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Boicean, A.; Bratu, D.; Bacila, C.; Tanasescu, C.; Fleacă, R.S.; Mohor, C.I.; Comaniciu, A.; Băluță, T.; Roman, M.D.; Chicea, R.; et al. Fecal Microbiota Transplantation in the Management of Cancer. Encyclopedia. Available online: https://encyclopedia.pub/entry/44966 (accessed on 27 July 2024).
Boicean A, Bratu D, Bacila C, Tanasescu C, Fleacă RS, Mohor CI, et al. Fecal Microbiota Transplantation in the Management of Cancer. Encyclopedia. Available at: https://encyclopedia.pub/entry/44966. Accessed July 27, 2024.
Boicean, Adrian, Dan Bratu, Ciprian Bacila, Ciprian Tanasescu, Radu Sorin Fleacă, Calin Ilie Mohor, Andra Comaniciu, Teodora Băluță, Mihai Dan Roman, Radu Chicea, et al. "Fecal Microbiota Transplantation in the Management of Cancer" Encyclopedia, https://encyclopedia.pub/entry/44966 (accessed July 27, 2024).
Boicean, A., Bratu, D., Bacila, C., Tanasescu, C., Fleacă, R.S., Mohor, C.I., Comaniciu, A., Băluță, T., Roman, M.D., Chicea, R., Cristian, A.N., Hasegan, A., Birsan, S., Dura, H., & Mohor, C.I. (2023, May 29). Fecal Microbiota Transplantation in the Management of Cancer. In Encyclopedia. https://encyclopedia.pub/entry/44966
Boicean, Adrian, et al. "Fecal Microbiota Transplantation in the Management of Cancer." Encyclopedia. Web. 29 May, 2023.
Fecal Microbiota Transplantation in the Management of Cancer
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This entry is adapted from the peer-reviewed paper 10.3390/pathogens12060766

In a mutually beneficial connection with its host, the gut microbiota affects the host’s nutrition, immunity, and metabolism. An increasing number of studies have shown links between certain types of disease and gut dysbiosis or specific microorganisms. Fecal microbiota transplantation (FMT) is strongly advised for the treatment of recurrent or resistant Clostridium difficile infection (CDI) due to its outstanding clinical effectiveness against CDI. The therapeutic potential of FMT for other disorders, particularly inflammatory bowel diseases and malignancies, is currently gaining more and more attention. 

fecal microbiota transplantation Clostridium difficile extra-digestive diseases melanoma cancer

1. Introduction

The gut microbiota, imprinted in our genes, is also influenced by a number of various triggers, such as food, environment, and many other factors. Genetic mapping of the gut microbiota established that it contains 100 billion microorganisms on average, which is 10 times more than the human body’s cells. It is important to outline that the phyla Firmicutes and Bacteroidetes make up the majority of the healthy gut microbiota, followed by the phyla Actinobacteria and Verrucomicrobia; dysbiosis may change the number of saprophytes microbes and cause different diseases [1]. Environmental factors might cause differences in gut microbiota at various times in the same anatomical location in the same person [2][3]. 

2. Fecal Microbiota Transplantation Clinical Benefits in Inflammatory Bowel Diseases

Despite receiving successful inflammatory bowel disease (IBD) treatment that has led to mucosal repair and disease remission, patients with an established diagnosis of IBD, such as those with Crohn’s disease (CD) or ulcerative colitis (UC), may nevertheless experience persistent gastrointestinal symptoms. Functional gastrointestinal symptoms are linked to anxiety, depression, poorer quality of life, and higher healthcare costs in IBD patients. As a result, it is critical to recognize functional gastrointestinal symptoms in this situation in order to select an efficient therapy strategy [4].
According to various scientific investigations, the modification of the gut microbiota composition (dysbiosis) is the primary stakeholder related to IBD pathogenesis. Unfortunately, the specific gut microbiota core composition and metabolic indicators that are thought to be important in the initiation of IBD pathogenesis remain unknown. Many animal studies have been conducted to evaluate fecal microbiota transplantation (FMT) as a potential therapy option for a variety of gastrointestinal and other metabolic disorders. A variety of data suggest an important role of gut microbiota in IBD. FMT has recently received a lot of interest as a new therapeutic strategy in IBD [4][5][6].
FMT can be seen as a promising method for the treatment if the microbiota composition is significantly altered in IBD. In patients with UC and CD, preliminary clinical reports of FMT showed clinical remission that was maintained over a long period of follow-up in many cases and in a small number of additional cases also documented endoscopic and histologic remission [7][8][9][10]. A 36.2% remission rate was discovered in a recent review and meta-analysis of nine studies that included 122 patients who received FMT (79 with UC, 39 with CD, and 4 with unclassified IBD). In contrast to UC patients, where only 22% of patients obtained remission, the rate of remission was higher in younger patients (7–20 years old) and in individuals with CD (64.1 and 60.5%, respectively) [4][5][6][11].
A double-blinded randomized control study in Vermont, USA, aimed to evaluate the viability and safety of performing induction FMT via initial colonoscopy infusion followed by 12 weeks of ambulatory oral maintenance therapy with frozen FMT capsules. Participants in the study were required to have a confirmed diagnosis of UC, with inflammation reaching proximally to at least the recto-sigmoid junction. In the study, 15 subjects were recruited, from which 7 subjects were randomly assigned to the FMT and 8 to the placebo group. Three patients were eliminated from the trial because they did not match the endoscopic criteria for inclusion (Mayo score > 1). The remaining 12 participants (6 in each group) received at least one trial treatment dosage. One patient in the placebo group dropped out after 6 weeks due to disease progression. Two subjects that received frozen FMT capsules achieved clinical remission compared to none in the placebo group. These preliminary findings show that daily encapsulated frozen FMT may increase the duration of index FMT-induced alterations in gut bacterial community composition. Oral frozen encapsulated FMT is a promising FMT delivery system and may be preferred for long-term treatment strategies in UC and other chronic diseases, but further evaluations will have to address home storage concerns [10].
Mańkowska-Wierzbicka et al. published a pilot study in 2020 to evaluate the efficacy of multi-session FMT (weeks 1–6) treatment in active UC patients. Ten UC patients received multi-session FMT (200 mL) from healthy donors by colonoscopy/gastroscopy. Stool sample analyses were performed after the sixth session of FMT administration (week 7) and at the conclusion of the follow-up period (6 months) to examine changes in the microbiome and the concentration of fecal calprotectin. After 6 months, the diversity and richness of the recipients’ fecal microbiota increased but then declined significantly. The trial found that six rounds of rigorous, weekly FMT treatment improved clinical (Truelove and Witts score) and biochemical (CRP, calprotectin) outcomes not just immediately after FMT but also up to six months later. The success of this trial appears to be connected to the good donor microbial features as well as the intended scheme and route of FMT (one colonoscopy and five rounds of gastroduodenoscopy). The substantial proportion of patients (60%) who improved clinically underlines the usefulness of FMT in long-term microbial diversity modification in UC patients [9].
A pilot study was carried out in Italy in which two pediatric UC patients were discussed. They had both been treated with a number of cycles of steroids and antibiotics during the year prior to FMT. They both had a relapsing disease with recurrent episodes of bloody diarrhea and abdominal pain. Patient 1 was receiving mesalamine maintenance treatment. Left-sided colitis was discovered by endoscopic evaluation at the time of FMT with a Mayo score of 0 in the ascending, transverse, descending colon and 2 in the sigmoid–rectum. The FMT follow-up went without a hitch, and the patient reported no symptoms. Colonoscopy results after 12 weeks showed a decrease in disease activity with a Mayo score of 0 in the ascending, transverse, descending colon and 1 in the sigmoid–rectum. Mesalamine and azathioprine were being used in maintenance therapy for patient 2. At the time of FMT, an endoscopic evaluation identified a pancolitis with a Mayo score of 1 in the ascending, transverse colon and 2 in the descending colon–sigmoid–rectum. After FMT, there were no complications, and the patient reported clinical improvement and a decrease in bowel motions [7].
Kunde et al. presented a study with 10 pediatric patients that received enemas for five days; patients achieved remission after one week of fecal microbiota transplantation by enemas. This study shows the importance of FMT administration, even by enemas, without the need for a total colonoscopy [8].
CD with fistula and formation of an intraperitoneal big inflammatory mass has significant morbidity and remains an unresolved challenge. Zhang et al. presented a case of refractory CD complicated by fistula, residual Barium sulfate, and the formation of an intraperitoneal big inflammatory mass that was successfully treated with standardized FMT as a rescue therapy. This case report brings new perspectives for patients with fistulas to prevent surgery [12].
Another study described 133 subjects who received FMT: 77 of the patients suffered from UC, and 56 patients from CD, and the majority of the patients were resistant to therapy or dependent corticotherapy. A total of 57 of the patients evaluated in the study were also associated with recurrent Clostridium difficile infection (CDI). The results of the study showed that FMT obtained a decrease of 71% in symptoms of the treated patients and also prevented relapsing of CDI infection [13] (Table 1).
Table 1. Studies on FMT clinical benefits in IBD patients.
Kunde, S. et al. (2013) [8]
  • Included 10 pediatric patients with active UC
  • FMT with enemas for 5 days
  • Clinical remission at 1 week after FMT
Zhang, F. M. et al. (2013) [12]
  • Study case of CD complicated with fistula
  • Treated with FMT as a rescue therapy
Gianluca Ianiro et al. (2014) [13]
  • A total of 42 patients received FMT nasogastric or nasojejunal tube and gastroscopy
  • A total of 20 patients received FMT enemas
  • A total of 23 through colonoscopy
  • A total of 11 patients had FMT via gastroscopy and colonoscopy
  • FMT obtained a reduction in symptoms of 71%
Mańkowska-Wierzbicka, D. et al. (2020) [9]
  • Included 10 patients with active UC
  • Multisession FMT by colonoscopy/gastroscopy
  • FMT improves calprotectin levels and Truelove and Witts scores
  • 16S rRNA gene sequencing was used for metagenomic analysis showing changes and enrichment in the gut microbiota with healthy microbes
Quagliariello, A. et al. (2020) [7]
  • Pilot study of two pediatric patients with refractory disease
  • FMT showed no adverse effects, and endoscopic appearance was improved
Crothers, J. et al. (2021) [10]
  • Included 12 patients with active UC
  • Ribosomal 16S bacterial sequencing revealed changes in the microbiota
  • FMT induced clinical remission compared to placebo
This treatment approach should still be viewed as experimental because the FMT results in IBD patients are variable. More research is required on choosing eligible donors, picking highly responsive patients, and processing feces in anaerobic environments. Furthermore, researchers are yet unsure of the ideal timing for FMT therapies in IBD patients. Should FMT be utilized as the main course of treatment or as a post-induction measure? The good news is that a number of ongoing trials may contribute to answering the problems raised above. Furthermore, this will make it possible for FMT to be used as a potential therapy option for IBD patients in the future [14].

3. Fecal Microbiota Transplantation Improving Treatment Response in Melanoma

Several studies have been conducted to investigate a possible link between gut microbiota and clinical response to cancer immunotherapy, particularly immune checkpoint inhibitors (ICPI) [15].
In a study published in 2019 by Youngster and colleagues, five patients with treatment-resistant metastatic melanoma were recruited. Two patients with advanced melanoma who experienced a long-lasting, full response to treatment served as the FMT donors. FMT was performed by both oral administration and colonoscopy, and then anti-PD-1 retreatment was used; each patient received complete body imaging, bowel and tumor tissue biopsies, and stool samples before and after treatment. Increased post-FMT infiltration of antigen-presenting cells CD68+ in the gut and tumor was seen by immunohistochemical labeling of samples. Following treatment, there was also an increase in CD8+ T cell infiltration. Following FMT, three patients experienced a full or partial response to treatment [16].
Sivan et al. describe the clinical benefits of commensal Bifidobacterium in improving antitumor immunity and also presents a role in facilitating anti-PD-L1 efficacy; the study was performed on mice. They investigated the formation of melanoma in mice with different commensal microbiota and discovered disparities in spontaneous antitumor immunity that were reduced after cohousing or fecal transfer. This could explain why patients resistant to immunotherapy recovered the response after FMT instillation. The conclusion of this study strengthens the importance of commensal microbes in antitumor immunity and the role of FMT in cancer, especially in patients that undergo immunotherapy [17].
Davar and a group of colleagues conducted a study in 2021 that included 15 patients with advanced melanoma whose condition had progressed or persisted despite taking ICPI. For three months, the researchers gave patients donor-derived FMT through colonoscopy every 14 days, followed by pembrolizumab; 6 out of the 15 patients who were evaluated reacted to the treatment by having their tumors diminish, or their diseases stabilize over time. Additionally, responders displayed a greater abundance of taxa previously linked to immunotherapy response, elevated CD8+ T cell activation, and reduced numbers of interleukin-8-expressing myeloid cells [18].
Baruch and colleagues published a study in 2021 in which he used FMT from 2 allogenic donors who had shown an excellent response to treat 10 patients with ICPI-refractory melanoma (progressive disease during or after ICPI therapy). Three of the ten patients recovered from the immunotherapy response after FMT. According to tumor regression on a PET-CT scan, one of these individuals had a complete response to nivolumab, while the other two had partial responses [19] (Table 2).
Table 2. FMT therapeutic perspectives in melanoma patients.
Youngster et al. 2019 [17]
  • Five patients with melanoma resistant to therapy
  • FMT via gastroscopy and colonoscopy
  • After treatment, three patients out of five recovered sensitivities to treatment and presented a response to immunotherapy
Davar et al. 2021 [19]
  • Included 15 patients with advanced melanoma resistant to immunotherapy
  • Patients received FMT every 14 days with pembrolizumab
  • Six patients diminished their tumors/ stabilized their disease
Baruch et al. 2021 [20]
  • Included 10 patients with refractory melanoma
  • Received FMT from two allogenic donorsThree patients recovered immunotherapy response
  • One patient presented a total response to nivolumab
  • Two patients presented a partial response
Regardless of the limitations of small sample sizes, the fact that two independent cancer centers in different parts of the world with different patient populations reported similar clinical and translational results in accordance with pre-clinical findings using different ICPI (nivolumab versus pembrolizumab) is highly supportive of the validity of these preliminary results [19][20].
Borgers et al. published in 2022 an ongoing double-blinded, randomized phase Ib/II trial in which it will be investigated the safety and efficacy of FMT in anti-PD-1 monoclonal antibodies comparing FMTs derived from ICPI responsive or nonresponding donors in refractory advanced-stage melanoma patients. In this trial, 24 advanced-stage cutaneous melanoma patients who are anti-PD1-refractory will receive an FMT from either an ICPI-responsive or non-responding donor. The investigation will last for almost two years entirely. The primary objective of this trial is the efficacy, defined as a clinical benefit (complete or partial response; durable, stable disease) at 12 weeks and confirmed on a CT scan at 16 weeks, of an FMT treatment in patients with advanced melanoma who were resistant to anti-PD-1 from responsive or non-responding ICPI donors [21].
In order to improve responses and/or reduce toxicity, FMT is increasingly being used to modify gut bacteria in patients receiving cancer immunotherapy [7][9]. In addition to the two studies described, several other clinical trials are investigating FMT along with ICPI in a broader range of tumor types, including renal cell carcinoma, non-small-cell lung cancer, urothelial cancer, and prostate cancer. The majority of these are aimed at patients with similar ICPI resistance and combine FMT with anti-PD-1 monoclonal antibodies [22]. The overall goal of all studies is efficacy and/or safety. The key to developing microbial-based and microbial-targeted therapeutics is the discovery of microbial biomarkers connected with improved responses to cancer treatment [23]. Researchers note that the uniformity of all phases of microbiome investigations, including sampling, storing fecal samples, selecting an experimental design, and using bioinformatics techniques, represents a crucial issue for ascertaining the composition of the microbiota [24].
The new perspectives that FMT opens in recovering response to treatment in melanoma represent an important key discovery in order to improve the survival of oncological patients, especially for patients with melanoma. Additionally, extensive investigations towards interaction between the gut microbiota, immune cells, and clinical response using feces, blood, and tumor samples will increase the effectiveness of FMT therapy in the oncological field.

4. Fecal Microbiota Transplantation and Graft-Versus-Host Disease

Graft-versus-host disease (GvHD) is characterized by inflammation in several organs; stem cell and bone marrow transplants are frequently linked to GvHD. Patients with specific blood illnesses may benefit from allogeneic hematopoietic cell transplantation as a possible curative treatment. Although allogeneic stem cell transplantation can cure many hematological illnesses, GvHD is a leading cause of morbidity and mortality [25]. Systemic administration of high-dose glucocorticoids is the first-line treatment for acute GvHD, but depending on the disease’s severity, only 40–60% of patients react to it [26].
The effectiveness of FMT has been analyzed in the review realized by Maroun Bou Zerdan et al., which compared different studies in patients with corticosteroid refractory GvHD. More than 50% of these patient groups showed responses. More importantly, all of the procedures were well tolerated, with the exception of one patient who experienced lower gastrointestinal hemorrhage and hypoxia and two other patients who experienced bacteremia, all of which were determined to be unrelated to the FMT [3][25][27][28].
Ye Zhao and a group of colleagues conducted a study in 2021, which included 55 patients with steroid-refractory GvHD of the gastrointestinal tract. FMT was administered to 23 patients with grade IV steroid-refractory gastrointestinal-GvHD. Most patients’ microbial richness in terms of variety following FMT was increased when compared to their pre-treatment gut microbiota. Beneficial bacteria, such as Bacteroidetes and Firmicutes, increased in most patients after FMT [27].
In another pilot study, in eight patients with steroid-refractory gastrointestinal tract GvHD, FMT was administered when immunosuppressive medication and other innovative treatments failed. As a result, all patients experienced reduced clinical symptoms (e.g., decreased stool volume and frequency and less abdominal pain), which could be attributed to the enhanced microbial richness [28].
In a teenager with stage IV GvHD who received four doses of FMT at weekly intervals, Zhang F. et al. looked at the longitudinal dynamics of the gut bacteriome (bacterial microbiome), mycobiome (fungal microbiome), and virome (viral microbiome). After FMT, they revealed inconsistent patterns of modification in the recipient’s gut bacteriome, mycobiome, and virome [29].
Numerous clinical investigations are currently being conducted in numerous institutions across the world as a result of the early achievements shown with FMT in patients with hematologic and oncologic illnesses. Borody et al. reported in 2011 the first “cure” of associated immune thrombocytopenia in a patient receiving FMT for UC [30]. In the study conducted by Goeser et al. on two German tertiary clinical centers, positive outcomes were recorded in patients with GVHD after FMT without observing significant side effects in patients [31].
Nearly 40 studies are now listed on Clinicaltrials.gov. The safety of FMT, its application to prevent and treat GvHD following allogeneic hematopoietic stem cell transplantation, improvement in ICPI response, and management of side effects associated with cancer therapy are the main focus points of these studies. Within the next five years, many of these researchers should disclose their mature data on these results [3][32].
Graft-versus-host disease (GvHD) is a systemic disorder that can be resistant to treatment and may cause irreversible organ failure; in light of this situation, researchers want to outline the clinical benefits of FMT in reducing symptoms and alleviating the clinical status of the patients, as well as improving the treatment response by restoring healthy microbiota.

5. Fecal Microbiota Transplantation Improves Response to Chemo and Immunotherapy in Colorectal Cancer

Colorectal cancer (CRC) is the second most frequent cancer in women and the third most common cancer in men worldwide. Males have significantly greater incidence and mortality rates than females. Environmental and genetic variables, such as a high-fat diet and disturbed gut flora, can contribute to the development of this illness [33].
One of the most popular treatment plans for colorectal cancer is FOLFOX (5-fluorouracil, leucovorin, oxaliplatin). Chemotherapeutic drugs cytotoxicity can easily lead to unbalanced gut flora, disrupt the gastrointestinal mucosa’s barrier, and mediate the mucosal inflammation known as “gastrointestinal mucositis” [34].
A pilot study was performed in Taiwan to examine the impact and safety of FMT on intestinal mucosal injury caused by 5-FU-based chemotherapy (FOLFOX) in mice with colon cancer. FMT was performed to restore microbial diversity and composition using faces from healthy wild-type donor mice. The results of the study showed that in mice with colon cancer, FOLFOX treatment greatly slowed the growth of tumors. In mice carrying colorectal cancer, FMT reduced FOLFOX-induced severe diarrhea, bacterial translocation, intestinal mucosal damage, and increased long-term survival. FMT also lessened the disturbance of the barrier integrity and intestinal mucosal inflammation brought on by FOLFOX. These findings suggest that FMT may be clinically effective in treating intestinal dysbiosis and toxicity brought on by chemotherapy [34][35][36].
A recent review realized by Sillo et al. describes the importance of the gut microbiome response in case of colorectal cancer; they note the importance of Proteobacteria Firmicutes in a pre-clinical study in responders in Anti-CTLA-4 therapy and an abundance of Bacteroides in non-responders [37]. Additionally, their review presents another pre-clinical study on mice that outlined that in anti-PD1 therapy, the fecal microbiome in responders was represented by Akkermansia municiphilia, Prevotella spp., while the non-responders presented more Bacteroides spp., Bacteroides_sp._CAG927 [37][38][39].
This research highlights the importance of a healthy gut microbiome for proper response in the case of immunotherapy and chemotherapy in colorectal cancer. Dysbiosis has been associated with the tumoral process in colorectal neoplasia; furthermore, according to cited studies, FMT may improve gastrointestinal symptoms during chemotherapy and increase the survival rate of the patients [40][41].

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Subjects: Gastroenterology & Hepatology
Contributors MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to https://encyclopedia.pub/register :
Adrian Boicean
,
Dan Bratu
,
Ciprian Bacila
,
Ciprian Tanasescu
,
Radu Sorin Fleacă
,
Calin Ilie Mohor
,
Andra Comaniciu
,
Teodora Băluță
,
Mihai Dan Roman
,
Radu Chicea
,
Adrian Nicolae Cristian
,
Adrian Hasegan
,
Sabrina Birsan
,
Horațiu Dura
,
Cosmin Ioan Mohor
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Revisions: 2 times (View History)
Update Date: 30 May 2023
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