Elimination of lymphatic filariasis: Where do we stand so far?

Abstract

Lymphatic filariasis (LF), an asymptomatic, acute, and chronic condition in human beings, is the second most common vector-borne disease after malaria. According to the World Health Organization, there are 120 million LF cases detected in 81 tropical and subtropical countries, and one billion people are at risk. Therefore, the Global Program to Eliminate Lymphatic Filariasis was launched in 2000, with the primary objective of stopping LF transmission among all at-risk groups using mass drug administration (MDA), managing morbidities, and preventing LF-related impairments using a minimum treatment package. Additionally, other programs such as epidemiological assessment including National Filaria Control Program and World Health Organization recommended routine and pre-MDA microfilaremia surveys also implemented to stop the LF transmission. The routine filaria surveys were also carried out in around 2 000-4 000 individuals/month throughout the year whereas pre-MDA surveys were also conducted every year in approximately 4 000 individuals in four fixed and four random sites. Furthermore, the Transmission Assessment Survey was also conducted to check the risk of LF among primary school children. Moreover, potential diagnostic methods, systematic surveillance regimes, the Direct Network Report system, and regular trainings and awareness may be also effective in preventing the recurrence of LF. Hence, this review emphasizes the potential advocacy tools and various strategies as well as procedures for monitoring, which could be impactful in eliminating LF.

Keywords

Lymphatic filariasis / Treatment / Challenges / Prospect / Elimination

References

[1] Gyapong JO, Owusu IO, da-Costa Vroom FB, Mensah EO, Gyapong M. Elimination of lymphatic filariasis: Current perspectives on mass drug administration. Res Rep Trop Med 2018; 9:25.

[2] Ghosh SK, Srivastava PK, Ghosh SK, Srivastava PK. A new outlook in lymphatic filariasis elimination in India. Parasitol Microbiol Res 2020. doi: 10.5772/INTECHOPEN.92454.

[3] WHO. Lymphatic filariasis: Fourth report of the WHO expert committee on filariasis. World Health Organ Tech Rep Ser 1984; 702:3-112.

[4] Chakraborty S, Gurusamy M, Zawieja DC, Muthuchamy M. Lymphatic filariasis: Perspectives on lymphatic remodeling and contractile dysfunction in filarial disease pathogenesis. Microcirculation 2013; 20(5):349.

[5] CDC. Lymphatic filariasis. 2021. [Online]. Available from:https://www.cdc.gov/parasites/lymphaticfilariasis/index.html. [Accessed on 11 April 2023].

[6] Agrawal VK, Sashindran VK. Lymphatic filariasis in India: Problems, challenges and new initiatives. Med J Armed Forces India 2006; 62(4):359.

[7] WHO. Morbidity management and disability prevention (MMDP). [Online]. Available from:https://www.who.int/activities/building-capacity-of-national-programmes-to-implement-who-recommended-strategies/morbidity-management-and-disability-prevention. [Accessed on 11 April 2023].

[8] Bizhani N, Hashemi Hafshejani S, Mohammadi N, Rezaei M, Rokni MB. Lymphatic filariasis in Asia: A systematic review and meta-analysis. Parasitol Res 2021; 120(2):411-422.

[9] Laman M, Tavul L, Karl S, Kotty B, Kerry Z, Kumai S, et al. Mass drug administration of ivermectin, diethylcarbamazine, plus albendazole compared with diethylcarbamazine plus albendazole for reduction of lymphatic filariasis endemicity in Papua New Guinea: A cluster-randomised trial. Lancet Infect Dis 2022; 22(8):1200.

[10] CDC. Lymphatic filariasis-diagnosis. 2019. [Online]. Available from:https://www.cdc.gov/parasites/lymphaticfilariasis/diagnosis.html. [Accessed on 11 April 2023].

[11] Fimbo AM, Minzi OMS, Mmbando BP, Barry A, Nkayamba AF, Mwamwitwa KW, et al. Prevalence and correlates of lymphatic filariasis infection and its morbidity following mass ivermectin and albendazole administration in Mkinga District, North-Eastern Tanzania. J Clin Med 2020; 9(5):1550.

[12] WHO. Control of Neglected Tropical Diseases. [Online]. Available from:https://www.who.int/teams/control-of-neglected-tropical-diseases/lymphatic-filariasis/diagnosis-and-treatment. [Accessed on 23 February 2023].

[13] McConnaughey M. Life cycle of parasites. Scofield: xPharm. The Comprehensive Pharmacology Reference; 2007. p, 1-15.

[14] Newman TE, Juergens AL. Filariasis. Treasure Island (FL): StatPearls Publishing; 2022.

[15] Specht S, Suma TK, Pedrique B, Hoerauf A. Elimination of lymphatic filariasis in South East Asia. BMJ 2019; 364:k5198.

[16] Sun DJ, Deng XL, Duan JH. The history of the elimination of lymphatic filariasis in China. Infect Dis Poverty 2013; 2(1):1-9.

[17] Patrick Manson. On the development of Filaria sanguinis hominis, and on the mosquito considered as a nurse. J Linnean Soc London Zool 1878; XIV:304-311.

[18] Correia M, Amonkar D, Audi P, Bhat C, Cruz P, Mitta N, et al. Filariasis in the arm-a diagnostic enigma! Internet J Surgery 2009; 25(2). doi: 10.5580/A3586.

[19] Sabesan S, Palaniyandi M, Das PK, Michael E. Mapping of lymphatic filariasis in India. Ann Trop Med Parasitol 2000; 94(6):591-606.

[20] Xavier A, Bonfim C, Medeiros Z. Socio-environmental risk indicator: A possible tool for surveillance of lymphatic filariasis. Iran J Parasitol 2023; 18(1):132-134.

[21] International Conference on Multimedia Retrieval. Prospects of elimination of lymphatic filariasis in India. ICMR Bull 2002; 32(5&6):1-14.

[22] Cross JH. Filarial nematodes. Galveston (TX): University of Texas Medical Branch at Galveston; 1996.

[23] Pantelias A, King JD, Lammie P, Weil GJ. Development and introduction of the filariasis test strip: A new diagnostic test for the global program to eliminate lymphatic filariasis. Am J Trop Med Hyg 2022; 106(5_Suppl):56-60.

[24] Babu S, Nutman TB. Immunology of lymphatic filariasis. Parasite Immunol 2014; 36(8):338-346.

[25] Reichwald JJ, Risch F, Neumann AL, Frohberger SJ, Scheunemann JF, Lenz B, et al. ILC2s control microfilaremia during litomosoides sigmodontis infection in Rag²-/- mice. Front Immunol 2022; doi: https://doi.org/10.3389/fimmu.2022.863663.

[26] Ganga L, Sharma P, Tiwari S, Satoeya N, Jha R, Srivastava M. Immunophenotypic and functional characterization of eosinophil and migratory dendritic cell subsets during filarial manifestation of tropical pulmonary eosinophilia. ACS Infect Dis 2023; 9(5):1105-1122.

[27] Grover P, Goel PN, Greene MI. Regulatory T cells: Regulation of identity and function. Front Immunol 2021; 12:750542.

[28] Kondĕlková K, Vokurková D, Krejsek J, Borská L, Fiala Z, Ctirad A. Regulatory T cells (TREG) and their roles in immune system with respect to immunopathological disorders. Acta Medica (Hradec Kralove) 2010; 53(2):73-77.

[29] Adinarayanan S, Critchley J, Das PK, Gelband H. Diethylcarbamazine (DEC)-medicated salt for community-based control of lymphatic filariasis. Cochrane Database System Rev 2007; doi: 10.1002/14651858.CD003758.PUB2.

[30] Macfarlane CL, Budhathoki SS, Johnson S, Richardson M, Garner P. Albendazole alone or in combination with microfilaricidal drugs for lymphatic filariasis. Cochrane Database System Rev 2019; doi: 10.1002/14651858.CD003753.PUB4.

[31] Kareh AM, Xu KY. Surgical management of lymphedema. Missouri Med 2020; 117(2):143.

[32] Medeiros ZM, Vieira AVB, Xavier AT, Bezerra GSN, Lopes M de FC, Bonfim CV, et al. Lymphatic filariasis: A systematic review on morbidity and its repercussions in countries in the americas. Intern J Environ Res Public Health 2022; doi: 10.3390/IJERPH19010316/S1.

[33] De Silva N, Guyatt H, Bundy D. Anthelmintics. A comparative review of their clinical pharmacology. Drugs 1997; 53(5):769-788.

[34] Nandha B, Sadanandane C, Jambulingam P, Das PK. Delivery strategy of mass annual single dose DEC administration to eliminate lymphatic filariasis in the urban areas of Pondicherry, South India: 5 years of experience. Filaria J 2007; 6:7.

[35] Mani TR, Rajendran R, Sunish IP, Munirathinam A, Arunachalam N, Satyanarayana K, et al. Effectiveness of two annual, single-dose mass drug administrations of diethylcarbamazine alone or in combination with albendazole on soil-transmitted helminthiasis in filariasis elimination programme. Trop Med Intern Health 2004; 9(9):1030-1035.

[36] Dobashi K. Changes in serum cholesterol in childhood and its tracking to adulthood. J Atherosclerosis Thrombosis 2022; 29(1):5.

[37] Rajendran R, Sunish IP, Mani TR, Munirathinam A, Abdullah SM, Arunachalam N, et al. Impact of two annual single-dose mass drug administrations with diethylcarbamazine alone or in combination with albendazole on Wuchereria bancrofti microfilaraemia and antigenaemia in South India. Transac Royal Soc Trop Med Hyg 2004; 98(3):174-181.

[38] Laigret J, Fagneaux G, Tuira E. Chimiothérapie de masse par la diéthylcarbamazine en doses espacées: Effets obtenus à tahiti sur la microfilarémie à Wuchereria bancrofti, var. pacifica. Bull World Health Organization 1980; 58(5):779.

[39] Ottesen EA. Efficacy of diethylcarbamazine in eradicating infection with lymphatic-dwelling filariae in humans. Rev Infect Dis 1985; 7(3):341-356.

[40] Ottesen EA, Campbell W. Ivermectin in human medicine. J Antimicrob Chemother 1994; 34(2):195-203.

[41] Brown KR, Ricci FM, Ottesen EA. Ivermectin: Effectiveness in lymphatic filariasis. Parasitology 2000; doi: 10.1017/S0031182000006570.

[42] Rossignol JF, Maisonneuve H. Albendazole: Placebo-controlled study in 870 patients with intestinal helminthiasis. Transac Royal Soci Trop Med Hyg 1983; 77(5):707-711.

[43] Shenoy RK, Suma TK, John A, Arun SR, Kumaraswami V, Fleckenstein LL, et al. The pharmacokinetics, safety and tolerability of the co-administration of diethylcarbamazine and albendazole. Ann Trop Med Parasitol 2013; 96(6):603-614.

[44] Canga AG, Prieto AMS, Diez Liébana MJ, Martínez NF, Sierra Vega M, García Vieitez JJ. The pharmacokinetics and interactions of ivermectin in humans-a mini-review. AAPS J 2008; 10(1):42.

[45] Weil GJ, Jacobson JA, King JD. A triple-drug treatment regimen to accelerate elimination of lymphatic filariasis: From conception to delivery. Intern Health 2021; 13(Suppl 1):S60.

[46] Weil GJ, Bogus J, Christian M, Dubray C, Djuardi Y, Fischer PU, et al. The safety of double- and triple-drug community mass drug administration for lymphatic filariasis: A multicenter, open-label, cluster-randomized study. PLoS Med 2019; doi: 10.1371/JOURNAL.PMED.1002839.

[47] Tripathi B, Roy N, Dhingra N. Introduction of triple-drug therapy for accelerating lymphatic filariasis elimination in India: Lessons learned. Am J Trop Med Hyg 2022; 106(5_Suppl):29-38.

[48] Rainima-Qaniuci M, Lepaitai HB, Bhagirov R, Padmasiri E, Naseri T, Thomsen R, et al. The importance of partnership in the rollout of triple-drug therapy to eliminate lymphatic filariasis in the Pacific. Am J Trop Med Hyg 2022; 106(Suppl 5):39.

[49] Budge PJ, Herbert C, Andersen BJ, Weil GJ. Adverse events following single dose treatment of lymphatic filariasis: Observations from a review of the literature. PLoS Negl Trop Dis 2018; doi:10.1371/JOURNAL.PNTD.0006454.

[50] Fang Y, Zhang Y. Lessons from lymphatic filariasis elimination and the challenges of post-elimination surveillance in China. Infect Dis Poverty 2019; 8(1). doi: 10.1186/S40249-019-0578-9.

[51] WHO. Global programme to eliminate lymphatic filariasis: Progress report, 2020. [Online]. Available from:https://www.who.int/publications-detail-redirect/who-wer9641-497-508. [Accessed on 23 February 2023].

[52] Collyer BS, Irvine MA, Hollingsworth TD, Bradley M, Anderson RM. Defining a prevalence level to describe the elimination of lymphatic filariasis (LF) transmission and designing monitoring & evaluating (M&E) programmes post the cessation of mass drug administration (MDA). PLoS Negl Trop Dis 2020; 14(10):e0008644.

[53] Press Information Bureau. Press Releases Details. [Online]. Available from:https://pib.gov.in/PressReleseDetail.aspx?PRID=1890935. [Accessed on 9 April 2023].

[54] Kumar D, Kumar A, Vikas K, Kumar C, Sircar S. Coverage of mass drug administration (MDA) and operational issues in elimination of lymphatic filariasis in selected districts of Jharkhand, India. J Family Med Prim Care 2023; 12(1):111-116.

[55] National Center for Vector Borne Diseases Control. Elimination of lymphatic filariasis. [Online]. Available from:https://nvbdcp.gov.in/index4.php?lang=1&level=0&linkid=461&lid=3739 [Accessed 24 January 2023].

[56] Kulkarni P, Kumar R, Rajegowda R, Channabasappa H, Ashok NC. MDA Program against lymphatic filariasis: Are we on the path to success? Experience from Uttara Kannada District, Karnataka. Intern J Med Public Health 2014; 4(3):243.

[57] Kulkarni P, Amoghashree SKY, Murthy MRN, Kumar KR. Coverage and compliance towards mass drug administration programme against lymphatic filariasis in Vijayapura (Bijapur) district, Karnataka, India. Intern J Comm Med Public Health 2018; 5(10):4311.

[58] Addiss DG, Beach MJ, Streit TG, Lutwick S, Leconte FH, Lafontant JG, et al. Randomised placebo-controlled comparison of ivermectin and albendazole alone and in combination for Wuchereria bancrofti microfilaraemia in Haitian children. Lancet 1997; 350(9076):480-484.

[59] Shenoy RK, Suma TK, Kumaraswami V, Rahmah N, Dhananjayan G, Padma S, et al. Preliminary findings from a cross-sectional study on lymphatic filariasis in children, in an area of India endemic for Brugia malayi infection. Ann Trop Med Parasitol 2007; 101(3):205-213.

[60] Ghosh SK. Human dirofilariasis: A fast emerging zoonosis in India. Indian J Med Microbiol 2015; 33(4):595-596.

[61] Wynd S, Melrose WD, Durrheim DN, Carron J, Gyapong M. Understanding the community impact of lymphatic filariasis: A review of the sociocultural literature. Bull World Health Organization 2007; 85(6):493-498.

[62] Sun C. Barriers to the elimination of lymphatic filariasis in Sub-Saharan Africa. Columbia Univ J Global Health 2015; 5(1):26-32.

[63] Gyapong M, Gyapong J, Weiss M, Tanner M. The burden of hydrocele on men in Northern Ghana. Acta Trop 2000; 77(3):287-294.

[64] Bandyopadhyay L. Lymphatic filariasis and the women of India. Social Sci Med 1996; 42(10):1401-1410.

[65] Jones C, Ngasala B, Derua YA, Tarimo D, Reimer L, Bockarie M, et al. Lymphatic filariasis transmission in Rufiji District, southeastern Tanzania: Infection status of the human population and mosquito vectors after twelve rounds of mass drug administration 11 Medical and Health Sciences 1 117 Public Health and Health Services. Parasit Vectors 2018; 11(1):1-8.

[66] Evans DB, Gelband H, Vlassoff C. Social and economic factors and the control of lymphatic filariasis: A review. Acta Trop 1993; 53(1):1-26.

[67] Sinka ME, Bangs MJ, Manguin S, Coetzee M, Mbogo CM, Hemingway J, et al. The dominant Anopheles vectors of human malaria in Africa, Europe and the Middle East: Occurrence data, distribution maps and bionomic précis. Parasit Vectors 2010; 3(1):1-34.

[68] Drake JM, Beier JC. Ecological niche and potential distribution of Anopheles arabiensis in Africa in 2050. Malar J 2014; 13(1):1-12.

[69] Uttah EC, Wokem GN, Okonofua C. The abundance and biting patterns of Culex quinquefasciatus say (Culicidae) in the coastal region of Nigeria. ISRN Zool 2013; 2013:1-7.

[70] Simonsen PE, Mwakitalu ME. Urban lymphatic filariasis. Parasitol Res 2013; 112(1):35-44.

[71] Derua YA, Alifrangis M, Hosea KM, Meyrowitsch DW, Magesa SM, Pedersen EM, et al. Change in composition of the Anopheles gambiae complex and its possible implications for the transmission of malaria and lymphatic filariasis in north-eastern Tanzania. Malar J 2012; 11(1):1-9.

[72] Mahande A, Mosha F, Mahande J, Kweka E. Feeding and resting behaviour of malaria vector, Anopheles arabiensis with reference to zooprophylaxis. Malar J 2007; 6(1):1-6.

[73] Mburu MM, Zembere K, Mzilahowa T, Terlouw AD, Malenga T, van den Berg H, et al. Impact of cattle on the abundance of indoor and outdoor resting malaria vectors in southern Malawi. Malar J 2021; 20(1):353.

[74] Hunter JM. Elephantiasis: A disease of development in North East Ghana. Soc Sci Med 1992; 35(5):627-645.

[75] Gambhir M, Bockarie M, Tisch D, Kazura J, Remais J, Spear R, et al. Geographic and ecologic heterogeneity in elimination thresholds for the major vector-borne helminthic disease, lymphatic filariasis. BMC Biol 2010; 8(1):1-13.

[76] Gambhir M, Michael E. Complex ecological dynamics and eradicability of the vector borne macroparasitic disease, lymphatic filariasis. PLoS One 2008; 3(8):e2874.

[77] Shin SJ, Cho D, Collins MT. Diagnosis of bovine paratuberculosis by a novel enzyme-linked immunosorbent assay based on early secreted antigens of Mycobacterium avium subsp. paratuberculosis. Clin Vacc Immunol 2008; 15(8):1277.

[78] Duerr HP, Dietz K, Eichner M. Determinants of the eradicability of filarial infections: A conceptual approach. Trends Parasitol 2005; 21(2):88-96.

[79] Bockarie MJ, Pedersen EM, White GB, Michael E. Role of vector control in the global program to eliminate lymphatic filariasis. Ann Rev Entomol 2009; 54:469-487.

[80] Rwegoshora RT, Pedersen EM, Mukoko DA, Meyrowitsch DW, Masese N, Malecela-Lazaro MN, et al. Bancroftian filariasis: Patterns of vector abundance and transmission in two East African communities with different levels of endemicity. Ann Trop Med Parasitol 2005; 99(3):253-265.

[81] Parker M, Allen T. Will mass drug administration eliminate lymphatic filariasis? Evidence from northern coastal Tanzania. J Biosoc Sci 2013; 45(4):517.

[82] Ottesen EA, Hooper PJ, Bradley M, Biswas G. The Global Programme to eliminate lymphatic filariasis: Health impact after 8 years. PLoS Negl Trop Dis 2008; 2(10):e317.

[83] Healthcare World. Dr Harsh Vardhan announces scale up of triple drug therapy to achieve the elimination of lymphatic filariasis by 2021-BW Healthcare. [Online]. Available from:http://bwhealthcareworld.businessworld.in/article/Dr-Harsh-Vardhan-announces-scale-up-of-triple-drug-therapy-to-achieve-the-elimination-of-lymphatic-filariasis-by-2021-/30-10-2019-178264/. [Accessed on 26 January 2023].

[84] Wilson AL, Courtenay O, Kelly-Hope LA, Scott TW, Takken W, Torr SJ, et al. The importance of vector control for the control and elimination of vector-borne diseases. PLoS Negl Trop Dis 2020; 14(1):1-31.

[85] Lobo NF, Achee NL, Greico J, Collins FH. Modern vector control. Cold Spring Harbor Persp Med 2018; doi: 10.1101/CSHPERSPECT.A025643.

[86] Sumption K, Domenech J, Ferrari G. Progressive control of FMD on a global scale. Vet Rec 2012; 170(25):637-639.

[87] Deshpande A, Miller-Petrie MK, Johnson KB, Abdoli A, Abrigo MRM, Adekanmbi V, et al. The global distribution of lymphatic filariasis, 2000-18: A geospatial analysis. Lancet Global Health 2020; 8(9):e1186-e1194.

[88] Fan PC. Elimination of bancroftian filariasis by diethylcarbamazine-medicated common salt on Little Kinmen (Liehyu District), Kinmen (Quemoy) Islands, Republic of China. Ann Trop Med Parasitol 1990; 84(1):25-33.

[89] Ichimori K, King JD, Engels D, Yajima A, Mikhailov A, Lammie P, et al. Global programme to eliminate lymphatic filariasis: The processes underlying programme success. PLoS Negl Trop Dis 2014; doi: 10.1371/journal.pntd.0003328.

[90] Shaw C, McLure A, Graves PM, Lau CL, Glass K. Lymphatic filariasis endgame strategies: Using GEOFIL to model mass drug administration and targeted surveillance and treatment strategies in American Samoa. PLoS Negl Trop Dis 2023; 17(5):e0011347.

[91] WHO. Preventive chemotherapy. [Online]. Available from:https://www.who.int/data/preventive-chemotherapy. [Accessed on 18 October 2022].

[92] Ottesen EA, Hooper PJ, Bradley M, Biswas G. The global programme to eliminate lymphatic filariasis. PLoS Negl Trop Dis 2008; 2(10):e317. doi: 10.1371/journal.pntd.0000317.

[93] Kalyanasundaram R, Khatri V, Chauhan N. Advances in vaccine development for human lymphatic filariasis. Trends Parasitol 2020; 36(2):195.

[94] Chen H, Liu K, Li Z, Wang P. Point of care testing for infectious diseases. Intern J Clin Chem 2019; 493:138.

[95] Abdulmalik J, Nwefoh E, Obindo J, Dakwak S, Ayobola M, Umaru J, et al. Emotional difficulties and experiences of stigma among persons with lymphatic filariasis in Plateau State, Nigeria. Health Human Rights 2018; 20(1):27.

[96] Macfarlane CL, Budhathoki SS, Johnson S, Richardson M, Garner P. Albendazole alone or in combination with microfilaricidal drugs for lymphatic filariasis. Cochrane Database System Rev 2019; doi: 10.1002/14651858.CD003753.PUB4.