A comprehensive assessment of lymphatic filariasis in Sri Lanka six years after cessation of mass drug administration

Ramakrishna U Rao, Kumara C Nagodavithana, Sandhya D Samarasekera, Asha D Wijegunawardana, Welmillage D Y Premakumara, Samudrika N Perera, Sunil Settinayake, J Phillip Miller, Gary J Weil, Ramakrishna U Rao, Kumara C Nagodavithana, Sandhya D Samarasekera, Asha D Wijegunawardana, Welmillage D Y Premakumara, Samudrika N Perera, Sunil Settinayake, J Phillip Miller, Gary J Weil

Abstract

Background: The Sri Lankan Anti-Filariasis Campaign conducted 5 rounds of mass drug administration (MDA) with diethycarbamazine plus albendazole between 2002 and 2006. We now report results of a comprehensive surveillance program that assessed the lymphatic filariasis (LF) situation in Sri Lanka 6 years after cessation of MDA.

Methodology and principal findings: Transmission assessment surveys (TAS) were performed per WHO guidelines in primary school children in 11 evaluation units (EUs) in all 8 formerly endemic districts. All EUs easily satisfied WHO criteria for stopping MDA. Comprehensive surveillance was performed in 19 Public Health Inspector (PHI) areas (subdistrict health administrative units). The surveillance package included cross-sectional community surveys for microfilaremia (Mf) and circulating filarial antigenemia (CFA), school surveys for CFA and anti-filarial antibodies, and collection of Culex mosquitoes with gravid traps for detection of filarial DNA (molecular xenomonitoring, MX). Provisional target rates for interruption of LF transmission were community CFA <2%, antibody in school children <2%, and filarial DNA in mosquitoes <0.25%. Community Mf and CFA prevalence rates ranged from 0-0.9% and 0-3.4%, respectively. Infection rates were significantly higher in males and lower in people who denied prior treatment. Antibody rates in school children exceeded 2% in 10 study sites; the area that had the highest community and school CFA rates also had the highest school antibody rate (6.9%). Filarial DNA rates in mosquitoes exceeded 0.25% in 10 PHI areas.

Conclusions: Comprehensive surveillance is feasible for some national filariasis elimination programs. Low-level persistence of LF was present in all study sites; several sites failed to meet provisional endpoint criteria for LF elimination, and follow-up testing will be needed in these areas. TAS was not sensitive for detecting low-level persistence of filariasis in Sri Lanka. We recommend use of antibody and MX testing as tools to complement TAS for post-MDA surveillance.

Conflict of interest statement

The filarial antigen test used in this study uses reagents licensed from Barnes-Jewish Hospital, an affiliation of GJW. All royalties from sales of these tests go to the Barnes Jewish Hospital Foundation, a not for profit charitable organization (http://www.barnesjewish.org/giving/about-us). This does not alter our adherence to all PLOS policies on sharing data and materials.

Figures

Figure 1. Graphic summary of comprehensive filariasis…
Figure 1. Graphic summary of comprehensive filariasis surveillance data for Public Health Inspector areas in Sri Lanka.
Data shown are rates (% with 95% confidence limits as vertical lines). The dotted line in the top panel and the lower dotted lines in the two lower panels show the old provisional targets for interruption of transmission. The upper dotted lines in the two lower panels are recommended revised targets for the upper confidence limits for antibody rates in first and second grade primary school children and for filarial DNA rates in mosquitoes, respectively.
Figure 2. Distribution of households and mosquito…
Figure 2. Distribution of households and mosquito collection sites tested for filariasis in Unawatuna PHI area in Galle district.
Panel A. Blue waypoints indicate households (HH) where all tested residents had negative filarial antigen tests; waypoints in red (CFA positivity) or yellow (microfilaremia and CFA positivity) indicate houses with at least one infected subject. Panel B shows molecular xenomonitoring results. Trap sites with no mosquito pools positive for filarial DNA are shown in blue, and traps with one or more positive mosquito pools are shown in red. Filarial DNA was detected in mosquitoes collected in 60% of the traps in this PHI.

References

    1. WHO (2013) Global programme to eliminate lymphatic filariasis: progress report for 2012. Wkly Epidemiol Rec 88: 389–399.
    1. Abdulcader MH, Sasa M (1966) Epidemiology and control of bancroftian filariasis in Ceylon. Jpn J Exp Med 36: 609–646.
    1. Schweinfurth U (1983) Filarial diseases in Ceylon: a geographic and historical analysis. Ecol Dis 2: 309–319.
    1. Dissanaike AS (1991) Filariasis in Ceylon then (1961) and in Sri Lanka now (1990–30 years on). Ann Trop Med Parasitol 85: 123–129.
    1. AntifilariasisCampaign (2013) Annual reports. Ministry of Health, Sri Lanka Available at .
    1. Horton J, Witt C, Ottesen EA, Lazdins JK, Addiss DG, et al. (2000) An analysis of the safety of the single dose, two drug regimens used in programmes to eliminate lymphatic filariasis. Parasitology 121 Suppl: S147–160.
    1. WHO (2000) Preparing and implementing a national plan to eliminate lymphatic filariasis (in countries where onchocerciasis is not co-endemic). World Health Organization, Geneva, WHO/CDS/CPE/CEE/200016.
    1. WHO (2011) Halfway towards eliminating lymphatic filariasis: Progress Report 2000–2009 and Strategic Plan 2010–2020 of the Global Programme to Eliminate Lymphatic Filariasis. WHO, 2011 (WHO/HTM/NTD/PCT/20106) Geneva: World Health Organization.
    1. Gunawardena GS, Ismail MM, Bradley MH, Karunaweera ND (2007) Impact of the 2004 mass drug administration for the control of lymphatic filariasis, in urban and rural areas of the Western province of Sri Lanka. Ann Trop Med Parasitol 101: 335–341.
    1. Weerasooriya MV, Yahathugoda CT, Wickramasinghe D, Gunawardena KN, Dharmadasa RA, et al. (2007) Social mobilisation, drug coverage and compliance and adverse reactions in a Mass Drug Administration (MDA) Programme for the Elimination of Lymphatic Filariasis in Sri Lanka. Filaria J 6: 11.
    1. Yahathugoda TC, Weerasooriya MV, Sunahara T, Kimura E, Samarawickrema WA, et al. (2014) Rapid assessment procedures to detect hidden endemic foci in areas not subjected to mass drug administration in Sri Lanka. Parasitol Int 63: 87–93.
    1. Yahathugoda TC, Weerasooriya M, Samarawickrema WA (2013) An independent evaluation of the programme for the elimination of lymphatic filariasis. Galle Medical Journal 18: 31–43.
    1. WHO (2012) Expert Mission to Sri Lanka for verification of elimination of lymphatic filariasis. Report. World Health Organization (SEA-CD-245) New Delhi, India: 1–37.
    1. Chu BK, Deming M, Biritwum NK, Bougma WR, Dorkenoo AM, et al. (2013) Transmission assessment surveys (TAS) to define endpoints for lymphatic filariasis mass drug administration: a multicenter evaluation. PLoS Negl Trop Dis 7: e2584.
    1. WHO (2011) Monitoring and epidemiological assessment of mass drug administration in the Global Programme to Eliminate Lymphatic Filariasis: A manual for national elimination programmes. WHO, (WHO/HTM/NTD/PCT/2011 4) Geneva: World Health Organization.
    1. Weil GJ, Ramzy RM (2007) Diagnostic tools for filariasis elimination programs. Trends Parasitol 23: 78–82.
    1. Irish SR, Moore SJ, Derua YA, Bruce J, Cameron MM (2013) Evaluation of gravid traps for the collection of Culex quinquefasciatus, a vector of lymphatic filariasis in Tanzania. Trans R Soc Trop Med Hyg 107: 15–22.
    1. Weil GJ, Lammie PJ, Weiss N (1997) The ICT Filariasis Test: A rapid-format antigen test for diagnosis of bancroftian filariasis. Parasitol Today 13: 401–404.
    1. Weil GJ, Curtis KC, Fischer PU, Won KY, Lammie PJ, et al. (2011) A multicenter evaluation of a new antibody test kit for lymphatic filariasis employing recombinant Brugia malayi antigen Bm-14. Acta Trop 120 Suppl 1: S19–22.
    1. Rao RU, Atkinson LJ, Ramzy RM, Helmy H, Farid HA, et al. (2006) A real-time PCR-based assay for detection of Wuchereria bancrofti DNA in blood and mosquitoes. Am J Trop Med Hyg 74: 826–832.
    1. Gass K, Beau de Rochars MV, Boakye D, Bradley M, Fischer PU, et al. (2012) A multicenter evaluation of diagnostic tools to define endpoints for programs to eliminate bancroftian filariasis. PLoS Negl Trop Dis 6: e1479.
    1. Katholi CR, Toe L, Merriweather A, Unnasch TR (1995) Determining the prevalence of Onchocerca volvulus infection in vector populations by polymerase chain reaction screening of pools of black flies. J Infect Dis 172: 1414–1417.
    1. Katholi CR, Unnasch TR (2006) Important experimental parameters for determining infection rates in arthropod vectors using pool screening approaches. Am J Trop Med Hyg 74: 779–785.
    1. Ramzy RM, El Setouhy M, Helmy H, Ahmed ES, Abd Elaziz KM, et al. (2006) Effect of yearly mass drug administration with diethylcarbamazine and albendazole on bancroftian filariasis in Egypt: a comprehensive assessment. Lancet 367: 992–999.
    1. Budge PJ, Dorkenoo AM, Sodahlon YK, Fasuyi OB, Mathieu E (2014) Ongoing surveillance for lymphatic filariasis in Togo: assessment of alternatives and nationwide reassessment of transmission status. Am J Trop Med Hyg 90: 89–95.
    1. WHO (2013) Lymphatic Filariasis: Practical Entomology. A Handbook for National Elimination Programmes. WHO Global Programme to Eliminate Lymphatic Filariasis: 1–90.
    1. Eigege A, Kal A, Miri E, Sallau A, Umaru J, et al. (2013) Long-lasting insecticidal nets are synergistic with mass drug administration for interruption of lymphatic filariasis transmission in Nigeria. PLoS Negl Trop Dis 7: e2508.
    1. Reimer LJ, Thomsen EK, Tisch DJ, Henry-Halldin CN, Zimmerman PA, et al. (2013) Insecticidal bed nets and filariasis transmission in Papua New Guinea. N Engl J Med 369: 745–753.
    1. Stolk WA, de Vlas SJ, Habbema JD (2006) Advances and challenges in predicting the impact of lymphatic filariasis elimination programmes by mathematical modelling. Filaria J 5: 5.

Source: PubMed

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