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Plasmodium Vivax Genetic Diversity in Panama: Challenges for Malaria Elimination in Mesoamerica

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Plasmodium Vivax Genetic Diversity in Panama: Challenges for Malaria Elimination in Mesoamerica pathogens Article Plasmodium vivax Genetic Diversity in Panama: Challenges for Malaria Elimination in Mesoamerica Ana María Santamaría 1,2,†, Vanessa Vásquez 1,†, Chystrie Rigg 1 , Franklyn Samudio 1, Dianik Moreno 3, Luis Romero 3, Azael Saldaña 1,2, Luis Fernando Chaves 4,* and José Eduardo Calzada 1,2,* 1 Departamento de Investigación en Parasitología, Instituto Conmemorativo Gorgas de Estudios de la Salud, Panama 0816-02593, Panama; [email protected] (A.M.S.); [email protected] (V.V.); [email protected] (C.R.); [email protected] (F.S.); [email protected] (A.S.) 2 Facultad de Medicina y Medicina Veterinaria, Universidad de Panamá, Panama 0816-03366, Panama 3 Laboratorio Central de Referencia en Salud Publica, Instituto Conmemorativo Gorgas de Estudios de la Salud, Panama 0816-02593, Panama; [email protected] (D.M.); [email protected] (L.R.) 4 Investigador Asociado, Instituto Conmemorativo Gorgas de Estudios de la Salud, Panama 0816-02593, Panama * Correspondence: [email protected] (L.F.C.); [email protected] (J.E.C.); Tel.: +506-88618433 (L.F.C.); +507-65171608 (J.E.C.) † These authors contributed equally to this work. Abstract: Panama and all nations within the Mesoamerican region have committed to eliminate malaria within this decade. With more than 90% of the malaria cases in this region caused by Plasmodium vivax, an efficient national/regional elimination plan must include a comprehensive study of this parasite’s genetic diversity. Here, we retrospectively analyzed P. vivax genetic diversity Citation: Santamaría, A.M.; Vásquez, in autochthonous and imported field isolates collected in different endemic regions in Panama from V.; Rigg, C.; Samudio, F.; Moreno, D.; 2007 to 2020, using highly polymorphic markers (csp, msp-1, and msp-3α). We did the analysis using Romero, L.; Saldaña, A.; Chaves, L.F.; molecular techniques that are cost-effective for malaria molecular surveillance within Mesoamerica. Calzada, J.E. Plasmodium vivax Genetic Thus, we used molecular analyses that are feasible for malaria molecular surveillance within the Diversity in Panama: Challenges for Malaria Elimination in Mesoamerica. region, and that can provide useful information for policy and decision making about malaria Pathogens 2021, 10, 989. https:// elimination. We also evaluated if haplotypes established by combining the genotypes found in doi.org/10.3390/pathogens10080989 these genes were associated with relevant epidemiological variables and showed structure across the transmission foci that have been observed in Panama. Ten different haplotypes were identified, Academic Editors: Kamala some of them strongly associated with geographical origin, age, and collection year. Phylogenetic Ley-Thriemer, Brioni Moore and analysis of csp (central repeat domain) revealed that both major variant types (vk210 and vk247) were Mohammad Shafiul Alam circulating in Panama. Variant vk247 was restricted to the eastern endemic regions, while vk210 was predominant (77.3%) and widespread, displaying higher diversity (14 alleles) and geographically Received: 11 May 2021 biased alleles. The regional implications of these molecular findings for the control of P. vivax malaria Accepted: 4 August 2021 to achieve elimination across Mesoamerica are discussed. Published: 5 August 2021 Keywords: Plasmodium vivax; genotype; molecular epidemiology; elimination; Panama; Mesoamerica Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affil- iations. 1. Introduction Given the relatively low number of malaria cases and deaths, and its strategic geo- graphical position as a corridor connecting South and North America (Figure1); Mesoamer- ica has been recently targeted by the World Health Organization (WHO) as a tactical Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. subregion with malaria elimination potential in the short term [1,2]. In fact, less than This article is an open access article 1% of the global malaria burden occurs in this subregion, which is mostly (around 95%) distributed under the terms and caused by Plasmodium vivax parasites [3]. From the nine countries comprising Mesoamerica conditions of the Creative Commons (southeastern Mexico and the countries of Central America, including Panama) (Figure1), Attribution (CC BY) license (https:// El Salvador was the first country in Central America to be recently certified malaria-free by creativecommons.org/licenses/by/ WHO, and three other countries (Mexico, Belize, and Costa Rica) were identified with the 4.0/). potential to achieve zero indigenous cases of malaria by 2021 [4,5]. However, despite the Pathogens 2021, 10, 989. https://doi.org/10.3390/pathogens10080989 https://www.mdpi.com/journal/pathogens Pathogens 2021, 10, x FOR PEER REVIEW 2 of 18 Pathogens 2021, 10, 989 ure 1), El Salvador was the first country in Central America to be recently certified ma- 2 of 18 laria-free by WHO, and three other countries (Mexico, Belize, and Costa Rica) were iden- tified with the potential to achieve zero indigenous cases of malaria by 2021 [4,5]. How- ever, despitefavorable the favorable epidemiological epidemiological conditions conditions in the region, in the many region, of thesemany countries of these coun- have not been tries haveable notto been meet able the to elimination meet the elimination goals set by goals WHO set [ 1by,3], WHO facing [1,3], important facing technical,important adminis- technical,trative, administrative, and financial and challenges financial thatchallenges have been that identified, have been but identified, not properly but addressed not by properlyheath addressed authorities by heath [6– 8authorities]. [6–8]. Figure 1. Map of theFigure Panama 1. Map showing of the health Panama regions showing with health active Plasmodiumregions with vivax activetransmission Plasmodium based vivax on transmission the cumulative number of cases betweenbased on 2000 the andcumulative 2019. The number dashed of linescases in between the map 2000 indicate and 2019. the Panama The dashed Canal lines pathway in the thatmap artificially indi- divides the countrycate into the eastern Panama and Canal western pathway Panama. that The artificially red circle divides represents the thecountry location into of eastern the Darien and western Gap consisting Pan- of a road-less swath ofama. swampland The red circle and rainforest represents within the location Panama’s of Darithe éDarienn Province Gap andconsisting the northern of a road portion-less ofswath Colombia’s of swampland and rainforest within Panama’s Darién Province and the northern portion of Colom- Chocó Department. The Darien Gap is a corridor used by migrants from around the globe intending to reach the United bia’s Chocó Department. The Darien Gap is a corridor used by migrants from around the globe States or Canada. The lower inset map shows the location of Panama within the Mesoamerican region, colored in yellow. intending to reach the United States or Canada. The lower inset map shows the location of Panama within the Mesoamerican region, colored in yellow. Panama, located at the southern end of Mesoamerica (Figure1), has also regionally committed to eliminate malaria by 2021 [9]. During the past years, however, a relentless Panama, located at the southern end of Mesoamerica (Figure 1), has also regionally malaria burden has been observed in recognized endemic areas; a situation further com- committed to eliminate malaria by 2021 [9]. During the past years, however, a relentless plicated by the reestablishment of P. falciparum transmission in the eastern region of the malaria burden has been observed in recognized endemic areas; a situation further com- country [10]. Moreover, indigenous populations account for more than 90% of local malaria plicated by the reestablishment of P. falciparum transmission in the eastern region of the cases [10,11]. Most of these indigenous populations (92%) live in extreme poverty, with country [10]. Moreover, indigenous populations account for more than 90% of local ma- significant higher rates of malnutrition, and infant and maternal mortality, especially when laria cases [10,11]. Most of these indigenous populations (92%) live in extreme poverty, compared with the rest of the Panamanian population [9–13]. Panama is also a hotspot with significant higher rates of malnutrition, and infant and maternal mortality, especially for the transit of economic migrants worldwide [14]. Recent studies have shown a grow- when compareding number with of the imported rest of malariathe Panamanian continuously population entering [9 from–13]. South Panama America is also through a the hotspot forDari theén transit Gap, an of area economic across themigrants Colombia worldwide and Panama [14]. borderRecent (Figurestudies1 )[have10, 15shown]. Plasmodium parasites isolated from these imported cases have shown a higher genetic diversity when compared with the genetic structure displayed by local cases [15]. Pathogens 2021, 10, 989 3 of 18 The majority (95%) of the malaria cases registered in Panama since 2000 have been caused by P. vivax [10]. This fact suggests that an efficient elimination plan must include a comprehensive study of P. vivax biology considering the species peculiarities that hamper its control. In this sense, knowing the genetic structure of P. vivax circulating in the country over years can elucidate not only the origins and connectivity of the transmission, but also evidence the association of certain genotypes
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