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).

Fig. 1
figure 1

PRISMA flow diagram for the article selection

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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).

Table 1 Data from the studies regarding the possible role of physical activity in IBD development
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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”.

Table 2 Data from the studies regarding the possible role of physical activity in IBD management
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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.