Mycobacterium tuberculosis Isolates from Single Outpatient Clinic in Panama City Exhibit Wide Genetic Diversity

Dilcia Sambrano Tuberculosis Biomarker Research Unit, Centro de Biología Celular y Molecular de las Enfermedades (CBCME) del Instituto de Investigaciones Científicas y Servicios de Alta Tecnología (INDICASAT AIP), Ciudad del Saber, Panamá; Department of Biotechnology, Acharya Nagarjuna University, Guntur, India; Laboratorio Clínico, Complejo Hospitalario Metropolitano Dr. Arnulfo Arias Madrid, Caja de Seguro Social (CHMDrAAM-CSS), Panamá, Panamá; Departamento de Ciencias de Laboratorio Clínico, Facultad de Medicina, Universidad de Panamá, Panamá, Panamá

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Ricardo Correa Tuberculosis Biomarker Research Unit, Centro de Biología Celular y Molecular de las Enfermedades (CBCME) del Instituto de Investigaciones Científicas y Servicios de Alta Tecnología (INDICASAT AIP), Ciudad del Saber, Panamá; Department of Biotechnology, Acharya Nagarjuna University, Guntur, India; Laboratorio Clínico, Complejo Hospitalario Metropolitano Dr. Arnulfo Arias Madrid, Caja de Seguro Social (CHMDrAAM-CSS), Panamá, Panamá; Departamento de Ciencias de Laboratorio Clínico, Facultad de Medicina, Universidad de Panamá, Panamá, Panamá

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Pedro Almengor Tuberculosis Biomarker Research Unit, Centro de Biología Celular y Molecular de las Enfermedades (CBCME) del Instituto de Investigaciones Científicas y Servicios de Alta Tecnología (INDICASAT AIP), Ciudad del Saber, Panamá; Department of Biotechnology, Acharya Nagarjuna University, Guntur, India; Laboratorio Clínico, Complejo Hospitalario Metropolitano Dr. Arnulfo Arias Madrid, Caja de Seguro Social (CHMDrAAM-CSS), Panamá, Panamá; Departamento de Ciencias de Laboratorio Clínico, Facultad de Medicina, Universidad de Panamá, Panamá, Panamá

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Amada Domínguez Tuberculosis Biomarker Research Unit, Centro de Biología Celular y Molecular de las Enfermedades (CBCME) del Instituto de Investigaciones Científicas y Servicios de Alta Tecnología (INDICASAT AIP), Ciudad del Saber, Panamá; Department of Biotechnology, Acharya Nagarjuna University, Guntur, India; Laboratorio Clínico, Complejo Hospitalario Metropolitano Dr. Arnulfo Arias Madrid, Caja de Seguro Social (CHMDrAAM-CSS), Panamá, Panamá; Departamento de Ciencias de Laboratorio Clínico, Facultad de Medicina, Universidad de Panamá, Panamá, Panamá

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Silvio Vega Tuberculosis Biomarker Research Unit, Centro de Biología Celular y Molecular de las Enfermedades (CBCME) del Instituto de Investigaciones Científicas y Servicios de Alta Tecnología (INDICASAT AIP), Ciudad del Saber, Panamá; Department of Biotechnology, Acharya Nagarjuna University, Guntur, India; Laboratorio Clínico, Complejo Hospitalario Metropolitano Dr. Arnulfo Arias Madrid, Caja de Seguro Social (CHMDrAAM-CSS), Panamá, Panamá; Departamento de Ciencias de Laboratorio Clínico, Facultad de Medicina, Universidad de Panamá, Panamá, Panamá

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Amador Goodridge Tuberculosis Biomarker Research Unit, Centro de Biología Celular y Molecular de las Enfermedades (CBCME) del Instituto de Investigaciones Científicas y Servicios de Alta Tecnología (INDICASAT AIP), Ciudad del Saber, Panamá; Department of Biotechnology, Acharya Nagarjuna University, Guntur, India; Laboratorio Clínico, Complejo Hospitalario Metropolitano Dr. Arnulfo Arias Madrid, Caja de Seguro Social (CHMDrAAM-CSS), Panamá, Panamá; Departamento de Ciencias de Laboratorio Clínico, Facultad de Medicina, Universidad de Panamá, Panamá, Panamá

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Understanding Mycobacterium tuberculosis biodiversity and transmission is significant for tuberculosis control. This short report aimed to determine the genetic diversity of M. tuberculosis isolates from an outpatient clinic in Panama City. A total of 62 M. tuberculosis isolates were genotyped by 12 loci mycobacterial interspersed repetitive units-variable number of tandem repeats (MIRU-VNTR) and Spoligotyping. Forty-five (72.6%) of the isolates showed unique MIRU-VNTR genotypes, and 13 (21%) of the isolates were grouped into four clusters. Four isolates showed polyclonal MIRU-VNTR genotypes. The MIRU-VNTR Hunter-Gaston discriminatory index reached 0.988. The Spoligotyping analysis revealed 16 M. tuberculosis families, including Latin American-Mediterranean, Harlem, and Beijing. These findings suggest a wide genetic diversity of M. tuberculosis isolates at one outpatient clinic. A detailed molecular epidemiology survey is now warranted, especially following second massive immigration for local Panama Canal expansion activities.

Author Notes

* Address correspondence to Amador Goodridge, Tuberculosis Biomarker Research Unit, Centro de Biología Molecular y Celular de Enfermedades (CBCME) Instituto de Investigaciones Científicas y Servicios de Alta Tecnología (INDICASAT-AIP), P.O. Box 0843-01103, Ciudad del Saber, Republic of Panamá. E-mail: agoodridge@indicasat.org.pa

Financial support: This study was partially funded by the Network for Research and Training in Tropical Diseases in Central America (NeTropica) Grant nos. 09-R-2003 and 05-N-2005.

Authors' addresses: Dilcia Sambrano, Centro de Biología Celular y Molecular (CBCME) del Instituto de Investigaciones Científicas y Servicios de Alta Tecnología INDICASAT-AIP, Ciudad del Saber, Panamá, Panamá, E-mail: dsambrano@indicasat.org.pa. Ricardo Correa, Centro de Biología Celular y Molecular (CBCME) del Instituto de Investigaciones Científicas y Servicios de Alta Tecnología INDICASAT-AIP, Ciudad del Saber, Panamá, Panamá Department of Biotechnology, Acharya Nagarjuna University, Guntur, India, E-mail: rcorrea@indicasat.org.pa. Pedro Almengor, Laboratorio de Microbiología del Complejo Hospitalario Dr. Arnulfo Arias Madrid de la Caja de Seguro Social CHMDrAAM-CSS, Panamá, Panamá. Amada Domínguez, Departamento de Ciencias de Laboratorio Clínico, Facultad de Medicina, Universidad de Panamá, Panamá, Panamá, E-mail: laboratorioup@yahoo.com. Silvio Vega, Laboratorio de Microbiología del Complejo Hospitalario Dr. Arnulfo Arias Madrid de la Caja de Seguro Social CHMDrAAM-CSS, Panamá, Panamá, E-mail: silviove@yahoo.com. Amador Goodridge, Centro de Biología Celular y Molecular (CBCME) del Instituto de Investigaciones Científicas y Servicios de Alta Tecnología INDICASAT-AIP, Ciudad del Saber, Panamá, Panamá, E-mail: agoodridge@indicasat.org.pa.

  • 1.

    WHO, 2012. The Global Tuberculosis Report 2012. Geneva: World Health Organization.

  • 2.

    Tarajia M, Goodridge A, 2014. Tuberculosis remains a challenge despite economic growth in Panama [Notes from the field]. Int J Tuberc Lung Dis 18: 286288.

  • 3.

    MINSA, 2013. Evolución de la incidencia notificada de TBC y mortalidad general 1999–2011. Epidemiologia, ed. Panama: Ministerio de Salud.

  • 4.

    Kean BH, 1946. The causes of death on the Isthmus of Panama; based on 14,304 autopsies performed at the Board of Health Laboratory, Gorgas Hospital, Ancon, Canal Zone, during the forty year period 1904–1944. Am J Trop Med Hyg 26: 733748.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5.

    Rosas S, Bravo J, Gonzalez F, de Moreno N, Sanchez J, Gavilan RG, Goodridge A, 2013. High clustering rates of multidrug-resistant Mycobacterium tuberculosis genotypes in Panama. BMC Infect Dis 13: 442.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6.

    Lanzas F, Karakousis PC, Sacchettini JC, Ioerger TR, 2013. Multidrug-resistant tuberculosis in panama is driven by clonal expansion of a multidrug-resistant Mycobacterium tuberculosis strain related to the KZN extensively drug-resistant M. tuberculosis strain from South Africa. J Clin Microbiol 51: 32773285.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7.

    Hricko A, 2012. Progress and pollution: port cities prepare for the Panama Canal expansion. Environ Health Perspect 120: A470A473.

  • 8.

    Kato-Maeda M, Metcalfe JZ, Flores L, 2011. Genotyping of Mycobacterium tuberculosis: application in epidemiologic studies. Future Microbiol 6: 203216.

  • 9.

    Ferdinand S, Millet J, Accipe A, Cassadou S, Chaud P, Levy M, Theodore M, Rastogi N, 2013. 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. BMC Infect Dis 13: 364.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10.

    van Soolingen D, Hermans PW, de Haas PE, Soll DR, van Embden JD, 1991. Occurrence and stability of insertion sequences in Mycobacterium tuberculosis complex strains: evaluation of an insertion sequence-dependent DNA polymorphism as a tool in the epidemiology of tuberculosis. J Clin Microbiol 29: 25782586.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11.

    Banu S, Uddin MK, Islam MR, Zaman K, Ahmed T, Talukder AH, Rahman MT, Rahim Z, Akter N, Khatun R, Brosch R, Endtz HP, 2012. Molecular epidemiology of tuberculosis in rural Matlab, Bangladesh. Int J Tuberc Lung Dis 16: 319326.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12.

    Blackwood KS, Wolfe JN, Kabani AM, 2004. Application of mycobacterial interspersed repetitive unit typing to Manitoba tuberculosis cases: can restriction fragment length polymorphism be forgotten? J Clin Microbiol 42: 50015006.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13.

    Cowan LS, Mosher L, Diem L, Massey JP, Crawford JT, 2002. Variable-number tandem repeat typing of Mycobacterium tuberculosis isolates with low copy numbers of IS6110 by using mycobacterial interspersed repetitive units. J Clin Microbiol 40: 15921602.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    Savine E, Warren RM, van der Spuy GD, Beyers N, van Helden PD, Locht C, Supply P, 2002. Stability of variable-number tandem repeats of mycobacterial interspersed repetitive units from 12 loci in serial isolates of Mycobacterium tuberculosis. J Clin Microbiol 40: 45614566.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15.

    Supply P, Mazars E, Lesjean S, Vincent V, Gicquel B, Locht C, 2000. Variable human minisatellite-like regions in the Mycobacterium tuberculosis genome. Mol Microbiol 36: 762771.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16.

    Hunter PR, Gaston MA, 1988. Numerical index of the discriminatory ability of typing systems: an application of Simpson's index of diversity. J Clin Microbiol 26: 24652466.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17.

    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, 1997. Simultaneous detection and strain differentiation of Mycobacterium tuberculosis for diagnosis and epidemiology. J Clin Microbiol 35: 907914.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18.

    Brudey K, Driscoll JR, Rigouts L, Prodinger WM, Gori A, Al-Hajoj SA, Allix C, Aristimuno L, Arora J, Baumanis V, Binder L, Cafrune P, Cataldi A, Cheong S, Diel R, Ellermeier C, Evans JT, Fauville-Dufaux M, Ferdinand S, Garcia de Viedma D, Garzelli C, Gazzola L, Gomes HM, Guttierez MC, Hawkey PM, van Helden PD, Kadival GV, Kreiswirth BN, Kremer K, Kubin M, Kulkarni SP, Liens B, Lillebaek T, Ho ML, Martin C, Mokrousov I, Narvskaia O, Ngeow YF, Naumann L, Niemann S, Parwati I, Rahim Z, Rasolofo-Razanamparany V, Rasolonavalona T, Rossetti ML, Rusch-Gerdes S, Sajduda A, Samper S, Shemyakin IG, Singh UB, Somoskovi A, Skuce RA, van Soolingen D, Streicher EM, Suffys PN, Tortoli E, Tracevska T, Vincent V, Victor TC, Warren RM, Yap SF, Zaman K, Portaels F, Rastogi N, Sola C, 2006. Mycobacterium tuberculosis complex genetic diversity: mining the fourth international spoligotyping database (SpolDB4) for classification, population genetics and epidemiology. BMC Microbiol 6: 23.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19.

    Kernodle DS, 2012. Warning: differences in the copy number of duplication unit 2 (DU2) within BCG Danish 1331 may influence findings involving genetically modified BCG Danish strains. Vaccine 30: 60136014, author reply 6015.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20.

    Sun YJ, Bellamy R, Lee AS, Ng ST, Ravindran S, Wong SY, Locht C, Supply P, Paton NI, 2004. Use of mycobacterial interspersed repetitive unit-variable-number tandem repeat typing to examine genetic diversity of Mycobacterium tuberculosis in Singapore. J Clin Microbiol 42: 19861993.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21.

    Lee AS, Tang LL, Lim IH, Bellamy R, Wong SY, 2002. Discrimination of single-copy IS6110 DNA fingerprints of Mycobacterium tuberculosis isolates by high-resolution minisatellite-based typing. J Clin Microbiol 40: 657659.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22.

    Mazars E, Lesjean S, Banuls AL, Gilbert M, Vincent V, Gicquel B, Tibayrenc M, Locht C, Supply P, 2001. High-resolution minisatellite-based typing as a portable approach to global analysis of Mycobacterium tuberculosis molecular epidemiology. Proc Natl Acad Sci USA 98: 19011906.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23.

    Supply P, Allix C, Lesjean S, Cardoso-Oelemann M, Rusch-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, 2006. Proposal for standardization of optimized mycobacterial interspersed repetitive unit-variable-number tandem repeat typing of Mycobacterium tuberculosis. J Clin Microbiol 44: 44984510.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24.

    Cerezo I, Jimenez Y, Hernandez J, Zozio T, Murcia MI, Rastogi N, 2012. A first insight on the population structure of Mycobacterium tuberculosis complex as studied by spoligotyping and MIRU-VNTRs in Bogota, Colombia. Infect Genet Evol 12: 657663.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25.

    Mendes NH, Melo FA, Santos AC, Pandolfi JR, Almeida EA, Cardoso RF, Berghs H, David S, Johansen FK, Espanha LG, Leite SR, Leite CQ, 2011. Characterization of the genetic diversity of Mycobacterium tuberculosis in Sao Paulo city, Brazil. BMC Res Notes 4: 269.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26.

    de Beer JL, Akkerman OW, Schurch AC, Mulder A, van der Werf TS, van der Zanden A, van Ingen J, van Soolingen D, 2014. Optimization of standard in-house 24-locus variable number of tandem repeat typing for Mycobacterium tuberculosis and its direct application to clinical material. J Clin Microbiol Epub ahead of print 5 February 2014. doi:10.1128/JCM.03436-13.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27.

    Driscoll JR, 2009. Spoligotyping for molecular epidemiology of the Mycobacterium tuberculosis complex. Methods Mol Biol 551: 117128.

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