Gut dysbiosis following c-section instigates higher colonisation of toxigenic clostridium perfringens in infants

Beneficial Microbes

Volumn 8, Issue 3, 2017, Pages 353-365

  Nagpal, R ^a   Tsuji, H ^b   Takahashi, T ^b   Nomoto, K ^b   Kawashima, K ^c   Nagata, S ^d   Yamashiro, Y ^a  

^a JUNTENDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b YAKULT CENTRAL INSTITUTE FOR MICROBIOLOGICAL RESEARCH   (Japan)

^c Gonohashi Obstetrics and Gynecology Hospital   (Japan)

^d TOKYO WOMEN'S MEDICAL UNIVERSITY   (Japan)

Author keywords

Bacteroides fragilis; Bifidobacterium; Clostridium perfringens enterotoxin; Gut microbiota; Lactobacillus; Phospholipase C

Indexed keywords

ARTICLE; ARTIFICIAL MILK; ATOPOBIUM; BACTERIAL COLONIZATION; BACTERIUM DETECTION; BACTEROIDES FRAGILIS; BIFIDOBACTERIUM; BREAST FEEDING; CESAREAN SECTION; CHILD; CLOSTRIDIUM; CLOSTRIDIUM COCCOIDES; CLOSTRIDIUM LEPTUM; CLOSTRIDIUM PERFRINGENS; DYSBIOSIS; ENTEROBACTERIACEAE; ENTEROCOCCUS; FECES ANALYSIS; FEMALE; HUMAN; INFANT; INTESTINE FLORA; LACTOBACILLUS; MALE; NONHUMAN; PREVOTELLA; STAPHYLOCOCCUS; VAGINAL DELIVERY; FECES; INTESTINE; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; NEWBORN; PATHOGENICITY; PHYSIOLOGY; PRESCHOOL CHILD;

ALPHA TOXIN, CLOSTRIDIUM PERFRINGENS; BACTERIAL TOXIN; CALCIUM BINDING PROTEIN; ENTEROTOXIN; ENTEROTOXIN, CLOSTRIDIUM; PHOSPHOLIPASE C;

BACTERIAL TOXINS; BACTEROIDES FRAGILIS; BIFIDOBACTERIUM; CALCIUM-BINDING PROTEINS; CESAREAN SECTION; CHILD, PRESCHOOL; CLOSTRIDIUM PERFRINGENS; DYSBIOSIS; ENTEROTOXINS; FECES; FEMALE; GASTROINTESTINAL MICROBIOME; HUMANS; INFANT; INFANT, NEWBORN; INTESTINES; LACTOBACILLUS; MALE; TYPE C PHOSPHOLIPASES;

EID: 85019694077     PISSN: 18762883     EISSN: 18762891     Source Type: Journal    
DOI: 10.3920/BM2016.0216     Document Type: Article

References (51)

1. Aagaard, K., Ma, J., Antony, K.M., Ganu, R., Petrosino, J. and Versalovic, J., 2014. The placenta harbors a unique microbiome. Science Translational Medicine 6: 237ra65.
2. Ahtonen, P., Lehtonen, O.P., Kero, P., Eerola, E. and Hartiala, K., 1994. Clostridium perfringens in stool, intrapartum antibiotics and gastrointestinal signs in a neonatal intensive care unit. Acta Paediatrica 83: 389-390.
3. Arrieta, M.C., Stiemsma, L.T., Dimitriu, P.A., Thorson, L., Russell, S., Yurist-Doutsch, S., Kuzeljevic, B., Gold, M.J., Britton, H.M., Lefebvre, D.L., Subbarao, P., Mandhane, P., Becker, A., McNagny, K.M., Sears, M.R., Kollmann, T. and the CHILD Study Investigators, Mohn, W.W., Turvey, S.E. and Finlay, B.B., 2015. Early infancy microbial and metabolic alterations affect risk of childhood asthma. Science Translational Medicine 7: 307ra152.
4. Avershina, E., Storro, O., Oien, T., Johnsen, R., Pope, P. and Rudi, K., 2014. Major faecal microbiota shifts in composition and diversity with age in a geographically restricted cohort of mothers and their children. FEMS Microbiology and Ecology 87: 280-90.
5. Backhed, F., Roswall, J., Peng, Y., Feng, Q., Jia, H., Kovatcheva-Datchary, P., Li, Y., Xia, Y., Xie, H., Zhong, H., Khan, M.T., Zhang, J., Li, J., Xiao, L., Al-Aama, J., Zhang, D., Lee, Y.S., Kotowska, D., Colding, C., Tremaroli, V., Yin, Y., Bergman, S., Xu, X., Madsen, L., Kristiansen, K., Dahlgren, J. and Jun, W., 2015. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host and Microbe 17: 690-703.
6. Benno, Y., Sawada, K. and Mitsuoka, T., 1984. The intestinal microflora of infants: composition of fecal flora in breast-fed and bottle-fed infants. Microbiology and Immunology 28: 975-986.
7. Bezirtzoglou, E., 1997. The intestinal microflora during the first weeks of life. Anaerobe 3: 173-177.
8. Bezirtzoglou, E. and Romond, C., 1990a. Apparition of Clostridium sp. and Bacteroides in the intestine of the newborn delivered by cesarean section. Comparative Immunology Microbiology and Infectious Diseases 13: 217-221. Bezirtzoglou, E. and Romond, C., 1990b. Effect of the feeding practices on the establishment of bacterial interactions in the intestine of the newborn delivered by cesarean section. Journal of Perinatal Medicine 18: 139-143.
9. Bezirtzoglou, E. and Romond, C., 1991. Behavior of Clostridium perfringens in the intestine of newborn infants born by cesarean section. Annals of Pediatrics 38: 331-335.
10. Bezirtzoglou, E. and Stavropoulou, E., 2011. Immunology and probiotic impact of the newborn and young children intestinal microflora. Anaerobe 17: 369-74.
11. Bezirtzoglou, E., Romond, M.B. and Romond, C., 1989. Modulation of Clostridium perfringens intestinal colonization in infants delivered by caesarean section. Infection 17: 232-236.
12. Brook, I., 1995. Clostridial infection in children. Journal of Medical Microbiology 42: 78-82.
13. Browne, H.P., Forster, S.C., Anonye, B.O., Kumar, N., Neville, B.A., Stares, M.D., Goulding, D. and Lawley, T.D., 2016. Culturing of 'unculturable' human microbiota reveals novel taxa and extensive sporulation. Nature 533: 543-546.
14. Charbonneau, M.R., Blanton, L.V., DiGiulio, D.B., Relman, D.A., Lebrilla, C.B., Mills, D.A. and Gordon, J.I., 2016. A microbial perspective of human developmental biology. Nature 535: 48-55.
15. Cree, B.A., Spencer, C.M., Varrin-Doyer, M., Baranzini, S.E. and Zamvil, S.S., 2016. Gut microbiome analysis in neuromyelitis optica reveals overabundance of Clostridium perfringens. Annals of Neurology 80: 443-447.
16. Darmasseelane, K., Hyde, M.J., Santhakumaran, S., Gale, C. and Modi, N., 2014. Mode of delivery and offspring body mass index, overweight and obesity in adult life: a systematic review and metaanalysis. PLoS One 9: e87896.
17. De la Cochetiere, M.F., Piloquet, H., Des Robert, C., Darmaun, D., Galmiche, J.P. and Roze, J.C., 2004. Early intestinal bacterial colonization and necrotizing enterocolitis in premature infants: the putative role of Clostridium. Pediatric Research 56: 366-370.
18. Dogra, S., Sakwinska, O., Soh, S.E., Ngom-Bru, C., Bruck, W.M., Berger, B., Brussow, H., Lee, Y.S., Yap, F., Chong, Y.S., Godfrey, K.M. and Holbrooka, J.D., 2015. Dynamics of infant gut microbiota are influenced by delivery mode and gestational duration and are associated with subsequent adiposity. MBio 6: e02419-14.
19. Dominguez-Bello, M.G., Costello, E.K., Contreras, M., Magris, M., Hidalgo, G., Fierer, N. and Knight, R., 2010. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proceedings of the National Academy of Sciences of the USA 107: 11971-11975.
20. Dominguez-Bello, M.G., De Jesus-Laboy, K.M., Shen, N., Cox, L.M., Amir, A., Gonzalez, A., Bokulich, N.A., Song, S.J., Hoashi, M., Rivera-Vinas, J.I., Mendez, K., Knight, R. and Clemente, J.C., 2016. Partial restoration of the microbiota of cesarean-born infants via vaginal microbial transfer. Nature Medicine 22: 250-253.
21. Falk, A., Olsson, C., Ahrne, S., Molin, G., Adawi, D. and Jeppsson, B., 2007. Ileal pelvic pouch microbiota from two former ulcerative colitis patients, analysed by DNA-based methods, were unstable over time and showed the presence of Clostridium perfringens. Scandinavian Journal of Gastroenterology 42: 973-985.
22. Freedman, J.C., Shrestha, A. and McClane, B.A., 2016. Clostridium perfringens enterotoxin: action, genetics, and translational applications. Toxins 8: 73.
23. Gronlund, M.M., Lehtonen, O.P., Eerola, E. and Kero, P., 1999. Fecal microflora in healthy infants born by different methods of delivery: permanent changes in intestinal flora after cesarean delivery. Journal of Pediatric Gastroenterology and Nutrition 28: 19-25.
24. Jakobsson, H.E., Abrahamsson, T.R., Jenmalm, M.C., Harris, K., Quince, C., Jernberg, C., Bjorksten, B., Engstrand, L. and Andersson, A.F., 2014. Decreased gut microbiota diversity, delayed Bacteroidetes colonization and reduced Th1 responses in infants delivered by caesarean section. Gut 63: 559-566.
25. Kerr, C.A., Grice, D.M., Tran, C.D., Bauer, D.C., Li, D., Hendry, P. and Hannan, G.N., 2015. Early life events influence whole-of-life metabolic health via gut microflora and gut permeability. Critical Reviews in Microbiology 41: 326-340.
26. Kleessen, B., Bunke, H., Tovar, K., Noack, J. and Sawatzki, G., 1995. Influence of two infant formulas and human milk on the development of the fecal flora in newborn infants. Acta Paediatrica 84: 1347-1356.
27. Komatsu, H., Inui, A., Sogo, T. and Fujisawa, T., 2012. Clostridium perfringens. Nihon Rinsho 70: 1357-1361.
28. Kurakawa, T., Ogata, K., Tsuji, H., Kado, Y., Takahashi, T., Kida, Y., Ito, M., Okada, N. and Nomoto, K., 2015. Establishment of a sensitive system for analysis of human vaginal microbiota on the basis of rRNA-targeted reverse transcription-quantitative PCR. Journal of Microbiological Methods 111: 93-104.
29. Lakshminarayanan, B., Harris, H.M., Coakley, M., O'Sullivan, O., Stanton, C., Pruteanu, M., Shanahan, F., O'Toole, P.W., Ross, R.P. and the ELDERMET consortium, 2013. Prevalence and characterization of Clostridium perfringens from the faecal microbiota of elderly Irish subjects. Journal of Medical Microbiology 62: 457-466.
30. Liu, D., Yu, J., Li, L., Ai, Q., Feng, J., Song, C. and Li, H., 2015. Bacterial community structure associated with elective cesarean section versus vaginal delivery in Chinese newborns. Journal of Pediatric Gastroenterology and Nutrition 60: 240-246.
31. Machiels, K., Sabino, J., Vandermosten, L., Joossens, M., Arijs, I., de Bruyn, M., Eeckhaut, V., Van Assche, G., Ferrante, M., Verhaegen, J., Van Steen, K., Van Immerseel, F., Huys, G., Verbeke, K., Wolthuis, A., de Buck Van Overstraeten, A., D'Hoore, A., Rutgeerts, P and Vermeire, S., 2015. Specific members of the predominant gut microbiota predict pouchitis following colectomy and IPAA in UC. Gut. DOI: https://doi.org/10.1136/gutjnl-2015-309398.
32. Mansson, I. and Olhagen, B., 1993. The abnormal faecal flora of Clostridium perfringens in rheumatoid arthritis and other diseases. British Journal of Rheumatology 32: 939-940.
33. Martin, R., Makino, H., Cetinyurek-Yavuz, A., Ben-Amor, K., Roelofs, M., Ishikawa, E., Kubota, H., Swinkels, S., Sakai, T., Oishi, K., Kushiro, A. and Knol, J., 2016. Early-life events, including mode of delivery and type of feeding, siblings and gender, shape the developing gut microbiota. PLoS One 11: e0158498.
34. Matamoros, S., Gras-Leguen, C., Le Vacon, F., Potel, G. and de La Cochetiere, M.F., 2013. Development of intestinal microbiota in infants and its impact on health. Trends in Microbiology 21: 167-173.
35. Matsuda, K., Tsuji, H., Asahara, T., Matsumoto, K., Takada, T. and Nomoto, K., 2009. Establishment of an analytical system for the human fecal microbiota, based on reverse transcription-quantitative PCR targeting of multicopy rRNA molecules. Applied and Environmental Microbiology 75: 1961-1969.
36. Matsuki, T., Tajima, S., Hara, T., Yahagi, K., Ogawa, E. and Kodama, H., 2016. Infant formula with galacto-oligosaccharides (OM55N) stimulates the growth of indigenous bifidobacteria in healthy term infants. Beneficial Microbes 7: 453-461.
37. Nagpal, R., Ogata, K., Tsuji, H., Matsuda, K., Takahashi, T., Nomoto, K., Nagata, S. and Yamashiro, Y., 2015. Sensitive quantification of Clostridium perfringens in human feces by quantitative PCR targeting alpha-toxin and enterotoxin genes. BMC Microbiology 15: 219.
38. Nagpal, R., Tsuji, H., Takahashi, T., Kawashima, K., Nagata, S., Nomoto, K. and Yamashiro, Y., 2016. Sensitive quantitative analysis of the meconium bacterial microbiota in healthy term infants born vaginally or by cesarean section. Frontiers in Microbiology 7: 1997.
39. Oda, M., Terao, Y., Sakurai, J. and Nagahama, M., 2015. Membranebinding mechanism of Clostridium perfringens alpha-toxin. Toxins 7: 5268-5275.
40. Penders, J., Thijs, C., van den Brandt, P.A., Kummeling, I., Snijders, B., Stelma, F., Adams, H., Van Ree, R. and Stobberingh, E.E., 2007. Gut microbiota composition and development of atopic manifestations in infancy: the KOALA Birth Cohort Study. Gut 56: 661-667.
41. Penders, J., Thijs, C., Vink, C., Stelma, F.F., Snijders, B., Kummeling, I., Van den Brandt, P.A. and Stobberingh, E.E., 2006. Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics 118: 511-521.
42. Putignani, L., Chierico, F.D., Petrucca, A., Vernocchi, P. and Dallapiccola, B., 2014. The human gut microbiota: a dynamic interplay with the host from birth to senescence settled during childhood. Pediatric Research 76: 2-10.
43. Sato, J., Kanazawa, A., Ikeda, F., Yoshihara, T., Goto, H., Abe, H., Komiya, K., Kawaguchi, M., Shimizu, T., Ogihara, T., Tamura, Y., Sakurai, Y., Yamamoto, R., Mita, T., Fujitani, Y., Fukuda, H., Nomoto, K., Takahashi, T., Asahara, T., Hirose, T., Nagata, S., Yamashiro, Y. and Watada, H., 2014. Gut dysbiosis and detection of 'live gut bacteria' in blood of Japanese patients with type 2 diabetes. Diabetes Care 37: 2343-2350.
44. Stark, P.L. and Lee, A., 1982. The microbial ecology of the large bowel of breast-fed and formula-fed infants during the first year of life. Journal of Medical Microbiology 15: 189-203.
45. Tanaka, D., Kimata, K., Shimizu, M., Isobe, J., Watahiki, M., Karasawa, T., Yamagishi, T., Kuramoto, S., Serikawa, T., Ishiguro, F., Yamada, M., Yamaoka, K., Tokoro, M., Fukao, T., Matsumoto, M., Hiramatsu, R., Monma, C. and Nagai, Y., 2007. Genotyping of Clostridium perfringens isolates collected from food poisoning outbreaks and healthy individuals in Japan based on the cpe locus. Japanese Journal of Infectious Diseases 60: 68-69.
46. Tonooka, T., Sakata, S., Kitahara, M., Hanai, M., Ishizeki, S., Takada, M., Sakamoto, M. and Benno, Y., 2005. Detection and quantification of four species of the genus Clostridium in infant feces. Microbiology and Immunology 49: 987-992.
47. Tsuji, H., Oozeer, R., Matsuda, K., Matsuki, T., Ohta, T., Nomoto, K., Tanaka, R., Kawashima, M., Kawashima, K., Nagata, S. and Yamashiro, Y., 2012. Molecular monitoring of the development of intestinal microbiota in Japanese infants. Beneficial Microbes 3: 113-125.
48. Uzal, F.A., Freedman, J.C., Shrestha, A., Theoret, J.R., Garcia, J., Awad, M.M., Adams, V., Moore, R.J., Rood, J.I. and McClane, B.A., 2014. Towards an understanding of the role of Clostridium perfringens toxins in human and animal disease. Future Microbiology 9: 361-377.
49. Van Best, N., Hornef, M.W., Savelkoul, P.H. and Penders, J., 2015. On the origin of species: factors shaping the establishment of infant's gut microbiota. Birth Defects Research Part C: Embryo Today 105: 240-251.
50. Vandenplas, Y., Zakharova, I. and Dmitrieva, Y., 2015. Oligosaccharides in infant formula: more evidence to validate the role of prebiotics. British Journal of Nutrition 113: 1339-1344.
51. Watanabe, Y., Arase, S., Nagaoka, N., Kawai, M. and Matsumoto, S., 2016. Chronic psychological stress disrupted the composition of the murine colonic microbiota and accelerated a murine model of inflammatory bowel disease. PLoS One 11: e0150559.