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Published in: BMC Infectious Diseases 1/2013

Open Access 01-12-2013 | Research article

Use of genotyping based clustering to quantify recent tuberculosis transmission in Guadeloupe during a seven years period: analysis of risk factors and access to health care

Authors: Séverine Ferdinand, Julie Millet, Annick Accipe, Sylvie Cassadou, Pascal Chaud, Maryse Levy, Max Théodore, Nalin Rastogi

Published in: BMC Infectious Diseases | Issue 1/2013

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Abstract

Background

The present study aimed to characterize Mycobacterium tuberculosis population structure and to identify transmission chains and risk factors by prospective molecular typing in conjunction with conventional epidemiological investigations in the French overseas department of Guadeloupe.

Methods

The study included all the culture-positive TB cases (1 clinical isolate per patient; n = 129) diagnosed between a seven year period (April 4th, 1999 to December 31st, 2005). Prospective molecular typing was performed using spoligotyping and VNTRs, and a subset of 44 M. tuberculosis isolates found to be clustered was retrospectively typed using 12-loci MIRUs. Data were compared using the SITVIT2 database, followed by analysis of risk factors in function of clustering of the isolates and available demographic and socioeconomic data.

Results

The study sample was characterized by a majority of new cases (87.4%); a moderate proportion of drug-resistance (7.8%); a high level of immigration (51.2% foreign-born) originating from high TB/HIV incidence neighboring islands such as Haiti or Dominican Republic; lower socioeconomic conditions (70.7% of jobless, average income 824 EUR/month); and a significantly higher proportion of TB/HIV co-infected cases (38.2% vs. 8.5%; p < 0.001), and extrapulmonary disease (18.2% vs. 4.8%; p < 0.02) among migrants as compared to French patients. The study revealed an important delay in access to healthcare with a median delay of 74.5 days between the 1st symptoms and clinical suspicion of TB. Prospective molecular typing based on spoligotyping and 5-loci VNTRs showed that evolutionary recent Euro-American lineages predominated in Guadeloupe (91.5% of isolates). In conjunction with epidemiological data, it allowed to estimate a recent transmission rate of 18.6%, which was close to the rate of 16.7% estimated using retrospective 12-loci MIRU typing. Although a higher proportion of cases in older age-group were apparently linked to reactivation; univariate analysis of risk factors did not allow pinpointing specific risk factors for a patient to belong to a TB transmission group.

Conclusions

Ongoing TB transmission in the insular, low TB-incidence setting of Guadeloupe can be defined as follows: (i) a significant proportion of imported cases of the disease from neighboring islands; (ii) significantly higher TB/HIV coinfection among foreign-born cases; and, (iii) a higher proportion of cases affecting older age-group among French patients due to reactivation. This study emphasizes the need for universal typing using spoligotyping and 15-loci MIRUs in prospective studies.
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Literature
2.
go back to reference Stop TB: Partnership: The Global Plan to Stop TB, 2006–2015. Actions for life: towards a world free of tuberculosis. Int J Tuberc Lung Dis. 2006, 10: 240-241. Stop TB: Partnership: The Global Plan to Stop TB, 2006–2015. Actions for life: towards a world free of tuberculosis. Int J Tuberc Lung Dis. 2006, 10: 240-241.
3.
go back to reference Small P, Behr M: Molecular fingerprinting of Mycobacterium tuberculosis: how can it help the clinician?. Clin Infect Dis. 1997, 25: 806-810. 10.1086/515550.CrossRefPubMed Small P, Behr M: Molecular fingerprinting of Mycobacterium tuberculosis: how can it help the clinician?. Clin Infect Dis. 1997, 25: 806-810. 10.1086/515550.CrossRefPubMed
4.
go back to reference Alland D, Kalkut G, Moss A, McAdam R, Hahn JA, Bosworth W, Drucker E, Bloom BR: Transmission of tuberculosis in New York City. An analysis by DNA fingerprinting and conventional epidemiologic methods. N Engl J Med. 1994, 330: 1710-1716. 10.1056/NEJM199406163302403.CrossRefPubMed Alland D, Kalkut G, Moss A, McAdam R, Hahn JA, Bosworth W, Drucker E, Bloom BR: Transmission of tuberculosis in New York City. An analysis by DNA fingerprinting and conventional epidemiologic methods. N Engl J Med. 1994, 330: 1710-1716. 10.1056/NEJM199406163302403.CrossRefPubMed
5.
go back to reference Small PM, Hopewell PC, Singh SP, Paz A, Parsonnet J, Ruston DC, Schecter GF, Daley CL, Schoolnik GK: The epidemiology of tuberculosis in San Francisco. A population-based study using conventional and molecular methods. N Engl J Med. 1994, 330: 1703-1709. 10.1056/NEJM199406163302402.CrossRefPubMed Small PM, Hopewell PC, Singh SP, Paz A, Parsonnet J, Ruston DC, Schecter GF, Daley CL, Schoolnik GK: The epidemiology of tuberculosis in San Francisco. A population-based study using conventional and molecular methods. N Engl J Med. 1994, 330: 1703-1709. 10.1056/NEJM199406163302402.CrossRefPubMed
6.
go back to reference Kamerbeek J, Schouls L, Kolk A, van Agterveld M, van Soolingen D, Kuijper S, Bunschoten A, Molhuizen H, Shaw R, Goyal M, van Embden J: Simultaneous detection and strain differentiation of Mycobacterium tuberculosis for diagnosis and epidemiology. J Clin Microbiol. 1997, 35: 907-914.PubMedPubMedCentral Kamerbeek J, Schouls L, Kolk A, van Agterveld M, van Soolingen D, Kuijper S, Bunschoten A, Molhuizen H, Shaw R, Goyal M, van Embden J: Simultaneous detection and strain differentiation of Mycobacterium tuberculosis for diagnosis and epidemiology. J Clin Microbiol. 1997, 35: 907-914.PubMedPubMedCentral
7.
go back to reference Frothingham R, Meeker-O’Connell WA: Genetic diversity in the Mycobacterium tuberculosis complex based on variable numbers of tandem DNA repeats. Microbiology. 1998, 144: 1189-1196. 10.1099/00221287-144-5-1189.CrossRefPubMed Frothingham R, Meeker-O’Connell WA: Genetic diversity in the Mycobacterium tuberculosis complex based on variable numbers of tandem DNA repeats. Microbiology. 1998, 144: 1189-1196. 10.1099/00221287-144-5-1189.CrossRefPubMed
8.
go back to reference Sola C, Horgen L, Goh KS, Rastogi N: Molecular fingerprinting of Mycobacterium tuberculosis on a Caribbean island with IS6110 and DRr probes. J Clin Microbiol. 1997, 35: 843-846.PubMedPubMedCentral Sola C, Horgen L, Goh KS, Rastogi N: Molecular fingerprinting of Mycobacterium tuberculosis on a Caribbean island with IS6110 and DRr probes. J Clin Microbiol. 1997, 35: 843-846.PubMedPubMedCentral
9.
go back to reference Sola C, Horgen L, Maïsetti J, Devallois A, Goh KS, Rastogi N: Spoligotyping followed by double-repetitive-element PCR as rapid alternative to IS6110 fingerprinting for epidemiological studies of tuberculosis. J Clin Microbiol. 1998, 36: 1122-1124.PubMedPubMedCentral Sola C, Horgen L, Maïsetti J, Devallois A, Goh KS, Rastogi N: Spoligotyping followed by double-repetitive-element PCR as rapid alternative to IS6110 fingerprinting for epidemiological studies of tuberculosis. J Clin Microbiol. 1998, 36: 1122-1124.PubMedPubMedCentral
10.
go back to reference Horgen L, Sola C, Devallois A, Goh KS, Rastogi N: Follow up of Mycobacterium tuberculosis transmission in the French West Indies by IS6110-DNA fingerprinting and DR-based spoligotyping. FEMS Immunol Med Microbiol. 1998, 21: 203-212. 10.1111/j.1574-695X.1998.tb01167.x.CrossRefPubMed Horgen L, Sola C, Devallois A, Goh KS, Rastogi N: Follow up of Mycobacterium tuberculosis transmission in the French West Indies by IS6110-DNA fingerprinting and DR-based spoligotyping. FEMS Immunol Med Microbiol. 1998, 21: 203-212. 10.1111/j.1574-695X.1998.tb01167.x.CrossRefPubMed
11.
go back to reference Filliol I, Ferdinand S, Negroni L, Sola C, Rastogi N: Molecular typing of Mycobacterium tuberculosis based on variable number of tandem DNA repeats used alone and in association with spoligotyping. J Clin Microbiol. 2000, 38: 2520-2524.PubMedPubMedCentral Filliol I, Ferdinand S, Negroni L, Sola C, Rastogi N: Molecular typing of Mycobacterium tuberculosis based on variable number of tandem DNA repeats used alone and in association with spoligotyping. J Clin Microbiol. 2000, 38: 2520-2524.PubMedPubMedCentral
12.
go back to reference van Soolingen D, de Haas PE, Hermans PW, van Embden JD: DNA fingerprinting of Mycobacterium tuberculosis. Methods Enzymol. 1994, 235: 196-205.CrossRefPubMed van Soolingen D, de Haas PE, Hermans PW, van Embden JD: DNA fingerprinting of Mycobacterium tuberculosis. Methods Enzymol. 1994, 235: 196-205.CrossRefPubMed
13.
go back to reference Supply P, Lesjean S, Savine E, Kremer K, van Soolingen D, Locht C: Automated high-throughput genotyping for study of global epidemiology of Mycobacterium tuberculosis based on mycobacterial interspersed repetitive units. J Clin Microbiol. 2001, 39: 3563-3571. 10.1128/JCM.39.10.3563-3571.2001.CrossRefPubMedPubMedCentral Supply P, Lesjean S, Savine E, Kremer K, van Soolingen D, Locht C: Automated high-throughput genotyping for study of global epidemiology of Mycobacterium tuberculosis based on mycobacterial interspersed repetitive units. J Clin Microbiol. 2001, 39: 3563-3571. 10.1128/JCM.39.10.3563-3571.2001.CrossRefPubMedPubMedCentral
14.
go back to reference Supply P, Mazars E, Lesjean S, Vincent V, Gicquel B, Locht C: Variable human minisatellite-like regions in the Mycobacterium tuberculosis genome. Mol Microbiol. 2000, 36: 762-771.CrossRefPubMed Supply P, Mazars E, Lesjean S, Vincent V, Gicquel B, Locht C: Variable human minisatellite-like regions in the Mycobacterium tuberculosis genome. Mol Microbiol. 2000, 36: 762-771.CrossRefPubMed
15.
go back to reference Millet J, Miyagi-Shiohira C, Yamane N, Sola C, Rastogi N: Assessment of mycobacterial interspersed repetitive unit-QUB markers to further discriminate the Beijing genotype in a population-based study of the genetic diversity of Mycobacterium tuberculosis clinical isolates from Okinawa, Ryukyu Islands, Japan. J Clin Microbiol. 2007, 45: 3606-3615. 10.1128/JCM.00348-07.CrossRefPubMedPubMedCentral Millet J, Miyagi-Shiohira C, Yamane N, Sola C, Rastogi N: Assessment of mycobacterial interspersed repetitive unit-QUB markers to further discriminate the Beijing genotype in a population-based study of the genetic diversity of Mycobacterium tuberculosis clinical isolates from Okinawa, Ryukyu Islands, Japan. J Clin Microbiol. 2007, 45: 3606-3615. 10.1128/JCM.00348-07.CrossRefPubMedPubMedCentral
16.
go back to reference Brudey K, et al: Mycobacterium tuberculosis complex genetic diversity: mining the fourth international spoligotyping database (SpolDB4) for classification, population genetics and epidemiology. BMC Microbiol. 2006, 6: 23-10.1186/1471-2180-6-23.CrossRefPubMedPubMedCentral Brudey K, et al: Mycobacterium tuberculosis complex genetic diversity: mining the fourth international spoligotyping database (SpolDB4) for classification, population genetics and epidemiology. BMC Microbiol. 2006, 6: 23-10.1186/1471-2180-6-23.CrossRefPubMedPubMedCentral
17.
go back to reference Demay C, Liens B, Burguiere T, Hill V, Couvin D, Millet J, Mokrousov I, Sola C, Zozio T, Rastogi N: SITVITWEB – a publicly available international multimarker database for studying Mycobacterium tuberculosis genetic diversity and molecular epidemiology. Infect Genet Evol. 2012, 12: 755-766. 10.1016/j.meegid.2012.02.004.CrossRefPubMed Demay C, Liens B, Burguiere T, Hill V, Couvin D, Millet J, Mokrousov I, Sola C, Zozio T, Rastogi N: SITVITWEB – a publicly available international multimarker database for studying Mycobacterium tuberculosis genetic diversity and molecular epidemiology. Infect Genet Evol. 2012, 12: 755-766. 10.1016/j.meegid.2012.02.004.CrossRefPubMed
18.
go back to reference Che D, Bitar D: Les cas de tuberculose déclarés en France en 2004. Bull Epidemiol Hebdo. 2006, 18: 121-125. Che D, Bitar D: Les cas de tuberculose déclarés en France en 2004. Bull Epidemiol Hebdo. 2006, 18: 121-125.
19.
go back to reference Khue PM, Truffot-Pernot C, Texier-Maugein J, Jarlier V, Robert J: A 10-year prospective surveillance of Mycobacterium tuberculosis drug resistance in France 1995–2004. Eur Respir J. 2007, 3: 937-944.CrossRef Khue PM, Truffot-Pernot C, Texier-Maugein J, Jarlier V, Robert J: A 10-year prospective surveillance of Mycobacterium tuberculosis drug resistance in France 1995–2004. Eur Respir J. 2007, 3: 937-944.CrossRef
20.
go back to reference Antoine D, Che D: Epidemiology of tuberculosis in France in 2005. Bull Epidemiol Hebdo. 2007, 11: 85-92. Antoine D, Che D: Epidemiology of tuberculosis in France in 2005. Bull Epidemiol Hebdo. 2007, 11: 85-92.
21.
go back to reference Brudey K, Filliol I, Ferdinand S, Guernier V, Duval P, Maubert P, Sola S, Rastogi N: Long-term population-based genotyping study of Mycobacterium tuberculosis complex isolates in the French Departments of the Americas. J Clin Microbiol. 2006, 44: 183-191. 10.1128/JCM.44.1.183-191.2006.CrossRefPubMedPubMedCentral Brudey K, Filliol I, Ferdinand S, Guernier V, Duval P, Maubert P, Sola S, Rastogi N: Long-term population-based genotyping study of Mycobacterium tuberculosis complex isolates in the French Departments of the Americas. J Clin Microbiol. 2006, 44: 183-191. 10.1128/JCM.44.1.183-191.2006.CrossRefPubMedPubMedCentral
22.
go back to reference World Health Organization (WHO): Global Tuberculosis Control – Surveillance, Planning, Financing. 2007, Geneva, Switzerland: WHO Library Cataloguing-in-Publication Data (WHO/HTM/TB/2007.376), World Health Organization World Health Organization (WHO): Global Tuberculosis Control – Surveillance, Planning, Financing. 2007, Geneva, Switzerland: WHO Library Cataloguing-in-Publication Data (WHO/HTM/TB/2007.376), World Health Organization
23.
go back to reference Cadelis G, Rossigneux E, Millet J, Rastogi N: Comparative epidemiological study of the tuberculosis - migrant and native subjects in Guadeloupe from 2006 to 2011. Rev Mal Respir. 2012, 29: 858-870. 10.1016/j.rmr.2012.05.003.CrossRefPubMed Cadelis G, Rossigneux E, Millet J, Rastogi N: Comparative epidemiological study of the tuberculosis - migrant and native subjects in Guadeloupe from 2006 to 2011. Rev Mal Respir. 2012, 29: 858-870. 10.1016/j.rmr.2012.05.003.CrossRefPubMed
26.
go back to reference Cazein F, Le Vu S, Pillonel J, Le Strat Y, Couturier S, Basselier B, Lot F, Semaille C: Dépistage de l’infection par le VIH en France, 2003–2009. Bull Epidemiol Hebd. 2010, 45–46: 451-454. Cazein F, Le Vu S, Pillonel J, Le Strat Y, Couturier S, Basselier B, Lot F, Semaille C: Dépistage de l’infection par le VIH en France, 2003–2009. Bull Epidemiol Hebd. 2010, 45–46: 451-454.
32.
go back to reference Sola C, Filliol I, Legrand E, Lesjean S, Locht C, Supply P, Rastogi N: Genotyping of the Mycobacterium tuberculosis complex using MIRUs: association with VNTR and spoligotyping for molecular epidemiology and evolutionary genetics. Infect Genet Evol. 2003, 3: 125-133. 10.1016/S1567-1348(03)00011-X.CrossRefPubMed Sola C, Filliol I, Legrand E, Lesjean S, Locht C, Supply P, Rastogi N: Genotyping of the Mycobacterium tuberculosis complex using MIRUs: association with VNTR and spoligotyping for molecular epidemiology and evolutionary genetics. Infect Genet Evol. 2003, 3: 125-133. 10.1016/S1567-1348(03)00011-X.CrossRefPubMed
33.
go back to reference Supply P, Allix C, Lesjean S, Cardoso-Oelemann M, Rüsch-Gerdes S, Willery E, Savine E, de Haas P, van Deutekom H, Roring S, Bifani P, Kurepina N, Kreiswirth B, Sola C, Rastogi N, Vatin V, Gutierrez MC, Fauville M, Niemann S, Skuce R, Kremer K, Locht C, van Soolingen D: Proposal for standardization of optimized mycobacterial interspersed repetitive unit-variable-number tandem repeat typing of Mycobacterium tuberculosis. J Clin Microbiol. 2006, 44: 4498-4510. 10.1128/JCM.01392-06.CrossRefPubMedPubMedCentral Supply P, Allix C, Lesjean S, Cardoso-Oelemann M, Rüsch-Gerdes S, Willery E, Savine E, de Haas P, van Deutekom H, Roring S, Bifani P, Kurepina N, Kreiswirth B, Sola C, Rastogi N, Vatin V, Gutierrez MC, Fauville M, Niemann S, Skuce R, Kremer K, Locht C, van Soolingen D: Proposal for standardization of optimized mycobacterial interspersed repetitive unit-variable-number tandem repeat typing of Mycobacterium tuberculosis. J Clin Microbiol. 2006, 44: 4498-4510. 10.1128/JCM.01392-06.CrossRefPubMedPubMedCentral
34.
go back to reference Allix-Béguec C, Fauville-Dufaux M, Supply P: Three-year population-based evaluation of standardized mycobacterial interspersed repetitive-unit-variable-number tandem-repeat typing of Mycobacterium tuberculosis. J Clin Microbiol. 2008, 46: 1398-1406. 10.1128/JCM.02089-07.CrossRefPubMedPubMedCentral Allix-Béguec C, Fauville-Dufaux M, Supply P: Three-year population-based evaluation of standardized mycobacterial interspersed repetitive-unit-variable-number tandem-repeat typing of Mycobacterium tuberculosis. J Clin Microbiol. 2008, 46: 1398-1406. 10.1128/JCM.02089-07.CrossRefPubMedPubMedCentral
36.
go back to reference Millet J, Baboolal S, Akpaka PE, Ramoutar D, Rastogi N: Phylogeographical and molecular characterization of an emerging Mycobacterium tuberculosis clone in Trinidad and Tobago. Infect Genet Evol. 2009, 9: 1336-1344. 10.1016/j.meegid.2009.09.006.CrossRefPubMed Millet J, Baboolal S, Akpaka PE, Ramoutar D, Rastogi N: Phylogeographical and molecular characterization of an emerging Mycobacterium tuberculosis clone in Trinidad and Tobago. Infect Genet Evol. 2009, 9: 1336-1344. 10.1016/j.meegid.2009.09.006.CrossRefPubMed
37.
go back to reference Walker TM, Ip CL, Harrell RH, Evans JT, Kapatai G, Dedicoat MJ, Eyre DW, Wilson DJ, Hawkey PM, Crook DW, Parkhill J, Harris D, Walker AS, Bowden R, Monk P, Smith EG, Peto TE: Whole-genome sequencing to delineate Mycobacterium tuberculosis outbreaks: a retrospective observational study. Lancet Infect Dis. 2013, 13 (2): 137-46. 10.1016/S1473-3099(12)70277-3. Epub 2012 Nov 15CrossRefPubMedPubMedCentral Walker TM, Ip CL, Harrell RH, Evans JT, Kapatai G, Dedicoat MJ, Eyre DW, Wilson DJ, Hawkey PM, Crook DW, Parkhill J, Harris D, Walker AS, Bowden R, Monk P, Smith EG, Peto TE: Whole-genome sequencing to delineate Mycobacterium tuberculosis outbreaks: a retrospective observational study. Lancet Infect Dis. 2013, 13 (2): 137-46. 10.1016/S1473-3099(12)70277-3. Epub 2012 Nov 15CrossRefPubMedPubMedCentral
38.
go back to reference Rastogi N: F1000Prime Recommendation of [Walker TM et al. Lancet Infect Dis. 2013, 13 (2): 137-46. 10.3410/f.717967420.793471198. In F1000Prime, 25 Feb 2013; F1000Prime.com/717967420#eval793471198CrossRef Rastogi N: F1000Prime Recommendation of [Walker TM et al. Lancet Infect Dis. 2013, 13 (2): 137-46. 10.3410/f.717967420.793471198. In F1000Prime, 25 Feb 2013; F1000Prime.com/717967420#eval793471198CrossRef
Metadata
Title
Use of genotyping based clustering to quantify recent tuberculosis transmission in Guadeloupe during a seven years period: analysis of risk factors and access to health care
Authors
Séverine Ferdinand
Julie Millet
Annick Accipe
Sylvie Cassadou
Pascal Chaud
Maryse Levy
Max Théodore
Nalin Rastogi
Publication date
01-12-2013
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2013
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/1471-2334-13-364

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