The potential role of prebiotics, probiotics, and synbiotics in adjuvant cancer therapy especially colorectal cancer
Zahoor Alam
School of Life Sciences, Northwestern Polytechnical University, Xi'an, China
Contribution: Writing - original draft
Search for more papers by this authorCorresponding Author
Xiaoya Shang
School of Life Sciences, Northwestern Polytechnical University, Xi'an, China
Correspondence
Xiaoya Shang, School of Life Sciences, Northwestern Polytechnical University, 127 West Youyi Road, Xi'an, Shaanxi 710072, China.
Email: [email protected]
Yong Zhang, Department of Surgical Oncology, the First Affiliated Hospital of Xi'an Jiaotong University, 227 Yanta West Road, Xi'an, Shaanxi 710061, China.
Email: [email protected]
Contribution: Supervision, Writing - review & editing
Search for more papers by this authorKhansa Effat
School of Life Sciences, Northwestern Polytechnical University, Xi'an, China
Contribution: Writing - review & editing
Search for more papers by this authorFreeha Kanwal
School of Life Sciences, Northwestern Polytechnical University, Xi'an, China
Contribution: Writing - review & editing
Search for more papers by this authorXiaoqin He
School of Life Sciences, Northwestern Polytechnical University, Xi'an, China
Contribution: Writing - review & editing
Search for more papers by this authorYanye Li
School of Life Sciences, Northwestern Polytechnical University, Xi'an, China
Contribution: Writing - review & editing
Search for more papers by this authorChunlan Xu
School of Life Sciences, Northwestern Polytechnical University, Xi'an, China
Contribution: Writing - review & editing
Search for more papers by this authorWeining Niu
School of Life Sciences, Northwestern Polytechnical University, Xi'an, China
Contribution: Writing - review & editing
Search for more papers by this authorAbdul Rouf War
School of Life Sciences, Northwestern Polytechnical University, Xi'an, China
Contribution: Writing - review & editing
Search for more papers by this authorCorresponding Author
Yong Zhang
Department of Surgical Oncology, the First Affiliated Hospital of Xi'an Jiaotong University, Xi'an, China
Correspondence
Xiaoya Shang, School of Life Sciences, Northwestern Polytechnical University, 127 West Youyi Road, Xi'an, Shaanxi 710072, China.
Email: [email protected]
Yong Zhang, Department of Surgical Oncology, the First Affiliated Hospital of Xi'an Jiaotong University, 227 Yanta West Road, Xi'an, Shaanxi 710061, China.
Email: [email protected]
Contribution: Supervision, Writing - review & editing
Search for more papers by this authorZahoor Alam
School of Life Sciences, Northwestern Polytechnical University, Xi'an, China
Contribution: Writing - original draft
Search for more papers by this authorCorresponding Author
Xiaoya Shang
School of Life Sciences, Northwestern Polytechnical University, Xi'an, China
Correspondence
Xiaoya Shang, School of Life Sciences, Northwestern Polytechnical University, 127 West Youyi Road, Xi'an, Shaanxi 710072, China.
Email: [email protected]
Yong Zhang, Department of Surgical Oncology, the First Affiliated Hospital of Xi'an Jiaotong University, 227 Yanta West Road, Xi'an, Shaanxi 710061, China.
Email: [email protected]
Contribution: Supervision, Writing - review & editing
Search for more papers by this authorKhansa Effat
School of Life Sciences, Northwestern Polytechnical University, Xi'an, China
Contribution: Writing - review & editing
Search for more papers by this authorFreeha Kanwal
School of Life Sciences, Northwestern Polytechnical University, Xi'an, China
Contribution: Writing - review & editing
Search for more papers by this authorXiaoqin He
School of Life Sciences, Northwestern Polytechnical University, Xi'an, China
Contribution: Writing - review & editing
Search for more papers by this authorYanye Li
School of Life Sciences, Northwestern Polytechnical University, Xi'an, China
Contribution: Writing - review & editing
Search for more papers by this authorChunlan Xu
School of Life Sciences, Northwestern Polytechnical University, Xi'an, China
Contribution: Writing - review & editing
Search for more papers by this authorWeining Niu
School of Life Sciences, Northwestern Polytechnical University, Xi'an, China
Contribution: Writing - review & editing
Search for more papers by this authorAbdul Rouf War
School of Life Sciences, Northwestern Polytechnical University, Xi'an, China
Contribution: Writing - review & editing
Search for more papers by this authorCorresponding Author
Yong Zhang
Department of Surgical Oncology, the First Affiliated Hospital of Xi'an Jiaotong University, Xi'an, China
Correspondence
Xiaoya Shang, School of Life Sciences, Northwestern Polytechnical University, 127 West Youyi Road, Xi'an, Shaanxi 710072, China.
Email: [email protected]
Yong Zhang, Department of Surgical Oncology, the First Affiliated Hospital of Xi'an Jiaotong University, 227 Yanta West Road, Xi'an, Shaanxi 710061, China.
Email: [email protected]
Contribution: Supervision, Writing - review & editing
Search for more papers by this authorAbstract
Cancer is a global health issue that is rising swiftly with younger people and an increased number of patients. The role of human microbiota in the pathophysiology of tumors has been paid more and more attention. Microecologics including prebiotics, probiotics, and synbiotics are among the best validated/proven resources for the application of microbiological prophylaxis and therapy. There is strong evidence that microecologics have anti-cancer activity and their potential association with cancer is significant. In this review, we will focus on the role of prebiotics, probiotics, and synbiotics in tumor suppression in maintaining the colon barrier, metabolism, immune regulation, inhibition of host tumor cell proliferation, and epidemiological-based recommendations. Besides, other signs illuminate the role of microecological agents to adjunct the cancer treatment and counter the toxic side effects of cancer drugs. In addition, we will explore their role in chemotherapy, where these probiotics can be used as an adjunct to chemotherapy, counteracting the toxic side effects of chemotherapy drugs to minimize or optimize the therapeutic effect. In the treatment of cancer, we can see the role of prebiotics, probiotics, synbiotics, and their application in cancer patients, and the effectiveness effect can be considered as a clinical benefit.
Practical applications
A large number of studies have shown that microecologics including prebiotics, probiotics, and synbiotics play an important role in regulating intestinal microecology and contribute to the prevention and treatment of cancer, indicating that prebiotics, probiotics, and synbiotics have the potential to be used as microecological modulators in the adjuvant therapy of cancer. However, it is not clear what is the anti-tumor mechanism of these microecologics and how they antagonize the side effects of cancer chemotherapy and protect normal cells. This paper reviews the role of prebiotics, probiotics, and synbiotics in tumor suppression in maintaining the colon barrier, metabolism, immune regulation, and prevention of rapid growth of host cells, as well as their potential role in cancer chemotherapy. This review helps to better understand the relationship between prebiotics, probiotics, and synbiotics with immune regulation, intestinal microecology, metabolic regulation, and cell proliferation and provides strong evidence for their potential application as microecologics in cancer adjuvant therapy.
CONFLICT OF INTEREST
The authors declared that they have no conflict of interest.
REFERENCES
- Airley, R. (2009). Cancer chemotherapy: Basic science to the clinic. John Wiley & Sons.
- Ambalam, P., Raman, M., Purama, R. K., & Doble, M. (2016). Probiotics, prebiotics and colorectal cancer prevention. Best Practice & Research Clinical Gastroenterology, 30(1), 119–131.
- Amitay, E. L., Carr, P. R., Gies, A., Laetsch, D. C., & Brenner, H. (2020). Probiotic/synbiotic treatment and postoperative complications in colorectal cancer patients: Systematic review and meta-analysis of randomized controlled trials. Clinical and Translational Gastroenterology, 11(12), e00268.
- Anandharaj, M., Sivasankari, B., & Rani, R. P. (2020). Corrigendum to “effects of probiotics, prebiotics, and Synbiotics on hypercholesterolemia: A review”. Chinese Journal of Biology, 2020, 1–8. https://doi.org/10.1155/2020/8236703
10.1155/2020/8236703 Google Scholar
- Arruebo, M., Vilaboa, N., Sáez-Gutierrez, B., Lambea, J., Tres, A., Valladares, M., & González-Fernández, A. (2011). Assessment of the evolution of cancer treatment therapies. Cancers, 3(3), 3279–3330. https://doi.org/10.3390/cancers3033279
- Aso, Y., Akaza, H., Kotake, T., Tsukamoto, T., Imai, K., Naito, S., & Group, B. S. (1995). Preventive effect of a Lactobacillus casei preparation on the recurrence of superficial bladder cancer in a double-blind trial. European Urology, 27, 104–109.
- Boyle, R. J., Robins-Browne, R. M., & Tang, M. L. (2006). Probiotic use in clinical practice: What are the risks? The American Journal of Clinical Nutrition, 83(6), 1256–1264.
- Braegger, C., Decsi, T., Dias, J. A., Hartman, C., Kolacek, S., Koletzko, B., Koletzko, S., Mihatsch, W., Moreno, L., Puntis, J., Shamir, R., Szajewska, H., Turck, D., van Goudoever, J., & ESPGHAN Committee on Nutrition. (2010). Practical approach to paediatric enteral nutrition: A comment by the ESPGHAN committee on nutrition. Journal of Pediatric Gastroenterology and Nutrition, 51(1), 110–122.
- Carvalho, R., Vaz, A., Pereira, F. L., Dorella, F., Aguiar, E., Chatel, J.-M., Bermudez, L., Langella, P., Fernandes, G., Figueiredo, H., Goes-Neto, A., & Azevedo, V. (2018). Gut microbiome modulation during treatment of mucositis with the dairy bacterium Lactococcus lactis and recombinant strain secreting human antimicrobial PAP. Scientific Reports, 8(1), 15072. https://doi.org/10.1038/s41598-018-33469-w
- Chabner, B. A., & Roberts, T. G., Jr. (2005). Chemotherapy and the war on cancer. Nature Reviews Cancer, 5(1), 65–72.
- Chahwan, B., Kwan, S., Isik, A., van Hemert, S., Burke, C., & Roberts, L. (2019). Gut feelings: A randomised, triple-blind, placebo-controlled trial of probiotics for depressive symptoms. Journal of Affective Disorders, 253, 317–326.
- Chaiyasut, C., Pattananandecha, T., Sirilun, S., Suwannalert, P., Peerajan, S., & Sivamaruthi, B. S. (2017). Synbiotic preparation with lactic acid bacteria and inulin as a functional food: In vivo evaluation of microbial activities, and preneoplastic aberrant crypt foci. Food Science and Technology, 37, 328–336.
- Chakraborti, C. (2011). The status of synbiotics in colorectal cancer. Life Sciences and Medicine Research, 2011, 1–15.
- Chan, H.-K., & Ismail, S. (2014). Side effects of chemotherapy among cancer patients in a Malaysian general hospital: Experiences, perceptions and informational needs from clinical pharmacists. Asian Pacific Journal of Cancer Prevention, 15(13), 5305–5309.
- Chattopadhyay, I., Dhar, R., Pethusamy, K., Seethy, A., Srivastava, T., Sah, R., Sharma, J., & Karmakar, S. (2021). Exploring the role of gut microbiome in colon cancer. Applied Biochemistry and Biotechnology, 193(6), 1780–1799.
- Chen, Y., Jungsuwadee, P., Vore, M., Butterfield, D. A., & St Clair, D. K. (2007). Collateral damage in cancer chemotherapy: Oxidative stress in nontargeted tissues. Molecular Interventions, 7(3), 147–156.
- Chen, Y., Qi, A., Teng, D., Li, S., Yan, Y., Hu, S., & Du, X. (2022). Probiotics and synbiotics for preventing postoperative infectious complications in colorectal cancer patients: A systematic review and meta-analysis. Techniques in Coloproctology, 26, 1–12.
- Chen, Y.-L., & Li, Q.-Z. (2007). Prediction of apoptosis protein subcellular location using improved hybrid approach and pseudo-amino acid composition. Journal of Theoretical Biology, 248(2), 377–381.
- Chong, E. S. L. (2014). A potential role of probiotics in colorectal cancer prevention: Review of possible mechanisms of action. World Journal of Microbiology and Biotechnology, 30(2), 351–374.
- Chundakkattumalayil, H. C., Kumar, S., Narayanan, R., & Thalakattil Raghavan, K. (2019). Role of L. plantarum KX519413 as probiotic and acacia gum as prebiotic in gastrointestinal tract strengthening. Microorganisms, 7(12), 659.
- Cruz, B. C., Sarandy, M. M., Messias, A. C., Gonçalves, R. V., Ferreira, C. L., & Peluzio, M. C. (2020). Preclinical and clinical relevance of probiotics and synbiotics in colorectal carcinogenesis: A systematic review. Nutrition Reviews, 78(8), 667–687.
- da Silva Almeida, A. P., Avi, C. M., Barbisan, L. F., de Moura, N. A., Caetano, B. F. R., Romualdo, G. R., & Sivieri, K. (2015). Yacon (Smallanthus sonchifolius) and Lactobacillus acidophilus CRL 1014 reduce the early phases of colon carcinogenesis in male Wistar rats. Food Research International, 74, 48–54.
- Davani-Davari, D., Negahdaripour, M., Karimzadeh, I., Seifan, M., Mohkam, M., Masoumi, S. J., Berenjian, A., & Ghasemi, Y. (2019). Prebiotics: Definition, types, sources, mechanisms, and clinical applications. Foods, 8(3), 92. https://doi.org/10.3390/foods8030092
- Davis, C. D., & Milner, J. A. (2009). Gastrointestinal microflora, food components and colon cancer prevention. The Journal of Nutritional Biochemistry, 20(10), 743–752.
- De Preter, V., Hamer, H. M., Windey, K., & Verbeke, K. (2011). The impact of pre-and/or probiotics on human colonic metabolism: Does it affect human health? Molecular Nutrition & Food Research, 55(1), 46–57.
- Dekaboruah, E., Suryavanshi, M. V., Chettri, D., & Verma, A. K. (2020). Human microbiome: An academic update on human body site specific surveillance and its possible role. Archives of Microbiology, 202(8), 2147–2167. https://doi.org/10.1007/s00203-020-01931-x
- den Besten, G., van Eunen, K., Groen, A. K., Venema, K., Reijngoud, D.-J., & Bakker, B. M. (2013). The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. Journal of Lipid Research, 54(9), 2325–2340. https://doi.org/10.1194/jlr.R036012
- Didari, T., Solki, S., Mozaffari, S., Nikfar, S., & Abdollahi, M. (2014). A systematic review of the safety of probiotics. Expert Opinion on Drug Safety, 13(2), 227–239.
- Donohoe, D. R., Holley, D., Collins, L. B., Montgomery, S. A., Whitmore, A. C., Hillhouse, A., Curry, K. P., Renner, S. W., Greenwalt, A., Ryan, E. P., Godfrey, V., Heise, M. T., Threadgill, D. S., Han, A., Swenberg, J. A., Threadgill, D. W., & Bultman, S. J. (2014). A gnotobiotic mouse model demonstrates that dietary fiber protects against colorectal tumorigenesis in a microbiota-and butyrate-dependent manner. Cancer Discovery, 4(12), 1387–1397.
- dos Santos Cruz, B. C., da Silva Duarte, V., Giacomini, A., Corich, V., de Paula, S. O., da Silva Fialho, L., Guimarães, V. M., de Luces Fortes Ferreira, C. L., & Gouveia Peluzio, M. D. C. (2020). Synbiotic VSL# 3 and yacon-based product modulate the intestinal microbiota and prevent the development of pre-neoplastic lesions in a colorectal carcinogenesis model. Applied Microbiology and Biotechnology, 104(20), 8837–8857.
- Dugoua, J.-J., Machado, M., Zhu, X., Chen, X., Koren, G., & Einarson, T. R. (2009). Probiotic safety in pregnancy: A systematic review and meta-analysis of randomized controlled trials of Lactobacillus, Bifidobacterium, and Saccharomyces spp. Journal of Obstetrics and Gynaecology Canada, 31(6), 542–552.
- Dunislawska, A., Slawinska, A., Bednarczyk, M., & Siwek, M. J. G. (2019). Transcriptome modulation by in ovo delivered Lactobacillus synbiotics in a range of chicken tissues. Gene, 698, 27–33.
- Ebede, C. C., Jang, Y., & Escalante, C. P. (2017). Cancer-related fatigue in cancer survivorship. Medical Clinics, 101(6), 1085–1097.
- FAO/WHO Consultation on Health Implications of Acrylamide in Food, World Health Organization. Food Safety Programme., and Food and Agriculture Organization of the United Nations. (2002). Health Implications of Acrylamide in Food: Report of a Joint FAO/WHO Consultation, WHO Headquarters, Geneva, Switzerland, 25–27 June 2002. World Health Organization.
- Femia, A. P., Luceri, C., Dolara, P., Giannini, A., Biggeri, A., Salvadori, M., Clune, Y., Collins, K. J., Paglierani, M., & Caderni, G. (2002). Antitumorigenic activity of the prebiotic inulin enriched with oligofructose in combination with the probiotics lactobacillus rhamnosus and Bifidobacterium lactis on azoxymethane-induced colon carcinogenesis in rats. Carcinogenesis, 23(11), 1953–1960.
- Femia, A. P., Salvadori, M., Broekaert, W. F., François, I. E., Delcour, J. A., Courtin, C. M., & Caderni, G. (2010). Arabinoxylan-oligosaccharides (AXOS) reduce preneoplastic lesions in the colon of rats treated with 1, 2-dimethylhydrazine (DMH). European Journal of Nutrition, 49(2), 127–132.
- Fidelis, M., Santos, J. S., Escher, G. B., Rocha, R. S., Cruz, A. G., Cruz, T. M., Marques, M. B., Nunes, J. B., do Carmo, M. A. V., de Almeida, L. A., Kaneshima, T., Azevedo, L., & Granato, D. (2021). Polyphenols of jabuticaba [Myrciaria jaboticaba (Vell.) O. Berg] seeds incorporated in a yogurt model exert antioxidant activity and modulate gut microbiota of 1, 2-dimethylhydrazine-induced colon cancer in rats. Food Chemistry, 334, 127565.
- Fijan, S. (2014). Microorganisms with claimed probiotic properties: An overview of recent literature. International Journal of Environmental Research and Public Health, 11(5), 4745–4767. https://doi.org/10.3390/ijerph110504745
- Fitzmaurice, C., Akinyemiju, T. F., Al Lami, F. H., Alam, T., Alizadeh-Navaei, R., Allen, C., & Anderson, B. O. (2018). Global, regional, and national cancer incidence, mortality, years of life lost, years lived with disability, and disability-adjusted life-years for 29 cancer groups, 1990 to 2016: A systematic analysis for the global burden of disease study. JAMA Oncology, 4(11), 1553–1568.
- Fong, W., Li, Q., & Yu, J. (2020). Gut microbiota modulation: A novel strategy for prevention and treatment of colorectal cancer. Oncogene, 39(26), 4925–4943. https://doi.org/10.1038/s41388-020-1341-1
- Fotiadis, C. I., Stoidis, C. N., Spyropoulos, B. G., & Zografos, E. D. (2008). Role of probiotics, prebiotics and synbiotics in chemoprevention for colorectal cancer. World Journal of Gastroenterology: WJG, 14(42), 6453–6457.
- Garg, S., Yoo, J., & Winquist, E. (2010). Nutritional support for head and neck cancer patients receiving radiotherapy: A systematic review. Supportive Care in Cancer, 18(6), 667–677.
- Geier, M. S., Butler, R. N., & Howarth, G. S. (2006). Probiotics, prebiotics and synbiotics: A role in chemoprevention for colorectal cancer? Cancer Biology & Therapy, 5(10), 1265–1269.
- Ghoneum, M., & Felo, N. (2015). Selective induction of apoptosis in human gastric cancer cells by lactobacillus kefiri (PFT), a novel kefir product. Oncology Reports, 34(4), 1659–1666.
- Gianotti, L., Morelli, L., Galbiati, F., Rocchetti, S., Coppola, S., Beneduce, A., Gilardini, C., Zonenschain, D., Nespoli, A., & Braga, M. (2010). A randomized double-blind trial on perioperative administration of probiotics in colorectal cancer patients. World Journal of Gastroenterology: WJG, 16(2), 167–175.
- Gibson, G. R., Hutkins, R., Sanders, M. E., Prescott, S. L., Reimer, R. A., Salminen, S. J., Scott, K., Stanton, C., Swanson, K. S., Cani, P. D., Verbeke, K., & Reid, G. (2017). Expert consensus document: The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nature Reviews Gastroenterology & Hepatology, 14(8), 491–502.
- Gibson, G. R., Probert, H. M., Van Loo, J., Rastall, R. A., & Roberfroid, M. B. (2004). Dietary modulation of the human colonic microbiota: Updating the concept of prebiotics. Nutrition Research Reviews, 17(2), 259–275.
- Gibson, G. R., & Roberfroid, M. B. (1995). Dietary modulation of the human colonic microbiota: Introducing the concept of prebiotics. The Journal of Nutrition, 125(6), 1401–1412. https://doi.org/10.1093/jn/125.6.1401
- Gogineni, V. K., Morrow, L. E., & Malesker, M. (2013). Probiotics: Mechanisms of action and clinical applications. Journal of Probiotics & Health, 1(101), 2.
- Goh, K. K., Liu, Y.-W., Kuo, P.-H., Chung, Y.-C. E., Lu, M.-L., & Chen, C.-H. (2019). Effect of probiotics on depressive symptoms: A meta-analysis of human studies. Psychiatry Research, 282, 112568.
- Grimoud, J., Durand, H., De Souza, S., Monsan, P., Ouarné, F., Theodorou, V., & Roques, C. (2010). In vitro screening of probiotics and synbiotics according to anti-inflammatory and anti-proliferative effects. International Journal of Food Microbiology, 144(1), 42–50.
- Gröber, U., Holzhauer, P., Kisters, K., Holick, M., & Adamietz, I. (2016). Micronutrients in oncological intervention. Nutrients, 8(3), 163.
- Guo, P., Zhang, K., Ma, X., & He, P. (2020). Clostridium species as probiotics: Potentials and challenges. Journal of Animal Science and Biotechnology, 11(1), 24. https://doi.org/10.1186/s40104-019-0402-1
- Hatakka, K., Holma, R., El-Nezami, H., Suomalainen, T., Kuisma, M., Saxelin, M., Poussa, T., Mykkänen, H., & Korpela, R. (2008). The influence of Lactobacillus rhamnosus LC705 together with Propionibacterium freudenreichii ssp. shermanii JS on potentially carcinogenic bacterial activity in human colon. International Journal of Food Microbiology, 128(2), 406–410.
- Hemarajata, P., Gao, C., Pflughoeft, K., Thomas, C., Saulnier, D., Spinler, J., & Versalovic, J. (2013). Lactobacillus reuteri-specific immunoregulatory gene rsiR modulates histamine production and immunomodulation by Lactobacillus reuteri. Journal of Bacteriology, 195(24), 5567–5576.
- Hempel, S., Newberry, S., Ruelaz, A., Wang, Z., Miles, J., Suttorp, M. J., Johnsen, B., Shanman, R., Slusser, W., Fu, N., Smith, A., Roth, B., Polak, J., Motala, A., Perry, T., & Shekelle, P. G. (2011). Safety of probiotics used to reduce risk and prevent or treat disease. Evidence REPORT/technology Assessment, (200), 1–645.
- Hong, B.-Y., Sobue, T., Choquette, L., Dupuy, A. K., Thompson, A., Burleson, J. A., Salner, A. L., Schauer, P. K., Joshi, P., Fox, E., Shin, D. G., Weinstock, G. M., Strausbaugh, L. D., Dongari-Bagtzoglou, A., Peterson, D. E., & Diaz, P. I. (2019). Chemotherapy-induced oral mucositis is associated with detrimental bacterial dysbiosis. Microbiome, 7(1), 66. https://doi.org/10.1186/s40168-019-0679-5
- Hotz, C., & Gibson, R. S. (2007). Traditional food-processing and preparation practices to enhance the bioavailability of micronutrients in plant-based diets. The Journal of Nutrition, 137(4), 1097–1100.
- Hsu, C. K., Liao, J. W., Chung, Y. C., Hsieh, C. P., & Chan, Y. C. (2004). Xylooligosaccharides and fructooligosaccharides affect the intestinal microbiota and precancerous colonic lesion development in rats. The Journal of Nutrition, 134(6), 1523–1528. https://doi.org/10.1093/jn/134.6.1523
- Hughes, R., & Rowland, I. (2001). Stimulation of apoptosis by two prebiotic chicory fructans in the rat colon. Carcinogenesis, 22(1), 43–47.
- Ishikawa, H., Akedo, I., Otani, T., Suzuki, T., Nakamura, T., Takeyama, I., Ishiguro, S., Miyaoka, E., Sobue, T., & Kakizoe, T. (2005). Randomized trial of dietary fiber and Lactobacillus casei administration for prevention of colorectal tumors. International Journal of Cancer, 116(5), 762–767.
- Johnstone, R. W. (2002). Histone-deacetylase inhibitors: Novel drugs for the treatment of cancer. Nature Reviews Drug Discovery, 1(4), 287–299.
- Johnstone, R. W., Ruefli, A. A., & Lowe, S. W. (2002). Apoptosis: A link between cancer genetics and chemotherapy. Cell, 108(2), 153–164.
- Jones, S. L., & Blikslager, A. T. (2004). Disorders of the gastrointestinal system. In Equine Internal Medicine (2nd ed., pp. 769–949). USA: Elsevier.
10.1016/B0-72-169777-1/50015-9 Google Scholar
- Kawasaki, T., & Kawai, T. (2014). Toll-like receptor signaling pathways. Frontiers in Immunology, 5, 461. https://doi.org/10.3389/fimmu.2014.00461
- Kaźmierczak-Siedlecka, K., Daca, A., Fic, M., van de Wetering, T., Folwarski, M., & Makarewicz, W. (2020). Therapeutic methods of gut microbiota modification in colorectal cancer management–fecal microbiota transplantation, prebiotics, probiotics, and synbiotics. Gut Microbes, 11(6), 1518–1530.
- Klinder, A., Forster, A., Caderni, G., Femia, A. P., & Pool-Zobel, B. L. (2004). Fecal water genotoxicity is predictive of tumor-preventive activities by inulin-like Oligofructoses, probiotics (Lactobacillus rhamnosus and Bifidobacterium lactis), and their Synbiotic combination. Nutrition and Cancer, 49(2), 144–155. https://doi.org/10.1207/s15327914nc4902_5
- Koh, J. H., Kim, N., Hwang, D., & Lim, Y. H. (2013). Effect of water-soluble fraction of cherry tomatoes on the adhesion of probiotics and Salmonella to intestinal epithelial cells. Journal of the Science of Food and Agriculture, 93(15), 3897–3900.
- Kotzampassi, K., Stavrou, G., Damoraki, G., Georgitsi, M., Basdanis, G., Tsaousi, G., & Giamarellos-Bourboulis, E. J. (2015). A four-probiotics regimen reduces postoperative complications after colorectal surgery: A randomized, double-blind, placebo-controlled study. World Journal of Surgery, 39(11), 2776–2783.
- Le Leu, R. K., Brown, I. L., Hu, Y., Bird, A. R., Jackson, M., Esterman, A., & Young, G. P. (2005). A synbiotic combination of resistant starch and Bifidobacterium lactis facilitates apoptotic deletion of carcinogen-damaged cells in rat colon. The Journal of Nutrition, 135(5), 996–1001.
- Le Leu, R. K., Hu, Y., Brown, I. L., Woodman, R. J., & Young, G. P. (2010). Synbiotic intervention of Bifidobacterium lactis and resistant starch protects against colorectal cancer development in rats. Carcinogenesis, 31(2), 246–251.
- Lee, C., & Longo, V. (2011). Fasting vs dietary restriction in cellular protection and cancer treatment: From model organisms to patients. Oncogene, 30(30), 3305–3316.
- Lee, D. K., Jang, S., Kim, M. J., Kim, J. H., Chung, M. J., Kim, K. J., & Ha, N. J. (2008). Anti-proliferative effects of Bifidobacterium adolescentis SPM0212 extract on human colon cancer cell lines. BMC Cancer, 8(1), 1–8.
- Lee, J.-W., Choi, S.-P., Thiruvenkatachari, R., Shim, W.-G., & Moon, H. (2006). Submerged microfiltration membrane coupled with alum coagulation/powdered activated carbon adsorption for complete decolorization of reactive dyes. Water Research, 40(3), 435–444.
- Li, Y., Elmén, L., Segota, I., Xian, Y., Tinoco, R., Feng, Y., Fujita, Y., Segura Muñoz, R. R., Schmaltz, R., Bradley, L. M., Ramer-Tait, A., Zarecki, R., Long, T., Peterson, S. N., & Ronai, Z. A. (2020). Prebiotic-induced anti-tumor immunity attenuates tumor growth. Cell reports, 30(6), 1753–1766.e6. https://doi.org/10.1016/j.celrep.2020.01.035
- Liao, W., Khan, I., Huang, G., Chen, S., Liu, L., Leong, W. K., Li, X. A., Wu, J., & Wendy Hsiao, W. (2021). Bifidobacterium animalis: The missing link for the cancer-preventive effect of Gynostemma pentaphyllum. Gut Microbes, 13(1), 1847629.
- Links, M., & Lewis, C. (1999). Chemoprotectants. Drugs, 57(3), 293–308.
- Liu, Z.-H., Huang, M.-J., Zhang, X.-W., Wang, L., Huang, N.-Q., Peng, H., Lan, P., Peng, J. S., Yang, Z., Xia, Y., Liu, W. J., Yang, J., Qin, H. L., & Wang, J. P. (2013). The effects of perioperative probiotic treatment on serum zonulin concentration and subsequent postoperative infectious complications after colorectal cancer surgery: A double-center and double-blind randomized clinical trial. The American Journal of Clinical Nutrition, 97(1), 117–126.
- Logan, R. M., Stringer, A. M., Bowen, J. M., Gibson, R. J., Sonis, S. T., & Keefe, D. M. (2009). Is the pathobiology of chemotherapy-induced alimentary tract mucositis influenced by the type of mucotoxic drug administered? Cancer Chemotherapy and Pharmacology, 63(2), 239–251.
- Logan, R. M., Stringer, A. M., Bowen, J. M., Yeoh, A. S.-J., Gibson, R. J., Sonis, S. T., & Keefe, D. M. (2007). The role of pro-inflammatory cytokines in cancer treatment-induced alimentary tract mucositis: Pathobiology, animal models and cytotoxic drugs. Cancer Treatment Reviews, 33(5), 448–460.
- Longo, D. L., Fauci, A. S., Kasper, D. L., Hauser, S. L., Jameson, J. L., & Loscalzo, J. (2012). Harrison's principles of internal medicine 18E Vol 2 EB. McGraw Hill Professional.
- Ma, H., Marti-Gutierrez, N., Park, S.-W., Wu, J., Lee, Y., Suzuki, K., Koski, A., Ji, D., Hayama, T., Ahmed, R., Darby, H., van Dyken, C., Li, Y., Kang, E., Park, A. R., Kim, D., Kim, S. T., Gong, J., Gu, Y., … Mitalipov, S. (2017). Correction of a pathogenic gene mutation in human embryos. Nature, 548(7668), 413–419.
- Macfarlane, G. T., Steed, H., & Macfarlane, S. (2008). Bacterial metabolism and health-related effects of galacto-oligosaccharides and other prebiotics. Journal of Applied Microbiology, 104(2), 305–344.
- Markowiak, P., & Śliżewska, K. (2017). Effects of probiotics, prebiotics, and synbiotics on human health. Nutrients, 9(9), 1021.
- Markowiak-Kopeć, P., & Śliżewska, K. (2020). The effect of probiotics on the production of short-chain fatty acids by human intestinal microbiome. Nutrients, 12(4), 1107. https://doi.org/10.3390/nu12041107
- McKean, J., Naug, H., Nikbakht, E., Amiet, B., & Colson, N. (2017). Probiotics and subclinical psychological symptoms in healthy participants: A systematic review and meta-analysis. The Journal of Alternative and Complementary Medicine, 23(4), 249–258.
- McQuade, J. L., Daniel, C. R., Helmink, B. A., & Wargo, J. A. (2019). Modulating the microbiome to improve therapeutic response in cancer. The Lancet Oncology, 20(2), e77–e91.
- McQuade, R. M., Stojanovska, V., Abalo, R., Bornstein, J. C., & Nurgali, K. (2016). Chemotherapy-induced constipation and diarrhea: Pathophysiology, current and emerging treatments. Frontiers in Pharmacology, 7, 414. https://doi.org/10.3389/fphar.2016.00414
- Mego, M., Holec, V., Drgona, L., Hainova, K., Ciernikova, S., & Zajac, V. (2013). Probiotic bacteria in cancer patients undergoing chemotherapy and radiation therapy. Complementary Therapies in Medicine, 21(6), 712–723.
- Miles, A., & Gibson, L. (2016). Everyday participation and cultural value (Vol. 25, pp. 151–157). Taylor & Francis.
- Molska, M., & Reguła, J. (2019). Potential mechanisms of probiotics action in the prevention and treatment of colorectal cancer. Nutrients, 11(10), 2453. https://doi.org/10.3390/nu11102453
- Nami, Y., Haghshenas, B., Haghshenas, M., Abdullah, N., & Yari Khosroushahi, A. (2015). The prophylactic effect of probiotic Enterococcus lactis IW5 against different human cancer cells. Frontiers in Microbiology, 6, 1317.
- Newman, A. M., & Arshad, M. (2020). The role of probiotics, prebiotics and synbiotics in combating multidrug-resistant organisms. Clinical Therapeutics, 42(9), 1637–1648.
- Ng, Q. X., Peters, C., Ho, C. Y. X., Lim, D. Y., & Yeo, W.-S. (2018). A meta-analysis of the use of probiotics to alleviate depressive symptoms. Journal of Affective Disorders, 228, 13–19.
- Ng, Q. X., Soh, A. Y. S., Venkatanarayanan, N., Ho, C. Y. X., Lim, D. Y., & Yeo, W.-S. (2019). A systematic review of the effect of probiotic supplementation on schizophrenia symptoms. Neuropsychobiology, 78(1), 1–6.
- Nowak, A., Śliżewska, K., & Otlewska, A. (2015). Antigenotoxic activity of lactic acid bacteria, prebiotics, and products of their fermentation against selected mutagens. Regulatory Toxicology and Pharmacology, 73(3), 938–946.
- Oh, N. S., Lee, J. Y., Kim, Y.-T., Kim, S. H., & Lee, J.-H. (2020). Cancer-protective effect of a synbiotic combination between Lactobacillus gasseri 505 and a Cudrania tricuspidata leaf extract on colitis-associated colorectal cancer. Gut Microbes, 12(1), 1785803.
- Ohara, T., & Suzutani, T. (2018). Intake of Bifidobacterium longum and Fructo-oligosaccharides prevents colorectal carcinogenesis. Euroasian Journal of Hepato-Gastroenterology, 8(1), 11–17.
- Pala, V., Sieri, S., Berrino, F., Vineis, P., Sacerdote, C., Palli, D., Masala, G., Panico, S., Mattiello, A., Tumino, R., Giurdanella, M. C., Agnoli, C., Grioni, S., & Krogh, V. (2011). Yogurt consumption and risk of colorectal cancer in the Italian European prospective investigation into cancer and nutrition cohort. International Journal of Cancer, 129(11), 2712–2719.
- Paone, P., & Cani, P. D. (2020). Mucus barrier, mucins and gut microbiota: The expected slimy partners? Gut, 69(12), 2232–2243. https://doi.org/10.1136/gutjnl-2020-322260
- Picardo, S. L., Coburn, B., & Hansen, A. R. (2019). The microbiome and cancer for clinicians. Critical Reviews in Oncology/Hematology, 141, 1–12.
- Piemontese, P., Giannì, M. L., Braegger, C. P., Chirico, G., Grüber, C., Riedler, J., Arslanoglu, S., van Stuijvenberg, M., Boehm, G., Jelinek, J., Roggero, P., & MIPS 1 Working Group. (2011). Tolerance and safety evaluation in a large cohort of healthy infants fed an innovative prebiotic formula: A randomized controlled trial. PLoS One, 6(11), e28010.
- Pirbaglou, M., Katz, J., de Souza, R. J., Stearns, J. C., Motamed, M., & Ritvo, P. (2016). Probiotic supplementation can positively affect anxiety and depressive symptoms: A systematic review of randomized controlled trials. Nutrition Research, 36(9), 889–898.
- Polakowski, C. B., Kato, M., Preti, V. B., Schieferdecker, M. E. M., & Campos, A. C. L. (2019). Impact of the preoperative use of synbiotics in colorectal cancer patients: A prospective, randomized, double-blind, placebo-controlled study. Nutrition, 58, 40–46.
- Pool-Zobel, B., Van Loo, J., Rowland, I., & Roberfroid, M. (2002). Experimental evidences on the potential of prebiotic fructans to reduce the risk of colon cancer. British Journal of Nutrition, 87(S2), S273–S281.
- Pöschl, G., & Seitz, H. K. (2004). Alcohol and cancer. Alcohol and Alcoholism, 39(3), 155–165. https://doi.org/10.1093/alcalc/agh057
- Powers, W. J., Rabinstein, A. A., Ackerson, T., Adeoye, O. M., Bambakidis, N. C., Becker, K., Biller, J., Brown, M., Demaerschalk, B. M., Hoh, B., Jauch, E. C., Kidwell, C. S., Leslie-Mazwi, T. M., Ovbiagele, B., Scott, P. A., Sheth, K. N., Southerland, A. M., Summers, D. V., Tirschwell, D. L., & American Heart Association Stroke Council. (2018). 2018 guidelines for the early management of patients with acute ischemic stroke: A guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke, 49(3), e46–e99.
- Rafter, J., Bennett, M., Caderni, G., Clune, Y., Hughes, R., Karlsson, P. C., Klinder, A., O'Riordan, M., O'Sullivan, G. C., Pool-Zobel, B., Rechkemmer, G., Roller, M., Rowland, I., Salvadori, M., Thijs, H., Van Loo, J., Watzl, B., & Collins, J. K. (2007). Dietary synbiotics reduce cancer risk factors in polypectomized and colon cancer patients. The American Journal of Clinical Nutrition, 85(2), 488–496.
- Rajendran, S. R. C. K., Okolie, C. L., Udenigwe, C. C., & Mason, B. (2017). Structural features underlying prebiotic activity of conventional and potential prebiotic oligosaccharides in food and health. Journal of Food Biochemistry, 41(5), e12389.
- Raman, M., Ambalam, P., Kondepudi, K. K., Pithva, S., Kothari, C., Patel, A. T., Purama, R. K., Dave, J. M., & Vyas, B. (2013). Potential of probiotics, prebiotics and synbiotics for management of colorectal cancer. Gut Microbes, 4(3), 181–192.
- Riley, R. S., June, C. H., Langer, R., & Mitchell, M. J. (2019). Delivery technologies for cancer immunotherapy. Nature reviews, Drug discovery, 18(3), 175–196.
- Roller, M., Clune, Y., Collins, K., Rechkemmer, G., & Watzl, B. (2007). Consumption of prebiotic inulin enriched with oligofructose in combination with the probiotics Lactobacillus rhamnosus and Bifidobacterium lactis has minor effects on selected immune parameters in polypectomised and colon cancer patients. British Journal of Nutrition, 97(4), 676–684.
- Roller, M., Femia, A. P., Caderni, G., Rechkemmer, G., & Watzl, B. (2004). Intestinal immunity of rats with colon cancer is modulated by oligofructose-enriched inulin combined with Lactobacillus rhamnosus and Bifidobacterium lactis. British Journal of Nutrition, 92(6), 931–938.
- Rowland, I., Rumney, C., Coutts, J., & Lievense, L. (1998). Effect of Bifidobacterium longum and inulin on gut bacterial metabolism and carcinogen-induced aberrant crypt foci in rats. Carcinogenesis, 19(2), 281–285.
- Sarao, L. K., & Arora, M. (2017). Probiotics, prebiotics, and microencapsulation: A review. Critical Reviews in Food Science and Nutrition, 57(2), 344–371.
- Scott, A. J., Merrifield, C. A., Younes, J. A., & Pekelharing, E. P. (2018). Pre-, pro- and synbiotics in cancer prevention and treatment—A review of basic and clinical research. Ecancermedicalscience, 12, 869. https://doi.org/10.3332/ecancer.2018.869
- Senapati, S., Mahanta, A. K., Kumar, S., & Maiti, P. (2018). Controlled drug delivery vehicles for cancer treatment and their performance. Signal Transduction and Targeted Therapy, 3(1), 1–19.
- Siegel, R., DeSantis, C., Virgo, K., Stein, K., Mariotto, A., Smith, T., Cooper, D., Gansler, T., Lerro, C., Fedewa, S., Lin, C., Leach, C., Cannady, R. S., Cho, H., Scoppa, S., Hachey, M., Kirch, R., Jemal, A., & Ward, E. (2012). Cancer treatment and survivorship statistics, 2012. CA: A Cancer Journal for Clinicians, 62(4), 220–241.
- Singh, C. K., George, J., Duster, M., Safdar, N., & Ahmad, N. (2014). Combination of the probiotic Lactobacillus rhamnosus GG with grape antioxidant resveratrol for the management of colorectal cancer: AACR.
- Slavin, J. (2013). Fiber and prebiotics: Mechanisms and health benefits. Nutrients, 5(4), 1417–1435.
- Soccol, C. R., de Souza Vandenberghe, L. P., Spier, M. R., Medeiros, A. B. P., Yamaguishi, C. T., Lindner, J. D. D., Pandey, A., & Thomaz-Soccol, V. (2010). The potential of probiotics: A review. Food Technology and Biotechnology, 48(4), 413–434.
- Sonis, S. T. (2002). The biologic role for nuclear factor-kappaB in disease and its potential involvement in mucosal injury associated with anti-neoplastic therapy. Critical Reviews in Oral Biology & Medicine, 13(5), 380–389.
- Sonis, S. T. (2004). The pathobiology of mucositis. Nature Reviews Cancer, 4(4), 277–284.
- Steenbergen, L., Sellaro, R., van Hemert, S., Bosch, J. A., & Colzato, L. S. (2015). A randomized controlled trial to test the effect of multispecies probiotics on cognitive reactivity to sad mood. Brain, Behavior, and Immunity, 48, 258–264.
- Stringer, A. M., Gibson, R. J., Logan, R. M., Bowen, J. M., Yeoh, A. S., Hamilton, J., & Keefe, D. M. (2009). Gastrointestinal microflora and mucins may play a critical role in the development of 5-Fluorouracil-induced gastrointestinal mucositis. Experimental Biology and Medicine (Maywood, N.J.), 234(4), 430–441. https://doi.org/10.3181/0810-RM-301
- Sugawara, G., Nagino, M., Nishio, H., Ebata, T., Takagi, K., Asahara, T., Nomoto, K., & Nimura, Y. (2006). Perioperative synbiotic treatment to prevent postoperative infectious complications in biliary cancer surgery: A randomized controlled trial. Annals of Surgery, 244(5), 706–714.
- Taper, H. S., & Roberfroid, M. B. (2005). Possible adjuvant cancer therapy by two prebiotics-inulin or oligofructose. In Vivo, 19(1), 201–204.
- Tasdemir, S. S., & Sanlier, N. (2020). An insight into the anticancer effects of fermented foods: A review. Journal of Functional Foods, 75, 104281. https://doi.org/10.1016/j.jff.2020.104281
- Terpou, A., Papadaki, A., Lappa, I. K., Kachrimanidou, V., Bosnea, L. A., & Kopsahelis, N. (2019). Probiotics in food systems: Significance and emerging strategies towards improved viability and delivery of enhanced beneficial value. Nutrients, 11(7), 1591.
- Theodoropoulos, G. E., Memos, N. A., Peitsidou, K., Karantanos, T., Spyropoulos, B. G., & Zografos, G. (2016). Synbiotics and gastrointestinal function-related quality of life after elective colorectal cancer resection. Annals of Gastroenterology: Quarterly Publication of the Hellenic Society of Gastroenterology, 29(1), 56.
- Thivat, E., Thérondel, S., Lapirot, O., Abrial, C., Gimbergues, P., Gadéa, E., Planchat, E., Kwiatkowski, F., Mouret-Reynier, M. A., Chollet, P., & Durando, X. (2010). Weight change during chemotherapy changes the prognosis in non metastatic breast cancer for the worse. BMC Cancer, 10(1), 1–9.
- Thomsen, M., & Vitetta, L. (2018). Adjunctive treatments for the prevention of chemotherapy- and radiotherapy- induced mucositis. Integrative Cancer Therapies, 17(4), 1027–1047.
- Thursby, E., & Juge, N. (2017). Introduction to the human gut microbiota. The Biochemical Journal, 474(11), 1823–1836. https://doi.org/10.1042/BCJ20160510
- Van den Nieuwboer, M., & Claassen, E. (2019). Dealing with the remaining controversies of probiotic safety. Beneficial Microbes, 10(6), 605–616.
- van Vliet, M. J., Harmsen, H. J., de Bont, E. S., & Tissing, W. J. (2010). The role of intestinal microbiota in the development and severity of chemotherapy-induced mucositis. PLoS Pathogens, 6(5), e1000879.
- Vandenplas, Y., Analitis, A., Tziouvara, C., Kountzoglou, A., Drakou, A., Tsouvalas, M., Mavroudi, A., & Xinias, I. (2017). Safety of a new synbiotic starter formula. Pediatric Gastroenterology, Hepatology & Nutrition, 20(3), 167–177.
- Varasteh, S., Braber, S., Garssen, J., & Fink-Gremmels, J. (2015). Galacto-oligosaccharides exert a protective effect against heat stress in a Caco-2 cell model. Journal of Functional Foods, 16, 265–277.
- Wada, M., Nagata, S., Saito, M., Shimizu, T., Yamashiro, Y., Matsuki, T., Asahara, T., & Nomoto, K. (2010). Effects of the enteral administration of Bifidobacterium breve on patients undergoing chemotherapy for pediatric malignancies. Supportive Care in Cancer, 18(6), 751–759.
- Wang, H., Geier, M. S., & Howarth, G. S. (2016). Prebiotics: A potential treatment strategy for the chemotherapy-damaged gut? Critical Reviews in Food Science and Nutrition, 56(6), 946–956.
- Wei, M.-Y., Shi, S., Liang, C., Meng, Q.-C., Hua, J., Zhang, Y.-Y., Liu, J., Zhang, B., Xu, J., & Yu, X.-J. (2019). The microbiota and microbiome in pancreatic cancer: More influential than expected. Molecular Cancer, 18(1), 1–15.
- Wilson, B., & Whelan, K. (2017). Prebiotic inulin-type fructans and galacto-oligosaccharides: Definition, specificity, function, and application in gastrointestinal disorders. Journal of Gastroenterology and Hepatology, 32, 64–68.
- Worthley, D. L., Le Leu, R. K., Whitehall, V. L., Conlon, M., Christophersen, C., Belobrajdic, D., Mallitt, K. A., Hu, Y., Irahara, N., Ogino, S., Leggett, B. A., & Young, G. P. (2009). A human, double-blind, placebo-controlled, crossover trial of prebiotic, probiotic, and synbiotic supplementation: Effects on luminal, inflammatory, epigenetic, and epithelial biomarkers of colorectal cancer. The American Journal of Clinical Nutrition, 90(3), 578–586.
- Yu, A. Q., & Li, L. (2016). The potential role of probiotics in cancer prevention and treatment. Nutrition and Cancer, 68(4), 535–544. https://doi.org/10.1080/01635581.2016.1158300
- Yun, E. J., Yu, S., Kim, Y.-A., Liu, J.-J., Kang, N. J., Jin, Y.-S., & Kim, K. H. (2021). In vitro prebiotic and anti-colon cancer activities of agar-derived sugars from red seaweeds. Marine Drugs, 19(4), 213.
- Zaharuddin, L., Mokhtar, N. M., Nawawi, K. N. M., & Ali, R. A. R. (2019). A randomized double-blind placebo-controlled trial of probiotics in post-surgical colorectal cancer. BMC Gastroenterology, 19(1), 1–8.
- Zawistowska-Rojek, A., & Tyski, S. (2018). Are probiotic really safe for humans? Polish Journal of Microbiology, 67(3), 251–258.
- Zhang, X., Yuan, X., Shi, H., Wu, L., Qian, H., & Xu, W. (2015). Exosomes in cancer: Small particle, big player. Journal of Hematology & Oncology, 8(1), 1–13.
- Zheng, D. W., Li, R. Q., An, J. X., Xie, T. Q., Han, Z. Y., Xu, R., Fang, Y., & Zhang, X. Z. (2020). Prebiotics-encapsulated probiotic spores regulate gut microbiota and suppress colon cancer. Advanced Materials, 32(45), 2004529.
- Zuccotti, G. V., Meneghin, F., Raimondi, C., Dilillo, D., Agostoni, C., Riva, E., & Giovannini, M. (2008). Probiotics in clinical practice: An overview. Journal of International Medical Research, 36(1_suppl), 1A–53A.