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Published in: European Journal of Clinical Microbiology & Infectious Diseases 9/2019

01-09-2019 | Fluorescence in Situ Hybridization | Original Article

Detection of Methanobrevibacter smithii in vaginal samples collected from women diagnosed with bacterial vaginosis

Authors: Ghiles Grine, Hortense Drouet, Florence Fenollar, Florence Bretelle, Didier Raoult, Michel Drancourt

Published in: European Journal of Clinical Microbiology & Infectious Diseases | Issue 9/2019

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Abstract

Vaginosis is a dysbiotic condition of the vaginal cavity that has deleterious effects during pregnancy. The role of methanogens in this disease is unknown since current methods of investigation are not appropriate for the search of methanogens. We prospectively investigated the presence of methanogens in vaginal specimens collected from 33 women thereafter diagnosed with bacterial vaginosis and 92 women thereafter diagnosed without bacterial vaginosis (control group) by direct microscopic examination and fluorescent in situ hybridization, PCR-sequencing, and real-time PCR and isolation and culture. These investigations found only one methanogen, Methanobrevibacter smithii, exclusively in 97% bacterial vaginosis specimens and in two intermediate microbiota specimens. M. smithii was detected microscopically in 2/20 specimens analyzed, by PCR-based observations in 34/125 specimens with 99% sequence similarity with the reference 16S rRNA and mcrA gene sequences and was cultured in 9/40 specimens. These data suggest that the detection of M. smithii could be used as a biomarker for the laboratory diagnosis of bacterial vaginosis.
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Literature
1.
go back to reference Bitew A, Abebaw Y, Bekele D, Mihret A (2017) Prevalence of bacterial vaginosis and associated risk factors among women complaining of genital tract infection. Int J Microbiol 150:1–13CrossRef Bitew A, Abebaw Y, Bekele D, Mihret A (2017) Prevalence of bacterial vaginosis and associated risk factors among women complaining of genital tract infection. Int J Microbiol 150:1–13CrossRef
2.
go back to reference Myer L, Denny L, Telerant R et al (2005) Bacterial vaginosis and susceptibility to HIV infection in south African women: a nested case control study. J Infect Dis 2:1372–1380CrossRef Myer L, Denny L, Telerant R et al (2005) Bacterial vaginosis and susceptibility to HIV infection in south African women: a nested case control study. J Infect Dis 2:1372–1380CrossRef
3.
go back to reference Kenyon C, Colebunders R, Crucitti T (2013) The global epidemiology of bacterial vaginosis: a systematic review. Am J Obstet Gynecol 209:505–523CrossRefPubMed Kenyon C, Colebunders R, Crucitti T (2013) The global epidemiology of bacterial vaginosis: a systematic review. Am J Obstet Gynecol 209:505–523CrossRefPubMed
5.
go back to reference Thorsen P, Jensen IP, Jeune B, Ebbesen N, Arpi M, Bremmelgaard A, Moller BR (1998) Few microorganisms associated with bacterial vaginosis may constitute the pathologic core: a population-based microbiologic study among 3596 pregnant women. Am J Obstet Gynecol 178:580–587CrossRefPubMed Thorsen P, Jensen IP, Jeune B, Ebbesen N, Arpi M, Bremmelgaard A, Moller BR (1998) Few microorganisms associated with bacterial vaginosis may constitute the pathologic core: a population-based microbiologic study among 3596 pregnant women. Am J Obstet Gynecol 178:580–587CrossRefPubMed
6.
go back to reference Sha BE, Chen HY, Wang QJ, Zariffard MR, Cohen MH, Spear GT (2005) Utility of Amsel Criteria, Nugent Score, and Quantitative PCR for for Diagnosis of Bacterial Vaginosis in Human Immunodeficiency Virus-Infected Women. Society 43:4607–4612 Sha BE, Chen HY, Wang QJ, Zariffard MR, Cohen MH, Spear GT (2005) Utility of Amsel Criteria, Nugent Score, and Quantitative PCR for for Diagnosis of Bacterial Vaginosis in Human Immunodeficiency Virus-Infected Women. Society 43:4607–4612
7.
go back to reference Mohammadzadeh F, Dolatian M, Jorjani M, Alavi Majd H (2014) Diagnostic value of Amsel’s clinical criteria for diagnosis of bacterial vaginosis. Global J Health Sci 7:8–14CrossRef Mohammadzadeh F, Dolatian M, Jorjani M, Alavi Majd H (2014) Diagnostic value of Amsel’s clinical criteria for diagnosis of bacterial vaginosis. Global J Health Sci 7:8–14CrossRef
8.
go back to reference Fredricks DN, Fiedler TL, Marrazzo JM (2005) Molecular identification of bacteria associated with bacterial vaginosis. N Engl J Med 353:1899–1911CrossRefPubMed Fredricks DN, Fiedler TL, Marrazzo JM (2005) Molecular identification of bacteria associated with bacterial vaginosis. N Engl J Med 353:1899–1911CrossRefPubMed
9.
go back to reference Thomason JL, Anderson RJ, Gelbart SM, Osypowski PJ, Scaglione NJ, el Tabbakh G et al (1992) Simplified gram stain interpretive method for diagnosis of bacterial vaginosis. Am J Obstet Gynecol 167:16–19CrossRefPubMed Thomason JL, Anderson RJ, Gelbart SM, Osypowski PJ, Scaglione NJ, el Tabbakh G et al (1992) Simplified gram stain interpretive method for diagnosis of bacterial vaginosis. Am J Obstet Gynecol 167:16–19CrossRefPubMed
10.
go back to reference Ison CA, Hay PE (2002) Validation of a simplified grading of gram stained vaginal smears for use in genitourinary medicine clinics. Sex Transm Infect 78:413–415CrossRefPubMedPubMedCentral Ison CA, Hay PE (2002) Validation of a simplified grading of gram stained vaginal smears for use in genitourinary medicine clinics. Sex Transm Infect 78:413–415CrossRefPubMedPubMedCentral
11.
go back to reference Nugent RP, Krohn MA, Hillier SL (1991) Reliability of diagnosing bacterial vaginosis is improved by a standardized method of gram stain interpretation. J Clin Microbiol 29:297–301PubMedPubMedCentral Nugent RP, Krohn MA, Hillier SL (1991) Reliability of diagnosing bacterial vaginosis is improved by a standardized method of gram stain interpretation. J Clin Microbiol 29:297–301PubMedPubMedCentral
12.
go back to reference Menard JP, Mazouni C, Salem-Cherif I et al (2010) High vaginal concentrations of Atopobium vaginae and Gardnerella vaginalis in women undergoing preterm labor. Obstet Gynecol 115:134–140CrossRefPubMed Menard JP, Mazouni C, Salem-Cherif I et al (2010) High vaginal concentrations of Atopobium vaginae and Gardnerella vaginalis in women undergoing preterm labor. Obstet Gynecol 115:134–140CrossRefPubMed
13.
go back to reference Menard JP, Mazouni C, Fenollar F, Raoult D, Boubli L, Bretelle F (2010) Diagnostic accuracy of quantitative real-time PCR assay versus clinical and gram stain identification of bacterial vaginosis. Eur J Clin Microbiol Infect Dis 29:1547–1552CrossRefPubMed Menard JP, Mazouni C, Fenollar F, Raoult D, Boubli L, Bretelle F (2010) Diagnostic accuracy of quantitative real-time PCR assay versus clinical and gram stain identification of bacterial vaginosis. Eur J Clin Microbiol Infect Dis 29:1547–1552CrossRefPubMed
14.
go back to reference Menard J, Fenollar F, Henry M, Bretelle F, Raoult D (2008) Molecular quantification of Gardnerella vaginalis and Atopobium vaginae loads to predict bacterial vaginosis. Clin Infect Dis 47:33–43CrossRefPubMed Menard J, Fenollar F, Henry M, Bretelle F, Raoult D (2008) Molecular quantification of Gardnerella vaginalis and Atopobium vaginae loads to predict bacterial vaginosis. Clin Infect Dis 47:33–43CrossRefPubMed
15.
go back to reference Bretelle F, Rozenberg P, Pascal A et al (2015) High Atopobium vaginae and Gardnerella vaginalis vaginal loads are associated with preterm birth. Clin Infect Dis 60:860–867CrossRefPubMed Bretelle F, Rozenberg P, Pascal A et al (2015) High Atopobium vaginae and Gardnerella vaginalis vaginal loads are associated with preterm birth. Clin Infect Dis 60:860–867CrossRefPubMed
16.
go back to reference Srinivasan S, Fredricks DN (2008) The human vaginal bacterial biota and bacterial vaginosis. Interdiscip Perspect Infect Dis 208:1–22CrossRef Srinivasan S, Fredricks DN (2008) The human vaginal bacterial biota and bacterial vaginosis. Interdiscip Perspect Infect Dis 208:1–22CrossRef
17.
go back to reference Hillier SL, Krohn MA, Rabe LK, Klebanoff SJ, Eschenbach DA (1993) The normal vaginal flora, H2 O2-producing lactobacilli, and bacterial vaginosis in pregnant women. Clin Infect Dis 16:273–281CrossRef Hillier SL, Krohn MA, Rabe LK, Klebanoff SJ, Eschenbach DA (1993) The normal vaginal flora, H2 O2-producing lactobacilli, and bacterial vaginosis in pregnant women. Clin Infect Dis 16:273–281CrossRef
18.
go back to reference Dominguez-Bello MG, De Jesus-Laboy KM, Shen N et al (2016) Partial restoration of the microbiota of cesarean-born infants via vaginal microbial transfer. Nat Med 22:250–253CrossRefPubMedPubMedCentral Dominguez-Bello MG, De Jesus-Laboy KM, Shen N et al (2016) Partial restoration of the microbiota of cesarean-born infants via vaginal microbial transfer. Nat Med 22:250–253CrossRefPubMedPubMedCentral
19.
go back to reference Ling Z, Kong J, Liu F, Zhu H, Chen X, Wang Y et al (2010) Molecular analysis of the diversity of vaginal microbiota associated with bacterial vaginosis. BMC Genomics 11:482–428CrossRef Ling Z, Kong J, Liu F, Zhu H, Chen X, Wang Y et al (2010) Molecular analysis of the diversity of vaginal microbiota associated with bacterial vaginosis. BMC Genomics 11:482–428CrossRef
21.
go back to reference Aagaard K, Riehle K, Ma J, Segata N, Mistretta TA, Coarfa C et al (2012) A metagenomic approach to characterization of the vaginal microbiome signature in pregnancy. PLoS One 7:12–20CrossRef Aagaard K, Riehle K, Ma J, Segata N, Mistretta TA, Coarfa C et al (2012) A metagenomic approach to characterization of the vaginal microbiome signature in pregnancy. PLoS One 7:12–20CrossRef
22.
go back to reference Liu Y, Whitman WB (2008) Metabolic, phylogenetic, and ecological diversity of the methanogenic archaea. Ann N Y Acad Sci 1125:171–189CrossRefPubMed Liu Y, Whitman WB (2008) Metabolic, phylogenetic, and ecological diversity of the methanogenic archaea. Ann N Y Acad Sci 1125:171–189CrossRefPubMed
23.
go back to reference Khelaifia S, Ramonet PY, Bedotto Buffet M, Drancourt M (2013) A semi-automated protocol for archaea DNA extraction from stools. BMC Res Notes 6:186–191CrossRefPubMedPubMedCentral Khelaifia S, Ramonet PY, Bedotto Buffet M, Drancourt M (2013) A semi-automated protocol for archaea DNA extraction from stools. BMC Res Notes 6:186–191CrossRefPubMedPubMedCentral
24.
go back to reference Belay N, Mukhopadhyay B, Conway de Macario E, Galask R, Daniels L (1990) Methanogenic bacteria in human vaginal samples. J Clin Microbiol 28:1666–1668PubMedPubMedCentral Belay N, Mukhopadhyay B, Conway de Macario E, Galask R, Daniels L (1990) Methanogenic bacteria in human vaginal samples. J Clin Microbiol 28:1666–1668PubMedPubMedCentral
25.
go back to reference Dridi B, Henry M, El Khéchine A, Raoult D, Drancourt M (2009) High prevalence of Methanobrevibacter smithii and Methanosphaera stadtmanae detected in the human gut using an improved DNA detection protocol. PLoS One 4:23–29CrossRef Dridi B, Henry M, El Khéchine A, Raoult D, Drancourt M (2009) High prevalence of Methanobrevibacter smithii and Methanosphaera stadtmanae detected in the human gut using an improved DNA detection protocol. PLoS One 4:23–29CrossRef
26.
go back to reference Dridi B, Fardeau ML, Ollivier B, Raoult D, Drancourt M (2011) The antimicrobial resistance pattern of cultured human methanogens reflects the unique phylogenetic position of archaea. J Antimicrob Chemother 66:2038–2044CrossRefPubMed Dridi B, Fardeau ML, Ollivier B, Raoult D, Drancourt M (2011) The antimicrobial resistance pattern of cultured human methanogens reflects the unique phylogenetic position of archaea. J Antimicrob Chemother 66:2038–2044CrossRefPubMed
27.
go back to reference Drancourt M, Nkamga VD, Lakhe NA, Régis JM, Dufour H, Fournier PE et al (2017) Evidence of archaeal methanogens in brain abscess. Clin Infect Dis 65:1–5CrossRefPubMed Drancourt M, Nkamga VD, Lakhe NA, Régis JM, Dufour H, Fournier PE et al (2017) Evidence of archaeal methanogens in brain abscess. Clin Infect Dis 65:1–5CrossRefPubMed
28.
go back to reference Nkamga VD, Lotte R, Roger PM, Drancourt M, Ruimy R (2016) Methanobrevibacter smithii and Bacteroides thetaiotaomicron cultivated from a chronic paravertebral muscle abscess. Clin Microbiol Infect 22:1008–1009CrossRefPubMed Nkamga VD, Lotte R, Roger PM, Drancourt M, Ruimy R (2016) Methanobrevibacter smithii and Bacteroides thetaiotaomicron cultivated from a chronic paravertebral muscle abscess. Clin Microbiol Infect 22:1008–1009CrossRefPubMed
29.
go back to reference Hungate R, Macy J (1973) The roll-tube method for cultivation of strict anaerobes. Modern methods in the study of microbial ecology. Oikos Editorial Office: Bulletins of the Ecological Research Committee, pp 123–126 Hungate R, Macy J (1973) The roll-tube method for cultivation of strict anaerobes. Modern methods in the study of microbial ecology. Oikos Editorial Office: Bulletins of the Ecological Research Committee, pp 123–126
30.
go back to reference Khelaifia S, Raoult D, Drancourt M (2013) A versatile medium for cultivating methanogenic archaea. PLoS One 8:13–20CrossRef Khelaifia S, Raoult D, Drancourt M (2013) A versatile medium for cultivating methanogenic archaea. PLoS One 8:13–20CrossRef
31.
go back to reference Nkamga VD, Drancourt M (2015) Methanomassiliicoccaceae. In: Whitman WB (ed) Bergey’s manual of systematics of archaea and bacteria. Wiley, Chichester Nkamga VD, Drancourt M (2015) Methanomassiliicoccaceae. In: Whitman WB (ed) Bergey’s manual of systematics of archaea and bacteria. Wiley, Chichester
32.
go back to reference Khelaifia S, Lagier JC, Nkamga VD, Guilhot E, Drancourt M, Raoult D (2016) Aerobic culture of methanogenic archaea without an external source of hydrogen. Eur J Clin Microbiol Infect Dis 35:985–991CrossRefPubMed Khelaifia S, Lagier JC, Nkamga VD, Guilhot E, Drancourt M, Raoult D (2016) Aerobic culture of methanogenic archaea without an external source of hydrogen. Eur J Clin Microbiol Infect Dis 35:985–991CrossRefPubMed
33.
go back to reference Lepp PW, Brinig MM, Ouverney CC, Palm K, Armitage GC, Relman DA (2004) Methanogenic archaea and human periodontal disease. Proc Natl Acad Sci 101:6176–6181CrossRefPubMed Lepp PW, Brinig MM, Ouverney CC, Palm K, Armitage GC, Relman DA (2004) Methanogenic archaea and human periodontal disease. Proc Natl Acad Sci 101:6176–6181CrossRefPubMed
34.
go back to reference Raskin L, Stromley JM, Rittmann BE, Stahl D (1994) Group-specific 16S ribosomal-Rna hybridization probes to describe natural communities of methanogens. Appl Environ Microbiol 60:1232–1240PubMedPubMedCentral Raskin L, Stromley JM, Rittmann BE, Stahl D (1994) Group-specific 16S ribosomal-Rna hybridization probes to describe natural communities of methanogens. Appl Environ Microbiol 60:1232–1240PubMedPubMedCentral
35.
go back to reference Grine G, Boualam MA, Drancourt M (2017) Methanobrevibacter smithii, a methanogen consistently colonising the newborn stomach. Eur J Clin Microbiol Infect Dis 12:1–7 Grine G, Boualam MA, Drancourt M (2017) Methanobrevibacter smithii, a methanogen consistently colonising the newborn stomach. Eur J Clin Microbiol Infect Dis 12:1–7
36.
go back to reference Demonfort V, Henrissat B, Drancourt M (2017) Archaea: essential inhabitants of the human digestive microbiota. Hum Microbiome J3:1–8 Demonfort V, Henrissat B, Drancourt M (2017) Archaea: essential inhabitants of the human digestive microbiota. Hum Microbiome J3:1–8
37.
go back to reference Dridi B, Fardeau ML, Ollivier B, Raoult D, Drancourt M (2012) Methanomassiliicoccus luminyensis gen. Nov., sp. nov., a methanogenic archaeon isolated from human faeces. Int J Syst Evol Microbiol 62:1902–1907CrossRefPubMed Dridi B, Fardeau ML, Ollivier B, Raoult D, Drancourt M (2012) Methanomassiliicoccus luminyensis gen. Nov., sp. nov., a methanogenic archaeon isolated from human faeces. Int J Syst Evol Microbiol 62:1902–1907CrossRefPubMed
38.
go back to reference Nguyen-Hieu T, Khelaifia S, Aboudharam G, Drancourt M (2013) Methanogenic archaea in subgingival sites: a review. Apmis 121:467–477CrossRefPubMed Nguyen-Hieu T, Khelaifia S, Aboudharam G, Drancourt M (2013) Methanogenic archaea in subgingival sites: a review. Apmis 121:467–477CrossRefPubMed
39.
go back to reference Gaci N, Borrel G, Tottey W, O’Toole PW, Brugère JF (2014) Archaea and the human gut: new beginning of an old story. World J Gastroenterol 20:16062–16078CrossRefPubMedPubMedCentral Gaci N, Borrel G, Tottey W, O’Toole PW, Brugère JF (2014) Archaea and the human gut: new beginning of an old story. World J Gastroenterol 20:16062–16078CrossRefPubMedPubMedCentral
40.
go back to reference Huynh HTT, Pignoly M, Drancourt M, Aboudharam G (2017) A new methanogen “Methanobrevibacter massiliense” isolated in a case of severe periodontitis. BMC Res Notes 10:657–663CrossRefPubMedPubMedCentral Huynh HTT, Pignoly M, Drancourt M, Aboudharam G (2017) A new methanogen “Methanobrevibacter massiliense” isolated in a case of severe periodontitis. BMC Res Notes 10:657–663CrossRefPubMedPubMedCentral
41.
go back to reference Koskinen K, Pausan MR, Perras AK, Beck M, Bang C, Mora M et al (2007) First insights into the diverse human Archaeome: specific detection of archaea in the gastrointestinal tract, lung, and Nose and on Skin. MBio 8:1–17 Koskinen K, Pausan MR, Perras AK, Beck M, Bang C, Mora M et al (2007) First insights into the diverse human Archaeome: specific detection of archaea in the gastrointestinal tract, lung, and Nose and on Skin. MBio 8:1–17
42.
go back to reference Grine G, Terrer E, Boualam MA, Aboudharam G, Chaudet H, Ruimy R et al (2018) Tobacco-smoking-related prevalence of methanogens in the oral fluid microbiota. Sci Rep 8:91–97CrossRef Grine G, Terrer E, Boualam MA, Aboudharam G, Chaudet H, Ruimy R et al (2018) Tobacco-smoking-related prevalence of methanogens in the oral fluid microbiota. Sci Rep 8:91–97CrossRef
43.
go back to reference Johnston C, Ufnar JA, Griffith JF, Gooch JA, Stewart JR (2010) A real-time qPCR assay for the detection of the nifH gene of Methanobrevibacter smithii, a potential indicator of sewage pollution. J Appl Microbiol 109:1946–1956CrossRefPubMed Johnston C, Ufnar JA, Griffith JF, Gooch JA, Stewart JR (2010) A real-time qPCR assay for the detection of the nifH gene of Methanobrevibacter smithii, a potential indicator of sewage pollution. J Appl Microbiol 109:1946–1956CrossRefPubMed
44.
go back to reference Ufnar JA, Wang SY, Christiansen JM, Yampara-Iquise H, Carson CA, Ellender RD (2006) Detection of the nifH gene of Methanobrevibacter smithii: a potential tool to identify sewage pollution in recreational waters. J Appl Microbiol 101:44–52CrossRefPubMed Ufnar JA, Wang SY, Christiansen JM, Yampara-Iquise H, Carson CA, Ellender RD (2006) Detection of the nifH gene of Methanobrevibacter smithii: a potential tool to identify sewage pollution in recreational waters. J Appl Microbiol 101:44–52CrossRefPubMed
45.
go back to reference Fenollar F, Raoult D (2009) Does bacterial vaginosis result from fecal transplantation? J infect dis. 2016;214:1784-90.Vianna ME, Conrads G, Gomes BPFA, Horz HP. T-RFLP based mcrA gene analysis of methanogenic archaea in association with oral infections and evidence of a novel Methanobrevibacter phylotype. Oral Microbiol Immunol 24:417–422CrossRef Fenollar F, Raoult D (2009) Does bacterial vaginosis result from fecal transplantation? J infect dis. 2016;214:1784-90.Vianna ME, Conrads G, Gomes BPFA, Horz HP. T-RFLP based mcrA gene analysis of methanogenic archaea in association with oral infections and evidence of a novel Methanobrevibacter phylotype. Oral Microbiol Immunol 24:417–422CrossRef
Metadata
Title
Detection of Methanobrevibacter smithii in vaginal samples collected from women diagnosed with bacterial vaginosis
Authors
Ghiles Grine
Hortense Drouet
Florence Fenollar
Florence Bretelle
Didier Raoult
Michel Drancourt
Publication date
01-09-2019
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Clinical Microbiology & Infectious Diseases / Issue 9/2019
Print ISSN: 0934-9723
Electronic ISSN: 1435-4373
DOI
https://doi.org/10.1007/s10096-019-03592-1

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