Risk factors for the carriage of Streptococcus infantarius subspecies infantarius isolated from African fermented dairy products
Autoři:
Kossia D. T. Gboko aff001; Sylvain G. Traoré aff001; Aimé R. Sanhoun aff001; Jérôme Kirioua aff002; Nize Otaru aff004; Fabienne Kurt aff004; Fabienne N. Jaeger aff005; Julia Isenring aff004; Dasel W. M. Kaindi aff007; Bernd Kreikemeyer aff008; Pierre Renault aff009; Jan Hattendorf aff005; Leo Meile aff004; Christoph Jans aff004; Roland Nguetta aff010; Bassirou Bonfoh aff001
Působiště autorů:
Centre Suisse de Recherches Scientifiques en Côte d’Ivoire (CSRS), Adiopodoumé Yopougon, Abidjan, Côte d'Ivoire
aff001; University of Peleforo Gon Coulibaly, Korhogo, Côte d'Ivoire
aff002; University of Nangui Abrogoua, Abidjan, Côte d'Ivoire
aff003; Laboratory of Food Biotechnology, Institute of Food, Nutrition and Health, ETH Zurich, Schmelzbergstrasse 7, Zurich, Switzerland
aff004; Department of Epidemiology and Public Health, Swiss Tropical and Public Health Institute, Basel, Switzerland
aff005; University of Basel, Basel, Switzerland
aff006; Department of Food Science, Nutrition and Technology, University of Nairobi, Nairobi, Kenya
aff007; Institute of Medical Microbiology, Virology, and Hygiene, Rostock University Medical Centre Rostock, Germany
aff008; Institut National de la Recherche Agronomique, UMR 1319 MICALIS, Jouy-en-Josas, France
aff009; Institut de cardiologie d’Abidjan (ICA), Abidjan, Côte d’Ivoire
aff010; Université Felix Houphouët-Boigny, Abidjan, Côte d’Ivoire
aff011
Vyšlo v časopise:
PLoS ONE 14(11)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0225452
Souhrn
Streptococcus infantarius subsp. infantarius (Sii) has been identified as predominant lactic acid bacteria in spontaneously fermented dairy products (FDPs) in sub-Saharan Africa including Côte d'Ivoire. However, Sii belongs to the Streptococcus bovis/Streptococcus equinus complex (SBSEC). Most SBSEC members are assumed to be involved as opportunistic pathogens in serious diseases in both humans and animals. A population-based cross-sectional survey, including 385 participants was conducted in Korhogo, northern Côte d'Ivoire, to identify risk factors for Sii fecal carriage, including consumption of local FDPs. A structured questionnaire was used to gather participant's socio-demographic and economic characteristics, their relation to livestock and dietary habits. In addition, fresh stool and milk samples were collected. The identification of Sii was done using a SBSEC-specific PCR assay targeting 16S rRNA and groEL genes. The overall prevalence of SBSEC and Sii carriage was 23.2% (confidence interval CI 95% = 18.9–27.5) and 12.0% (CI 95% = 8.4–15.5) for stool, respectively. Prevalence of Sii was significantly higher in consumers of artisanal butter compared with non-consumers (57.1% vs 10.1%, odds ratio OR: 11.9, 95% CI: 3.9–36.6), as well as in persons handling livestock (OR = 3.9; 95% CI = 1.6–9.3) and livestock primary products (OR = 5.7; 95% CI = 2.3–14.3). The closer contact with livestock was a risk factor for Sii fecal carriage. Sii strains were isolated from fresh and fermented milk products with a prevalence of 30.4% and 45.4%, respectively. Analysis of Sii population structure through the SBSEC multi locus sequence typing assay revealed a close relationship across human and dairy isolates, possibly linked to a Kenyan human isolate. All these outcomes underline the interest of in-depth investigations on the ecology, potential reservoirs and pathways of contamination by Sii at the human-animal-environment interface in comparison to yet to be collected data from Europe, Asia and the Americas to further elucidate the various roles of Sii.
Klíčová slova:
Africa – Meat – Milk – Livestock – Food consumption – Medical risk factors – Streptococcus – Group D streptococci
Zdroje
1. Herrera P, Min Kwon Y, Ricke SC. Ecology and pathogenicity of gastrointestinal Streptococcus bovis. Anaerobe. 2009;15:44–54. doi: 10.1016/j.anaerobe.2008.11.003 19100852
2. Schlegel L, Grimont F, Ageron E, Grimont PAD, Bouvet A. Reappraisal of the taxonomy of the Streptococcus bovis/Streptococcus equinus complex and related species: description of Streptococcus gallolyticus subsp. gallolyticus subsp. nov., S. gallolyticus subsp. macedonicus subsp. nov. and S. gallolyticus subsp. pasteurianus subsp. nov. Int J Syst Evol Microbiol. 2003;53:631–645. doi: 10.1099/ijs.0.02361-0 12807180
3. Jans C, Meile L, Lacroix C, Stevens MJA. Genomics, evolution, and molecular epidemiology of the Streptococcus bovis/Streptococcus equinus complex (SBSEC). Infect, Genet Evol. 2015;33:419–436. doi: 10.1016/j.meegid.2014.09.017 25233845
4. Schulz J, Dumke J, Hinse D, Dreier J, Habig C, Kemper N. Organic Turkey flocks: A reservoir of Streptococcus gallolyticus subspecies gallolyticus. PLoS One. 2015;10:e0144412. doi: 10.1371/journal.pone.0144412 26657757
5. Dumke J, Vollmer T, Akkermann O, Knabbe C, Dreier J. Case-control study: Determination of potential risk factors for the colonization of healthy volunteers with Streptococcus gallolyticus subsp. gallolyticus. PLoS One. 2017;12:e0176515. doi: 10.1371/journal.pone.0176515 28459818
6. Kaindi DWM, Kogi-Makau W, Lule GN, Kreikemeyer B, Renault P, Bonfoh B, et al. Investigating the association between African spontaneously fermented dairy products, faecal carriage of Streptococcus infantarius subsp. infantarius and colorectal adenocarcinoma in Kenya. Acta Trop. 2017;178:10–18. doi: 10.1016/j.actatropica.2017.10.018 29079186
7. Jans C, Boleij A. The road to infection: Host-microbe interactions defining the pathogenicity of Streptococcus bovis/Streptococcus equinus complex members Front Microbiol. 2018;9:603. doi: 10.3389/fmicb.2018.00603 29692760
8. Grant RJ, Shang WY, Whitehead TR. Isolated septic arthritis due to Streptococcus bovis. Clin Infect Dis. 1997;24:1021. doi: 10.1093/clinids/24.5.1021 9142824
9. Fernández-Ruiz M, Villar-Silva J, Llenas-García J, Caurcel-Díaz L, Vila-Santos J, Sanz-Sanz F, et al. Streptococcus bovis bacteraemia revisited: clinical and microbiological correlates in a contemporary series of 59 patients. J Infect. 2010;61:307–313. doi: 10.1016/j.jinf.2010.07.007 20659498
10. Counihan-Edgar KL, Gill VA, Doroff AM, Burek KA, Miller WA, Shewmaker PL, et al. Genotypic characterization of Streptococcus infantarius subsp. coli isolates from sea otters with infective endocarditis and/or septicemia and from environmental mussel samples. J Clin Microbiol. 2012;50:4131–4133. doi: 10.1128/JCM.02581-12 23052307
11. Corredoira J, Alonso MP, García-Garrote F, García-Pais MJ, Coira A, Rabuñal R, et al. Streptococcus bovis group and biliary tract infections: an analysis of 51 cases. Clin Microbiol Infect. 2014;20:405–409. doi: 10.1111/1469-0691.12333 24033711
12. Alozie A, Köller K, Pose L, Raftis M, Steinhoff G, Westphal B, et al. Streptococcus bovis infectious endocarditis and occult gastrointestinal neoplasia: experience with 25 consecutive patients treated surgically. Gut Pathog. 2015;7:27. doi: 10.1186/s13099-015-0074-0 26473016
13. Alvarez A, Jia Y, Garcia CJ, Rosas-Blum ED, Boman D, Zuckerman MJ. Streptococcus bovis Bacteremia in Neonates in a Predominantly Hispanic Population. Front Pediatr. 2015;3:92. doi: 10.3389/fped.2015.00092 26579502
14. Ruoff KL, Miller SI, Garner CV, Ferraro MJ, Calderwood SB. Bacteremia with Streptococcus bovis and Streptococcus salivarius: clinical correlates of more accurate identification of isolates. J Clin Microbiol. 1989;27:305–308. 2915024
15. Gold JS, Bayar S, Salem RR. Association of Streptococcus bovis bacteremia with colonic neoplasia and extracolonic malignancy. Arch Surg. 2004;139:760–765. doi: 10.1001/archsurg.139.7.760 15249410
16. Corredoira-Sánchez J, García-Garrote F, Rabuñal R, López-Roses L, García-País MJ, Castro E, et al. Association between bacteremia due to Streptococcus gallolyticus subsp. gallolyticus (Streptococcus bovis I) and colorectal neoplasia: a case-control study. Clin Infect Dis. 2012;55:491–496. cis434 [pii] doi: 10.1093/cid/cis434 22563018
17. Corredoira J, Grau I, Garcia-Rodriguez JF, Alonso-Garcia P, Garcia-Pais MJ, Rabuñal R, et al. The clinical epidemiology and malignancies associated with Streptococcus bovis biotypes in 506 cases of bloodstream infections. J Infect. 2015;71:317–325. doi: 10.1016/j.jinf.2015.05.005 25982024
18. Ben-Chetrit E, Wiener-Well Y, Kashat L, Yinnon AM, Assous MV. Streptococcus bovis new taxonomy: does subspecies distinction matter? Eur J Clin Microbiol Infect Dis. 2017;36:387–393. doi: 10.1007/s10096-016-2814-6 27796646
19. Krishnan S, Eslick GD. Streptococcus bovis infection and colorectal neoplasia: a meta-analysis. Colorectal Dis. 2014;16:672–680. doi: 10.1111/codi.12662 24824513
20. Boleij A, van Gelder M, Swinkels DW, Tjalsma H. Clinical importance of Streptococcus gallolyticus infection among colorectal cancer patients: systematic review and meta-analysis. Clin Infect Dis. 2011;53:870–878. doi: 10.1093/cid/cir609 21960713
21. Lazarovitch T, Shango M, Levine M, Brusovansky R, Akins R, Hayakawa K, et al. The relationship between the new taxonomy of Streptococcus bovis and its clonality to colon cancer, endocarditis, and biliary disease. Infection. 2013;41:329–337. doi: 10.1007/s15010-012-0314-x 22886774
22. Habib G, Lancellotti P, Antunes MJ, Bongiorni MG, Casalta JP, Del Zotti F, et al. 2015 ESC Guidelines for the management of infective endocarditis: The Task Force for the Management of Infective Endocarditis of the European Society of Cardiology (ESC). Endorsed by: European Association for Cardio-Thoracic Surgery (EACTS), the European Association of Nuclear Medicine (EANM). European Heart Journal. 2015;36:3075–3128. doi: 10.1093/eurheartj/ehv319 26320109
23. Corredoira Sánchez J, García-Garrote F, García-País MJ, Fernández AT, Gonzalez-Juanatey C, Alonso García MP. Endocarditis caused by Streptococcus infantarius subsp. infantarius: a report of two cases. Int J Clin Pract. 2014;68:653–654. doi: 10.1111/ijcp.12376 24750527
24. Jans C, Bugnard J, Njage PMK, Lacroix C, Meile L. Lactic acid bacteria diversity of African raw and fermented camel milk products reveals a highly competitive, potentially health-threatening predominant microflora. LWT-Food Sci Technol. 2012;47:371–379. doi: 10.1016/j.lwt.2012.01.034
25. Jans C, Meile L, Kaindi DWM, Kogi-Makau W, Lamuka P, Renault P, et al. African fermented dairy products–overview of predominant technologically important microorganisms focusing on African Streptococcus infantarius variants and potential future applications for enhanced food safety and security. Int J Food Microbiol. 2017;250:27–36. doi: 10.1016/j.ijfoodmicro.2017.03.012 28364623
26. Wullschleger S, Lacroix C, Bonfoh B, Sissoko-Thiam A, Hugenschmidt S, Romanens E, et al. Analysis of lactic acid bacteria communities and their seasonal variations in a spontaneously fermented dairy product (Malian fènè) by applying a cultivation/genotype-based binary model. Int Dairy J. 2013;29:28–35. doi: 10.1016/j.idairyj.2012.08.001
27. Abdelgadir W, Nielsen DS, Hamad S, Jakobsen M. A traditional Sudanese fermented camel's milk product, Gariss, as a habitat of Streptococcus infantarius subsp. infantarius. Int J Food Microbiol. 2008;127:215–219. doi: 10.1016/j.ijfoodmicro.2008.07.008 18774196
28. Jans C, Kaindi DWM, Böck D, Njage PMK, Kouamé-Sina SM, Bonfoh B, et al. Prevalence and comparison of Streptococcus infantarius subsp. infantarius and Streptococcus gallolyticus subsp. macedonicus in raw and fermented dairy products from East and West Africa. Int J Food Microbiol. 2013;167:186–195. doi: 10.1016/j.ijfoodmicro.2013.09.008 24131584
29. Jans C, Follador R, Hochstrasser M, Lacroix C, Meile L, Stevens MJA. Comparative genome analysis of Streptococcus infantarius subsp. infantarius CJ18, an African fermented camel milk isolate with adaptations to dairy environment. BMC Genomics. 2013;14:200. doi: 10.1186/1471-2164-14-200 23521820
30. Kaindi DWM, Kogi-Makau W, Lule GN, Kreikemeyer B, Renault P, Bonfoh B, et al. Colorectal cancer-associated Streptococcus infantarius subsp. infantarius differ from a major dairy lineage providing evidence for pathogenic, pathobiont and food-grade lineages. Sci Rep. 2018;8:9181. doi: 10.1038/s41598-018-27383-4 29907746
31. WHO. Physical status: the use and interpretation of anthropometry. Report of a WHO expert committee. Geneva: World Health Organization, 1995 Contract No.: TRS No 854.
32. Gunnarsdóttir R, Müller K, Jensen PE, Jenssen PD, Villumsen A. Effect of long-term freezing and freeze-thaw cycles on indigenous and inoculated microorganisms in dewatered blackwater. Environ Sci Technol. 2012;46:12408–12416. doi: 10.1021/es3018489 23113759
33. Hubálek Z. Protectants used in the cryopreservation of microorganisms. Cryobiology. 2003;46:205–229. doi: 10.1016/s0011-2240(03)00046-4 12818211
34. Goldenberger D, Perschil I, Ritzler M, Altwegg M. A simple universal DNA extraction procedure using SDS and proteinase K is compatible with direct PCR amplification. PCR Methods Appl. 1995;4:368–370. doi: 10.1101/gr.4.6.368 7580932
35. Jans C, de Wouters T, Bonfoh B, Lacroix C, Kaindi DWM, Anderegg J, et al. Phylogenetic, epidemiological and functional analyses of the Streptococcus bovis/Streptococcus equinus complex through an overarching MLST scheme. BMC Microbiol. 2016;16:117. doi: 10.1186/s12866-016-0735-2 27329036
36. Jans C, Lacroix C, Meile L. A novel multiplex PCR/RFLP assay for the identification of Streptococcus bovis/Streptococcus equinus complex members from dairy microbial communities based on the 16S rRNA gene. FEMS Microbiol Lett. 2012;326:144–150. doi: 10.1111/j.1574-6968.2011.02443.x 22092382
37. Feil EJ, Li BC, Aanensen DM, Hanage WP, Spratt BG. eBURST: Inferring patterns of evolutionary descent among clusters of related bacterial genotypes from multilocus sequence typing data. J Bacteriol. 2004;186:1518–1530. doi: 10.1128/JB.186.5.1518-1530.2004 14973027
38. Spratt BG, Hanage WP, Li B, Aanensen DM, Feil EJ. Displaying the relatedness among isolates of bacterial species—the eBURST approach. FEMS Microbiol Lett. 2004;241:129–134. doi: 10.1016/j.femsle.2004.11.015 15598523
39. O'Donnell O, van Doorslaer E, Wagstaff A, Lindelow M. Analyzing Health Equity Using Household Survey Data: The World Bank.
40. World Medical Association. World Medical Association Declaration of Helsinki: ethical principles for medical research involving human subjects. JAMA. 2013;310:2191–2194. doi: 10.1001/jama.2013.281053 24141714
41. Lopes PG, Cantarelli VV, Agnes G, Costabeber AM, d'Azevedo PA. Novel real-time PCR assays using TaqMan minor groove binder probes for identification of fecal carriage of Streptococcus bovis/Streptococcus equinus complex from rectal swab specimens. J Clin Microbiol. 2014;52:974–976. doi: 10.1128/JCM.03253-13 24391203
42. Corredoira J, Alonso MP, Pita J, Alonso-Mesonero D. Association between rural residency, group D streptococcal endocarditis and colon cancer? Clin Microbiol Infect. 2008;14:190–190.
43. Pergola V, Di Salvo G, Habib G, Avierinos JF, Philip E, Vailloud JM, et al. Comparison of clinical and echocardiographic characteristics of Streptococcus bovis endocarditis with that caused by other pathogens. Am J Cardiol. 2001;88:871–875. doi: 10.1016/s0002-9149(01)01914-2 [pii]. 11676950
44. Giannitsioti E, Chirouze C, Bouvet A, Béguinot I, Delahaye F, Mainardi JL, et al. Characteristics and regional variations of group D streptococcal endocarditis in France. Clin Microbiol Infect. 2007;13:770–776. doi: 10.1111/j.1469-0691.2007.01753.x 17501973
45. Duval X, Papastamopoulos V, Longuet P, Benoit C, Perronne C, Leport C, et al. Definite Streptococcus bovis endocarditis: characteristics in 20 patients. Clin Microbiol Infect. 2001;7:3–10. doi: 10.1046/j.1469-0691.2001.00190.x 11284936
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