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Exercise on bipolar disorder in humans
CHAPTER SEVEN
Exercise on bipolar disorder in humans Kangguang Lin*, Tao Liu Department of Mood Disorders, The Affiliated Brain Hospital of Guangzhou Medical University, Guangzhou, China *Corresponding author: e-mail address: [email protected]
Contents 1. Sedentary behavior and physical activity in patients with BD 2. Effects of exercise on BD patients 3. Barriers and facilitators for exercise in patients with BD References
190 191 194 195
Abstract People with Bipolar disorder (BD) often have a sedentary lifestyle and low level of physical activity which in part contribute to the high co-occurrence of medical diseases including cardiovascular disease, type 2 diabetes, and metabolic syndrome, etc. Exercise especially aerobic exercise may be beneficial not only to mental health but also physical health outcomes. Targeting barriers for exercise such as high BMI and making the best use of facilitators (e.g., concept of fitness) can result in higher levels of exercise engagement in people with BD.
Bipolar disorder (BD) is a major disabling mental disease characterized by episodes of mania and depression. It has been ranked as one of the 20 leading medical causes of disability (Lima, Peckham, & Johnson, 2018) and its standardized mortality ratios is 2–3 times as high as the general population (Crump, Sundquist, Winkleby, & Sundquist, 2013; Lomholt et al., 2019). BD is commonly comorbid with chronic somatic diseases, such as cardiovascular disease, diabetes, obesity and metabolic syndrome (Chauvet-Gelinier, Gaubil, Kaladjian, & Bonin, 2012), with the most common being cardiovascular diseases (Kessing, Vradi, McIntyre, & Andersen, 2015). Comorbid somatic diseases in return can lead to increased likelihood of suicide risk, anxiety disorder, and rapid cycling mood episodes, resulting in worse prognosis and decreased life expectancy (Forty et al., 2014). It is estimated that patients with BD, and including patients with major International Review of Neurobiology, Volume 147 ISSN 0074-7742 https://doi.org/10.1016/bs.irn.2019.07.001
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depressive disorder or schizophrenia, die prematurely up to 25 years due to comorbid somatic diseases (Parks, Svendsen, Singer, Foti, & Mauer, 2006). For cardiovascular diseases, type 2 diabetes, and all-cause mortality, low levels of physical activity and sedentary behavior (e.g., sitting or lying down during waking hours) are independent risk factors of mortality that are modifiable. Exercise has been suggested to be an effective intervention on the physical conditions that are often comorbid with BD, including cardiovascular disease, type 2 diabetes, obesity, and metabolic syndrome (Aune, Norat, Leitzmann, Tonstad, & Vatten, 2015; Chin, Kahathuduwa, & Binks, 2016; Lanier, Bury, & Richardson, 2016). For instance, exercise works equally effectively as medications in reducing mortality rate in patients with cardiovascular disease (Naci & Ioannidis, 2015). Moreover, exercise has protective effects against increased incidence for depressive symptoms or major depression (Schuch et al., 2018). And it can alleviate depressive symptoms of patients with postpartum depression (Nakamura et al., 2019), patients with Parkinson’s disease (Wu, Lee, & Huang, 2017) and people of the general population (Harvey et al., 2018; Northey, Cherbuin, Pumpa, Smee, & Rattray, 2018). This chapter reviews evidence of the effects of exercise on BD patients. Before doing so, we first describe exercise and physical activity in patients with BD. Then we discuss the barriers and facilitators for exercise in patients with BD.
1. Sedentary behavior and physical activity in patients with BD Patients with BD more than often engage in sedentary behavior and have low levels of physical activity. Over 50% patients with BD reported a sedentary lifestyle in self-rated questionnaires (Kilbourne et al., 2007). It is estimated that patients with BD spend average 615 min per day on sedentary behavior, even more serve than patients with schizophrenia and patients with major depressive disorder (493 min per day and 414 min per day, respectively) (Vancampfort et al., 2017). Daily time spent on sedentary behavior is longer when measured by objective measures compared to self-reported ones (Vancampfort et al., 2016). Patients with BD often fail to meet the physical activity guideline (i.e., 150 min per week at the intensity of at least moderate level) ( Janney et al., 2014). One meta-analysis study estimated the time patients with severe mental illness (SMI) including BD
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engaged in moderate physical activity was on average of 3.5 h per day less than healthy controls (Vancampfort et al., 2016). In general, BD patients may be less likely engaging in moderate/vigorous physical activity. Different mood phases or states (i.e., depressive, manic and euthymic states) are in close relations with physical activity (Gershon, Ram, Johnson, Harvey, & Zeitzer, 2016). Motor slowness or retardation is often seen in a major depressive episode, a depressive syndrome lasting at least 2 weeks. While increased activity is considered as a core criterion for hypo/manic episode. Yet it is unclear their causal relationships. Perhaps for some patients, elevated mood may motivate them to execute an exercise plan. Nevertheless, for others, vigorous exercise is in complex association with hypo/manic symptoms (Thomson et al., 2015). Relative to patients with schizophrenia or major depressive disorder, BD patients may be more likely engaging in moderate or vigorous exercise and longer (Vancampfort et al., 2017). At the same time, patients with BD could be the most sedentary group. Sedentary behavior is independent of physical activity and associated with poorer cognition (Depp, Dev, & Eyler, 2016) that are affected in different degrees in BD patients. In addition, patterns of motor activity may be different across different types of BD. During the same euthymic state, a state where patients are emotionally stable for a certain period of time (e.g., 3 months), patients with bipolar type I had greater variability in motor activity in the afternoon and patients with bipolar type II in the night time as opposed to healthy controls (Shou et al., 2017). Exercise tolerance perhaps is reduced in patients with BD. One study arranged 24 patients with BD to exercise on a treadmill. They were asked to run at the 70% of maximal oxygen consumption until they felt too exhausted to continue. The result showed that BD patients performed significantly worse than healthy controls, with approximately 20 min shorter (Shah et al., 2007). And foot and back pain are important negative predictors of functional exercise capacity in patients with BD (Vancampfort et al., 2015).
2. Effects of exercise on BD patients Exercise is an effective non-pharmaceutical treatment for depression, particularly recommended for mild/moderate depression (Knapen, Vancampfort, Morie¨n, & Marchal, 2015; Stubbs et al., 2018). However, the evidence of effectiveness of exercise on BD is limited. Despite this, there are a few clinical studies that help clinicians to recommend exercise to patients with BD (Table 1). In a retrospective cohort study
Table 1 Details of the included studies on physical activity in patients with bipolar disorder. Intervention Authors Study design Participants components Assessed outcomes
Ng, Dodd, and Berk (2007)
Retrospective cohort study
Adults; ICD-10; n ¼ 98 (Intervention: 24, non-participants: 24)
Walking, 24 months
Effect sizes
• Participants had lower DASS score
• Participants had lower DASS subscales (depression, anxiety, stress)
Sylvia, Nierenberg, Stange, Peckham, and Deckersbach (2011)
Self-controlled study
Sylvia, Salcedo, et al. (2013)
Self-controlled study
Adults; MINI Plus, BDI (83%); n ¼ 6 (Intervention)
NEW Tx, 14 weeks
• Reduce in weight
0.13
• Reduce in MADRS
0.42
score Adults; MINI Plus, BDI (80%); n ¼ 5 (Intervention)
NEW Tx, 20 weeks
• Reduce in weight
0.59
• Increase in exercise
2.00
duration Sylvia et al. (2019)
Randomized control trial and self-controlled study
Adults; MINI Plus, BDI (84.2%), NEW Tx, 20 weeks BDII (15.8%); n ¼ 38 (Intervention: 19, control: 19)
Change in invention group
0.80
• Reduce in CGI-BP: depression
• Reduce in CGI-BP:
1.74
overall severity
• Increase in overall
0.75
functioning ICD, International Statistical Classification of Diseases and Related Health Problems; MINI, Mini International Neuropsychiatric Interview; BD, bipolar disorder; NEW Tx, Nutrition Exercise and Wellness Treatment; DASS, Depression Anxiety Stress Scales; MADRS, Montgomery Asberg Depression Rating Scale; CGI-BP, Clinical Global Impression Scale-Bipolar Version.
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of small sample size by Ng et al. (2007), walking exercise (i.e., walking for 40 min per day) was added as an adjunctive treatment for BD patients during an acute phase when admitted to a private psychiatric unit. Those who attended the exercise sections were significantly improved in depressive and anxious symptoms and felt less stressful than those who did not. In several studies by Sylvia et al. (2011, 2019) and Sylvia, Salcedo, et al. (2013) from Massachusetts General Hospital who developed an operational program, called the Nutrition, Exercise, and Wellness treatment (NEW Tx), its goal was to help individuals with BD adopt an healthy lifestyle. To this end, the project is designed to include three elements: eat nutritiously, promote weekly exercise, and adopt other healthy habits (i.e., sleep hygiene and stop smoking/substance use). Participants who participated in the NEW Tx were satisfied with the treatments and had improvements in depressive symptoms and overall functioning. Importantly, they tripled their amount of exercise which maybe in large part contributed to the declines in weight, cholesterol, and triglycerides after 20 weeks of follow-up. These findings suggest that exercise combined with other lifestyle changes is beneficial to the well-being of individuals with BD. We recently conducted an aerobic exercise trial (i.e., running at moderate intensity, 30 min per day, 4 times a week, lasting for 3 months) in adolescents who manifested subthreshold depressive or hypomanic symptoms that fall short of the official BD diagnostic criteria. Participants were randomized to the exercise intervention or psycho-education controlled arm. Though we do not find significant improvement in clinical symptoms including depressive and hypomanic symptoms, there are positive effects of exercise on the brain structures. Adolescent who are in the exercise group show increased gray matter volumes in the orbitofrontal cortex and increased cortical thickness in the rostral anterior cingulate cortex that are involved in mood regulation and social functioning. The changes of the brain structures are correlated with the changes in emotion and cognitive functioning. These preliminary results are promising as it seems that exercise may benefit not only mental health in individuals with BD but it positively affects brain development in adolescents with subthreshold syndromes. This arena clearly is under-investigated and the findings need to replicate. The negative impact of exercise in individuals with BD is unclear. A study by Wright, Armstrong, Taylor, and Dean (2012) concerned its detrimental potential in exacerbating hypo/manic symptoms. This is a crosssectional observational study that asks 25 BD patients’ view on the relations
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of exercise with BD. The relations are complex. They showed that some individuals became more active following exercise while others thought exercise had a calming effect on hypomanic symptoms. More research on this topic is needed, particularly on different mood states. Increasing evidence shows that acute exercise can lead to complex biological changes in the brain, including reduced cerebral blood flow (CBF) and decreased level of brain-derived neurotrophic factor (BDNF), a protein that has potent effects in promoting the survival of nerve cells (e.g., neurons) (Kucyi, Alsuwaidan, Liauw, & McIntyre, 2010), in BD patients (MacIntosh et al., 2017; Metcalfe et al., 2016; Schuch et al., 2015; Subramaniapillai et al., 2016). Using CBF magnetic resonance images (MRI) technique, MacIntosh et al. (2017) found that following 20 min of acute exercise of bicycle ergometer, individuals with BD had more exercise-related decrease in CBF in the medial frontal cortex as opposed to health controls. Moreover, in adolescent with BD, exercise could cancel off the correlations of activation levels in the bilateral accumbens during an executive task with depressive symptoms (Metcalfe et al., 2016). This finding suggests that exercise may alleviate depressive symptoms by having an impact on the accumbens in individuals with BD when loaded with cognitive task, a sub-cortical region that plays a key role in the “reward circuit” of the brain (Kupchik & Kalivas, 2017). Furthermore, serum level of BDNF is reported to be increased in female individuals with BD following a single section of exercise of bicycle ergometer at a vigorous level (i.e., 95% maximum heart rate (220-age), 1.15 respiratory exchange rate, or both) (Schuch et al., 2015). These studies may indicate potential mechanisms by which exercise impacts on our body and the brain in particular.
3. Barriers and facilitators for exercise in patients with BD To better promote exercise, it is important to know the barriers and facilitators for exercise among patients with BD. Research in this area is largely on demographics and clinical characteristics of patients with BD. The barriers included older age, high body mass index (BMI), low educational status, social isolation and financial strains. Older patients with SMI reported lower exercise level than their counterpart (Muralidharan, Klingaman, Molinari, & Goldberg, 2018). Older age predicates lower exercise levels in BD (Vancampfort et al., 2016). In fact, older BD patients are more likely to be commorbid with medical conditions such as cardiovascular diseases that limit their mobility, which harms their ability and/or will to
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engage in or sustain exercise (Vancampfort et al., 2013). Second, Higher BMI is associated with lower exercise levels in individuals with BD (Sylvia, Friedman, et al., 2013; Vancampfort et al., 2013, 2016). Third, social and cultural factors including unemployment, lower educational status, and financial strains are not specific barriers to individuals with BD (Vancampfort et al., 2017), which should be taken into account when designing physical activity program. Finally, severe symptoms, poor global function, illness duration, and medication use all have negative impacts on the physical activity levels of individuals with BD (Melo et al., 2019; Pereira, Padoan, Garcia, Patusco, & Magalha˜es, 2019; Sylvia, Friedman, et al., 2013; Vancampfort et al., 2017). Weight loss is the primary incentive reported by individuals with SMI for engaging in exercise (Firth et al., 2016), which is also the motivating factor endorsed by the general population (Sherwood & Jeffery, 2000). The endorsement of “fitness” as an incentive that is readily improved (Vancampfort et al., 2016) can be serve as a vehicle not only for promoting mental health but also for reducing amendable risk factors for metabolicrelated disease (Hu et al., 2005). To make the best use of the “fitness” perception, physical promotion program should maximize exercise uptake in this clinical population. Moreover, the view that exercise can reduce stress and enhance mood is endorsed by many people with SMI (Rosenbaum, Tiedemann, Sherrington, Curtis, & Ward, 2014). Furthermore, many patients claim that professional support (e.g., exercise supervision) can motivate them to exercise more (Carpiniello, Primavera, Pilu, Vaccargiu, & Pinna, 2013). It also can benefit better adherence to physical activity and has larger beneficial effects on cardiorespiratory fitness (Stubbs, Rosenbaum, Vancampfort, Ward, & Schuch, 2016). With adequate support including exercise supervision and social support, they may feel more confident in overcoming the barriers for exercise (Firth et al., 2016; Pereira et al., 2019; Soundy et al., 2014). There are woven relationships among the factors described. For instance, individuals with BD who is motivated by weight loss tend to exercise more, are more likely to be symptom-free and employed, which in turn promote social support, and vice versa.
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Chauvet-Gelinier, J. C., Gaubil, I., Kaladjian, A., & Bonin, B. (2012). Bipolar disorders and somatic comorbidities: A focus on metabollic syndrome, diabetes and cardiovascular disease. Encephale, 38, 167–172. Chin, S. H., Kahathuduwa, C. N., & Binks, M. (2016). Physical activity and obesity: What we know and what we need to know. Obesity Reviews, 17, 1226–1244. Crump, C., Sundquist, K., Winkleby, M. A., & Sundquist, J. (2013). Comorbidities and mortality in bipolar disorder: A Swedish national cohort study. JAMA Psychiatry, 70, 931–939. Depp, C. A., Dev, S., & Eyler, L. T. (2016). Bipolar depression and cognitive impairment: Shared mechanisms and new treatment avenues. The Psychiatric Clinics of North America, 39, 95–109. Firth, J., Carney, R., Jerome, L., Elliott, R., French, P., & Yung, A. R. (2016). The effects and determinants of exercise participation in first-episode psychosis: A qualitative study. BMC Psychiatry, 16, 36. Forty, L., Ulanova, A., Jones, L., Jones, I., Gordon-Smith, K., Fraser, C., et al. (2014). Comorbid medical illness in bipolar disorder. The British Journal of Psychiatry, 205, 465–472. Gershon, A., Ram, N., Johnson, S. L., Harvey, A. G., & Zeitzer, J. M. (2016). Daily Actigraphy profiles distinguish depressive and interepisode states in bipolar disorder. Clinical Psychological Science: A Journal of the Association for Psychological Science, 4, 641–650. Harvey, S. B., Øverland, S., Hatch, S. L., Wessely, S., Mykletun, A., & Hotopf, M. (2018). Exercise and the prevention of depression: Results of the HUNT cohort study. The American Journal of Psychiatry, 175, 28–36. Hu, G., Jousilahti, P., Barengo, N. C., Qiao, Q., Lakka, T. A., & Tuomilehto, J. (2005). Physical activity, cardiovascular risk factors, and mortality among Finnish adults with diabetes. Diabetes Care, 28, 799–805. Janney, C. A., Fagiolini, A., Swartz, H. A., Jakicic, J. M., Holleman, R. G., & Richardson, C. R. (2014). Are adults with bipolar disorder active? Objectively measured physical activity and sedentary behavior using accelerometry. Journal of Affective Disorders, 152–154, 498–504. Kessing, L. V., Vradi, E., McIntyre, R. S., & Andersen, P. K. (2015). Causes of decreased life expectancy over the life span in bipolar disorder. Journal of Affective Disorders, 180, 142–147. Kilbourne, A. M., Rofey, D. L., McCarthy, J. F., Post, E. P., Welsh, D., & Blow, F. C. (2007). Nutrition and exercise behavior among patients with bipolar disorder. Bipolar Disorders, 9, 443–452. Knapen, J., Vancampfort, D., Morie¨n, Y., & Marchal, Y. (2015). Exercise therapy improves both mental and physical health in patients with major depression. Disability and Rehabilitation, 37, 1490–1495. Kucyi, A., Alsuwaidan, M. T., Liauw, S. S., & McIntyre, R. S. (2010). Aerobic physical exercise as a possible treatment for neurocognitive dysfunction in bipolar disorder. Postgraduate Medicine, 122, 107–116. Kupchik, Y. M., & Kalivas, P. W. (2017). The direct and indirect pathways of the nucleus accumbens are not what you think. Neuropsychopharmacology, 42, 369–370. Lanier, J. B., Bury, D. C., & Richardson, S. W. (2016). Diet and physical activity for cardiovascular disease prevention. American Family Physician, 93, 919–924. Lima, I. M. M., Peckham, A. D., & Johnson, S. L. (2018). Cognitive deficits in bipolar disorders: Implications for emotion. Clinical Psychology Review, 59, 126–136. Lomholt, L. H., Andersen, D. V., Sejrsgaard-Jacobsen, C., Øzdemir, C. M., Graff, C., Schjerning, O., et al. (2019). Mortality rate trends in patients diagnosed with schizophrenia or bipolar disorder: A nationwide study with 20 years of follow-up. International Journal of Bipolar Disorders, 7, 6.
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MacIntosh, B. J., Shirzadi, Z., Scavone, A., Metcalfe, A. W., Islam, A. H., Korczak, D., et al. (2017). Increased cerebral blood flow among adolescents with bipolar disorder at rest is reduced following acute aerobic exercise. Journal of Affective Disorders, 208, 205–213. Melo, M. C. A., Garcia, R. F., de Arau´jo, C. F. C., Rangel, D. M., de Bruin, P. F. C., & de Bruin, V. M. S. (2019). Physical activity as prognostic factor for bipolar disorder: An 18-month prospective study. Journal of Affective Disorders, 251, 100–106. Metcalfe, A. W., MacIntosh, B. J., Scavone, A., Ou, X., Korczak, D., & Goldstein, B. I. (2016). Effects of acute aerobic exercise on neural correlates of attention and inhibition in adolescents with bipolar disorder. Translational Psychiatry, 6, e814. Muralidharan, A., Klingaman, E. A., Molinari, V., & Goldberg, R. W. (2018). Perceived barriers to physical activity in older and younger veterans with serious mental illness. Psychiatric Rehabilitation Journal, 4, 67–71. Naci, H., & Ioannidis, J. P. (2015). Comparative effectiveness of exercise and drug interventions on mortality outcomes: Metaepidemiological study. British Journal of Sports Medicine, 49, 1414–1422. Nakamura, A., van der Waerden, J., Melchior, M., Bolze, C., El-Khoury, F., & Pryor, L. (2019). Physical activity during pregnancy and postpartum depression: Systematic review and meta-analysis. Journal of Affective Disorders, 246, 29–41. Ng, F., Dodd, S., & Berk, M. (2007). The effects of physical activity in the acute treatment of bipolar disorder: A pilot study. Journal of Affective Disorders, 101, 259–262. Northey, J. M., Cherbuin, N., Pumpa, K. L., Smee, D. J., & Rattray, B. (2018). Exercise interventions for cognitive function in adults older than 50: A systematic review with meta-analysis. British Journal of Sports Medicine, 52, 154–160. Parks, J., Svendsen, D., Singer, P., Foti, M., & Mauer, B. (2006). Morbidity and mortality in people with serious mental illness. National Association of State Mental Health Program Directors. Pereira, C. S., Padoan, C. S., Garcia, L. F., Patusco, L., & Magalha˜es, P. V. S. (2019). Barriers and facilitators perceived by people with bipolar disorder for the practice of exercise: A qualitative study. Trends Psychiatry Psychotherapy, 41, 1–8. Rosenbaum, S., Tiedemann, A., Sherrington, C., Curtis, J., & Ward, P. B. (2014). Physical activity interventions for people with mental illness: A systematic review and metaanalysis. The Journal of Clinical Psychiatry, 75, 964–974. Schuch, F. B., da Silveira, L. E., de Zeni, T. C., da Silva, D. P., Wollenhaupt-Aguiar, B., Ferrari, P., et al. (2015). Effects of a single bout of maximal aerobic exercise on BDNF in bipolar disorder: A gender-based response. Psychiatry Research, 229, 57–62. Schuch, F. B., Vancampfort, D., J1, F., Rosenbaum, S., PB1, W., Silva, E. S., et al. (2018). Physical activity and incident depression: A meta-analysis of prospective cohort studies. The American Journal of Psychiatry, 175, 631–648. Shah, A., Alshaher, M., Dawn, B., Siddiqui, T., Longaker, R. A., Stoddard, M. F., et al. (2007). Exercise tolerance is reduced in bipolar illness. Journal of Affective Disorders, 104, 191–195. Sherwood, N. E., & Jeffery, R. W. (2000). The behavioral determinants of exercise: Implications for physical activity interventions. Annual Review of Nutrition, 20, 21–44. Shou, H., Cui, L., Hickie, I., Lameira, D., Lamers, F., Zhang, J., et al. (2017). Dysregulation of objectively assessed 24-hour motor activity patterns as a potential marker for bipolar I disorder: Results of a community-based family study. Translational Psychiatry, 7, e1211. Soundy, A., Freeman, P., Stubbs, B., Probst, M., Coffee, P., & Vancampfort, D. (2014). The transcending benefits of physical activity for individuals with schizophrenia: A systematic review and meta-ethnography. Psychiatry Research, 220, 11–19. Stubbs, B., Rosenbaum, S., Vancampfort, D., Ward, P. B., & Schuch, F. B. (2016). Exercise improves cardiorespiratory fitness in people with depression: A meta-analysis of randomized control trials. Journal of Affective Disorders, 190, 249–253.
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Stubbs, B., Vancampfort, D., Hallgren, M., Firth, J., Veronese, N., Solmi, M., et al. (2018). EPA guidance on physical activity as a treatment for severe mental illness: A meta-review of the evidence and position statement from the European psychiatric association (EPA), supported by the international organization of physical therapists in mental health (IOPTMH). European Psychiatry, 54, 124–144. Subramaniapillai, M., Goldstein, B. I., MacIntosh, B. J., Korczak, D. J., Ou, X., Scavone, A., et al. (2016). Characterizing exercise-induced feelings after one bout of exercise among adolescents with and without bipolar disorder. Journal of Affective Disorders, 190, 467–473. Sylvia, L. G., Friedman, E. S., Kocsis, J. H., Bernstein, E. E., Brody, B. D., Kinrys, G., et al. (2013). Association of exercise with quality of life and mood symptoms in a comparative effectiveness study of bipolar disorder. Journal of Affective Disorders, 151, 722–777. Sylvia, L. G., Nierenberg, A. A., Stange, J. P., Peckham, A. D., & Deckersbach, T. (2011). Development of an integrated psychosocial treatment to address the medical burden associated with bipolar disorder. Journal of Psychiatric Practice, 17, 224–232. Sylvia, L. G., Pegg, S. L., Dufour, S. C., Janos, J. A., Bernstein, E. E., Chang, W. C., et al. (2019). Pilot study of a lifestyle intervention for bipolar disorder: Nutrition exercise wellness treatment (NEW Tx). Journal of Affective Disorders, 250, 278–283. Sylvia, L. G., Salcedo, S., Bernstein, E. E., Baek, J. H., Nierenberg, A. A., & Deckersbach, T. (2013). Nutrition, exercise, and wellness treatment in bipolar disorder: Proof of concept for a consolidated intervention. International Journal of Bipolar Disorders, 1, 24. Thomson, D., Turner, A., Lauder, S., Gigler, M. E., Berk, L., Singh, A. B., et al. (2015). A brief review of exercise, bipolar disorder, and mechanistic pathways. Frontiers in Psychology, 6, 147. Vancampfort, D., Correll, C. U., Probst, M., Sienaert, P., Wyckaert, S., De Herdt, A., et al. (2013). A review of physical activity correlates in patients with bipolar disorder. Journal of Affective Disorders, 145, 285–291. Vancampfort, D., Firth, J., Schuch, F., Rosenbaum, S., De Hert, M., Mugisha, J., et al. (2016). Physical activity and sedentary behavior in people with bipolar disorder: A systematic review and meta-analysis. Journal of Affective Disorders, 201, 145–152. Vancampfort, D., Firth, J., Schuch, F. B., Rosenbaum, S., Mugisha, J., Hallgren, M., et al. (2017). Sedentary behavior and physical activity levels in people with schizophrenia, bipolar disorder and major depressive disorder: A global systematic review and metaanalysis. World Psychiatry, 16, 308–315. Vancampfort, D., Wyckaert, S., Sienaert, P., De Hert, M., Stubbs, B., Buys, R., et al. (2015). The functional exercise capacity in patients with bipolar disorder versus healthy controls: A pilot study. Psychiatry Research, 229, 194–199. Wright, K., Armstrong, T., Taylor, A., & Dean, S. (2012). ‘It’s a double edged sword’: A qualitative analysis of the experiences of exercise amongst people with bipolar disorder. Journal of Affective Disorders, 136, 634–642. Wu, P. L., Lee, M., & Huang, T. T. (2017). Effectiveness of physical activity on patients with depression and Parkinson’s disease: A systematic review. PLoS One, 12, e0181515.
Exercise on bipolar disorder in humans Kangguang Lin*, Tao Liu Department of Mood Disorders, The Affiliated Brain Hospital of Guangzhou Medical University, Guangzhou, China *Corresponding author: e-mail address: [email protected]
Contents 1. Sedentary behavior and physical activity in patients with BD 2. Effects of exercise on BD patients 3. Barriers and facilitators for exercise in patients with BD References
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Abstract People with Bipolar disorder (BD) often have a sedentary lifestyle and low level of physical activity which in part contribute to the high co-occurrence of medical diseases including cardiovascular disease, type 2 diabetes, and metabolic syndrome, etc. Exercise especially aerobic exercise may be beneficial not only to mental health but also physical health outcomes. Targeting barriers for exercise such as high BMI and making the best use of facilitators (e.g., concept of fitness) can result in higher levels of exercise engagement in people with BD.
Bipolar disorder (BD) is a major disabling mental disease characterized by episodes of mania and depression. It has been ranked as one of the 20 leading medical causes of disability (Lima, Peckham, & Johnson, 2018) and its standardized mortality ratios is 2–3 times as high as the general population (Crump, Sundquist, Winkleby, & Sundquist, 2013; Lomholt et al., 2019). BD is commonly comorbid with chronic somatic diseases, such as cardiovascular disease, diabetes, obesity and metabolic syndrome (Chauvet-Gelinier, Gaubil, Kaladjian, & Bonin, 2012), with the most common being cardiovascular diseases (Kessing, Vradi, McIntyre, & Andersen, 2015). Comorbid somatic diseases in return can lead to increased likelihood of suicide risk, anxiety disorder, and rapid cycling mood episodes, resulting in worse prognosis and decreased life expectancy (Forty et al., 2014). It is estimated that patients with BD, and including patients with major International Review of Neurobiology, Volume 147 ISSN 0074-7742 https://doi.org/10.1016/bs.irn.2019.07.001
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depressive disorder or schizophrenia, die prematurely up to 25 years due to comorbid somatic diseases (Parks, Svendsen, Singer, Foti, & Mauer, 2006). For cardiovascular diseases, type 2 diabetes, and all-cause mortality, low levels of physical activity and sedentary behavior (e.g., sitting or lying down during waking hours) are independent risk factors of mortality that are modifiable. Exercise has been suggested to be an effective intervention on the physical conditions that are often comorbid with BD, including cardiovascular disease, type 2 diabetes, obesity, and metabolic syndrome (Aune, Norat, Leitzmann, Tonstad, & Vatten, 2015; Chin, Kahathuduwa, & Binks, 2016; Lanier, Bury, & Richardson, 2016). For instance, exercise works equally effectively as medications in reducing mortality rate in patients with cardiovascular disease (Naci & Ioannidis, 2015). Moreover, exercise has protective effects against increased incidence for depressive symptoms or major depression (Schuch et al., 2018). And it can alleviate depressive symptoms of patients with postpartum depression (Nakamura et al., 2019), patients with Parkinson’s disease (Wu, Lee, & Huang, 2017) and people of the general population (Harvey et al., 2018; Northey, Cherbuin, Pumpa, Smee, & Rattray, 2018). This chapter reviews evidence of the effects of exercise on BD patients. Before doing so, we first describe exercise and physical activity in patients with BD. Then we discuss the barriers and facilitators for exercise in patients with BD.
1. Sedentary behavior and physical activity in patients with BD Patients with BD more than often engage in sedentary behavior and have low levels of physical activity. Over 50% patients with BD reported a sedentary lifestyle in self-rated questionnaires (Kilbourne et al., 2007). It is estimated that patients with BD spend average 615 min per day on sedentary behavior, even more serve than patients with schizophrenia and patients with major depressive disorder (493 min per day and 414 min per day, respectively) (Vancampfort et al., 2017). Daily time spent on sedentary behavior is longer when measured by objective measures compared to self-reported ones (Vancampfort et al., 2016). Patients with BD often fail to meet the physical activity guideline (i.e., 150 min per week at the intensity of at least moderate level) ( Janney et al., 2014). One meta-analysis study estimated the time patients with severe mental illness (SMI) including BD
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engaged in moderate physical activity was on average of 3.5 h per day less than healthy controls (Vancampfort et al., 2016). In general, BD patients may be less likely engaging in moderate/vigorous physical activity. Different mood phases or states (i.e., depressive, manic and euthymic states) are in close relations with physical activity (Gershon, Ram, Johnson, Harvey, & Zeitzer, 2016). Motor slowness or retardation is often seen in a major depressive episode, a depressive syndrome lasting at least 2 weeks. While increased activity is considered as a core criterion for hypo/manic episode. Yet it is unclear their causal relationships. Perhaps for some patients, elevated mood may motivate them to execute an exercise plan. Nevertheless, for others, vigorous exercise is in complex association with hypo/manic symptoms (Thomson et al., 2015). Relative to patients with schizophrenia or major depressive disorder, BD patients may be more likely engaging in moderate or vigorous exercise and longer (Vancampfort et al., 2017). At the same time, patients with BD could be the most sedentary group. Sedentary behavior is independent of physical activity and associated with poorer cognition (Depp, Dev, & Eyler, 2016) that are affected in different degrees in BD patients. In addition, patterns of motor activity may be different across different types of BD. During the same euthymic state, a state where patients are emotionally stable for a certain period of time (e.g., 3 months), patients with bipolar type I had greater variability in motor activity in the afternoon and patients with bipolar type II in the night time as opposed to healthy controls (Shou et al., 2017). Exercise tolerance perhaps is reduced in patients with BD. One study arranged 24 patients with BD to exercise on a treadmill. They were asked to run at the 70% of maximal oxygen consumption until they felt too exhausted to continue. The result showed that BD patients performed significantly worse than healthy controls, with approximately 20 min shorter (Shah et al., 2007). And foot and back pain are important negative predictors of functional exercise capacity in patients with BD (Vancampfort et al., 2015).
2. Effects of exercise on BD patients Exercise is an effective non-pharmaceutical treatment for depression, particularly recommended for mild/moderate depression (Knapen, Vancampfort, Morie¨n, & Marchal, 2015; Stubbs et al., 2018). However, the evidence of effectiveness of exercise on BD is limited. Despite this, there are a few clinical studies that help clinicians to recommend exercise to patients with BD (Table 1). In a retrospective cohort study
Table 1 Details of the included studies on physical activity in patients with bipolar disorder. Intervention Authors Study design Participants components Assessed outcomes
Ng, Dodd, and Berk (2007)
Retrospective cohort study
Adults; ICD-10; n ¼ 98 (Intervention: 24, non-participants: 24)
Walking, 24 months
Effect sizes
• Participants had lower DASS score
• Participants had lower DASS subscales (depression, anxiety, stress)
Sylvia, Nierenberg, Stange, Peckham, and Deckersbach (2011)
Self-controlled study
Sylvia, Salcedo, et al. (2013)
Self-controlled study
Adults; MINI Plus, BDI (83%); n ¼ 6 (Intervention)
NEW Tx, 14 weeks
• Reduce in weight
0.13
• Reduce in MADRS
0.42
score Adults; MINI Plus, BDI (80%); n ¼ 5 (Intervention)
NEW Tx, 20 weeks
• Reduce in weight
0.59
• Increase in exercise
2.00
duration Sylvia et al. (2019)
Randomized control trial and self-controlled study
Adults; MINI Plus, BDI (84.2%), NEW Tx, 20 weeks BDII (15.8%); n ¼ 38 (Intervention: 19, control: 19)
Change in invention group
0.80
• Reduce in CGI-BP: depression
• Reduce in CGI-BP:
1.74
overall severity
• Increase in overall
0.75
functioning ICD, International Statistical Classification of Diseases and Related Health Problems; MINI, Mini International Neuropsychiatric Interview; BD, bipolar disorder; NEW Tx, Nutrition Exercise and Wellness Treatment; DASS, Depression Anxiety Stress Scales; MADRS, Montgomery Asberg Depression Rating Scale; CGI-BP, Clinical Global Impression Scale-Bipolar Version.
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of small sample size by Ng et al. (2007), walking exercise (i.e., walking for 40 min per day) was added as an adjunctive treatment for BD patients during an acute phase when admitted to a private psychiatric unit. Those who attended the exercise sections were significantly improved in depressive and anxious symptoms and felt less stressful than those who did not. In several studies by Sylvia et al. (2011, 2019) and Sylvia, Salcedo, et al. (2013) from Massachusetts General Hospital who developed an operational program, called the Nutrition, Exercise, and Wellness treatment (NEW Tx), its goal was to help individuals with BD adopt an healthy lifestyle. To this end, the project is designed to include three elements: eat nutritiously, promote weekly exercise, and adopt other healthy habits (i.e., sleep hygiene and stop smoking/substance use). Participants who participated in the NEW Tx were satisfied with the treatments and had improvements in depressive symptoms and overall functioning. Importantly, they tripled their amount of exercise which maybe in large part contributed to the declines in weight, cholesterol, and triglycerides after 20 weeks of follow-up. These findings suggest that exercise combined with other lifestyle changes is beneficial to the well-being of individuals with BD. We recently conducted an aerobic exercise trial (i.e., running at moderate intensity, 30 min per day, 4 times a week, lasting for 3 months) in adolescents who manifested subthreshold depressive or hypomanic symptoms that fall short of the official BD diagnostic criteria. Participants were randomized to the exercise intervention or psycho-education controlled arm. Though we do not find significant improvement in clinical symptoms including depressive and hypomanic symptoms, there are positive effects of exercise on the brain structures. Adolescent who are in the exercise group show increased gray matter volumes in the orbitofrontal cortex and increased cortical thickness in the rostral anterior cingulate cortex that are involved in mood regulation and social functioning. The changes of the brain structures are correlated with the changes in emotion and cognitive functioning. These preliminary results are promising as it seems that exercise may benefit not only mental health in individuals with BD but it positively affects brain development in adolescents with subthreshold syndromes. This arena clearly is under-investigated and the findings need to replicate. The negative impact of exercise in individuals with BD is unclear. A study by Wright, Armstrong, Taylor, and Dean (2012) concerned its detrimental potential in exacerbating hypo/manic symptoms. This is a crosssectional observational study that asks 25 BD patients’ view on the relations
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of exercise with BD. The relations are complex. They showed that some individuals became more active following exercise while others thought exercise had a calming effect on hypomanic symptoms. More research on this topic is needed, particularly on different mood states. Increasing evidence shows that acute exercise can lead to complex biological changes in the brain, including reduced cerebral blood flow (CBF) and decreased level of brain-derived neurotrophic factor (BDNF), a protein that has potent effects in promoting the survival of nerve cells (e.g., neurons) (Kucyi, Alsuwaidan, Liauw, & McIntyre, 2010), in BD patients (MacIntosh et al., 2017; Metcalfe et al., 2016; Schuch et al., 2015; Subramaniapillai et al., 2016). Using CBF magnetic resonance images (MRI) technique, MacIntosh et al. (2017) found that following 20 min of acute exercise of bicycle ergometer, individuals with BD had more exercise-related decrease in CBF in the medial frontal cortex as opposed to health controls. Moreover, in adolescent with BD, exercise could cancel off the correlations of activation levels in the bilateral accumbens during an executive task with depressive symptoms (Metcalfe et al., 2016). This finding suggests that exercise may alleviate depressive symptoms by having an impact on the accumbens in individuals with BD when loaded with cognitive task, a sub-cortical region that plays a key role in the “reward circuit” of the brain (Kupchik & Kalivas, 2017). Furthermore, serum level of BDNF is reported to be increased in female individuals with BD following a single section of exercise of bicycle ergometer at a vigorous level (i.e., 95% maximum heart rate (220-age), 1.15 respiratory exchange rate, or both) (Schuch et al., 2015). These studies may indicate potential mechanisms by which exercise impacts on our body and the brain in particular.
3. Barriers and facilitators for exercise in patients with BD To better promote exercise, it is important to know the barriers and facilitators for exercise among patients with BD. Research in this area is largely on demographics and clinical characteristics of patients with BD. The barriers included older age, high body mass index (BMI), low educational status, social isolation and financial strains. Older patients with SMI reported lower exercise level than their counterpart (Muralidharan, Klingaman, Molinari, & Goldberg, 2018). Older age predicates lower exercise levels in BD (Vancampfort et al., 2016). In fact, older BD patients are more likely to be commorbid with medical conditions such as cardiovascular diseases that limit their mobility, which harms their ability and/or will to
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engage in or sustain exercise (Vancampfort et al., 2013). Second, Higher BMI is associated with lower exercise levels in individuals with BD (Sylvia, Friedman, et al., 2013; Vancampfort et al., 2013, 2016). Third, social and cultural factors including unemployment, lower educational status, and financial strains are not specific barriers to individuals with BD (Vancampfort et al., 2017), which should be taken into account when designing physical activity program. Finally, severe symptoms, poor global function, illness duration, and medication use all have negative impacts on the physical activity levels of individuals with BD (Melo et al., 2019; Pereira, Padoan, Garcia, Patusco, & Magalha˜es, 2019; Sylvia, Friedman, et al., 2013; Vancampfort et al., 2017). Weight loss is the primary incentive reported by individuals with SMI for engaging in exercise (Firth et al., 2016), which is also the motivating factor endorsed by the general population (Sherwood & Jeffery, 2000). The endorsement of “fitness” as an incentive that is readily improved (Vancampfort et al., 2016) can be serve as a vehicle not only for promoting mental health but also for reducing amendable risk factors for metabolicrelated disease (Hu et al., 2005). To make the best use of the “fitness” perception, physical promotion program should maximize exercise uptake in this clinical population. Moreover, the view that exercise can reduce stress and enhance mood is endorsed by many people with SMI (Rosenbaum, Tiedemann, Sherrington, Curtis, & Ward, 2014). Furthermore, many patients claim that professional support (e.g., exercise supervision) can motivate them to exercise more (Carpiniello, Primavera, Pilu, Vaccargiu, & Pinna, 2013). It also can benefit better adherence to physical activity and has larger beneficial effects on cardiorespiratory fitness (Stubbs, Rosenbaum, Vancampfort, Ward, & Schuch, 2016). With adequate support including exercise supervision and social support, they may feel more confident in overcoming the barriers for exercise (Firth et al., 2016; Pereira et al., 2019; Soundy et al., 2014). There are woven relationships among the factors described. For instance, individuals with BD who is motivated by weight loss tend to exercise more, are more likely to be symptom-free and employed, which in turn promote social support, and vice versa.
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