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Molecular Xenomonitoring for Wuchereria Bancrofti in Culex Quinquefasciatus in Two Districts in Bangladesh Supports Transmission Assessment Survey Findings

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Molecular Xenomonitoring for Wuchereria Bancrofti in Culex Quinquefasciatus in Two Districts in Bangladesh Supports Transmission Assessment Survey Findings RESEARCH ARTICLE Molecular xenomonitoring for Wuchereria bancrofti in Culex quinquefasciatus in two districts in Bangladesh supports transmission assessment survey findings Seth R. Irish1,2*, Hasan Mohammad Al-Amin3, Heather N. Paulin1, A. S. M. Sultan Mahmood4, Rajaul K. Khan4, A. K. M. Muraduzzaman5, Caitlin M. Worrell1, Meerjady S. Flora5, Mohammed J. Karim4, Tahmina Shirin5, A. K. M. Shamsuzzaman4, a1111111111 Sanya Tahmina3,4, Audrey Lenhart1, Christine Dubray1 a1111111111 a1111111111 1 Division of Parasitic Diseases and Malaria, Center for Global Health, Centers for Disease Control and Prevention, Atlanta, Georgia, United States of America, 2 President's Malaria Initiative, Bureau for Global a1111111111 Health, Office of Infectious Disease, United States Agency for International Development, Washington, DC, a1111111111 United States of America, 3 International Centre for Diarrhoeal Disease Research, Bangladesh, Dhaka, Bangladesh, 4 Ministry of Health and Family Welfare, Communicable Disease Control, Directorate General of Health Services, Dhaka, Bangladesh, 5 Institute of Epidemiology Disease Control & Research, Dhaka, Bangladesh * [email protected] OPEN ACCESS Citation: Irish SR, Al-Amin HM, Paulin HN, Mahmood ASMS, Khan RK, Muraduzzaman AKM, et al. (2018) Molecular xenomonitoring for Abstract Wuchereria bancrofti in Culex quinquefasciatus in two districts in Bangladesh supports transmission assessment survey findings. PLoS Negl Trop Dis Background 12(7): e0006574. https://doi.org/10.1371/journal. pntd.0006574 Careful monitoring for recrudescence of Wuchereria bancrofti infection is necessary Editor: Samuel Wanji, University of Buea, in communities where mass drug administration (MDA) for the elimination of lymphatic CAMEROON filariasis (LF) as a public health problem has been stopped. During the post-MDA period, Received: February 9, 2018 transmission assessment surveys (TAS) are recommended by the World Health Organiza- tion to monitor the presence of the parasite in humans. Molecular xenomonitoring (MX), a Accepted: June 1, 2018 method by which parasite infection in the mosquito population is monitored, has also been Published: July 26, 2018 proposed as a sensitive method to determine whether the parasite is still present in the Copyright: This is an open access article, free of all human population. The aim of this study was to conduct an MX evaluation in two areas of copyright, and may be freely reproduced, Bangladesh, one previously endemic district that had stopped MDA (Panchagarh), and part distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. of a non-endemic district (Gaibandha) that borders the district where transmission was most The work is made available under the Creative recently recorded. Commons CC0 public domain dedication. Data Availability Statement: All relevant data are within the paper and in its Supporting Information Methodology/Principal findings files. Mosquitoes were systematically collected from 180 trap sites per district and mosquito Funding: This work received financial support from pools were tested for W. bancrofti using real-time PCR. A total of 23,436 intact mosquitoes, the Neglected Tropical Disease Support Center representing 31 species, were collected from the two districts, of which 10,344 (41%) were (NTDSC), which is funded at the Task Force for Culex quinquefasciatus, the vector of W. bancrofti in Bangladesh. All of the 594 pools of Cx. Global Health principally by grants from the Bill & Melinda Gates Foundation and United States quinquefasciatus tested by real-time PCR were negative for the presence of W. bancrofti Agency for International Development. The funders DNA. PLOS Neglected Tropical Diseases | https://doi.org/10.1371/journal.pntd.0006574 July 26, 2018 1 / 12 Molecular xenomonitoring in Bangladesh had no role in the study design, data collection and Conclusions/Significance analysis, decision to publish or preparation of the manuscript. This study suggested the absence of W. bancrofti in these districts. MX could be a sensitive tool to confirm interruption of LF transmission in areas considered at higher risk of recrudes- Competing interests: The authors have declared that no competing interests exist. cence, particularly in countries like Bangladesh where entomological and laboratory capac- ity to perform MX is available. Author summary To ensure elimination of lymphatic filariasis, efficient surveillance methods are needed. While some available methods rely on the detection of Wuchereria bancrofti microfilaria, antigen or antibody in human blood samples, molecular xenomonitoring can identify par- asite DNA in vector mosquitoes. We collected the main vector of lymphatic filariasis in Bangladesh, Culex quinquefasciatus mosquitoes, in two districts in Bangladesh to see if W. bancrofti could be detected. One of the districts never had evidence of widespread trans- mission but borders another district where transmission was most recently detected. The other district had previously had W. bancrofti transmission, but after 12 rounds of mass drug administration, had been deemed to have little to no ongoing transmission. In each district, traps were set at 180 sites to collect mosquitoes. Over ten thousand Cx. quinque- fasciatus mosquitoes were collected, but none of them tested positive for presence of W. bancrofti. The practice of trapping mosquitoes was feasible for the national program to execute, and the absence of infected mosquitoes suggests that parasite rates are nearing zero. Introduction Lymphatic filariasis (LF), an important cause of acute and chronic morbidity worldwide, is caused by infection with the thread-like nematodes Wuchereria bancrofti, Brugia malayi and Brugia timori. The Global Programme to Eliminate Lymphatic Filariasis was established in 2000 by the World Health Organization (WHO) and has two objectives: (i) the interruption of LF transmission through mass drug administration (MDA) using the combination of albenda- zole plus diethylcarbamazine or ivermectin, or all three drugs together in specific contexts as recommended recently by WHO [1] and (ii) the alleviation of the suffering of affected popula- tions through morbidity management and disability prevention [2]. Interruption of transmis- sion is thought to require at least five rounds of MDA, after which national LF elimination programs conduct a Transmission Assessment Survey (TAS) to determine whether MDA can be stopped [3]. After MDA is ceased, programs must conduct surveillance to identify and respond to the possibility of re-emergence of transmission. Current WHO recommendations for post-MDA surveillance include repeating TAS twice at 2±3 year intervals after stopping MDA, and ongo- ing surveillance [3]. Detection of parasites in vector mosquitoes is one of the surveillance strat- egies that countries can consider. Molecular xenomonitoring (MX), the use of PCR to identify parasite DNA in vector mosquitoes, has previously been used for LF surveillance after cessa- tion of MDA [4±6] to identify residual foci of transmission. It has the advantage of being non- invasive to humans and could be useful when willingness of people to be tested is an issue, especially as households (HH) that refused MDA may also refuse testing during post-MDA PLOS Neglected Tropical Diseases | https://doi.org/10.1371/journal.pntd.0006574 July 26, 2018 2 / 12 Molecular xenomonitoring in Bangladesh surveillance. However, MX requires entomological expertise and laboratories with molecular capacity. In Bangladesh, 70 million individuals were at risk of LF before the Ministry of Health and Family Welfare (MoHFW) started its LF elimination program in 2000 [7±8]. Wuchereria ban- crofti is the only species of human filarial worm currently known to be present in Bangladesh and the main vector is Culex quinquefasciatus [9]. Based on initial mapping, 19 of 64 districts were classified as endemic (baseline microfilaria prevalence between 1% and 16%) and therefore required MDA [7], which began in 2001. By 2016, all 19 districts had passed the TAS and were eligible to cease MDA activities [7]. An ongoing surveillance project was initiated in April 2014 in Panchagarh (one of the previously treated endemic districts) and in Gaibandha (a non- endemic district that had never conducted MDA). The latter district was selected because it bor- ders a district with recent LF transmission and was considered at high risk for re-introduction. The objective of the project was to monitor W. bancrofti transmission trends through the assess- ment of microfilaremia (Mf), antibodies, and antigenemia among adults in these two districts. Molecular xenomonitoring [10] was implemented as a complementary strategy for identifying areas of active transmission [11]. We sought to use MX to measure if the mosquito infection rate with W. bancrofti in the two districts was less than the cut-off point of 0.25%, a threshold that has been suggested for areas where Culex mosquitoes are the vector [10]. Methods Study site Mosquitoes were collected in two evaluation units, one in Panchagarh district and one in Gai- bandha district (Fig 1). Panchagarh district is part of the Rangpur division and is the most northeasterly district in Bangladesh, with a population of 987,644 and an area of 1404 km2 [12]. It is bordered on three sides by India and in the south by three other districts belonging to the Rangpur division, all of them previously endemic for LF but without any positive cases identified during the TAS1 and
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