World Health Organization , 2022. Global Tuberculosis Report. Geneva, Switzerland: World Health Organization.
Tarajia M , Goodridge A , 2014. Tuberculosis remains a challenge despite economic growth in Panama. Int J Tuberc Lung Dis 18: 286–288.
Asemahagn MA , Alene GD , Yimer SA , 2020. Geographic accessibility, readiness, and barriers of health facilities to offer tuberculosis services in East Gojjam Zone, Ethiopia: a convergent parallel design. Res Rep Trop Med 11: 3–16.
Smith JP , Cohen T , Smith JP , Dowdy D , Shrestha S , Smith JP , Ghandi NR , Hill AN , 2022. Characterizing tuberculosis transmission dynamics in high-burden urban and rural settings. Sci Rep 12: 6780.
Mutembo S , Mutanga JN , Musokotwane K , Kanene C , Dobbin K , Yao X , Li C , Marconi VC , Whalen CC , 2019. Urban-rural disparities in treatment outcomes among recurrent TB cases in Southern Province, Zambia. BMC Infect Dis 19: 1087.
Xu B , Hu Y , Wang WB , Jiang WL , 2010. Molecular-epidemiological study on the transmission of drug resistant tuberculosis and its influencing factors in rural areas of eastern China. Zhonghua Liu Xing Bing Xue Za Zhi 31: 525–529.
Wang W , Hu Y , Mathema B , Jiang W , Kreiswirth B , Xu B , 2012. Recent transmission of W-Beijing family Mycobacterium tuberculosis in rural eastern China. Int J Tuberc Lung Dis 16: 306–311.
Chamie G , Wandera B , Marquez C , Kato-Maeda M , Kamya MR , Havlir DV , Charlebois ED , 2015. Identifying locations of recent TB transmission in rural Uganda: a multidisciplinary approach. Trop Med Int Health 20: 537–545.
Lopez A , Acosta F , Sambrano D , Tarajia M , Navajas S , Arias F , Escobar B , Ortis P , Adames F , Goodridge A , 2021. Direct molecular characterization of acid-fast bacilli smear of nontuberculosis Mycobacterium species causing pulmonary tuberculosis in Guna Yala Region, Panama. Am J Trop Med Hyg 105: 633–637.
MINSA , 2017. Ministerio de Salud: Indicadores Básicos de País Panamá. Panamá: MINSA.
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.
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: 3277–3285.
Sambrano D , Correa R , Almengor P , Domínguez A , Vega S , Goodridge A , 2014. Short report: Mycobacterium tuberculosis isolates from single outpatient clinic in Panama City exhibit wide genetic diversity. Am J Trop Med Hyg 91: 310–213.
Domínguez J et al., 2019. Simplified model to survey tuberculosis transmission in countries without systematic molecular epidemiology programs. Emerg Infect Dis 25: 507–514.
Acosta F et al., 2021. Probable long-term prevalence for a predominant Mycobacterium tuberculosis clone of a Beijing genotype in Colon, Panama. Transbound Emerg Dis 68: 2229–2238.
Gauthier M et al., 2015. High-throughput mycobacterial interspersed repetitive-unit-variable-number tandem-repeat genotyping for Mycobacterium tuberculosis epidemiological studies. J Clin Microbiol 53: 498–503.
Hadifar S , Kamakoli MK , Fateh A , Siadat SD , Vaziri F , 2019. Enhancing the differentiation of specific genotypes in Mycobacterium tuberculosis population. Sci Rep 9: 17946.
de Beer JL , Ködmön C , van Ingen J , Supply P , van Soolingen D , 2014. Second worldwide proficiency study on variable number of tandem repeats typing of Mycobacterium tuberculosis complex. Int J Tuberc Lung Dis 18: 594–600.
Van Soolingen D , Hermans PWM , De Haas PEW , Soll DR , Van Embden JDA , 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: 2578–2586.
Supply P et al., 2006. Proposal for standardization of optimized mycobacterial interspersed repetitive unit-variable-number tandem repeat typing of Mycobacterium tuberculosis. J Clin Microbiol 44: 4498–4510.
Walker TM et al., 2013. Whole-genome sequencing to delineate Mycobacterium tuberculosis outbreaks: a retrospective observational study. Lancet Infect Dis 13: 137–146.
Cerezo-Cortés MI , Rodríguez-Castillo JG , Hernández-Pando R , Murcia MI , 2019. Circulation of Beijing genotype in Latin America and the Caribbean. Pathog Glob Health 113: 336–351.
Pérez-Lago L et al., 2019. A Mycobacterium tuberculosis Beijing strain persists at high rates and extends its geographic boundaries 20 years after importation. Sci Rep 9: 4687.
Eldholm V , Monteserin J , Rieux A , Lopez B , Sobkowiak B , Ritacco V , Balloux F , 2015. Four decades of transmission of a multidrug-resistant Mycobacterium tuberculosis outbreak strain. Nat Commun 6: 7119.
Samper S , Iglesias MJ , Rabanaque MJ , Lezcano MA , Vitoria LA , Rubio MC , Gómez-Lus R , Gómez LI , Otal I , Martín C , 1998. The molecular epidemiology of tuberculosis in Zaragoza, Spain: a retrospective epidemiological study in 1993. Int J Tuberc Lung Dis 2: 281–287.
López-Calleja AI et al., 2007. Genotyping of Mycobacterium tuberculosis over two periods: a changing scenario for tuberculosis transmission. Int J Tuberc Lung Dis 11: 1080–1086.
Gagneux S , 2018. Ecology and evolution of Mycobacterium tuberculosis. Nat Rev Microbiol16: 202–213.
Briquet A et al., 2019. Clinical features of Mycobacterium canettii infection: a retrospective study of 20 cases among French soldiers and relatives. Clin Infect Dis 69: 2003–2010.
Miltgen J , Morillon M , Koeck JL , Varnerot A , Briant JF , Nguyen G , Verrot D , Bonnet D , Vincent V , 2002. Two cases of pulmonary tuberculosis caused by Mycobacterium tuberculosis subsp. canetti. Emerg Infect Dis 8: 1350–1352.
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Tuberculosis remains a challenge in both rural and urban areas. Although a majority of countries display a higher burden in urban areas compared with rural areas, Panama continues to report the highest mortality rate in Central America. Urban areas, such as Panama City, report a high tuberculosis burden, whereas Panama’s western region, including the provinces of Chiriquí, Bocas del Toro (both semiurban) and Ngäbe-Bugle (rural), show a lower burden. We aimed to identify highly transmitted Mycobacterium tuberculosis strains within rural and semiurban settings of Panama’s western region during a 3-year period (2017, 2019, 2021). We randomly selected 87 M. tuberculosis isolates from a biobank from Panama’s western region and analyzed them using allele-specific oligonucleotide polymerase chain reaction and 24-mycobacterial interspersed repetitive unit-variable number tandem repeat (MIRU-VNTR). Our results show only 11.7% (10/85) of M. tuberculosis strains identified as prevalent A-Beijing, B-Haarlem, or C-LAM Strains. We found a low prevalence of A, B, and C M. tuberculosis strains in both rural and semirural settings compared with isolates collected from the Eastern Colon Province. MIRU-VNTR genotyping revealed a high degree of diversity with no clusters with single loci variation of ≥ 2 loci. These results support the notion that tuberculosis prevalence in the rural and semiurban western region of Panama are not due to previously described highly transmitted strains but is influenced instead by other health determinants, including poor health system access and a lack of systematic transmission chain monitoring. For remote rural and semiurban settings, we recommend allocating resources to reinforce efforts to prevent tuberculosis spread.
These authors contributed equally to this work.
Financial support: This research was funded by
Disclosure: The study was approved by Bioethics Committee of the Universidad Santander of Panama with the following Protocols: CBI-USantander-M-041-2022 and CBI-USantander-M-081-2022 (2022).
Authors’ addresses: Fermin Acosta, Daniela Candanedo, Dilcia Sambrano, Mitchelle Morán, and Amador Goodridge, Tuberculosis Biomarker Research Unit at Centro de Biologia Celular y Molecular de Enfermedades (CBCME) Instituto de Investigaciones Científicas y Servicios de Alta Tecnología (INDICASAT-AIP), City of Knowledge, Panama City, Panama, E-mails: fermin2819@gmail.com, danielacandanedo@gmail.com, ludy25305@gmail.com, mitchellemoran@gmail.com, and agoodridge@indicasat.org.pa. Ricardo Saldaña, Saily Bejarano, Yeraldine De Arriba, Angel Reigosa, Elizabeth De Dixon, and María Atencio, Hospital Materno Infantil José Domingo de Obaldía, David City, Provincia de Chiriquí, Panama, E-mails: ricardo.saldana@obaldia.sld.pa, sailyara@hotmail.com, yeraldinedearriba@gmail.com, Angelreigosa@hotmail.com, eliprdixon@gmail.com, anethg89@gmail.com. Sara Miranda, Tuberculosis Biomarker Research Unit at Centro de Biologia Celular y Molecular de Enfermedades (CBCME) Instituto de Investigaciones Científicas y Servicios de Alta Tecnología (INDICASAT-AIP), City of Knowledge, Panama City, Panama, and Universidad Autónoma de Chiriqui (UNACHI), David City, Provincia de Chiriquí, Panama, E-mail: saramirandaro@gmail.com. Ramón Castillo, Programa Regional de Tuberculosis de la Provincia de Chiriquí, Ministerio de Salud, David City, Provincia de Chiriquí, Panama, E-mail: dr.moncho@hotmail.com.
World Health Organization , 2022. Global Tuberculosis Report. Geneva, Switzerland: World Health Organization.
Tarajia M , Goodridge A , 2014. Tuberculosis remains a challenge despite economic growth in Panama. Int J Tuberc Lung Dis 18: 286–288.
Asemahagn MA , Alene GD , Yimer SA , 2020. Geographic accessibility, readiness, and barriers of health facilities to offer tuberculosis services in East Gojjam Zone, Ethiopia: a convergent parallel design. Res Rep Trop Med 11: 3–16.
Smith JP , Cohen T , Smith JP , Dowdy D , Shrestha S , Smith JP , Ghandi NR , Hill AN , 2022. Characterizing tuberculosis transmission dynamics in high-burden urban and rural settings. Sci Rep 12: 6780.
Mutembo S , Mutanga JN , Musokotwane K , Kanene C , Dobbin K , Yao X , Li C , Marconi VC , Whalen CC , 2019. Urban-rural disparities in treatment outcomes among recurrent TB cases in Southern Province, Zambia. BMC Infect Dis 19: 1087.
Xu B , Hu Y , Wang WB , Jiang WL , 2010. Molecular-epidemiological study on the transmission of drug resistant tuberculosis and its influencing factors in rural areas of eastern China. Zhonghua Liu Xing Bing Xue Za Zhi 31: 525–529.
Wang W , Hu Y , Mathema B , Jiang W , Kreiswirth B , Xu B , 2012. Recent transmission of W-Beijing family Mycobacterium tuberculosis in rural eastern China. Int J Tuberc Lung Dis 16: 306–311.
Chamie G , Wandera B , Marquez C , Kato-Maeda M , Kamya MR , Havlir DV , Charlebois ED , 2015. Identifying locations of recent TB transmission in rural Uganda: a multidisciplinary approach. Trop Med Int Health 20: 537–545.
Lopez A , Acosta F , Sambrano D , Tarajia M , Navajas S , Arias F , Escobar B , Ortis P , Adames F , Goodridge A , 2021. Direct molecular characterization of acid-fast bacilli smear of nontuberculosis Mycobacterium species causing pulmonary tuberculosis in Guna Yala Region, Panama. Am J Trop Med Hyg 105: 633–637.
MINSA , 2017. Ministerio de Salud: Indicadores Básicos de País Panamá. Panamá: MINSA.
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.
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: 3277–3285.
Sambrano D , Correa R , Almengor P , Domínguez A , Vega S , Goodridge A , 2014. Short report: Mycobacterium tuberculosis isolates from single outpatient clinic in Panama City exhibit wide genetic diversity. Am J Trop Med Hyg 91: 310–213.
Domínguez J et al., 2019. Simplified model to survey tuberculosis transmission in countries without systematic molecular epidemiology programs. Emerg Infect Dis 25: 507–514.
Acosta F et al., 2021. Probable long-term prevalence for a predominant Mycobacterium tuberculosis clone of a Beijing genotype in Colon, Panama. Transbound Emerg Dis 68: 2229–2238.
Gauthier M et al., 2015. High-throughput mycobacterial interspersed repetitive-unit-variable-number tandem-repeat genotyping for Mycobacterium tuberculosis epidemiological studies. J Clin Microbiol 53: 498–503.
Hadifar S , Kamakoli MK , Fateh A , Siadat SD , Vaziri F , 2019. Enhancing the differentiation of specific genotypes in Mycobacterium tuberculosis population. Sci Rep 9: 17946.
de Beer JL , Ködmön C , van Ingen J , Supply P , van Soolingen D , 2014. Second worldwide proficiency study on variable number of tandem repeats typing of Mycobacterium tuberculosis complex. Int J Tuberc Lung Dis 18: 594–600.
Van Soolingen D , Hermans PWM , De Haas PEW , Soll DR , Van Embden JDA , 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: 2578–2586.
Supply P et al., 2006. Proposal for standardization of optimized mycobacterial interspersed repetitive unit-variable-number tandem repeat typing of Mycobacterium tuberculosis. J Clin Microbiol 44: 4498–4510.
Walker TM et al., 2013. Whole-genome sequencing to delineate Mycobacterium tuberculosis outbreaks: a retrospective observational study. Lancet Infect Dis 13: 137–146.
Cerezo-Cortés MI , Rodríguez-Castillo JG , Hernández-Pando R , Murcia MI , 2019. Circulation of Beijing genotype in Latin America and the Caribbean. Pathog Glob Health 113: 336–351.
Pérez-Lago L et al., 2019. A Mycobacterium tuberculosis Beijing strain persists at high rates and extends its geographic boundaries 20 years after importation. Sci Rep 9: 4687.
Eldholm V , Monteserin J , Rieux A , Lopez B , Sobkowiak B , Ritacco V , Balloux F , 2015. Four decades of transmission of a multidrug-resistant Mycobacterium tuberculosis outbreak strain. Nat Commun 6: 7119.
Samper S , Iglesias MJ , Rabanaque MJ , Lezcano MA , Vitoria LA , Rubio MC , Gómez-Lus R , Gómez LI , Otal I , Martín C , 1998. The molecular epidemiology of tuberculosis in Zaragoza, Spain: a retrospective epidemiological study in 1993. Int J Tuberc Lung Dis 2: 281–287.
López-Calleja AI et al., 2007. Genotyping of Mycobacterium tuberculosis over two periods: a changing scenario for tuberculosis transmission. Int J Tuberc Lung Dis 11: 1080–1086.
Gagneux S , 2018. Ecology and evolution of Mycobacterium tuberculosis. Nat Rev Microbiol16: 202–213.
Briquet A et al., 2019. Clinical features of Mycobacterium canettii infection: a retrospective study of 20 cases among French soldiers and relatives. Clin Infect Dis 69: 2003–2010.
Miltgen J , Morillon M , Koeck JL , Varnerot A , Briant JF , Nguyen G , Verrot D , Bonnet D , Vincent V , 2002. Two cases of pulmonary tuberculosis caused by Mycobacterium tuberculosis subsp. canetti. Emerg Infect Dis 8: 1350–1352.
Past two years | Past Year | Past 30 Days | |
---|---|---|---|
Abstract Views | 1462 | 1462 | 102 |
Full Text Views | 98 | 98 | 4 |
PDF Downloads | 38 | 38 | 3 |