not miss out on what has been described recently as “the indisputable” benefits of exercise in relation to treatment and prevention of disease (Khan, Weiler, & Blair, 2011); neither should inactivity in this patient group contribute to an increased prevalence of obesity and osteoporosis. However, barriers to exercise in the IBD population have not been studied. The present nonspecific and ad hoc advice regarding physical activities is unlikely to alter the status quo for the sedentary IBD population. According to our interviewees, healthcare professionals are giving vague advice regarding exercise and there is confusion among both clinicians and patients as to what is appropriate. To enable patients to vary exercise levels according to their disease activity, effects of medication, and severity of symptoms, there is a need to test individually prescribed exercise for the patient with IBD. ✪
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