Elimination of Onchocerciasis from Mexico

Mario A Rodríguez-Pérez, Nadia A Fernández-Santos, María E Orozco-Algarra, José A Rodríguez-Atanacio, Alfredo Domínguez-Vázquez, Kristel B Rodríguez-Morales, Olga Real-Najarro, Francisco G Prado-Velasco, Eddie W Cupp, Frank O Richards Jr, Hassan K Hassan, Jesús F González-Roldán, Pablo A Kuri-Morales, Thomas R Unnasch, Mario A Rodríguez-Pérez, Nadia A Fernández-Santos, María E Orozco-Algarra, José A Rodríguez-Atanacio, Alfredo Domínguez-Vázquez, Kristel B Rodríguez-Morales, Olga Real-Najarro, Francisco G Prado-Velasco, Eddie W Cupp, Frank O Richards Jr, Hassan K Hassan, Jesús F González-Roldán, Pablo A Kuri-Morales, Thomas R Unnasch

Abstract

Background: Mexico is one of the six countries formerly endemic for onchocerciasis in Latin America. Transmission has been interrupted in the three endemic foci of that country and mass drug distribution has ceased. Three years after mass drug distribution ended, post-treatment surveillance (PTS) surveys were undertaken which employed entomological indicators to check for transmission recrudescence.

Methodology/principal findings: In-depth entomologic assessments were performed in 18 communities in the three endemic foci of Mexico. None of the 108,212 Simulium ochraceum s.l. collected from the three foci were found to contain parasite DNA when tested by polymerase chain reaction-enzyme-linked immunosorbent assay (PCR-ELISA), resulting in a maximum upper bound of the 95% confidence interval (95%-ULCI) of the infective rate in the vectors of 0.035/2,000 flies examined. This is an order of magnitude below the threshold of a 95%-ULCI of less than one infective fly per 2,000 flies tested, the current entomological criterion for interruption of transmission developed by the international community. The point estimate of seasonal transmission potential (STP) was zero, and the upper bound of the 95% confidence interval for the STP ranged from 1.2 to 1.7 L3/person/season in the different foci. This value is below all previous estimates for the minimum transmission potential required to maintain the parasite population.

Conclusions/significance: The results from the in-depth entomological post treatment surveillance surveys strongly suggest that transmission has not resumed in the three foci of Mexico during the three years since the last distribution of ivermectin occurred; it was concluded that transmission remains undetectable without intervention, and Onchocerca volvulus has been eliminated from Mexico.

Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1. Location, number of cases, and…
Fig 1. Location, number of cases, and population at risk when ivermectin distribution began at the study sites: Panel A: Map of the Southern Mexico states showing the three endemic foci for onchocerciasis. Panels B-D: the eighteen sentinel and extra-sentinel communities in Oaxaca (Panel B; prevalence data from 1995), Northern Chiapas (Panel C; prevalence data from 1999), and Southern Chiapas (Panel D; prevalence data from 1995).
Fig 2. The onchocerciasis communities under post-treatment…
Fig 2. The onchocerciasis communities under post-treatment surveillance (PTS) phase in Mexico: Panel A: Map of the Southern Mexico states showing the two endemic States for onchocerciasis. A total of 98 communities were under PTS phase in the Oaxaca focus (Panel B). In addition, 13 and 559 communities were also under PTS phase in the Northern (Panel C) and Southern Chiapas foci, respectively (Panel D).
Fig 3. Mass drug administration (MDA) with…
Fig 3. Mass drug administration (MDA) with ivermectin in two endemic foci: Coverage rate, expressed in percent, of the eligible population.
The eligible population excluded pregnant and lactating women and children under 5 years of age. These groups represented 9.5% of the total population during the last year of MDA in the Southern Chiapas focus in 2011. Panel A: Semi-annual treatment regimen was employed in Northern Chiapas from 2000 through 2007 when MDA ceased. Panels B-C. Semi-annual regimen was employed in Southern Chiapas from 1995 through 2011 (Panel B; Figure taken from Rodriguez-Perez et al., 2013 [18]); in addition, quarterly treatment was employed in 50 communities from 2003 through 2008 and in 163 communities from 2009 through 2011 when MDA ceased (Panel C). The semi-annual treatment regimen was employed in Oaxaca from 1996 through 2008 when MDA ceased (see Fig 2 in Rodriguez-Perez et al., 2010 [20]). The line at 85% indicates the coverage needed to be maintained in order to interrupt transmission.
Fig 4. Number of new clinical cases…
Fig 4. Number of new clinical cases in two endemic foci: The number of new clinical cases, (individuals diagnosed for the first time as positive by Mazzotti reaction, nodules, or skin biopsies) in the Oaxaca focus (Panel A) in the Southern Chiapas focus (Panel B; Figure taken from Rodriguez-Perez et al., 2013 [18]).
The number of new clinical cases in the Northern Chiapas focus can be found in Fig 2 of Rodriguez-Perez et al., 2010 [19].

References

    1. Prost A (1986) The burden of blindness in adult males in the savanna villages of West Africa exposed to onchocerciasis. Trans R Soc Trop Med Hyg. 80: 525–7.
    1. Zimmerman PA, Katholi CR, Wooten MC, Lang-Unnasch N, Unnasch TR (1994) Recent evolutionary history of American Onchocerca volvulus, based on analysis of a tandemly repeated DNA sequence family. Mol Biol Evol. 11: 384–92.
    1. Expert Committee of the World Health Organization (1995) Onchocerciasis and its control. Geneva: World Health Organization, Report No.: 852.
    1. Murdoch ME, Asuzu MC, Hagan M, Makunde WH, Ngoumou P, Ogbuagu KF, et al. (2002) Onchocerciasis: the clinical and epidemiological burden of skin disease in Africa. Ann Trop Med Parasitol. 96: 283–96.
    1. Mathers CD, Ezzati M, Lopez AD. (2007) Measuring the burden of neglected tropical diseases: the global burden of disease framework. PLoS Negl Trop Dis. 1: e114
    1. Sauerbrey M. (2008) The Onchocerciasis Elimination Program for the Americas (OEPA). Ann Trop Med Parasitol. 102 Suppl 1: 25–9. 10.1179/136485908X337454
    1. Rodriguez-Perez MA, Lizarazo-Ortega C, Hassan HK, Dominguez-Vasquez A, Mendez-Galvan J, Lugo-Moreno P, et al. (2008) Evidence for suppression of Onchocerca volvulus transmission in the Oaxaca focus in Mexico. Am J Trop Med Hyg. 78: 147–52.
    1. Rodriguez-Perez MA, Lutzow-Steiner MA, Segura-Cabrera A, Lizarazo-Ortega C, Dominguez-Vazquez A, Sauerbrey M, et al. (2008) Rapid suppression of Onchocerca volvulus transmission in two communities of the Southern Chiapas focus, Mexico, achieved by quarterly treatments with Mectizan. Am J Trop Med Hyg. 79: 239–44.
    1. Katabarwa M, Walsh F, Habomugisha P, Lakwo T, Agunyo S, Oguttu D, et al. (2012) Transmission of onchocerciasis in Wadelai focus of Northwestern Uganda has been interrupted and the disease eliminated. J Parasitol Res. 2012: 748540 10.1155/2012/748540
    1. Tekle AH, Elhassan E, Isiyaku S, Amazigo UV, Bush S, Noma M, et al. (2012) Impact of long-term treatment of onchocerciasis with ivermectin in Kaduna State, Nigeria: First evidence of the potential for elimination in the operational area of the African Programme for Onchocerciasis Control. Parasit Vect. 5: 28.
    1. Traore MO, Sarr MD, Badji A, Bissan Y, Diawara L, Doumbia K, et al. (2012) Proof-of-principle of onchocerciasis elimination with ivermectin treatment in endemic foci in Africa: Final results of a study in Mali and Senegal. PLOS Neg Trop Dis. 6: e1825. Epub 2012/10/03.
    1. Anonymous (2013) Progress towards eliminating onchocerciasis in the WHO region of the Americas: Verification by WHO of elimination of transmission in Colombia. Wkly Epidemiol Rec 381–5.
    1. World Health Organization; (2001) Certification of elimination of human onchocerciasis: Criteria and procedures. Geneva: World Health Organization, WHO/CDS/CPE/CEE/2001.18b.
    1. Program Coordinating Committee and Staff, Onchocerciasis Elimination Program for the Americas (2012) Guide to detecting potential recrudescence of onchocerciasis during the posttreatment period: The American paradigm. Res Rep Trop Med. 3: 21–33.
    1. Basanez MG, Rodriguez-Perez MA, Reyes-Villanueva F, Collins RC, Rodriguez MH (1998) Determination of sample sizes for the estimation of Onchocerca volvulus (Filarioidea: Onchocercidae) infection rates in biting populations of Simulium ochraceum s.l. (Diptera: Simuliidae) and its application to ivermectin control programs. J Med Entomol. 35: 745–57.
    1. Gu W, Lampman R, Novak RJ. (2003) Problems in estimating mosquito infection rates using minimum infection rate. J Med Entomol. 40: 595–6.
    1. World Health Organization; (2001) Criteria for Certification of Interruption of Transmission/Elimination of Human Onchocerciasis. Geneva: World Health Organization, WHO/CDS/CPE/CEE/2001.18a.
    1. Rodríguez-Pérez M, Domínguez-Vázquez A, Unnasch TR, Hassan HK, Arredondo-Jiménez JI, Orozco-Algarra ME, et al. (2013) Interruption of transmission of Onchocerca volvulus in the Southern Chiapas focus, México. PLOS Neg Trop Dis. 7: e2133.
    1. Rodriguez-Perez MA, Unnasch TR, Dominguez-Vasquez A, Morales-Castro AL, Richards F, Pena-Flores GP, et al. (2010) Lack of active Onchocerca volvulus transmission in the Northern Chiapas focus of Mexico. Am J Trop Med Hyg. 83: 15–20. 10.4269/ajtmh.2010.09-0626
    1. Rodriguez-Perez MA, Unnasch TR, Dominguez-Vazquez A, Morales-Castro AL, Pena-Flores GP, Algarra-Orozco ME, et al. (2010) Interruption of transmission of Onchocerca volvulus in the Oaxaca focus, Mexico. Am J Trop Med Hyg. 83: 21–7. 10.4269/ajtmh.2010.09-0544
    1. Martín-Tellaeche A. (2008). Oncocercosis. Endemia Rural de los Ríos que Ciega. 1875–2008. Editorial Bayer Envionmental Science. 309 pp
    1. Collins RC, Merino ME, Cupp EW (1981) Seasonal trends and diurnal patterns of man-biting activity of four species of Guatemalan black flies (Simuliidae). Am J Trop Med Hyg. 30: 728–33.
    1. Rodríguez-Pérez MA, Lilley BG, Domínguez-Vázquez A, Segura-Arenas R, Lizarazo-Ortega C, Mendoza-Herrera A, et al. (2004) Polymerase chain reaction monitoring of transmission of Onchocerca volvulus in two endemic states in Mexico. Am J Trop Med Hyg. 70: 38–45.
    1. Gopal H, Hassan HK, Rodríguez-Pérez MA, Toé LD, Lustigman S, Unnasch TR (2012) Oligonucleotide based magnetic bead capture of Onchocerca volvulus DNA for PCR pool screening of vector black flies. PLOS Neg Trop Dis. 6: e1712.
    1. Guevara AG, Vieira JC, Lilley BG, López A, Vieira N, Rumbea J, et al. (2003) Entomolological evaluation by pool screen polymerase chain reaction of Onchocerca volvulus transmission in Ecuador following mass Mectizan distribution. Am J Trop Med Hyg. 68: 222–7.
    1. Katholi C. Poolscreen v2.0. 2010 [June 19, 2015]; 2.0. Available from .
    1. Wada Y (1982) Theoretical approach to the epidemiology of onchocerciasis in Guatemala. Jpn J Med Sci Biol. 35: 183–96.
    1. Porter CH, Collins RC, Brandling-Bennett AD (1988) Vector density, parasite prevalence, and transmission of Onchocerca volvulus in Guatemala. Am J Trop Med Hyg. 39: 567–74.
    1. Rodriguez-Perez MA, Rodriguez MH, Margeli-Perez HM, Rivas-Alcala AR (1995) Effect of semiannual treatments of ivermectin on the prevalence and intensity of Onchocerca volvulus skin infection, ocular lesions, and infectivity of Simulium ochraceum populations in southern Mexico. Am J Trop Med Hyg. 52: 429–34.
    1. Rodríguez-Pérez MA, Katholi CR, Hassan HK, Unnasch TR (2006) A large-scale entomologic assessment of Onchocerca volvulus transmission by pool-screen PCR in Mexico. Am J Trop Med Hyg. 74: 1026–33.
    1. Walsh JF, Davies JB, LeBerre R, Garms R (1978) Standardization of criteria for assessing the effects of Simulium control in onchocerciasis control programmes. Trans R Soc Trop Med Hyg. 72: 675–6.
    1. Collins RC, Ochoa JO, Cupp EW, Gonzales-Peralta C, Porter CH (1992) Microepidemiology of onchocerciasis in Guatemala: Dispersal and survival of Simulium ochraceum . Am J Trop Med Hyg. 47: 147–55. Epub 1992/08/01.
    1. Anonymous (2013) Progress toward elimination of onchocerciasis in the Americas—1993–2012. MMWR. 62: 405–8. Epub 2013/05/24.
    1. Anonymous (2014) Programa de Acción Específico: Eliminación de la Oncocercosis Programa Sectorial de Salud 2013–2018. Secretaria de Salud, Mexico: pp 66.
    1. Rodríguez-Pérez MA, Adeleke MA, Burkett-Cadena ND, Garza-Hernández JA, Reyes-Villanueva F, Cupp EW, et al. (2013) Development of a novel trap for the collection of black flies of the Simulium ochraceum complex. PLOS One. 8: e76814 10.1371/journal.pone.0076814
    1. Lovato R, Guevara A, Guderian R, Proano R, Unnasch T, Criollo H, et al. (2014) Interruption of infection transmission in the onchocerciasis focus of Ecuador leading to the cessation of ivermectin distribution. PLOS Neg Trop Dis. 8: e2821.
    1. Lindblade KA, Arana B, Zea-Flores G, Rizzo N, Porter CH, Dominguez A, et al. (2007) Elimination of Onchocerca volvulus transmission in the Santa Rosa focus of Guatemala. Am J Trop Med Hyg. 77: 334–41.
    1. Gonzalez RJ, Cruz-Ortiz N, Rizzo N, Richards J, Zea-Flores G, Dominguez A, et al. (2009) Successful interruption of transmission of Onchocerca volvulus in the Escuintla-Guatemala focus, Guatemala. PLoS Negl Trop Dis. 3: e404.
    1. Cruz-Ortiz N, Gonzalez RJ, Lindblade KA, Richards FO Jr., Sauerbrey M, Zea-Flores, et al. (2012) Elimination of Onchocerca volvulus transmission in the Huehuetenango focus of Guatemala. J Parasitol Res. 2012: 638429 Epub 2012/09/13. 10.1155/2012/638429
    1. Diawara L, Traore MO, Badji A, Bissan Y, Doumbia K, Goita SF, et al. (2009) Feasibility of onchocerciasis elimination with ivermectin treatment in endemic foci in Africa: First evidence from studies in Mali and Senegal. PLOS Neg Trop Dis. 3: e497.
    1. Katabarwa M, Lakwo T, Habomugisha P, Agunyo S, Byamukama E, Oguttu D, et al. (2014) Transmission of Onchocerca volvulus by Simulium neavei in Mount Elgon focus of eastern Uganda has been interrupted. Am J Trop Med Hyg. 90: 1159–66. 10.4269/ajtmh.13-0501
    1. Higazi TB, Zarroug IMA, Mohamed HA, ElMubark WA, Deran TCM, Aziz N, et al. (2013) Interruption of onchocerciasis transmission in the Abu Hamed Focus, Sudan. Am J Trop Med Hyg. 89: 51–7. 10.4269/ajtmh.13-0112

Source: PubMed

3
Subskrybuj