Characteristics of the microbiome in patients with symptomatic uncomplicated colonic diverticular disease in the central region of Ukraine

Authors

DOI:

https://doi.org/10.14739/2310-1210.2023.4.275412

Keywords:

diverticulosis, diverticular disease, microbiome, bifidobacteria, lactobacilli, Еscherichia coli, enterotype, Faecalibacterium prausnitzii, Akkermansia

Abstract

The aim of the study was to analyze the age structure, correlation with body mass index in patients with symptomatic uncomplicated diverticular disease (SUDD) in the central region of Ukraine. To reveal the prevalence of left-sided, right-sided or total diverticular lesions of the large intestine, to evaluate the microbiota composition, to identify peculiarities of the enterotype.

Materials and methods. The study included 125 patients with SUDD aged 18 to 90 years who were at a Gastroenterology Hospital in the period from 2019 to 2022. All the patients were residents of the central region of Ukraine. Body mass index was calculated for all patients, total colonoscopy was performed, and fecal analysis was done using culturing and qRT-PCR methods.

Results. The incidence of SUDD among patients in the central region of Ukraine increases with age and reaches its peak in the 71–80 age group. Almost all age groups are dominated by women. Left-sided localization of diverticula occurs in 84.8 % of patients, right-sided in 8.0 %, total in 7.2 %. The majority of patients with diverticular disease (87.2 %) are overweight or with varying degrees of obesity. Patients with SUDD are characterized by a decrease in the main representatives of obligate microflora, namely, Bifidobacterium, Lactobacillus, Escherichia coli. In 46.4 % of patients, representatives of opportunistic flora are detected, in 24.0 % – an increase in fungi from the genus Candida. Also, changes in enterotypes are detected, namely an increase in Firmicutes and Actinobacteria, with a decrease in Bacteroides. The number of Faecalibacterium prausnitzii tends to decrease, while the Akkermansia muciniphila count is unchanged.

Conclusions. The incidence of SUDD increases with age among the population of the central region of Ukraine. Among patients with SUDD, women predominate in almost all age groups. 87.2 % of patients with SUDD are overweight or with various degrees of obesity. The left-sided localization of diverticula prevails among patients with SUDD in the central region of Ukraine – 84.8 %. Patients with SUDD in the central region of Ukraine are characterized by the decrease in the main representatives of obligate microflora, namely: Bifidobacterium, Lactobacillus, Escherichia coli. In 46.4 % of patients with SUDD, representatives of conditionally pathogenic flora are found, in 24.0 % – the increase in fungi from the genus Candida. Changes in enterotypes are detected, namely the increase in Firmicutes and Actinobacteria, with the decrease in Bacteroides. Faecalibacterium prausnitzii tends to decrease, while Akkermansia muciniphila are unchanged.

Author Biographies

A. E. Dorofieiev, Shupyk National University of Health Care of Ukraine, Kyiv

MD, PhD, DSc, Professor, Head of the Department of Therapy and Geriatrics

H. A. Dorohavtseva, Feofaniya Clinical Hospital, Kyiv, Ukraine

MD, PhD, Head of the Gastroenterology and Endocrinology Center

References

Sharara, A. I., Ziade, N., Shayto, R. H., Rustom, L. B. O., Chehab, H., Rimmani, H. H., Hanna, K., Chalhoub, J. M., Sarkis, F. S., Rahal, M. A., Soweid, A., Mourad, F. H., Barada, K., & Harb, A. H. (2018). The Natural History of Incidental Colonic Diverticulosis on Screening Colonoscopy. Canadian journal of gastroenterology & hepatology, 2018, 3690202. https://doi.org/10.1155/2018/3690202

Gregersen, R., Andresen, K., Burcharth, J., Pommergaard, H. C., & Rosenberg, J. (2018). Long-term mortality and recurrence in patients treated for colonic diverticulitis with abscess formation: a nationwide register-based cohort study. International journal of colorectal disease, 33(4), 431-440. https://doi.org/10.1007/s00384-018-2990-1

Strate, L. L., & Morris, A. M. (2019). Epidemiology, Pathophysiology, and Treatment of Diverticulitis. Gastroenterology, 156(5), 1282-1298.e1. https://doi.org/10.1053/j.gastro.2018.12.033

Peery, A. F., Keku, T. O., Galanko, J. A., & Sandler, R. S. (2020). Sex and Race Disparities in Diverticulosis Prevalence. Clinical gastroenterology and hepatology, 18(9), 1980-1986. https://doi.org/10.1016/j.cgh.2019.10.022

Kanda, N., & Watanabe, S. (2005). Regulatory roles of sex hormones in cutaneous biology and immunology. Journal of dermatological science, 38(1), 1-7. https://doi.org/10.1016/j.jdermsci.2004.10.011

Tursi, A., Scarpignato, C., Strate, L. L., Lanas, A., Kruis, W., Lahat, A., & Danese, S. (2020). Colonic diverticular disease. Nature reviews. Disease primers, 6(1), 20. https://doi.org/10.1038/s41572-020-0153-5

Turner, G. A., O'Grady, M. J., Purcell, R. V., & Frizelle, F. A. (2021). The Epidemiology and Etiology of Right-Sided Colonic Diverticulosis: A Review. Annals of coloproctology, 37(4), 196-203. https://doi.org/10.3393/ac.2021.00192.0027

Maguire L. H. (2020). Genetic Risk Factors for Diverticular Disease-Emerging Evidence. Journal of gastrointestinal surgery, 24(10), 2314-2317. https://doi.org/10.1007/s11605-020-04693-5

Hjern, F., Wolk, A., & Håkansson, N. (2012). Obesity, physical inactivity, and colonic diverticular disease requiring hospitalization in women: a prospective cohort study. The American journal of gastroenterology, 107(2), 296-302. https://doi.org/10.1038/ajg.2011.352

Kopylov, U., Ben-Horin, S., Lahat, A., Segev, S., Avidan, B., & Carter, D. (2012). Obesity, metabolic syndrome and the risk of development of colonic diverticulosis. Digestion, 86(3), 201-205. https://doi.org/10.1159/000339881

Nagata, N., Sakamoto, K., Arai, T., Niikura, R., Shimbo, T., Shinozaki, M., Aoki, T., Sekine, K., Okubo, H., Watanabe, K., Sakurai, T., Yokoi, C., Akiyama, J., Yanase, M., Noda, M., Itoh, T., Mizokami, M., & Uemura, N. (2015). Visceral Abdominal Obesity Measured by Computed Tomography is Associated With Increased Risk of Colonic Diverticulosis. Journal of clinical gastroenterology, 49(10), 816-822. https://doi.org/10.1097/MCG.0000000000000267

Peery, A. F., Sandler, R. S., Ahnen, D. J., Galanko, J. A., Holm, A. N., Shaukat, A., Mott, L. A., Barry, E. L., Fried, D. A., & Baron, J. A. (2013). Constipation and a low-fiber diet are not associated with diverticulosis. Clinical gastroenterology and hepatology, 11(12), 1622-1627. https://doi.org/10.1016/j.cgh.2013.06.033

Peery, A. F., Barrett, P. R., Park, D., Rogers, A. J., Galanko, J. A., Martin, C. F., & Sandler, R. S. (2012). A high-fiber diet does not protect against asymptomatic diverticulosis. Gastroenterology, 142(2), 266-72.e1. https://doi.org/10.1053/j.gastro.2011.10.035

Strate, L. L., Keeley, B. R., Cao, Y., Wu, K., Giovannucci, E. L., & Chan, A. T. (2017). Western Dietary Pattern Increases, and Prudent Dietary Pattern Decreases, Risk of Incident Diverticulitis in a Prospective Cohort Study. Gastroenterology, 152(5), 1023-1030.e2. https://doi.org/10.1053/j.gastro.2016.12.038

Jones, R. B., Fodor, A. A., Peery, A. F., Tsilimigras, M. C. B., Winglee, K., McCoy, A., Sioda, M., Sandler, R. S., & Keku, T. O. (2018). An Aberrant Microbiota is not Strongly Associated with Incidental Colonic Diverticulosis. Scientific reports, 8(1), 4951. https://doi.org/10.1038/s41598-018-23023-z

Peery, A. F., Keku, T. O., Addamo, C., McCoy, A. N., Martin, C. F., Galanko, J. A., & Sandler, R. S. (2018). Colonic Diverticula Are Not Associated With Mucosal Inflammation or Chronic Gastrointestinal Symptoms. Clinical gastroenterology and hepatology, 16(6), 884-891.e1. https://doi.org/10.1016/j.cgh.2017.05.051

Violi, A., Cambiè, G., Miraglia, C., Barchi, A., Nouvenne, A., Capasso, M., Leandro, G., Meschi, T., De' Angelis, G. L., & Di Mario, F. (2018). Epidemiology and risk factors for diverticular disease. Acta bio-medica : Atenei Parmensis, 89(9-S), 107-112. https://doi.org/10.23750/abm.v89i9-S.7924

Cao, Y., Strate, L. L., Keeley, B. R., Tam, I., Wu, K., Giovannucci, E. L., & Chan, A. T. (2018). Meat intake and risk of diverticulitis among men. Gut, 67(3), 466-472. https://doi.org/10.1136/gutjnl-2016-313082

Burgell, R. E., Muir, J. G., & Gibson, P. R. (2013). Pathogenesis of colonic diverticulosis: repainting the picture. Clinical gastroenterology and hepatology, 11(12), 1628-1630. https://doi.org/10.1016/j.cgh.2013.08.046

Young-Fadok T. M. (2018). Diverticulitis. The New England journal of medicine, 379(17), 1635-1642. https://doi.org/10.1056/NEJMcp1800468

Brook, I., & Frazier, E. H. (2000). Aerobic and anaerobic microbiology in intra-abdominal infections associated with diverticulitis. Journal of medical microbiology, 49(9), 827-830. https://doi.org/10.1099/0022-1317-49-9-827

Barbara, G., Scaioli, E., Barbaro, M. R., Biagi, E., Laghi, L., Cremon, C., Marasco, G., Colecchia, A., Picone, G., Salfi, N., Capozzi, F., Brigidi, P., & Festi, D. (2017). Gut microbiota, metabolome and immune signatures in patients with uncomplicated diverticular disease. Gut, 66(7), 1252-1261. https://doi.org/10.1136/gutjnl-2016-312377

Magne, F., Gotteland, M., Gauthier, L., Zazueta, A., Pesoa, S., Navarrete, P., & Balamurugan, R. (2020). The Firmicutes/Bacteroidetes Ratio: A Relevant Marker of Gut Dysbiosis in Obese Patients?. Nutrients, 12(5), 1474. https://doi.org/10.3390/nu12051474

Lopez-Siles, M., Duncan, S. H., Garcia-Gil, L. J., & Martinez-Medina, M. (2017). Faecalibacterium prausnitzii: from microbiology to diagnostics and prognostics. The ISME journal, 11(4), 841-852. https://doi.org/10.1038/ismej.2016.176

Tursi, A., Mastromarino, P., Capobianco, D., Elisei, W., Campagna, G., Picchio, M., Giorgetti, G., Fabiocchi, F., & Brandimarte, G. (2023). Faecalibacterium prausnitzii is not decreased in symptomatic uncomplicated diverticular disease of the colon. Bioscience of microbiota, food and health, 42(1), 1-2. https://doi.org/10.12938/bmfh.2022-046

Testing (2021, November 9). Stool Culture. https://www.testing.com/tests/stool-culture/

Talutis, S. D., & Kuhnen, F. A. H. (2021). Pathophysiology and Epidemiology of Diverticular Disease. Clinics in colon and rectal surgery, 34(2), 81-85. https://doi.org/10.1055/s-0040-1716698

Bharucha, A. E., Parthasarathy, G., Ditah, I., Fletcher, J. G., Ewelukwa, O., Pendlimari, R., Yawn, B. P., Melton, L. J., Schleck, C., & Zinsmeister, A. R. (2015). Temporal Trends in the Incidence and Natural History of Diverticulitis: A Population-Based Study. The American journal of gastroenterology, 110(11), 1589-1596. https://doi.org/10.1038/ajg.2015.302

Steele, S. R., Hull, T. L., Read, T. E., Saclarides, T. J., Senagore, A. J., & Whitlow. C. B. (Eds.). (2016). The ASCRS Textbook of Colon and rectal surgery. Springer International Publishing. https://doi.org/10.1007/978-3-319-25970-3

Alnzaer, A. A., Mohamedahmed, A. Y. Y., Adam, Y. A., Eltyiep, E., & Suliman, S. H. (2020). Presentation and anatomical distribution of diverticular disease in four hospitals in Sudan. The Pan African medical journal, 36, 64. https://doi.org/10.11604/pamj.2020.36.64.22987

Mehrzad, R., Mishra, S., Faller, G., Memon, B., & Fiore, J. (2015). Right-Sided Diverticulosis and Disparities from Left-Sided Diverticulosis in the Vietnamese Population Living in Boston, Mass., USA: A Retrospective Cohort Study. Medical principles and practice, 24(4), 355-361. https://doi.org/10.1159/000381548

Delvaux M. (2003). Diverticular disease of the colon in Europe: epidemiology, impact on citizen health and prevention. Alimentary pharmacology & therapeutics, 18 Suppl 3, 71-74. https://doi.org/10.1046/j.0953-0673.2003.01720.x

Hadrian, K. A., Basaj, A., Nehring, P., & Ziółkowski, B. A. (2016). Prevalence and distribution of colonic diverticulosis in patients undergoing colonoscopy. Four years’ experience from a single center in Warsaw. Archives of Medical Science - Civilization Diseases, 1, 30-35. https://doi.org/10.5114/amscd.2016.60164

Rodríguez-Wong, U., Cruz-Rubin, C., Pinto-Angulo, V. M., & García Álvarez, J. (2015). Obesidad y enfermedad diverticular del colon complicada [Obesity and complicated diverticular disease of the colon]. Cirugia y cirujanos, 83(4), 292-296. https://doi.org/10.1016/j.circir.2015.02.003

Al Bander, Z., Nitert, M. D., Mousa, A., & Naderpoor, N. (2020). The Gut Microbiota and Inflammation: An Overview. International journal of environmental research and public health, 17(20), 7618. https://doi.org/10.3390/ijerph17207618

Gueimonde, M., Ouwehand, A., Huhtinen, H., Salminen, E., & Salminen, S. (2007). Qualitative and quantitative analyses of the bifidobacterial microbiota in the colonic mucosa of patients with colorectal cancer, diverticulitis and inflammatory bowel disease. World journal of gastroenterology, 13(29), 3985-3989. https://doi.org/10.3748/wjg.v13.i29.3985

Dempsey, E., & Corr, S. C. (2022). Lactobacillus spp. for Gastrointestinal Health: Current and Future Perspectives. Frontiers in immunology, 13, 840245. https://doi.org/10.3389/fimmu.2022.840245

De Souza, H. L., de Carvalho, V. R., Romeiro, F. G., Sassaki, L. Y., Keller, R., & Rodrigues, J. (2012). Mucosa-associated but not luminal Escherichia coli is augmented in Crohn's disease and ulcerative colitis. Gut pathogens, 4(1), 21. https://doi.org/10.1186/1757-4749-4-21

Ticinesi, A., Nouvenne, A., Corrente, V., Tana, C., Di Mario, F., & Meschi, T. (2019). Diverticular Disease: a Gut Microbiota Perspective. Journal of gastrointestinal and liver diseases : JGLD, 28(3), 327-337. https://doi.org/10.15403/jgld-277

Daniels, L., Budding, A. E., de Korte, N., Eck, A., Bogaards, J. A., Stockmann, H. B., Consten, E. C., Savelkoul, P. H., & Boermeester, M. A. (2014). Fecal microbiome analysis as a diagnostic test for diverticulitis. European journal of clinical microbiology & infectious diseases, 33(11), 1927-1936. https://doi.org/10.1007/s10096-014-2162-3

Tursi, A., Mastromarino, P., Capobianco, D., Elisei, W., Miccheli, A., Capuani, G., Tomassini, A., Campagna, G., Picchio, M., Giorgetti, G., Fabiocchi, F., & Brandimarte, G. (2016). Assessment of Fecal Microbiota and Fecal Metabolome in Symptomatic Uncomplicated Diverticular Disease of the Colon. Journal of clinical gastroenterology, 50 Suppl 1, S9-S12. https://doi.org/10.1097/MCG.0000000000000626

Jeganathan, N. A., Davenport, E. R., Yochum, G. S., & Koltun, W. A. (2021, August 1). The microbiome of diverticulitis. Current Opinion in Physiology. Elsevier Ltd. https://doi.org/10.1016/j.cophys.2021.06.006

Kvasnovsky, C. L., Leong, L. E. X., Choo, J. M., Abell, G. C. J., Papagrigoriadis, S., Bruce, K. D., & Rogers, G. B. (2018). Clinical and symptom scores are significantly correlated with fecal microbiota features in patients with symptomatic uncomplicated diverticular disease: a pilot study. European journal of gastroenterology & hepatology, 30(1), 107-112. https://doi.org/10.1097/MEG.0000000000000995

Knox, N. C., Forbes, J. D., Peterson, C. L., Van Domselaar, G., & Bernstein, C. N. (2019). The Gut Microbiome in Inflammatory Bowel Disease: Lessons Learned From Other Immune-Mediated Inflammatory Diseases. The American journal of gastroenterology, 114(7), 1051-1070. https://doi.org/10.14309/ajg.0000000000000305

Downloads

Published

2023-07-20

How to Cite

1.
Dorofieiev AE, Dorohavtseva HA. Characteristics of the microbiome in patients with symptomatic uncomplicated colonic diverticular disease in the central region of Ukraine. Zaporozhye Medical Journal [Internet]. 2023Jul.20 [cited 2024Nov.20];25(4):316-25. Available from: http://zmj.zsmu.edu.ua/article/view/275412

Issue

Vol. 25 No. 4 (2023): Zaporozhye medical journal

Section

Original research

License

Authors who publish with this journal agree to the following terms:

    1. Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.  Лицензия Creative Commons
    2. Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
    3. Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access)