Abstract
Aim
This study aimed to assess the potential role of physical activity (PA) in reducing the risk of developing inflammatory bowel diseases (IBDs) and in their management.
Subject and methods
A systematic review of literature was conducted up to October 2023 using the PubMed, Scopus, Web of Science and Cochrane Library databases. Observational studies, semi-experimental and experimental studies reporting PA effects were considered eligible. Data on disease status and PA characteristics, main outcomes and possible confounders were collected in a database. The Newcastle–Ottawa Quality Assessment Scale was used to assess risk of bias.
Results
Of the 29 articles included, six investigated PA and risk of IBDs and four of them showed an inverse relationship. Among the others, seven reported positive effects of PA on IBD symptoms, while all showed improvements in comorbidities, complications and quality of life.
Conclusion
PA seems to be effective in preventing or treating IBDs and their complications. Owing to the low quality of the majority of the studies and their heterogeneity, further research is needed to better understand which type and level of PA may be useful in the prevention and treatment of these diseases.
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Introduction
The term inflammatory bowel disease (IBD) indicates a group of chronic and lifelong diseases characterized by inflammation of the gastrointestinal tract, including Crohn’s disease (CD) and ulcerative colitis (UC) (Yeshi et al. 2020). CD can affect any part of the gastrointestinal tract, but it most commonly affects the large and small intestines, while UC refers to recurring inflammation of the rectum and the colon (Gohil and Carramusa 2014). IBD is characterized by symptoms such as abdominal pain, fever, constipation or diarrhoea, and presence of blood and/or mucus in faeces (O’Reilly et al. 2023). In the early 2000s, more than 1.5 million people in North America and over 2 million people in Europe suffered from IBD (Burisch et al. 2013). It is projected that by 2030, the number of people suffering from IBD in Europe and the United States of America will exceed 7 million, or the 0.3% of the population in North America, Oceania and many countries in Europe (Hammer and Langholz 2020; Coward et al. 2019; Molodecky et al. 2012). The incidence rate of IBDs is higher than the mortality rate; although their incidence has remained constant, their prevalence is expected to increase in the next decade due to advancements in maintenance therapy (Kaplan 2015; Kaplan and Windsor 2021). However, currently there are no specific pharmaceutical treatments for IBD, given that these diseases are multifaceted disorders. Therapeutics that are used to treat IBD generally include non-specific anti-inflammatory and immunosuppressive agents and focus on the immune system, aiming to reduce inflammation and fostering mucosal healing. Beyond such conventional treatments, stem cell therapies, including hematopoietic stem cell transplantation and mesenchymal stem cell therapy, have been shown to improve patients’ conditions (Imbrizi et al. 2023; Parigi et al. 2023). In addition, IBD is a chronic illness that can lead to frequent relapses and complications and these conditions put a significant burden on the healthcare system due to hospitalization and cost of medications, as well as on society in terms of productivity loss (Kuenzig et al. 2020; Caviglia et al. 2020, 2023).
Therefore, it is important to properly understand the risk and protective factors associated with the disease to reduce its global burden. The aetiology of IBD is unknown, but there are many factors suspected to be involved such as genetic susceptibility, environmental factors like gastrointestinal infections, an altered immune response, shifts in microbial composition, often due to antibiotic use, concomitant immune-mediated diseases, smoking, stress, and the use of nonsteroidal anti-inflammatory drugs (NSAIDs) or oral contraceptives (Axelrad et al. 2019; Ungaro et al. 2014; Torres et al. 2023; Van Der Sloot et al. 2017). In contrast to these risk factors, the dietary intake of fibre, fruits, vitamin C, breast milk and omega-3 polyunsaturated fatty acids, living in southern latitudes, possibly because of UV radiation exposure, higher vitamin D level and physical activity (PA) seem to be protective against IBD (Sahu et al. 2021; Khalili et al. 2012; Holik et al. 2019). PA in particular has been proven to also be beneficial in the course of IBDs (Parigi et al. 2023). Indeed, literature shows that PA plays a crucial role in mechanisms related to the intestinal function that involve downregulating the intestinal pro-inflammatory cell network, reducing oxidative stress and modulating the gut microbiota (Wojcik-Grzybek et al. 2022; Dorelli et al. 2021; Gallè et al. 2020). Moderate PA can have positive effects on the immune system and reduce inflammatory markers, which may be helpful for IBD patients (Nishida et al. 2023). Moreover, exercise also has psychological benefits, such as reducing stress and anxiety, which are commonly experienced by IBD patients and can trigger relapses (Ordille and Phadtare 2023). However, the role of PA in IBD prevention and treatment has not yet been defined clearly.
This systematic review was conducted to explore the evidence coming from structured PA interventions aimed at preventing IBD or at managing IBD symptoms, looking for consistent elements that could lead to future strategies.
Methods
Selection protocol and search strategy
The present systematic review was conducted according to the Preferred Reporting Items for Systematic Review and Meta-Analysis (PRISMA) guidelines (Page et al. 2021). The protocol was registered in PROSPERO (CRD42023446860). The review question was framed using the PICO framework and the following eligibility criteria (a) Population: adult individuals of any gender; (b) Intervention: any type of PA, including exercise and sport; (c) Comparison: age-, gender- and condition-matched control group (if present); (d) Outcome: assessment of the effects of PA in prevention or treatment of IBD; (e) Study: observational studies, semi-experimental and experimental studies. The review focused on the role of PA in prevention and therapy of IBD in adults of any gender. Only studies which measured PA and its effects on human IBD development and progression were considered eligible. Four electronic databases (PubMed, Scopus, Web of Science and Cochrane Library) were interrogated using the following terms: (“physical activity” OR “exercise*”) AND (“IBD” OR “Inflammatory bowel disease*” OR “gastrointestinal inflammatory disease*” OR “Crohn’s disease” OR “ulcerative colitis”). The search on PubMed was carried out by title, abstract and MeSH terms; the search on Scopus, Web of Science and Cochrane Library included topic by title, abstract and keywords. The search was performed from 10 October 2023 to 31 October 2023.
Inclusion and exclusion criteria
Only those studies which specifically analysed the role of PA in prevention or treatment of IBD among adult patients of any gender were considered. Furthermore, the possible presence of confounding factors was also considered. All the studies which included individuals under the age of 18 years who were affected by any chronic conditions other than IBD or did not concern PA were excluded. Only articles presenting observational studies, semi-experimental and experimental studies were considered eligible. Reviews, meta-analysis, case studies, proceedings, qualitative studies, editorials, commentary studies and any other type were excluded. Reviews and meta-analyses were examined to identify further articles in their references that may not have been part of the baseline research results. We included only articles published in English and Italian languages. Titles and abstracts acquired from the four databases were transferred to the reference software Zotero systematic review manager for the relevance assessment process. The next step was screening the title and abstract of the potentially eligible studies, following the previously stated inclusion criteria; the screening was conducted by four authors (ADG, EM, FU, VV) independently. Then, full-texts were read independently by the same four authors (ADG, EM, FU, VV) with a later discussion about their inclusion in the review. Disagreements were mediated by the evaluation of the other three authors (CP, FV, FG) and consensus among the authors.
Data extraction process and quality assessment
The following data were extracted: author, publication year, country, sample characteristics (size, age, gender, ethnicity, socio-economic status, education, anthropometric parameters), type of control, type of IBD and disease status, PA-related information (type, frequency and duration of PA/exercise), main outcomes, confounding factors assessed and main findings. The quality assessment was performed using the Newcastle–Ottawa Quality Assessment Scale (NOS) for cohort, case–control studies and clinical trials, then adapted from cohort and case control studies to perform a quality assessment for cross-sectional studies (Wells et al. 2021). An overall rating of “poor”, “fair” or “good” quality was assigned to each eligible article according to the proportion of criteria met. Four authors (ADG, EM, FU, VV) independently assigned a score to each study, and disagreements were achieved by the evaluation of the other three authors (CP, FV, FG) and consensus among the authors.
Results
The database search yielded a total of 3129 records. Of these, 1147 duplicates were removed and 1982 were screened by title and abstract. After the full-text assessment, 29 of the 68 eligible articles were included in the review (Fig. 1).
Six of them (Furuya et al. 2022; Hlavaty et al. 2013; Khalili et al. 2013; Klein et al. 1998; Lautenschlager et al. 2023; Rasmussen et al. 2021) investigated the role of PA in the development of the disease, while the others evaluated the potential beneficial effects of PA in individuals affected by IBD.
Table 1 shows the information regarding the first group. It included three cohort studies (Khalili et al. 2013; Lautenschlager et al. 2023; Rasmussen et al. 2021), two case–control studies (Furuya et al. 2022; Hlavaty et al. 2013) and a cross-sectional study (Klein et al. 1998), which were performed in Europe (Hlavaty et al. 2013; Lautenschlager et al. 2023; Rasmussen et al. 2021), Asia (Furuya et al. 2022; Klein et al. 1998) and the USA (Khalili et al. 2013). Both genders were observed in all the studies, with a sample size ranging from 232 to 57,053 individuals. Both CD and UC were considered across all the studies. With regard to quality assessment, three studies were considered “poor”, two “fair” and one “good”. As for the results, four studies (Hlavaty et al. 2013; Khalili et al. 2013; Klein et al. 1998; Lautenschlager et al. 2023) showed an inverse association between PA and onset of IBDs or at least of CD. The study by Rasmussen et al. did not find any association between PA and risk of developing IBDs (Rasmussen et al. 2021). However, in the same study, a higher time spent in do-it-yourself work appeared to be associated with IBD onset. The study by Furuya et al. registered a positive association between occupational PA level and UC risk (Furuya et al. 2022).
The data from the selected studies which investigated the role of PA in IBD treatment are reported in Table 2. As for the design of the study, nine of the selected articles described randomized controlled trials (Cronin et al. 2019; Elsenbruch et al. 2005; Jones et al. 2020; Klare et al. 2015; Lamers et al. 2021a, b; Lamers et al. 2022; Ng et al. 2007; Robinson et al. 1998; Watters et al. 2001), while the others reported observational studies. Seventeen studies were performed in Europe (Cronin et al. 2019; Elsenbruch et al. 2005; D’Incà et al. 1999; Henderson et al. 2022; Holik et al. 2019; Jones et al. 2020; Klare et al. 2015; Lamers et al. 2021a, b; Lamers et al. 2021a, b; Lamers et al. 2022; Ratajczak-Pawłowska et al. 2023; Spijkerman et al. 2021; Tew et al. 2016; Wiestler et al. 2019; Ng et al. 2007; Robinson et al. 1998; Watters et al. 2001), four in the Americas (Jones et al. 2015; Lo et al. 2021; Mack et al. 2011; Taylor et al. 2018) and two in Asia (Kim et al. 2021; Watanabe et al. 2021). The sample size varied across the selected studies from 20 to 117 for RCTs and from 12 to 289,658 individuals for observational studies. Both genders were represented in all the studies but one which involved only men (D’Incà et al. 1999) and two which did not report this information (Watters et al. 2001; Jones et al. 2015). Of the 16 studies which reported the status of the disease for participants, all but three (Cronin et al. 2019; D’Incà et al. 1999; Jones et al. 2015) included participants with different clinical conditions. As for quality, 12 of these studies were considered “poor”, ten “fair” and one “good”.
The results differ across the selected studies. As for RCTs, the study by Cronin et al. showed a significant reduction in body fat percentage among patients who underwent 8 weeks of aerobic and resistance training, together with improvements in IBD-related sarcopenia and obesity-related metabolic disorders (Cronin et al. 2019). The study by Elsenbruch et al. reported a significant improvement in mental health, but this resulted from a multicomponent intervention, including stress management training, moderate exercise, Mediterranean diet, behavioural techniques and self-care strategies (Elsenbruch et al. 2005). Jones K et al. found significant improvements in bone mineral density and muscular function among IBD patients who underwent the 26-week exercise programme and not among those who did not exercise; quality of life and fatigue improvements were also registered in this study (Jones et al. 2020). Even Klare et al. registered an improvement in quality of life among patients who practiced moderate-intensity running (Klare et al. 2015). Lamers et al. observed an exercise-related increase in cytokine production among IBD-walkers and non-walkers and no changes in faecal calprotectin concentration; a significant increase in disease activity was registered among CD and not in UC walkers (Lamers et al. 2021a, b). In the subsequent RCT by Lamers et al., significant improvements in impact of disease in daily life and fatigue were obtained after a multidisciplinary intervention, but they were related to changes in diet and not to PA level, which remained the same (Lamers et al. 2022). Ng et al. reported a significantly higher improvement in quality of life and symptoms in patients involved in walking with respect to controls (Ng et al. 2007). The 12-month exercise intervention implemented by Robinson et al. led to significant improvements in bone mineral density among participants, which were not observed in controls Robinson et al. 1998. Instead, the resistance training intervention applied by Watters et al. showed a positive relationship between exercise and wellbeing in IBD patients (Watters et al. 2001).
As for the observational studies, the study by D’Incà et al. showed a post-exercise increase in orocaecal transit time and neutrophils which did not differ from that observed in healthy controls (D’Incà et al. 1999). Henderson et al. registered similar changes among IBD patients and healthy controls in breath volatile organic compounds and cytokines production after repeated prolonged moderate exercise (Henderson et al. 2022). Holik et al. found a significant relationship between daily PA and disease activity, which was independent by intensity level and type of IBD (Holik et al. 2019). Even in the study by Jones P et al., higher exercise level was associated with decreased risk of relapse or active disease for IBD patients (Jones et al. 2015). Kim et al. found an association between weekly PA level and quality of life (Kim et al. 2021). Lamers et al. found a significant association between disease activity and PA in CD but not in UC patients, and an improvement in general fitness, quality of life and self-image was reported by the majority of participants (Lamers et al. 2021a, b). The findings of Lo et al. indicated a lower mortality rate related to PA in IBD patients (Lo et al. 2021). In the study by Mack et al., LTPA has been associated with reduced risk of onset and management of IBD comorbidities such as osteoporosis and colon cancer (Mack et al. 2011). In the study by Ratajczak-Pawłowska et al., vigorous, moderate and total PA were found to be positively related to bone mineral density and body mass among IBD patients, while only moderate PA was related to BMD in controls (Ratajczak-Pawłowska et al. 2023). Spijkerman et al. found an apparent suppression of the proinflammatory response in IBD patients after three consecutive days of walking (Spijkerman et al. 2021). In the study by Taylor et al., MVPA and walking were associated with physical and mental health-related quality of life (Taylor et al. 2018). Tew et al. found that PA was negatively and independently associated with depression, disease activity and perceived barriers to exercise in people with CD, and with depression and age in people with UC (Tew et al. 2016). Watanabe et al. showed that strenuous activity is significantly inversely associated with mucosal healing but not with clinical remission (Watanabe et al. 2021). The study by Wiestler et al. reported that disease activity and quality of life were significantly correlated with the duration of strenuous PA per day (Wiestler et al. 2019).
Adverse events were reported in four studies (Lamers et al. 2022; Ratajczak-Pawłowska et al. 2023; Spijkerman et al. 2021; Wiestler et al. 2019). Apart from one fall, they consisted of limitations to PA related to the disease.
Discussion
IBDs pose a major public health concern due to increasing prevalence, deaths and disability-adjusted life-years and, thus, require specific preventive and management policies (Wang et al. 2019). Considering that PA positively influences all physiologic systems and it can be used as a “medicine” towards several conditions and diseases (Anderson and Durstine 2019), the present systematic review was performed to examine the beneficial role of PA in counteracting the development of IBDs and/or managing these diseases after their occurrence (Holik et al. 2019).
The first finding of this systematic review is that the preventive role of PA towards IBD is considered to a lesser extent than the therapeutic one. In fact, only six articles evaluate PA for this purpose (Furuya et al. 2022; Hlavaty et al. 2013; Khalili et al. 2013; Klein et al. 1998; Lautenschlager et al. 2023; Rasmussen et al. 2021). Four of these found positive and encouraging results (Hlavaty et al. 2013; Khalili et al. 2013; Klein et al. 1998; Lautenschlager et al. 2023). Conversely, an included study found no association (Rasmussen et al. 2021), while another one found a direct association between PA and UC and an inverse association with CD (Furuya et al. 2022).
In this respect, it is well demonstrated that regular PA is a protective factor for several noncommunicable diseases (NCDs) such as cardiovascular diseases, diabetes and several cancers (Anderson and Durstine 2019). With regard to the IBDs, it should be considered that PA can influence several features of the immune system and the development of autoimmune diseases (Sharif et al. 2018). Indeed, it has been proved that the lack of PA can cause an altered Th1/Th2 balance. Th1 and Th2 influence, respectively, the secretion of pro-inflammatory and anti-inflammatory cytokines; thus, the shift of T1/T2 cells ratio determines and alteration of the balance between pro-inflammatory and anti-inflammatory mechanisms, responsible for the immune responses developed by the patients (Steensberg et al. 2001; Huang and Chen 2016). This explanation is supported by the evidence that the incidence of other autoimmune diseases, such as rheumatoid arthritis, multiple sclerosis or psoriasis is higher in participants less engaged in PA (Lautenschlager et al. 2023; Sharif et al. 2018). In addition to the effects associated directly with PA on the immune system, lack of PA is related to a major threat of overweight and obesity, known risk factors for chronic low-grade inflammation (Winer et al. 2016) and for the development of IBDs (Lautenschlager et al. 2023; Kugathasan et al. 2007).
As for the role of PA on IBDs management, seven studies (Holik et al. 2019; Ng et al. 2007; Lamers et al. 2021a, b; Tew et al. 2016; Jones et al. 2015; Watanabe et al. 2021) reported positive effects of PA/exercise on disease symptoms and activity, while three (Elsenbruch et al. 2005; D’Incà et al. 1999; Henderson et al. 2022) did not observe significant improvements with respect to controls and one (Lamers et al. 2021a, b) showed negative effects. These contrasting results can be due to the type and the intensity level of PA practiced by the studied populations; additionally, the different periods of life in which PA was carried out, the characteristics of the population included in the study, the stage of the disease and the presence of complications, as well as the methodological quality of the study, can also affect the evidence of an association between PA and the development and/or the course of IBDs.
Another important finding of the present systematic review is related to the preventive role of PA towards the complications associated with IBDs, mainly bone loss, osteoporosis and metabolic bone diseases (Robinson et al. 1998; Lee et al. 2005). The effect of PA on bone health can be explained considering that exercise, increasing muscle mass, can determine osteogenic effects through muscle pull on the bones, whereas activities promoting high-impact weight-bearing such as running or step aerobics can produce positive changes in bone strength and can reduce fracture risk (Lee et al. 2005). In addition, PA can aid in the prevention of cardiovascular disease outcomes in IBDs (Jaiswal et al. 2023). Indeed, even if the potential biological pathways of PA effects on cardiovascular diseases still need to be clarified, the inverse relationship between PA and cardiovascular diseases has been amply demonstrated (Zhuo et al. 2021; Carnethon 2009) and the mechanisms involved seem to be related to a healthier metabolic milieu with a reduction of systemic chronic inflammation and to antiatherogenic effects, myocardial regeneration and cardioprotection (Valenzuela et al. 2023).
Moreover, with the exception of the study by Lamers et al., all the studies included in this review which examined the possible consequences of PA on IBD comorbidities or mental health reported positive effects (Cronin et al. 2019; Elsenbruch et al. 2005; Jones et al. 2020; Lamers et al. 2022; Robinson et al. 1998; Lamers et al. 2021a, b; Ratajczak-Pawłowska et al. 2023; Tew et al. 2016; Lo et al. 2021; Mack et al. 2011). This result is in line with the scientific evidence reporting that PA can contribute to decreasing the frequency of mental disorders, in particular depression and anxiety, by reducing health disparities and mental health symptoms (Schuch & Vancampfort 2021). Furthermore, nine of the selected studies investigated the effects of PA or exercise on patients’ quality of life (Jones et al. 2020; Klare et al. 2015; Lamers et al. 2022; Ng et al. 2007; Watters et al. 2001; Lamers et al. 2021a, b; Wiestler et al. 2019; Taylor et al. 2018; Kim et al. 2021). With the exception of the findings of Lamers et al. (Lamers et al. 2021a, b), the other studies reported an improvement in quality of life among active patients affected by IBDs.
Notwithstanding the differences in the design of the studies and in the aspects examined, the majority of the articles highlighted the possible benefits that could derive from PA in patients with IBDs. However, the question of whether or not these patients are able to engage in PA must be considered. In fact, although data support the assumption that PA is feasible in IBDs patients (Klare et al. 2015; Lamers et al. 2021a, b), PA may not always be easy to practice due to abdominal pain (Coates et al. 2023). De Filippis et al. found that nearly 40% of the respondents felt that IBD limited their exercise for various reasons, most commonly fatigue, joint pain, embarrassment, weakness and abdominal pain, while some reported a subjective increase in symptoms immediately following exercise (De Filippis et al. 2016). These limitations may result in lower PA levels after the diagnosis of IBDs than before, with a reduction in the percentage of patients participating in sports activities at amateur, semi-professional and professional levels (Gatt et al. 2019; van Langenberg and Gibson 2010), including and most notably in relation to the stage of disease as assessed in some studies (Tew et al. 2016; Wiestler et al. 2019; Mack et al. 2011).
Some limitations should be considered when interpreting these results. First, the examined studies differed in design, type and level of PA/exercise, outcomes investigated and assessment methods, and this did not allow us to perform a meta-analysis of the results nor to obtain more consistent results. Moreover, it should be noted that the results were not controlled for possible confounding factors in all the selected studies, which contributed to their generally low quality. As mentioned earlier, the insufficient number of papers concerning the preventive aspect of PA does not allow us to state its effectiveness for public health purposes.
Conclusions
The results of the present systematic review suggest that PA could be considered a useful factor both for preventing and managing IBDs. In particular, the available literature shows that PA may represent a preventive factor towards the development of these diseases. In fact, even if the biological process is not yet elucidated, it seems that the lack of PA can determine a shift of the balance between pro-inflammatory and anti-inflammatory mechanisms responsible for the alteration of immune responses developed by the patients. In addition, evidence shows that in patients affected by IBDs, PA can prevent the complications such as bone loss, osteoporosis, metabolic bone diseases and cardiovascular diseases, and it can be used for managing associated comorbidities and mental disorders and for improving the patients’ quality of life.
However, further research on this topic is needed to develop individualized and customized exercise plans according to individual risk and type of IBD.
Data availability
All the data are reported in the manuscript.
References
Anderson E, Durstine JL (2019) Physical activity, exercise, and chronic diseases: a brief review. Sports Med Health Sci 1(1):3–10. https://doi.org/10.1016/j.smhs.2019.08.006
Axelrad JE, Olén O, Askling J, Lebwohl B, Khalili H, Sachs MC, Ludvigsson JF (2019) Gastrointestinal infection increases odds of inflammatory bowel disease in a nationwide case-control study. Clin Gastroenterol Hepatol: Off Clin Pract J Am Gastroenterol Assoc 17(7):311-1322.e7. https://doi.org/10.1016/j.cgh.2018.09.034
Burisch J, Jess T, Martinato M, Lakatos PL, ECCO -EpiCom, (2013) The burden of inflammatory bowel disease in Europe. J Crohn’s Colitis 7(4):322–337. https://doi.org/10.1016/j.crohns.2013.01.010
Carnethon MR (2009) Physical activity and cardiovascular disease: how much is enough? Am J Lifestyle Med 3(1):44S-49S. https://doi.org/10.1177/1559827609332737
Caviglia GP, Rosso C, Stalla F, Rizzo M, Massano A, Abate ML, Olivero A, Armandi A, Vanni E, Younes R, Fagoonee S, Pellicano R, Astegiano M, Saracco GM, Bugianesi E, Ribaldone DG (2020) On-treatment decrease of serum interleukin-6 as a predictor of clinical response to biologic therapy in patients with inflammatory bowel diseases. J Clin Med 9(3):800. https://doi.org/10.3390/jcm9030800
Caviglia GP, Garrone A, Bertolino C, Vanni R, Bretto E, Poshnjari A, Tribocco E, Frara S, Armandi A, Astegiano M, Saracco GM, Bertolusso L, Ribaldone DG (2023) Epidemiology of inflammatory bowel diseases: a population study in a healthcare district of North-West Italy. J Clin Med 12(2):641. https://doi.org/10.3390/jcm12020641
Coates MD, Dalessio S, Walter V, Stuart A, Tinsley A, Williams ED, Clarke K (2023) Lifestyle factors associated with abdominal pain in quiescent inflammatory bowel disease. Dig Dis Sci 68(11):4156–4165. https://doi.org/10.1007/s10620-023-08075-0
Coward S, Clement F, Benchimol EI, Bernstein CN, Avina-Zubieta JA, Bitton A, Carroll MW, Hazlewood G, Jacobson K, Jelinski S, Deardon R, Jones JL, Kuenzig ME, Leddin D, McBrien KA, Murthy SK, Nguyen GC, Otley AR, Panaccione R, Rezaie A, Kaplan GG (2019) Past and future burden of inflammatory bowel diseases based on modeling of population-based data. Gastroenterology 156(5):1345-1353.e4. https://doi.org/10.1053/j.gastro.2019.01.002
Cronin O, Barton W, Moran C, Sheehan D, Whiston R, Nugent H, McCarthy Y, Molloy CB, O’Sullivan O, Cotter PD, Molloy MG, Shanahan F (2019) Moderate-intensity aerobic and resistance exercise is safe and favorably influences body composition in patients with quiescent Inflammatory bowel disease: a randomized controlled cross-over trial. BMC Gastroenterol 19(1):29. https://doi.org/10.1186/s12876-019-0952-x
DeFilippis EM, Tabani S, Warren RU, Christos PJ, Bosworth BP, Scherl EJ (2016) Exercise and self-reported limitations in patients with inflammatory bowel disease. Dig Dis Sci 61(1):215–220. https://doi.org/10.1007/s10620-015-3832-4
D’Incà R, Varnier M, Mestriner C, Martines D, D’Odorico A, Sturniolo GC (1999) Effect of moderate exercise on Crohn’s disease patients in remission. Ital J Gastroenterol Hepatol 31(3):205–210
Dorelli B, Gallè F, De Vito C, Duranti G, Iachini M, Zaccarin M, Preziosi Standoli J, Ceci R, Romano F, Liguori G, Romano Spica V, Sabatini S, Valeriani F, Cattaruzza MS (2021) Can physical activity influence human gut microbiota composition independently of diet? Syst Rev Nutri 13(6):1890. https://doi.org/10.3390/nu13061890
Elsenbruch S, Langhorst J, Popkirowa K, Müller T, Luedtke R, Franken U, Paul A, Spahn G, Michalsen A, Janssen OE, Schedlowski M, Dobos GJ (2005) Effects of mind-body therapy on quality of life and neuroendocrine and cellular immune functions in patients with ulcerative colitis. Psychother Psychosom 74(5):277–287. https://doi.org/10.1159/000086318
Furuya Y, Fukai K, Nakazawa S, Kojimahara N, Hoshi K, Toyota A, Tatemichi M (2022) Occupational physical activity differentially affects the risk for developing later-onset Crohn’s disease and ulcerative colitis among middle-aged and older populations. Scand J Gastroenterol 57(2):206–213. https://doi.org/10.1080/00365521.2021.1999495
Gallè F, Valeriani F, Cattaruzza MS, Gianfranceschi G, Liguori R, Antinozzi M, Mederer B, Liguori G, Romano Spica V (2020) Mediterranean diet, physical activity and gut microbiome composition: a cross-sectional study among healthy young Italian adults. Nutrients 12(7):2164. https://doi.org/10.3390/nu12072164
Gatt K, Schembri J, Katsanos KH, Christodoulou D, Karmiris K, Kopylov U, Pontas C, Koutroubakis IE, Foteinogiannopoulou K, Fabian A, Molnar T, Zammit D, Fragaki M, Balomenos D, Zingboim N, Ben Horin S, Mantzaris GJ, Ellul P (2019) Inflammatory Bowel Disease [IBD] and physical activity: a study on the impact of diagnosis on the level of exercise amongst patients With IBD. J Crohns Colitis 13(6):686–692. https://doi.org/10.1093/ecco-jcc/jjy214
Gohil K, Carramusa B (2014) Ulcerative colitis and Crohn’s disease. P & t: A Peer-Rev J Formul Manag 39(8):576–577
Hammer T, Langholz E (2020) The epidemiology of inflammatory bowel disease: balance between East and West? A narrative review. Digest Med Res 3. https://doi.org/10.21037/dmr-20-149
Henderson B, Meurs J, Lamers CR, Batista GL, Materić D, Bertinetto CG, Bongers CCWG, Holzinger R, Harren FJM, Jansen JJ, Hopman MTE, Cristescu SM (2022) Non-invasive monitoring of inflammation in inflammatory bowel disease patients during prolonged exercise via exhaled breath volatile organic compounds. Metabolites 12(3):224. https://doi.org/10.3390/metabo12030224
Hlavaty T, Toth J, Koller T, Krajcovicova A, Oravcova S, Zelinkova Z, Huorka M (2013) Smoking, breastfeeding, physical inactivity, contact with animals, and size of the family influence the risk of inflammatory bowel disease: a Slovak case-control study. United Eur Gastroenterol J 1(2):109–119. https://doi.org/10.1177/2050640613478011
Holik D, Včev A, Milostić-Srb A, Salinger Ž, Ivanišević Z, Včev I, Miškulin M (2019) The effect of daily physical activity on the activity of inflammatory bowel diseases in therapy-free patients. Acta Clinica Croatica 58(2):202–212. https://doi.org/10.20471/acc.2019.58.02.02
Huang Y, Chen Z (2016) Inflammatory bowel disease related innate immunity and adaptive immunity. Am J Transl Res 8(6):2490–2497
Imbrizi M, Magro F, Coy CSR (2023) Pharmacological therapy in inflammatory bowel diseases: a narrative review of the past 90 years. Pharmaceuticals (basel, Switzerland) 16(9):1272. https://doi.org/10.3390/ph16091272
Jaiswal V, Batra N, Dagar M, Butey S, Huang H, Chia JE, Naz S, Endurance EO, Raj N, Patel S, Maroo D, Ang SP, Hanif M, Mukherjee D, Sarfraz Z, Shrestha AB, Song D (2023) Inflammatory bowel disease and associated cardiovascular disease outcomes: a systematic review. Medicine 102(6):e32775. https://doi.org/10.1097/MD.0000000000032775
Jones PD, Kappelman MD, Martin CF, Chen W, Sandler RS, Long MD (2015) Exercise decreases risk of future active disease in patients with inflammatory bowel disease in remission. Inflamm Bowel Dis 21(5):1063–1071. https://doi.org/10.1097/MIB.0000000000000333
Jones K, Baker K, Speight RA, Thompson NP, Tew GA (2020) Randomised clinical trial: combined impact and resistance training in adults with stable Crohn’s disease. Aliment Pharmacol Ther 52(6):964–975. https://doi.org/10.1111/apt.16002
Kaplan GG (2015) The global burden of IBD: from 2015 to 2025. Nat Rev Gastroenterol Hepatol 12(12):720–727. https://doi.org/10.1038/nrgastro.2015.150
Kaplan GG, Windsor JW (2021) The four epidemiological stages in the global evolution of inflammatory bowel disease. Nat Rev Gastroenterol Hepatol 18(1):56–66. https://doi.org/10.1038/s41575-020-00360-x
Khalili H, Huang ES, Ananthakrishnan AN, Higuchi L, Richter JM, Fuchs CS, Chan AT (2012) Geographical variation and incidence of inflammatory bowel disease among US women. Gut 61(12):1686–1692. https://doi.org/10.1136/gutjnl-2011-301574
Khalili H, Ananthakrishnan AN, Konijeti GG, Liao X, Higuchi LM, Fuchs CS, Spiegelman D, Richter JM, Korzenik JR, Chan AT (2013) Physical activity and risk of inflammatory bowel disease: prospective study from the Nurses’ Health Study cohorts. BMJ (clinical Research Ed) 347:f6633. https://doi.org/10.1136/bmj.f6633
Kim B, Chae J, Kim EH, Yang HI, Cheon JH, Kim TI, Kim WH, Jeon JY, Park SJ (2021) Physical activity and quality of life of patients with inflammatory bowel disease. Medicine 100(27):e26290. https://doi.org/10.1097/MD.0000000000026290
Klare P, Nigg J, Nold J, Haller B, Krug AB, Mair S, Thoeringer CK, Christle JW, Schmid RM, Halle M, Huber W (2015) The impact of a ten-week physical exercise program on health-related quality of life in patients with inflammatory bowel disease: a prospective randomized controlled trial. Digestion 91(3):239–247. https://doi.org/10.1159/000371795
Klein I, Reif S, Farbstein H, Halak A, Gilat T (1998) Preillness non dietary factors and habits in inflammatory bowel disease. Ital J Gastroenterol Hepatol 30(3):247–251
Kuenzig ME, Manuel DG, Donelle J, Benchimol EI (2020) Life expectancy and health-adjusted life expectancy in people with inflammatory bowel disease. CMAJ: Can Med Assoc J 192(45):E1394-E1402. https://doi.org/10.1503/cmaj.190976
Kugathasan S, Nebel J, Skelton JA, Markowitz J, Keljo D, Rosh J, LeLeiko N, Mack D, Griffiths A, Bousvaros A, Evans J, Mezoff A, Moyer S, Oliva-Hemker M, Otley A, Pfefferkorn M, Crandall W, Wyllie R, Hyams J, Wisconsin Pediatric Inflammatory Bowel Disease Alliance, Pediatric Inflammatory Bowel Disease Collaborative Research Group (2007) Body mass index in children with newly diagnosed inflammatory bowel disease: observations from two multicenter North American inception cohorts. J Pediats 151(5):523-527https://doi.org/10.1016/j.jpeds.2007.04.004
Lamers CR, de Roos NM, Bongers CCWG, Ten Haaf DSM, Hartman YAW, Witteman BJM, Hopman MTE (2021a) Repeated prolonged moderate-intensity walking exercise does not appear to have harmful effects on inflammatory markers in patients with inflammatory bowel disease. Scand J Gastroenterol 56(1):30–37. https://doi.org/10.1080/00365521.2020.1845791
Lamers CR, de Roos NM, Koppelman LJM, Hopman MTE, Witteman BJM (2021b) Patient experiences with the role of physical activity in inflammatory bowel disease: results from a survey and interviews. BMC Gastroenterol 21(1):172. https://doi.org/10.1186/s12876-021-01739-z
Lamers CR, de Roos NM, Heerink HH, van de Worp-Kalter LA, Witteman BJM (2022) Lower impact of disease on daily life and less fatigue in patients with inflammatory bowel disease following a lifestyle intervention. Inflamm Bowel Dis 28(12):1791–1799. https://doi.org/10.1093/ibd/izac027
Lautenschlager SA, Barry MP, Rogler G, Biedermann L, Schreiner P, Siebenhüner AR, Swiss IBD Cohort Study Group (2023) Lifestyle factors associated with inflammatory bowel disease: data from the Swiss IBD cohort study. BMC Gastroenterol 23(1):71.https://doi.org/10.1186/s12876-023-02692-9
Lee N, Radford-Smith G, Taaffe DR (2005) Bone loss in Crohn’s disease: exercise as a potential countermeasure. Inflamm Bowel Dis 11(12):1108–1118. https://doi.org/10.1097/01.mib.0000192325.28168.08
Lo CH, Khalili H, Song M, Lochhead P, Burke KE, Richter JM, Giovannucci EL, Chan AT, Ananthakrishnan AN (2021) Healthy lifestyle is associated with reduced mortality in patients with inflammatory bowel diseases. Clin Gastroenterol Hepatol: Off Clin Pract J Am Gastroenterol Assoc 19(1):87–95. https://doi.org/10.1016/j.cgh.2020.02.047
Mack DE, Wilson PM, Gilmore JC, Gunnell KE (2011) Leisure-time physical activity in Canadians living with Crohn disease and ulcerative colitis: population-based estimates. Gastroenterol Nurs: Off J Soc Gastroenterol Nurses Associat 34(4):288–294. https://doi.org/10.1097/SGA.0b013e3182248732
Molodecky NA, Soon IS, Rabi DM, Ghali WA, Ferris M, Chernoff G, Benchimol EI, Panaccione R, Ghosh S, Barkema HW, Kaplan GG (2012) Increasing incidence and prevalence of the inflammatory bowel diseases with time, based on systematic review. Gastroenterology 142(1):46-e30. https://doi.org/10.1053/j.gastro.2011.10.001
Ng V, Millard W, Lebrun C, Howard J (2007) Low-intensity exercise improves quality of life in patients with Crohn’s disease. Clin J Sport Med: Off J Can Acad Sport Med 17(5):384–388. https://doi.org/10.1097/JSM.0b013e31802b4fda
Nishida Y, Hosomi S, Kobayashi Y, Nakata R, Ominami M, Nadatani Y, Fukunaga S, Otani K, Tanaka F, Nagami Y, Taira K, Kamata N, Fujiwara Y (2023) Impact of the COVID-19 pandemic on the lifestyle and psychosocial behavior of patients with inflammatory bowel diseases: a narrative review. Healthcare (basel, Switzerland) 11(19):2642. https://doi.org/10.3390/healthcare11192642
O’Reilly C, Mills S, Rea MC, Lavelle A, Ghosh S, Hill C, Ross RP (2023) Interplay between inflammatory bowel disease therapeutics and the gut microbiome reveals opportunities for novel treatment approaches. Microbiome Res Rep 2(4):35. https://doi.org/10.20517/mrr.2023.41
Ordille AJ, Phadtare S (2023) Intensity-specific considerations for exercise for patients with inflammatory bowel disease. Gastroenterol Report 11:goad004. https://doi.org/10.1093/gastro/goad004
Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, Shamseer L, Tetzlaff JM, Akl EA, Brennan SE, Chou R, Glanville J, Grimshaw JM, Hróbjartsson A, Lalu MM, Li T, Loder EW, Mayo-Wilson E, McDonald S, McGuinness LA, Moher D (2021) The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ (clinical Research Ed) 372:71. https://doi.org/10.1136/bmj.n71
Parigi TL, D’Amico F, Abreu MT, Dignass A, Dotan I, Magro F, Griffiths AM, Jairath V, Iacucci M, Mantzaris GJ, O’Morain C, Reinisch W, Sachar DB, Turner D, Yamamoto T, Rubin DT, Peyrin-Biroulet L, Ghosh S, Danese S (2023) Difficult-to-treat inflammatory bowel disease: results from an international consensus meeting. Lancet Gastroenterol Hepatol 8(9):853–859. https://doi.org/10.1016/S2468-1253(23)00154-1
Rasmussen NF, Bech BH, Rubin KH, Andersen V (2021) Associations between participation in, intensity of, and time spent on leisure time physical activity and risk of inflammatory bowel disease among older adults (PA-IBD): a prospective cohort study. BMC Public Health 21(1):634. https://doi.org/10.1186/s12889-021-10492-7
Ratajczak-Pawłowska AE, Michalak M, Szymczak-Tomczak A, Rychter AM, Zawada A, Skoracka K, Dobrowolska A, Krela-Kaźmierczak I (2023) Physical activity, quality of diet and bone mineral density in patients with inflammatory bowel disease. J Human Nutri Dietetics: Off J British Dietetic Assoc 36(5):1692–1700. https://doi.org/10.1111/jhn.13199
Robinson RJ, Krzywicki T, Almond L, al-Azzawi F, Abrams K, Iqbal SJ, Mayberry JF (1998) Effect of a low-impact exercise program on bone mineral density in Crohn’s disease: a randomized controlled trial. Gastroenterology 115(1):36-41.https://doi.org/10.1016/s0016-5085(98)70362-2
Sahu P, Kedia S, Ahuja V, Tandon RK (2021) Diet and nutrition in the management of inflammatory bowel disease. Indian J Gastroenterol: Off J Indian Soc Gastroenterol 40(3):253–264. https://doi.org/10.1007/s12664-021-01163-x
Schuch FB, Vancampfort D (2021) Physical activity, exercise, and mental disorders: it is time to move on. Trends in Psychiat Psychother 43(3):177–184. https://doi.org/10.47626/2237-6089-2021-0237
Sharif K, Watad A, Bragazzi NL, Lichtbroun M, Amital H, Shoenfeld Y (2018) Physical activity and autoimmune diseases: get moving and manage the disease. Autoimmun Rev 17(1):53–72. https://doi.org/10.1016/j.autrev.2017.11.010
Spijkerman R, Hesselink L, Bertinetto C, Bongers CCWG, Hietbrink F, Vrisekoop N, Leenen LPH, Hopman MTE, Jansen JJ, Koenderman L (2021) Refractory neutrophils and monocytes in patients with inflammatory bowel disease after repeated bouts of prolonged exercise. Cytometry. part B, clinical cytometry 100(6):676–682. https://doi.org/10.1002/cyto.b.21996
Steensberg A, Toft AD, Bruunsgaard H, Sandmand M, Halkjaer-Kristensen J, Pedersen BK (2001) Strenuous exercise decreases the percentage of type 1 T cells in the circulation. J Appl Physiol (Bethesda, Md.: 1985) 91(4):1708–1712. https://doi.org/10.1152/jappl.2001.91.4.1708
Taylor K, Scruggs PW, Balemba OB, Wiest MM, Vella CA (2018) Associations between physical activity, resilience, and quality of life in people with inflammatory bowel disease. Eur J Appl Physiol 118(4):829–836. https://doi.org/10.1007/s00421-018-3817-z
Tew GA, Jones K, Mikocka-Walus A (2016) Physical activity habits, limitations, and predictors in people with inflammatory bowel disease: a large cross-sectional online survey. Inflamm Bowel Dis 22(12):2933–2942. https://doi.org/10.1097/MIB.0000000000000962
Torres J, Gomes C, Jensen CB, Agrawal M, Ribeiro-Mourão F, Jess T, Colombel JF, Allin KH, Burisch J (2023) Risk factors for developing inflammatory bowel disease within and across families with a family history of IBD. J Crohns Colitis 17(1):30–36. https://doi.org/10.1093/ecco-jcc/jjac111
Ungaro R, Bernstein CN, Gearry R, Hviid A, Kolho KL, Kronman MP, Shaw S, Van Kruiningen H, Colombel JF, Atreja A (2014) Antibiotics associated with increased risk of new-onset Crohn’s disease but not ulcerative colitis: a meta-analysis. Am J Gastroenterol 109(11):1728–1738. https://doi.org/10.1038/ajg.2014.246
Valenzuela PL, Ruilope LM, Santos-Lozano A, Wilhelm M, Kränkel N, Fiuza-Luces C, Lucia A (2023) Exercise benefits in cardiovascular diseases: from mechanisms to clinical implementation. Eur Heart J 44(21):1874–1889. https://doi.org/10.1093/eurheartj/ehad170
Van Der Sloot KW, Joshi AD, Bellavance DR, Gilpin KK, Stewart KO, Lochhead P, Garber JJ, Giallourakis C, Yajnik V, Ananthakrishnan AN, Alizadeh BZ, Xavier RJ, Khalili H (2017) Visceral adiposity, genetic susceptibility, and risk of complications among individuals with Crohn’s disease. Inflamm Bowel Dis 23(1):82–88. https://doi.org/10.1097/MIB.0000000000000978
van Langenberg DR, Gibson PR (2010) Systematic review: fatigue in inflammatory bowel disease. Aliment Pharmacol Ther 32(2):131–143. https://doi.org/10.1111/j.1365-2036.2010.04347.x
Wang R, Li Z, Liu S, Zhang D (2023) Global, regional and national burden of inflammatory bowel disease in 204 countries and territories from 1990 to 2019: a systematic analysis based on the global burden of disease study 2019. BMJ Open 13(3):e065186. https://doi.org/10.1136/bmjopen-2022-065186
Watanabe J, Furukawa S, Yagi S, Shiraishi K, Hanayama M, Tange K, Hashimoto Y, Kitahata S, Mori K, Ninomiya T, Suzuki S, Shibata N, Murakami H, Ohashi K, Hasebe A, Tomida H, Yamamoto Y, Takeshita E, Ikeda Y, Hiasa Y (2021) Time spent per day in strenuous activity and total physical activity are inversely associated with mucosal healing but not with clinical remission in patients with ulcerative colitis. Ann Gastroenterol 34(6):796–801. https://doi.org/10.20524/aog.2021.0663
Watters C, Wright S, Robinson R, Krzywicki T, Almond L, Shevlin M, Mayberry JF (2001) Positive and negative wellbeing as predictors of exercise uptake in Crohn’s disease: an exploratory study. Psychol Health Med 6(3):293–299. https://doi.org/10.1080/13548500123365
Wells GA, Shea B, O’Connell D, Peterson J, Welch V, Losos M, Tugwell P (2021) The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. Available from: http://www.ohri.ca/programs/clinical_epidemiology/oxford.htm. Accessed 7 Feb 2024
Wiestler M, Kockelmann F, Kück M, Kerling A, Tegtbur U, Manns MP, Attaran-Bandarabadi M, Bachmann O (2019) Quality of life is associated with wearable-based physical activity in patients with inflammatory bowel disease: a prospective, observational study. Clin Transl Gastroenterol 10(11):e00094. https://doi.org/10.14309/ctg.0000000000000094
Winer DA, Luck H, Tsai S, Winer S (2016) The Intestinal Immune System in Obesity and Insulin Resistance. Cell Metab 23(3):413–426. https://doi.org/10.1016/j.cmet.2016.01.003
Wojcik-Grzybek D, Hubalewska-Mazgaj M, Surmiak M, Sliwowski Z, Dobrut A, Mlodzinska A, Wojcik A, Kwiecien S, Magierowski M, Mazur-Bialy A, Bilski J, Brzozowski T (2022) The combination of intestinal alkaline phosphatase treatment with moderate physical activity alleviates the severity of experimental colitis in obese mice via modulation of gut microbiota, attenuation of proinflammatory cytokines, oxidative stress biomarkers and DNA oxidative damage in colonic mucosa. Int J Mol Sci 23(6):2964. https://doi.org/10.3390/ijms23062964
Yeshi K, Ruscher R, Hunter L, Daly NL, Loukas A, Wangchuk P (2020) Revisiting inflammatory bowel disease: pathology, treatments, challenges and emerging therapeutics including drug leads from natural products. J Clin Med 9(5):1273. https://doi.org/10.3390/jcm9051273
Zhuo C, Zhao J, Chen M, Lu Y (2021) Physical activity and risks of cardiovascular diseases: a mendelian randomization study. Front Cardiovasc Med 8:722154. https://doi.org/10.3389/fcvm.2021.722154
Funding
Open access funding provided by Università Parthenope di Napoli within the CRUI-CARE Agreement.
Author information
Authors and Affiliations
Contributions
Conceptualization: Carmela Protano, Federica Valeriani and Francesca Gallè; literature search and data analysis: Veronica Volpini, Andrea De Giorgi, Elisa Mazzeo and Francesca Ubaldi; Writing—original draft preparation: Carmela Protano, Francesca Gallè, Veronica Volpini, Andrea De Giorgi, Elisa Mazzeo and Francesca Ubaldi; Writing—review and editing: Carmela Protano, Federica Valeriani and Francesca Gallè; Critical review: Vincenzo Romano Spica; Matteo Vitali.
Corresponding author
Ethics declarations
Ethics approval
Not applicable.
Informed consent
Not applicable.
Conflicts of interest
The authors declare that they have no conflicts of interest.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
About this article
Cite this article
Protano, C., Gallè, F., Volpini, V. et al. Physical activity in the prevention and management of inflammatory bowel disease: a systematic review. J Public Health (Berl.) (2024). https://doi.org/10.1007/s10389-024-02278-z
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10389-024-02278-z