Managing inflammatory bowel disease in patients receiving cancer-associated chemotherapy and beyond

Introduction

Managing inflammatory bowel disease (IBD) in patients with active or prior cancer is particularly challenging, given the limited availability of safety and efficacy data for this population. Patients with malignancy are often excluded from clinical trials, and available safety and efficacy data for therapies in this population are frequently derived from small observational studies conducted years after market entry. These limited studies [1,2] suggest that the immunosuppressive effects of cytotoxic chemotherapy improve IBD activity and highlight the higher risks of IBD flare in those IBD patients on hormonal cancer therapies. However, these studies have large confidence intervals (CI) due to their small size, resulting in uncertainty surrounding their conclusions.

In regard to IBD medications in those with a prior history of cancer, one of the first guidelines on the topic, published by the European Crohn’s and Colitis Organisation (ECCO) in 2015 [3], and a subsequent review article [4], recommended delaying immunosuppressant and anti-tumor necrosis factor (TNF) agents for at least 2 years after cancer diagnosis, and up to 5 years for high-recurrence cancers. This recommendation was mostly based on a study by Penn [5], which showed that immunosuppressed renal transplant patients with a prior diagnosis of cancer had the highest recurrence (54%) in the 2 years following completion of chemotherapy, decreasing progressively thereafter (33% at 2-5 years and 13% after 5 years). Although Penn’s study was limited by its retrospective design, and its population did not include IBD patients, its findings influenced early guideline recommendations. The extensive range of biologics, especially gut-selective therapies, adds further complexity to extrapolating Penn’s conclusions to IBD patients. The most recent ECCO 2023 guidelines [6] no longer recommended a 5-year delay in restarting IBD therapy post-cancer, reflecting the distinct cancer risk factors of the IBD population compared to renal transplant recipients.

This review provides a comprehensive analysis of current evidence to help manage IBD in patients with a previous or current history of cancer. While a systematic review answers a focused question through critical appraisal, a scoping review maps the breadth of the existing literature, allowing identification of knowledge gaps and guidance of future research. A scoping review was also considered the most appropriate methodology, given the heterogeneity of studies, and the range of malignancies, treatments and outcomes measured.

Materials and methods

This scoping review was conducted in line with the JBI Evidence Synthesis recommendations and is reported according to Preferred Reporting Items for Systematic Reviews and Meta- Analyses for Scoping Reviews (PRISMA-ScR) standards.

Results

Search and study selection

The PRISMA flow diagram in Fig. 1 summarizes the identification, screening and exclusion of studies. The literature search yielded 3380 citations, including 2373 unique entries. Of these, 2307 were excluded during abstract screening for not meeting eligibility criteria. Sixty-six citations underwent full text review, resulting in the exclusion of 34 studies for the following reasons: wrong study design (n=12), updates or duplicate studies (n=14), observational studies with fewer than 20 patients (n=4), studies with only surgery or radiation as a treatment modality (n=1), studies of the wrong population (n=2), and insufficiently reported results (n=1). An additional study was identified from reference review, and a full paper that was initially found as a poster was also included [7]. Ultimately, 33 studies met the inclusion criteria and were included in the final analysis: 17 studies that evaluated the incident risk of new or recurrent malignancy, 10 studies that examined the use of immune checkpoint inhibitors (ICIs) among patients with prior IBD, and 7 studies that examined IBD patients with active cancer on therapy. One study by Holmer et al [8] evaluated both the risk of cancer recurrence in those with prior malignancies and the safety of IBD medications in those with active cancer.

Figure 1 PRISMA flow diagram

Initiating IBD medications post-malignancy: studies of incident cancer risk

Among the 17 studies [7-23] evaluating the incident risk of new or recurrent malignancies in IBD patients with prior cancers (Table 1), multiple retrospective cohort studies [7-10,12-14,16,17,19], 2 meta-analyses [21,22] and an ongoing prospective study [23] found no increased risk of cancer with IBD medications. However, there were some notable exceptions [15,18]. Khan et al reported a higher risk of basal cell carcinoma (BCC) recurrence with thiopurine use (hazard ratio [HR] 1.65, 95%CI 1.24-2.19; P=0.0005) but no increased risk with anti-TNF or combination therapies [15]. Shani et al found that infliximab monotherapy was associated with a higher risk of non-melanoma skin cancer (NMSC) recurrence (odds ratio [OR] 9.85, 95%CI 2.3-51.7; P=0.003) [18].

Table 1 Studies examining the risk of new or recurrent malignancies in IBD patients with a history of cancer

One study created a risk prediction model to attempt to identify risk factors for the development of new or recurrent cancers in IBD patients with a history of malignancy [11]. Predictors included starting immunosuppressive therapy within 2 years after the diagnosis of index cancer (univariate OR 2.58, 95%CI 1.51-4.39), requiring chemotherapy for index cancer (univariate OR 1.39, 95%CI 0.82-2.31), older age at index cancer diagnosis (univariate OR 2.37, 95%CI 1.24-4.49), and a diagnosis of NMSC (univariate OR 2.45, 95%CI 1.58-3.79) [11].

Conversely, Manosa et al analyzed the ENEIDA registry of 520 IBD patients with extracolonic cancer and found that those treated with anti-TNF or thiopurines had no higher risk of new or recurrent cancers compared to non-exposed patients (16% vs. 18%, P=0.53) [9]. A supplementary analysis of the meta-analysis by Gupta et al, which included 6642 IBD patients with prior cancer, found comparable incident cancer rates among patients not on immunosuppression (39/1000 person-years, 95%CI 25-53), those on anti-TNF (43/1000 person-years, 95%CI 26-60), immunomodulators (60/1000 person-years, 95%CI 25-87), and combination immunosuppression (60/1000 person-years, 95%CI 20-100) [21]. A study by Poullenot et al, which included 538 IBD patients with prior non-digestive cancer [13], evaluated therapy with vedolizumab and came to a similar conclusion. After comparing those on immunomodulators (thiopurines and methotrexate), anti-TNF or vedolizumab, and those not on therapy, they found no significant difference in incident cancer between the treatment groups [13].

Other studies also included evaluation of anti-interleukins. Pang et al’s analysis of a large cohort of 5062 IBD patients with prior cancer found that patients exposed to vedolizumab (59 patients) or ustekinumab (18 patients) did not have a higher risk of new or recurrent cancer compared to historical cancer risk data in patients treated with anti-TNFs, immunomodulators, or without immunosuppressive therapy following cancer diagnosis [16]. Hasan et al’s multicenter retrospective study (341 IBD patients with a history of cancer) found no greater risk of incident cancer in patients receiving post malignancy treatment with ustekinumab (HR 0.88, 95%CI 0.25-3.03), vedolizumab (HR 0.18, 95%CI 0.03-1.35), or anti-TNF (HR 0.47, 95%CI 0.20-1.12) [14].

Studies also evaluated the timing of IBD treatments in relation to the cancer diagnosis. Holmer et al studied a cohort of 170 patients who had recent prior cancer (within 5 years) treated with biologics and immunomodulators, but excluding those on oral small molecule medications, and found the risk of recurrence-free survival was similar between patients who received TNF and non-TNF biologics (HR 0.94, 95%CI 0.24-3.77) [8]. Another cohort study of 463 IBD patients with prior cancer diagnosis found that neither vedolizumab (HR 1.38, 95%CI 0.38-1.36) nor anti-TNF therapy (HR 1.03, 95%CI 0.65-1.64) was associated with a higher risk of cancer recurrence or new cancer development [17]. The median time before the initiation of anti-TNF therapy in this study was 1.3 years, and the above conclusion continued to hold true even when the analysis was restricted to biologic initiation within the first 5 years after cancer diagnosis. A final retrospective cohort study of 390 IBD patients with prior cancer, which used a multivariable Cox model, adjusting for age, IBD subtype, smoking, cancer recurrence risk and cancer stage, found no greater incidence of new or subsequent cancer associated with vedolizumab (adjusted HR 1.36, 95%CI 0.27-7.01) or ustekinumab (adjusted HR 0.96, 95%CI 0.17-5.41), despite the median time to starting treatment with ustekinumab after cancer diagnosis being 5 months [19]. Interestingly, even patients who were exposed to more than 1 biologic did not have a greater risk of subsequent cancer.

Meta-analyses by Micic et al and Waljee et al examined the risk of recurrent or new primary malignancy in larger populations, which included patients with rheumatoid arthritis, psoriasis and IBD. Micic et al (1046 IBD patients) reported no greater cancer risk with anti-TNF (incidence rate ratio 0.68, 95%CI 0.40-1.16) [22]. Waljee et al (25,738 patients, including 1641 with IBD) found similar cancer incidence rates between anti-TNF (30.3 cases/1000 person-years) and control groups (34.4 cases/1000 person-years) [12]. Sensitivity analysis showed no difference in cancer risk between individuals treated with anti-TNF within 2 years of their initial cancer diagnosis and those who started treatment more than 2 years after cancer diagnosis.

The SAPPHIRE registry [23] is investigating the risk of new cancer or cancer recurrence in patients with IBD who are exposed to immunosuppression within 5-10 years of cancer diagnosis, compared to those not exposed to immunosuppression. This study is one of the few studies to include Janus kinase (JAK) inhibitors and ozanimod in the analysis, in addition to immunomodulators, anti-TNFs, vedolizumab and ustekinumab. This study followed 305 patients: 51 were exposed to immunomodulators, 199 to biologics and 16 to small molecules, while 95 patients did not have exposure to these therapies. Some patients were exposed to more than 1 agent. Data from these 305 patients showed that exposure to the above immunosuppressive IBD monotherapies was not associated with a statistically significant risk of new or recurrent cancers compared to no therapy [23].

Managing IBD patients with current active malignancy

Seven cohort studies evaluated outcomes in IBD patients with active cancer receiving cancer therapies, including cytotoxic chemotherapy, hormonal therapy and targeted therapies (Table 2) [8,24-29].

Table 2 Studies of IBD patients with active cancer receiving cancer therapies

Use of IBD medications in patients with active cancer

Guerra Marina’s retrospective study looked at IBD medications in lymphoma patients and found that 58% of patients had changes made to their IBD medications after cancer diagnosis, although the investigators noted no difference in mortality or lymphoma recurrence related to the use of biologics or thiopurines [27]. Holmer et al performed a multicenter retrospective cohort study of 125 IBD patients with active cancer who were treated with biologics (anti-TNF, vedolizumab, ustekinumab), immunomodulators or combination therapy after their cancer diagnosis [8]. Interestingly, there was no difference in the risk of progression-free survival between patients who were treated with anti-TNFs and those treated with non-TNF biologics, including vedolizumab and ustekinumab [8]. Of those treated with anti-TNFs, 18% (incidence rate [IR] 4.4 per 100 person-years) had progression of their cancer, compared to 23% (IR 10.4 per 100 person-years) in the vedolizumab/ustekinumab group, and therefore the study surmised that anti-TNFs, vedolizumab and ustekinumab have comparable safety in active cancer [8].

Types of chemotherapy and their impact on IBD activity

Cytotoxic chemotherapy: Severyns et al (52 patients with lymphoma) found no IBD relapses during cancer treatment with cytotoxic chemotherapy, despite discontinuation of IBD treatments such as thiopurines, anti-TNFs and vedolizumab [25]. Similarly, Hammoudi et al (49 patients with colorectal cancer receiving adjuvant chemotherapy) reported a low IBD relapse rate (4%), despite discontinuation of IBD therapies, with relapses effectively managed using 5-aminosalicylic acid (5-ASA) medications [28]. This study also noted no significantly greater level of chemotherapy-related toxicity in IBD patients [28]. A larger study by Perez-Galindo et al (a multi-center cohort of 180 IBD patients with extraintestinal malignancy), again showed a lower risk of IBD relapse among patients receiving cytotoxic chemotherapy [26].

Hormonal therapy: In contrast, Axelrad et al studied 400 patients with quiescent IBD at the time of breast or prostate cancer diagnosis and found a higher risk of IBD flare with hormonal therapy, either alone (HR 2, 95%CI 1.21-3.29) or combined with cytotoxic chemotherapy (HR 1.86, 95%CI 1.01-3.43) [24]. Notably, patients receiving cytotoxic chemotherapy alone had higher IBD remission rates (75%) compared to those on hormonal therapy alone (42%) at 250 months [24]. The authors recommended close monitoring and a lower threshold for escalation of IBD therapies for patients on hormonal regimens [24].

Targeted chemotherapies: For targeted treatments, Herrera-Gomez et al found that the use of bevacizumab while on chemotherapy among solid tumor patients (n=27) was generally safe in patients with moderately active or quiescent IBD [29]. No IBD flares were observed, although 1 patient experienced perforation due to mesenteric ischemia.

Discussion

The therapeutic options available for managing patients with IBD are ever-expanding, including new anti-interleukins and small molecules. With the emergence of new treatment options, safety data from both randomized controlled studies and real-world data must be considered. This was recently summarized by Bhat et al 2024 [40]. Examples include the elevated risks of infections, venous thromboembolism and dyslipidemia with JAK inhibitors, and the side-effects of bradycardia and liver enzyme elevations with sphingosine 1-phosphate (S1P) receptor modulators.

Unfortunately, most randomized controlled trials do not include data on patients with IBD with active or prior cancer; therefore, managing these patients remains a clinical challenge, given the limited high-quality data. Most evidence to inform decisions in this patient population comes from retrospective observational studies or meta-analyses consisting of such data, limiting generalizability because of potential factors that include selection bias and unmeasured confounding factors. Prospective data, such as those from the SAPPHIRE registry in the US, remain rare, and tend to include patients managed at specialized centers.

Previous recommendations to delay IBD therapy for 5 years after cancer diagnosis were largely based on post-transplant literature. However, more recent studies [12,17,19,21] have challenged this paradigm, with biologics being initiated earlier, often within months of cancer diagnosis. Reflecting this shift, the 2023 ECCO guidelines no longer recommend a 5-year delay in restarting IBD therapy post-cancer, instead advocating for case-by-case decision making [6]. Our review found that most IBD therapies can be safely continued or initiated in patients with prior malignancy (Table 3). Notable exceptions were thiopurines in patients with IBD with prior BCC [15] and infliximab in patients with IBD with prior NMSC [18], where initiation of these medications led to an increased risk of cancer recurrence. This is echoed in the recent American Gastroenterological Association (AGA) clinical practice update [41], which advises one should consider holding thiopurines in patients who develop multiple or recurrent NMSC (such as BCC), non-lymphoma hematological malignancy or cervical/genitourinary cancers. For active lymphoma, this AGA clinical practice update made a stronger recommendation that thiopurines should be held. This AGA practice update also advises stopping anti-TNF therapy in patients with melanoma and considering holding it in patients with lymphoma [41].

Table 3 Recommendations for IBD-related medications in patients with active or prior cancer

Our review also examined the management of IBD in patients with active cancer. Diagnosing an IBD flare during cancer treatment is challenging because of the overlapping symptoms of IBD, infections, and side-effects of cancer therapies [42,43]. Therefore, a comprehensive diagnostic workup, including endoscopic evaluation to rule out infection, is essential prior to initiating treatment for an IBD flare [42]. Although corticosteroids remain the first-line treatment for flares, their potential impact on tumor immunosurveillance should prompt multidisciplinary discussions with oncologists [42,44]. Biologics, such as anti-TNFs, vedolizumab and ustekinumab, are effective second-line options, with early studies suggesting comparable safety profiles [42,44]. Mild flares can often be managed with 5-ASA in ulcerative colitis, and enteral nutrition can be considered in Crohn’s [42]. Coordinating IBD care in cancer patients requires close collaboration between oncologists and gastroenterologists to balance IBD control and cancer management. Treatment decisions should consider both IBD factors (disease activity, severity and flare risk) and malignancy characteristics (cancer type, stage, prognosis and treatment-related immunosuppression), with oncological management often taking precedence [45].

Our review suggests that cytotoxic chemotherapy has a dual role in managing cancer and suppressing IBD activity, as suggested by studies showing lower rates of IBD relapse during treatment. In contrast, hormonal therapies are associated with a greater risk of IBD flare-ups. As ICI therapies are increasingly used across various cancers, IBD flares should be expected, with a pooled estimate of 33-40%. Currently, no data or consensus support treating high-risk IBD patients proactively before starting ICIs, though this remains an area for future study. Targeted therapies, such as bevacizumab, appear to be generally safe in patients with quiescent or moderately active IBD, although rare complications, such as mesenteric ischemia, have been reported.

Despite some uncertainty, our scoping review aligns with the current ECCO 2023 guidelines [6] and the recent AGA clinical practice update [41], which state that, with a few exceptions, most IBD-related medications can generally be continued or initiated in patients with active or prior cancer (Table 3).

The ECCO guidelines state that thiopurines should preferably be withdrawn in patients with active cancer. The AGA practice update suggests stopping azathioprine in patients with lymphoma, other hematological cancers, NMSC or cervical/genitourinary cancers, but suggests that azathioprine can be continued in patients with melanoma.

For patients with a history of cancer, the ECCO guidelines suggest that thiopurines can be initiated with caution. Our scoping review concurs with this conclusion.

The ECCO guidelines recommend the use of anti-TNFs in patients with IBD with active or previous history of cancer; however, the AGA practice update suggests stopping anti-TNF therapy in patients with active melanoma and considering alternatives in patients with active lymphoma.

Data on vedolizumab and ustekinumab in active cancer remain limited, but the AGA practice update supports no change in therapy for patients taking vedolizumab or ustekinumab, whereas the ECCO recommends that decisions be made on a case-by-case basis.

The ECCO guidelines concur with our scoping review, showing that neither vedolizumab nor ustekinumab appears to increase the risk of cancer recurrence in patients with prior malignancy.

There is insufficient evidence on JAK inhibitors or S1P receptor modulators in patients with current or prior malignancy, and this is stated in the ECCO guidelines. The AGA practice update, however, supports no change in therapy in those with active cancer. Our scoping review, mainly influenced by the SAPPHIRE registry, showed no increased cancer risk with JAK inhibitors or ozanimod in prior cancer patients, though sample sizes are small.

Given the uncertainty concerning optimal IBD management for patients with active or prior malignancy, treatment decisions should be collaborative, involving patients, gastroenterologists, and oncologists. As new therapies emerge, prospective registries will be crucial for guiding evidence-based care.

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