Detection of Wuchereria bancrofti DNA in wild caught vector and non-vector mosquitoes: implications for elimination of lymphatic filariasis.

Lymphatic filariasis Real-time PCR assay Wuchereria bancrofti Xenomonitoring

Journal

Molecular biology reports
ISSN: 1573-4978
Titre abrégé: Mol Biol Rep
Pays: Netherlands
ID NLM: 0403234

Informations de publication

Date de publication:
08 Feb 2024
Historique:
received: 30 11 2023
accepted: 15 01 2024
medline: 8 2 2024
pubmed: 8 2 2024
entrez: 8 2 2024
Statut: epublish

Résumé

Transmission Assessment Survey (TAS) is the WHO recommended method used for decision-making to stop or continue the MDA in lymphatic filariasis (LF) elimination programme. The WHO has also recommended Molecular Xenomonitoring (MX) of LF infection in vectors as an adjunct tool in settings under post-MDA or validation period. Screening of non-vectors by MX in post-MDA / validation settings could be useful to prevent a resurgence of LF infection, as there might be low abundance of vectors, especially in some seasons. In this study, we investigated the presence of LF infection in non-vectors in an area endemic for LF and has undergone many rounds of annual MDA with two drugs (Diethylcarbamazine and Albendazole, DA) and two rounds of triple drug regimens (Ivermectin + DA). Mosquitoes were collected from selected villages of Yadgir district in Karnataka state, India, during 2019. A total of 680 female mosquitoes were collected, identified morphologically by species and separated as pools. The female mosquitoes belonging to 3 species viz., Anopheles subpictus, Culex gelidus and Culex quinquefaciatus were separated, pooled, and the DNA extracted using less expensive method and followed by LDR based real-time PCR assay for detecting Wuchereria bancrofti infection in vector as well as non-vector mosquitoes. One pool out of 6 pools of An. subpictus, 2 pools out of 6 pools of Cx. gelidus, and 4 pools out of 8 pools of Cx. quinquefaciatus were found to be positive for W. bancrofti infection by RT-PCR. The infection rate in vectors and non-vectors was found to be 1.8% (95% CI: 0.5-4.2%) and 0.9% (95% CI: 0.2-2.3%), respectively. Our study showed that non-vectors also harbour W. bancrofti, thus opening an opportunity of using these mosquitoes as surrogate vectors for assessing risk of transmission to humans in LF endemic and post MDA areas.

Sections du résumé

BACKGROUND BACKGROUND
Transmission Assessment Survey (TAS) is the WHO recommended method used for decision-making to stop or continue the MDA in lymphatic filariasis (LF) elimination programme. The WHO has also recommended Molecular Xenomonitoring (MX) of LF infection in vectors as an adjunct tool in settings under post-MDA or validation period. Screening of non-vectors by MX in post-MDA / validation settings could be useful to prevent a resurgence of LF infection, as there might be low abundance of vectors, especially in some seasons. In this study, we investigated the presence of LF infection in non-vectors in an area endemic for LF and has undergone many rounds of annual MDA with two drugs (Diethylcarbamazine and Albendazole, DA) and two rounds of triple drug regimens (Ivermectin + DA).
METHODS AND RESULTS RESULTS
Mosquitoes were collected from selected villages of Yadgir district in Karnataka state, India, during 2019. A total of 680 female mosquitoes were collected, identified morphologically by species and separated as pools. The female mosquitoes belonging to 3 species viz., Anopheles subpictus, Culex gelidus and Culex quinquefaciatus were separated, pooled, and the DNA extracted using less expensive method and followed by LDR based real-time PCR assay for detecting Wuchereria bancrofti infection in vector as well as non-vector mosquitoes. One pool out of 6 pools of An. subpictus, 2 pools out of 6 pools of Cx. gelidus, and 4 pools out of 8 pools of Cx. quinquefaciatus were found to be positive for W. bancrofti infection by RT-PCR. The infection rate in vectors and non-vectors was found to be 1.8% (95% CI: 0.5-4.2%) and 0.9% (95% CI: 0.2-2.3%), respectively.
CONCLUSIONS CONCLUSIONS
Our study showed that non-vectors also harbour W. bancrofti, thus opening an opportunity of using these mosquitoes as surrogate vectors for assessing risk of transmission to humans in LF endemic and post MDA areas.

Identifiants

pubmed: 38329553
doi: 10.1007/s11033-024-09256-4
pii: 10.1007/s11033-024-09256-4
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

291

Informations de copyright

© 2024. The Author(s), under exclusive licence to Springer Nature B.V.

Références

WHO.int/news/item/29-10-2020-lymphatic-filariasis-reporting-continued-progress-towards-elimination-as-a-public-health-problem
Cameron MM, Ramesh A (2021) The use of molecular xenomonitoring for surveillance of mosquito-borne diseases. Philosophical Trans Royal Soc B 376(1818):20190816. https://doi.org/10.1098/rstb.2019.0816
doi: 10.1098/rstb.2019.0816
WHO (2011) Monitoring and epidemiological assessment of mass drug administration in the global programme to eliminate lymphatic filariasis: a manual for national elimination programmes. Geneva: World Health Organization. Available: http://apps.who.int/iris/bitstream/10665/44580/1/9789241501484_eng.pdf . Accessed 14 January 2014
WHO (2013) Practical entomology in the global programme to eliminate lymphatic filariasis: a handbook for national elimination programmes. Geneva: World Health Organization. Available: http://apps.who.int/iris/bitstream/10665/87989/1/9789241505642_eng.pdf . Accessed 14 January 2014
Zhong M, McCarthy J, Bierwert L, Lizotte-Waniewski M, Chanteau S, Nutman TB, Ottesen EA, Williams SA (1996) A polymerase chain reaction assay for detection of the parasite Wuchereria bancrofti in human blood samples. Am J Trop Med Hyg 54(4):357–363. https://doi.org/10.4269/ajtmh.1996.54.357
doi: 10.4269/ajtmh.1996.54.357 pubmed: 8615447
Chanteau S, Luquiaud P, Failloux AB, Williams SA (1994) Detection of Wuchereria bancrofti larvae in pools of mosquitoes by the polymerase chain reaction. Trans R Soc Trop Med Hyg 88(6):665–666. https://doi.org/10.1016/0035-9203(94)90219-4
doi: 10.1016/0035-9203(94)90219-4 pubmed: 7886765
Vasuki V, Subramanian S, Hoti SL, Jambulingam P (2012) Use of a simple DNA extraction method for high-throughput detection of filarial parasite Wuchereria bancrofti in the vector mosquitoes. Parasitol Res 111(6):2479–2481. https://doi.org/10.1007/s00436-012-3026-3
doi: 10.1007/s00436-012-3026-3 pubmed: 22777703
Rao RU, Nagodavithana KC, Samarasekera SD, Wijegunawardana AD, Premakumara WD, Perera SN, Settinayake S, Miller JP, Weil GJ (2014) A comprehensive assessment of lymphatic filariasis in Sri Lanka six years after cessation of mass drug administration. PLoS Negl Trop Dis 8(11):e3281. https://doi.org/10.1371/journal.pntd.0003281
doi: 10.1371/journal.pntd.0003281 pubmed: 25393404 pmcid: 4230885
Rao RU, Samarasekera SD, Nagodavithana KC, Dassanayaka TDM, Punchihewa MW, Ranasinghe USB, Weil GJ (2017) Reassessment of areas with persistent lymphatic filariasis nine years after cessation of mass drug administration in Sri Lanka. PLoS Negl Trop Dis 11(10):e0006066. https://doi.org/10.1371/journal.pntd.0006066
doi: 10.1371/journal.pntd.0006066 pubmed: 29084213 pmcid: 5679644
Rao RU, Samarasekera SD, Nagodavithana KC, Goss CW, Punchihewa MW, Dassanayaka TDM, Ranasinghe USB, Mendis D, Weil GJ (2018) Comprehensive Assessment of a Hotspot with Persistent Bancroftian Filariasis in Coastal Sri Lanka. Am J Trop Med Hyg 99(3):735–742. https://doi.org/10.4269/ajtmh.18-0169
doi: 10.4269/ajtmh.18-0169 pubmed: 30014812 pmcid: 6169179
Subramanian S, Jambulingam P, Chu BK, Sadanandane C, Vasuki V, Srividya A, Mohideen AbdulKader MS, Krishnamoorthy K, Raju HK, Laney SJ, Williams SA, Henderson RH (2017) Application of a household-based molecular xenomonitoring strategy to evaluate the lymphatic filariasis elimination program in Tamil Nadu, India. PLoS Negl Trop Dis 11(4):e0005519. https://doi.org/10.1371/journal.pntd.0005519
doi: 10.1371/journal.pntd.0005519 pubmed: 28406927 pmcid: 5404881
Subramanian S, Jambulingam P, Krishnamoorthy K, Sivagnaname N, Sadanandane C, Vasuki V, Palaniswamy C, Vijayakumar B, Srividya A, Raju HKK (2020) Molecular xenomonitoring as a post-MDA surveillance tool for global programme to eliminate lymphatic filariasis: field validation in an evaluation unit in India. PLoS neglected tropical diseases PLoS. Negl Trop Dis 14(1):e0007862. https://doi.org/10.1371/journal.pntd.0007862
doi: 10.1371/journal.pntd.0007862
Paily KP, Hoti SL, Balaraman K (2006) Development of lymphatic filarial parasite Wuchereria bancrofti (Spirurida: Onchocercidae) in mosquito species (Diptera: Culicidae) fed artificially on microfilaremic blood. J Med Entomol 43(6):1222–1226. https://doi.org/10.1603/0022-2585(2006)43[1222:dolfpw]2.0.co;2
doi: 10.1603/0022-2585(2006)43[1222:dolfpw]2.0.co;2 pubmed: 17162957
Supriyono S, Tan S (2020) DNA of Brugia malayi detected in several mosquito species collected from Balangan District, South Borneo Province, Indonesia. Vet World 13(5):996–1000. https://doi.org/10.14202/vetworld.2020.996-1000
doi: 10.14202/vetworld.2020.996-1000 pubmed: 32636599 pmcid: 7311887
Jambulingam, P., Kuttiatt, V. S., Krishnamoorthy, K., Subramanian, S., Srividya, A.,Raju, H. K. K., … Weil, G. J. (2021). An open label, block randomized, community study of the safety and efficacy of co-administered ivermectin, diethylcarbamazine plus albendazole vs. diethylcarbamazine plus albendazole for lymphatic filariasis in India.PLoS Negl Trop Dis 15(2):e0009069. https://doi.org/10.1371/journal.pntd.0009069
Kuttiatt VS, Somani RK, Swaminathan S, Krishnamoorthy K, Weil GJ, Purushothaman J (2020) Frequency and clinical significance of localized adverse events following mass drug administration for lymphatic filariasis in an endemic area in South India. Am J Trop Med Hyg 102(1):96. https://doi.org/10.4269/ajtmh.19-0532
doi: 10.4269/ajtmh.19-0532 pubmed: 31769393
Shivalingaiah AH, Ravikumar K, Gurupadaswamy SM (2019) Evaluation of coverage and compliance to mass drug administration for lymphatic filariasis elimination in two endemic districts of Karnataka. Int J Community Med Public Health 6(8):3583–3587. https://doi.org/10.18203/2394-6040.ijcmph20193492
doi: 10.18203/2394-6040.ijcmph20193492
Weil GJ, Bogus J, Christian M, Dubray C, Djuardi Y, Fischer PU, DOLF IDA Safety Study Group (2019) The safety of double-and triple-drug community mass drug administration for lymphatic filariasis: a multicenter, open-label, cluster-randomized study. PLoS Med 16(6):e1002839
doi: 10.1371/journal.pmed.1002839 pubmed: 31233507 pmcid: 6590784
Krentel, A., Basker, N., Beau de Rochars, M., Bogus, J., Dilliott, D., Direny, A.N., … Weil, G. J. (2021). A multicenter, community-based, mixed methods assessment of the acceptability of a triple drug regimen for elimination of lymphatic filariasis.PLoS Negl Trop Dis 15(3):e0009002
Barraud PJ (1934) The Fauna of British India, including Ceylon and Burma. Diptera. Family Culieldae. Tribes Megarhinini and Culicini. The Fauna of British India, including Ceylon and Burma. Diptera, vol 5. Vol. 5. Family Culieldae. Tribes Megarhinini and Culicini.
Vasuki V, Hoti SL, Sadanandane C, Jambulingam P (2003) A simple and rapid DNA extraction method for the detection of Wuchereria bancrofti infection in the vector mosquito, Culex quinquefasciatus by Ssp I PCR assay. Acta Trop 86(1):109–114. https://doi.org/10.1016/s0001-706x(02)00267-x
doi: 10.1016/s0001-706x(02)00267-x pubmed: 12711110
Rao RU, Atkinson LJ, Ramzy RM, HelmyH, Farid HA, Bockarie MJ, Susapu M, Laney SJ, Williams SA, Weil GJ (2006) A real-time PCR-based assay for detection of Wuchereria bancrofti DNA in blood and mosquitoes. Am J Trop Med Hyg 74(5):826–832
doi: 10.4269/ajtmh.2006.74.826 pubmed: 16687688
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(5):779–785
doi: 10.4269/ajtmh.2006.74.779 pubmed: 16687680
Katholi CR, Toé 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(5):1414–1417. https://doi.org/10.1093/infdis/172.5.1414
doi: 10.1093/infdis/172.5.1414 pubmed: 7594692
Ministry of Health and Family Welfare (India). Ministry of Health & Family Welfare launches nationwide (LF); 2023 [Cited 2023 June 11]. [Internet]. https://pib.gov.in/PressReleasePage.aspx?PRID=1898214
Subramanian S, Krishnamoorthy K, Ramaiah KD, Habbema JD, Das PK, Plaisier AP (1998) The relationship between microfilarial load in the human host and uptake and development of Wuchereria bancrofti microfilariae by Culex quinquefasciatus: a study under natural conditions. Parasitology 116(Pt 3):243–255. https://doi.org/10.1017/s0031182097002254
doi: 10.1017/s0031182097002254 pubmed: 9550218
Erickson SM, Fischer K, Weil GJ, Christensen BM, Fischer PU (2009) Distribution of Brugia malayi larvae and DNA in vector and non-vector mosquitoes: implications for molecular diagnostics. Parasit Vectors 2(1):56. https://doi.org/10.1186/1756-3305-2-56
doi: 10.1186/1756-3305-2-56 pubmed: 19922607 pmcid: 2781795
Fischer P, Erickson SM, Fischer K, Fuchs JF, Rao RU, Christensen BM, Weil GJ (2007) Persistence of Brugia malayi DNA in vector and non-vector mosquitoes: implications for xenomonitoring and transmission monitoring of lymphatic filariasis. Am J Trop Med Hyg 76(3):502–507
doi: 10.4269/ajtmh.2007.76.502 pubmed: 17360875
AmuzuH, Wilson MD, Boakye DA (2010) Studies of Anopheles gambiae s.l (Diptera: Culicidae) exhibiting different vectorial capacities in lymphatic filariasis transmission in the Gomoa district. Ghana Parasit Vectors 3:85. https://doi.org/10.1186/1756-3305-3-85
doi: 10.1186/1756-3305-3-85 pubmed: 20840757
Ughasi J, Bekard HE, Coulibaly M, Adabie-Gomez D, Gyapong J, Appawu M, Wilson MD, Boakye DA (2012) Mansonia africana and Mansonia uniformis are vectors in the transmission of Wuchereria bancrofti lymphatic filariasis in Ghana. Parasit Vectors 5:89. https://doi.org/10.1186/1756-3305-5-89
de Souza DK, Koudou B, Kelly-Hope LA, Wilson MD, Bockarie MJ, Boakye DA (2012) Diversity and transmission competence in lymphatic filariasis vectors in West Africa, and the implications for accelerated elimination of Anopheles-transmitted filariasis. Parasit Vectors 5:259. https://doi.org/10.1186/1756-3305-5-259
doi: 10.1186/1756-3305-5-259 pubmed: 23151383 pmcid: 3533928
Anosike JC, Nwoke BE, Ajayi EG, Onwuliri CO, Okoro OU, Oku EE, Asor JE, Amajuoyi OU, Ikpeama CA, Ogbusu FI, Meribe CO (2005) Lymphatic filariasis among the Ezza people of Ebonyi State, eastern Nigeria. Ann Agric Environ Med 12(2):181–186
pubmed: 16457471
Agi PI, Ebenezer A (2009) Observations on filarial infection in Amassoma community in the Niger Delta. Nigeria J Appl SCI Environ Manag 13(1)
Atmosoedjono S, Dennis DT (1977) Anopheles Aconitus and An. Subpictus naturally infected with Wuchereria bancrofti in Flores. Indonesia Mosq News 37(3)
Hoedojo, Partono F, Atmosoedjono S, Purnomo, Teren T (1980) A study on vectors of bancroftian filariasis in West Flores, Indonesia. Southeast Asian J Trop Med Public Health 11(3):399–404
pubmed: 7003734
Lee VH, Atmosoedjono S, Dennis DT, Suhaepi A, Suwarta A (1983) The anopheline (Diptera: Culicidae) vectors of malaria and bancroftian filariasis in Flores Island, Indonesia. J Med Entomo 20(5):577–578. https://doi.org/10.1093/jmedent/20.5.577
doi: 10.1093/jmedent/20.5.577
Dorkenoo MA, de Souza DK, Apetogbo Y, Oboussoumi K, Yehadji D, Tchalim M, Etassoli S, Koudou B, Ketoh GK, Sodahlon Y, Bockarie MJ, Boakye DA (2018) Molecular xenomonitoring for post-validation surveillance of lymphatic filariasis in Togo: no evidence for active transmission. Parasit Vectors 11(1):52. https://doi.org/10.1186/s13071-017-2611-9
doi: 10.1186/s13071-017-2611-9 pubmed: 29361964 pmcid: 5781303
Ramesh D, Muniaraj M, Samuel PP, Thenmozhi V, Venkatesh A, Nagaraj J, Tyagi BK (2015) Seasonal abundance & role of predominant Japanese encephalitis vectors Culex Tritaeniorhynchus & Cx. Gelidus Theobald in Cuddalore district, Tamil Nadu. Indian J Med Res 142(Suppl 1):S23–S29. https://doi.org/10.4103/0971-5916.176607
doi: 10.4103/0971-5916.176607 pubmed: 26905238 pmcid: 4795343
Schmaedick M A, Koppel A L, Pilotte N, Torres M, Williams S A, Dobson S L, … Won K Y (2014). Molecular xenomonitoring using mosquitoes to map lymphatic filariasis after mass drug administration in American Samoa. PLoS Negl Trop Dis 8(8):e3087. https://doi.org/10.1371/journal.pntd.0003087
Sinha A, Kumar S, Dayal D, Yadav V, Pramanik A, Chaubey KK, Kumar S (2023) Elimination of lymphatic filariasis: where do we stand so far? Asian Pac J Trop Med 16(9):385–399. https://doi.org/10.4103/1995-7645.380729
doi: 10.4103/1995-7645.380729
Pryce J, Reimer LJ (2021) Evaluating the diagnostic test accuracy of molecular xenomonitoring methods for characterizing community burden of lymphatic filariasis. Clin Infect Dis 72(Supplement3):S203–S209. https://doi.org/10.1093/cid/ciab197
doi: 10.1093/cid/ciab197 pubmed: 33906238 pmcid: 8201559
Pryce J, Unnasch TR, Reimer LJ (2021) Evaluating the diagnostic test accuracy of molecular xenomonitoring methods for characterising the community burden of Onchocerciasis. PLoS Negl Trop Dis 15(10):e0009812. https://doi.org/10.1371/journal.pntd.0009812
doi: 10.1371/journal.pntd.0009812 pubmed: 34637436 pmcid: 8509893
Meetham P, Kumlert R, Gopinath D, Yongchaitrakul S, Tootong T, Rojanapanus S, Padungtod C (2023) Five years of post-validation surveillance of lymphatic filariasis in Thailand. Infect Dis Poverty 12(1):113. https://doi.org/10.1186/s40249-023-01158-0
doi: 10.1186/s40249-023-01158-0 pubmed: 38053222 pmcid: 10698969
Premkumar A, Shriram AN, Krishnamoorthy K, Subramanian S, Vasuki V, Vijayachari P, Jambulingam P (2020) Molecular xenomonitoring of diurnally subperiodic Wuchereria bancrofti infection in Aedes (Downsiomyia) niveus (Ludlow, 1903) after nine rounds of Mass Drug Administration in Nancowry Islands, Andaman and Nicobar Islands, India. PLoS Negl Trop Dis 14(10):e0008763 https://doi.org/10.1371/journal.pntd.0008763
Coulibaly S, Sawadogo SP, Hien AS, Nikièma AS, Sangaré I, Rabila B, … Dabiré RK (2021)Malaria and lymphatic filariasis co-transmission in endemic health districts in Burkina Faso. Adv. entomol 9(4):155–175. https://doi.org/10.4236/ae.2021.94014
Araújo TAD, Lima de Albuquerque A, Melo DCTVD, Santos EMDM, Oliveira ALSD, Ayres CFJ, Oliveira CMFD (2023) Detection of Wuchereria bancrofti in the city of São Luís, state of Maranhão, Brazil: New incursion or persisting problem? PLoS Negl Trop Dis 17(1):e0011091. https://doi.org/10.1371/journal.pntd.0011091
doi: 10.1371/journal.pntd.0011091 pubmed: 36716339 pmcid: 9910792
Kinyatta N, Wachira D, Githae R, Lusweti J, Ingonga J, Ichugu C, Kamau L (2023) Detection of Wuchereria bancrofti in human blood samples and mosquitoes in Matayos, Busia County-Kenya. Sci Rep 13(1):19420. https://doi.org/10.1038/s41598-023-46329-z
doi: 10.1038/s41598-023-46329-z pubmed: 37940673 pmcid: 10632445
Lupenza E, Gasarasi DB, Minzi OM (2021) Lymphatic filariasis, infection status in Culex quinquefasciatus and Anopheles species after six rounds of mass drug administration in Masasi District, Tanzania. Infect Dis Poverty 10:1–11. https://doi.org/10.1186/s40249-021-00808-5
doi: 10.1186/s40249-021-00808-5
Njenga SM, Kanyi HM, Mwatele CM, Mukoko DA, Bockarie MJ, Kelly-Hope LA (2022) Integrated survey of helminthic neglected tropical diseases and comparison of two mosquito sampling methods for lymphatic filariasis molecular xenomonitoring in the River Galana area, Kilifi County, coastal Kenya. PLoS ONE 17(12):e0278655. https://doi.org/10.1371/journal.pone.0278655
doi: 10.1371/journal.pone.0278655 pubmed: 36490233 pmcid: 9733851
Bhuvaneswari A, Shriram AN, Raju KHK, Kumar A (2023) Mosquitoes, Lymphatic Filariasis, and Public Health: A Systematic Review of Anopheles and Aedes Surveillance Strategies. Pathogens 12(12):1406. https://doi.org/10.3390/pathogens12121406
Panda BB, Krishnamoorthy K, Das A, Jain HK, Dixit S, Rahi M, … Bal M (2023) Mini-TAS as a confirmatory mapping tool for remapping areas with uncertain filarial endemicity to exclude/include for mass drug administration: A report from field validation in India. PLoS One 18(11):e0293641. https://doi.org/10.1371/journal.pone.0293641

Auteurs

Balasubramaniyan Ramalingam (B)

ICMR-Vector Control Research Centre, Puducherry 605006, India. balasubramaniyan_ram@yahoo.com.

Vasuki Venkatesan (V)

ICMR-Vector Control Research Centre, Puducherry 605006, India.

Philip Raj Abraham (PR)

ICMR-Vector Control Research Centre, Puducherry 605006, India.

Srividya Adinarayanan (S)

ICMR-Vector Control Research Centre, Puducherry 605006, India.

Subramanian Swaminathan (S)

ICMR-Vector Control Research Centre, Puducherry 605006, India.

Konuganti Hari Kishan Raju (KHK)

ICMR-Vector Control Research Centre, Puducherry 605006, India.

Sugeerappa Laxmanappa Hoti (SL)

ICMR-Vector Control Research Centre, Puducherry 605006, India.

Ashwani Kumar (A)

Centre for Global Health Research, Saveetha Medical College and Hospital, Saveetha Institute of Medical and Technical Sciences, Saveetha University, Chennai 605102, India.

Classifications MeSH