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Lymphatic filariasis in children: Clinical features, infection burdens and future prospects for elimination

Published online by Cambridge University Press:  03 August 2011

RANGANATHA KRISHNA SHENOY
Affiliation:
Filariasis Chemotherapy Unit, TD Medical College Hospital, Alappuzha 688 011, Kerala, India
MOSES J. BOCKARIE*
Affiliation:
Centre for Neglected Tropical Diseases, Liverpool School of Tropical Medicine, Pembroke Place, Liverpool, L3 5QA, UK
*
*Corresponding author: Centre for Neglected Tropical Diseases, Liverpool School of Tropical Medicine, Pembroke Place, Liverpool, L3 5QA, UK. Phone: +44(0)1517053343. Fax: +44(0)151 7053370. Mobile: +44 07595020694. E-mail: [email protected]

Summary

Lymphatic filariasis (LF), a common parasitic infection in tropical countries, causes lymphoedema of limbs, hydrocele and acute attacks of dermato-lymphangio-adenitis. Recent advances in diagnosis have helped to recognize that LF infection is often acquired in childhood. Newly available diagnostic techniques like sensitive antigen and antibody assays, Doppler ultrasonography and lymphoscintigraphy have helped to understand the subclinical pathology caused by this infection, which was hitherto generally believed to be irreversible. Recent studies indicate that drugs used in the mass drug administration (MDA) programme under GPELF are capable of reversing the sub-clinical lymphatic damage in children and provide benefits other than interruption of transmission. Albendazole and ivermectin used in MDA are effective against soil-transmitted helminthic infections common in children in LF endemic areas. Thus MDA had other ‘beyond LF’ benefits in treated children including increased appetite, weight gain, greater learning ability and concentration, better school attendance and prevention of anaemia. MDA should no longer be viewed as a measure for interrupting transmission alone. Recent findings of reversibility of early lymphatic pathology in treated children indicate that both MDA and ‘foot-hygiene’ measures are effective strategies in preventing and managing morbidity. Programme managers should effectively utilize this information to strengthen their advocacy efforts to achieve high and sustainable coverage in MDA.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2011

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References

REFERENCES

Adams, E. J., Stephenson, L. S., Latham, M. C. and Kinoti, S. N. (1994). Physical activity and growth of Kenyan school children with hookworm, Trichuris trichiura and Ascaris lumbricoides infections are improved after treatment with albendazole. Journal of Nutrition 124, 11991206.CrossRefGoogle ScholarPubMed
Alexander, N. D., Kazura, J. W., Bockarie, M. J., Perry, R. T., Dimber, Z. B., Grenfell, B. T. and Alpers, M. P. (1998). Parental infection confounded with local infection intensity as risk factors for childhood microfilaraemia in bancroftian filariasis. Transactions of the Royal Society of Tropical Medicine and Hygiene 92, 2324.CrossRefGoogle ScholarPubMed
Bockarie, M. J. and Molyneux, D. H. (2009). The end of lymphatic filariasis? British Medical Journal 338, b1686.CrossRefGoogle ScholarPubMed
Bockarie, M. J., Pedersen, E. M., White, G. B. and Michael, E. (2009). Role of vector control in the global program to eliminate lymphatic filariasis. Annual Review of Entomology 54, 469487. doi: 10.1146/annurev.ento.54.110807.090626.Google ScholarPubMed
Bockarie, M. J., Tisch, D. J., Kastens, W., Alexander, N. D., Dimber, Z., Bockarie, F., Ibam, E., Alpers, M. P. and Kazura, J. W. (2002). Mass treatment to eliminate filariasis in Papua New Guinea. New England Journal of Medicine 347, 18411848. doi: 10.1056/NEJMoa021309 347/23/1841 [pii].CrossRefGoogle ScholarPubMed
Das, P. K., Sirvidya, A., Vanamail, P., Ramaiah, K. D., Pani, S. P., Michael, E. and Bundy, D. A. (1997). Wuchereria bancrofti microfilaraemia in children in relation to parental infection status. Transactions of Royal Society of Tropical Medicine and Hygiene 91, 677679.CrossRefGoogle ScholarPubMed
de Silva, N. R., Brooker, S., Hotez, P. J., Montresor, A., Engels, D. and Savioli, L. (2003). Soil-transmitted helminth infections: updating the global picture. Trends in Parasitology 19, 547551. doi: S1471492203002757 [pii].CrossRefGoogle ScholarPubMed
Dreyer, G., Figueredo-Silva, J., Carvalho, K., Amaral, F. and Ottesen, E. A. (2001). Lymphatic filariasis in children: adenopathy and its evolution in two young girls. American Journal of Tropical Medicine and Hygiene 65, 204207.CrossRefGoogle ScholarPubMed
Dreyer, G., Noroes, J., Addiss, D., Santos, A., Medeiros, Z. and Figueredo-Silva, J. (1999). Bancroftian filariasis in a paediatric population: an ultrasonographic study. Transactions of Royal Society of Tropical Medicine and Hygiene 93, 633636.CrossRefGoogle Scholar
Figueredo-Silva, J., Dreyer, G., Guimaraes, K., Brandt, C. and Medeiros, Z. (1994). Bancroftian lymphadenopathy: absence of eosinophils in tissues despite peripheral blood hypereosinophilia. Journal of Tropical Medicine and Hygiene 97, 5559.Google ScholarPubMed
Figueredo-Silva, J., Noroes, J., Cedenho, A. and Dreyer, G. (2002). The histopathology of bancroftian filariasis revisited: the role of the adult worm in the lymphatic-vessel disease. Annals of Tropical Medicine & Parasitology 96, 531541. doi: 10.1179/000349802125001348.CrossRefGoogle ScholarPubMed
Fox, L. M., Furness, B. W., Haser, J. K., Brissau, J. M., Louis-Charles, J., Wilson, S. F., Addiss, D. G., Lammie, P. J. and Beach, M. J. (2005). Ultrasonographic examination of Haitian children with lymphatic filariasis: a longitudinal assessment in the context of antifilarial drug treatment. American Journal of Tropical Medicine and Hygiene 72, 642648. doi: 72/5/642 [pii].CrossRefGoogle ScholarPubMed
Freedman, D. O., Bui, T., De Almeida Filho, P. J., Braga, C., Maia e Silva, M. C., Maciel, A. and Furtado, A. F. (1995). Lymphoscintigraphic assessment of the effect of diethylcarbamazine treatment on lymphatic damage in human bancroftian filariasis. American Journal of Tropical Medicine and Hygiene 52, 258261.CrossRefGoogle ScholarPubMed
Freedman, D. O., de Almeida Filho, P. J., Besh, S., Maia e Silva, M. C., Braga, C. and Maciel, A. (1994). Lymphoscintigraphic analysis of lymphatic abnormalities in symptomatic and asymptomatic human filariasis. Journal of Infectious Diseases 170, 927933.Google ScholarPubMed
Gyapong, J. O., Kumaraswami, V., Biswas, G. and Ottesen, E. A. (2005). Treatment strategies underpinning the global programme to eliminate lymphatic filariasis. Expert Opinion Pharmacotherapy 6, 179200. doi: EOP060203 [pii] 10.1517/14656566.6.2.179.CrossRefGoogle ScholarPubMed
Jungmann, P., Figueredo-Silva, J. and Dreyer, G. (1991). Bancroftian lymphadenopathy: a histopathologic study of fifty-eight cases from northeastern Brazil. American Journal of Tropical Medicine and Hygiene 45, 325331.CrossRefGoogle ScholarPubMed
Knopp, S., Mohammed, K. A., Speich, B., Hattendorf, J., Khamis, I. S., Stothard, J. R., Rollinson, D., Marti, H. and Utzinger, J. (2010). Albendazole and mebendazole administered alone or in combination with ivermectin against Trichuris trichiura: a randomized controlled trial. Clinical Infectious Diseases 51, 14201428.CrossRefGoogle ScholarPubMed
Lammie, P. J., Hitch, W. L., Walker Allen, E. M., Hightower, W. and Eberhard, M. L. (1991). Maternal filarial infection as risk factor for infection in children. Lancet 337, 10051006.CrossRefGoogle ScholarPubMed
Lammie, P. J., Reiss, M. D., Dimock, K. A., Streit, T. G., Roberts, J. M. and Eberhard, M. L. (1998). Longitudinal analysis of the development of filarial infection and antifilarial immunity in a cohort of Haitian children. American Journal of Tropical Medicine and Hygiene 59, 217221.CrossRefGoogle Scholar
Mand, S., Supali, T., Djuardi, J., Kar, S., Ravindran, B. and Hoerauf, A. (2006). Detection of adult Brugia malayi filariae by ultrasonography in humans in India and Indonesia. Tropical Medicine and International Health 11, 13751381. doi: TMI1693 [pii]10.1111/j.1365-3156.2006.01693.x.CrossRefGoogle ScholarPubMed
March, H. N., Laigret, J., Kessel, J. F. and Bambridge, B. (1960). Reduction in the prevalence of clinical filariasis in Tahiti following adoption of a control program. American Journal of Tropical Medicine and Hygiene 9, 180184.Google ScholarPubMed
Meyrowitsch, D. W. and Simonsen, P. E. (1998). Long-term effect of mass diethylcarbamazine chemotherapy on bancroftian filariasis, results at four years after start of treatment. Transactions of the Royal Society of Tropical Medicine and Hygiene 92, 98103.CrossRefGoogle ScholarPubMed
Meyrowitsch, D. W., Simonsen, P. E. and Magesa, S. M. (2004). Long-term effect of three different strategies for mass diethylcarbamazine administration in bancroftian filariasis: follow-up at 10 years after treatment. Transactions of the Royal Society of Tropical Medicine and Hygiene 98, 627634. doi: 10.1016/j.trstmh.2004.01.004 S0035920304001300 [pii].CrossRefGoogle ScholarPubMed
Ottesen, E. A. (2000). The global programme to eliminate lymphatic filariasis. Tropical Medicine and International Health 5, 591594. doi: tmi620 [pii].CrossRefGoogle ScholarPubMed
Ottesen, E. A., Hooper, P. J., Bradley, M. and Biswas, G. (2008). The global programme to eliminate lymphatic filariasis: health impact after 8 years. PLOS Neglected Tropical Diseases 2, e317. doi: 10.1371/journal.pntd.0000317.CrossRefGoogle Scholar
Pani, S. P., Balakrishnan, N., Srividya, A., Bundy, D. A. and Grenfell, B. T. (1991). Clinical epidemiology of bancroftian filariasis: effect of age and gender. Transactions of Royal Society of Tropical Medicine and Hygiene 85, 260264.CrossRefGoogle ScholarPubMed
Pani, S. P., Yuvaraj, J., Vanamail, P., Dhanda, V., Michael, E., Grenfell, B. T. and Bundy, D. A. (1995). Episodic adenolymphangitis and lymphoedema in patients with bancroftian filariasis. Transactions of Royal Society of Tropical Medicine and Hygiene 89, 7274.CrossRefGoogle ScholarPubMed
Ramaiah, K. D., Ramu, K., Kumar, K. N. and Guyatt, H. (1996). Epidemiology of acute filarial episodes caused by Wuchereria bancrofti infection in two rural villages in Tamil, Nadu, south India. Transactions of Royal Society of Tropical Medicine and Hygiene 90, 639643.CrossRefGoogle ScholarPubMed
Ramaiah, K. D., Vanamail, P. and Das, P. K. (2007). Changes in Wuchereria bancrofti infection in a highly endemic community following 10 rounds of mass administration of diethylcarbamazine. Transactions of Royal Society of Tropical Medicine and Hygiene 101, 250255. doi: S0035-9203(06)00196-9 [pii] 10.1016/j.trstmh.2006.05.007.CrossRefGoogle Scholar
Ramaiah, K. D., Vanamail, P., Pani, S. P., Yuvaraj, J. and Das, P. K. (2002). The effect of six rounds of single dose mass treatment with diethylcarbamazine or ivermectin on Wuchereria bancrofti infection and its implications for lymphatic filariasis elimination. Tropical Medicine and International Health 7, 767774. doi: 935 [pii].CrossRefGoogle ScholarPubMed
Ramaiah, K. D. and Vijay Kumar, K. N. (2000). Effect of lymphatic filariasis on school children. Acta Tropica 76, 197199. doi: S0001-706X(00)00102-9 [pii].CrossRefGoogle ScholarPubMed
Rahmah, N., Shenoy, R. K., Nutman, T. B., Weiss, N., Gilmour, K., Maizels, R. M., Yazdanbakhsh, M. and Sartono, E. (2003). Multicentre laboratory evaluation of Brugia Rapid dipstick test for detection of brugian filariasis. Tropical Medicine and International Health 8, 895900. doi: 1102 [pii].CrossRefGoogle ScholarPubMed
Rahmah, N., Taniawati, S., Shenoy, R. K., Lim, B. H., Kumaraswami, V., Anuar, A. K., Hakim, S. L., Hayati, M. I., Chan, B. T., Suharni, M. and Ramachandran, C. P. (2001). Specificity and sensitivity of a rapid dipstick test (Brugia Rapid) in the detection of Brugia malayi infection. Transactions of Royal Society of Tropical Medicine and Hygiene 95, 601604.CrossRefGoogle ScholarPubMed
Seim, A. R., Dreyer, G. and Addiss, D. G. (1999). Controlling morbidity and interrupting transmission: twin pillars of lymphatic filariasis elimination. Revista da Sociedade Brasileria de Medicina Tropical 32, 325328.CrossRefGoogle ScholarPubMed
Shenoy, R. K. (2006). Lymphatic filariasis in children. Journal of Communicable Diseases 38, 118123.Google ScholarPubMed
Shenoy, R. K., John, A., Hameed, S., Suma, T. K. and Kumaraswami, V. (2000). Apparent failure of ultrasonography to detect adult worms of Brugia malayi. Annals of Tropical Medicine and Parasitology 94, 7782.CrossRefGoogle ScholarPubMed
Shenoy, R. K., Kumaraswami, V., Suma, T. K., Rajan, K. and Radhakuttyamma, G. (1999). A double-blind, placebo-controlled study of the efficacy of oral penicillin, diethylcarbamazine or local treatment of the affected limb in preventing acute adenolymphangitis in lymphoedema caused by brugian filariasis. Annals of Tropical Medicine and Parasitology 93, 367377.CrossRefGoogle ScholarPubMed
Shenoy, R. K., Suma, T. K., Kumaraswami, V., Padma, S., Rahmah, N., Abhilash, G. and Ramesh, C. (2007 a). Doppler ultrasonography reveals adult-worm nests in the lymph vessels of children with brugian filariasis. Annals of Tropical Medicine and Parasitology 101, 173180. doi: 10.1179/136485907X154566.CrossRefGoogle ScholarPubMed
Shenoy, R. K., Suma, T. K., Kumaraswami, V., Rahmah, N., Dhananjayan, G., Padma, S., Abhilash, G. and Ramesh, C. (2007 b). Preliminary findings from a cross-sectional study on lymphatic filariasis in children, in an area of India endemic for Brugia malayi infection. Annals of Tropical Medicine and Parasitology 101, 205213. doi: 10.1179/136485907X154548.CrossRefGoogle Scholar
Shenoy, R. K., Suma, T. K., Rajan, K. and Kumaraswami, V. (1998). Prevention of acute adenolymphangitis in brugian filariasis: comparison of the efficacy of ivermectin and diethylcarbamazine, each combined with local treatment of the affected limb. Annals of Tropical Medicine and Parasitology 92, 587594.CrossRefGoogle ScholarPubMed
Shenoy, R. K., Suma, T. K., Kumaraswami, V., Dhananjayan, G., Rahmah, N., Abhilash, G. and Ramesh, C. (2008). Lymphoscintigraphic evidence of lymph vessel dilation in the limbs of children with Brugia malayi infection. Journal of Communicable Diseases 40, 91100.Google ScholarPubMed
Shenoy, R. K., Suma, T. K., Kumaraswami, V., Rahmah, N., Dhananjayan, G. and Padma, S. (2009). Antifilarial drugs, in the doses employed in mass drug administrations by the Global Programme to Eliminate Lymphatic Filariasis, reverse lymphatic pathology in children with Brugia malayi infection. Annals of Tropical Medicine and Parasitology 103, 235247. doi: 10.1179/136485909X398249.CrossRefGoogle ScholarPubMed
Stanton, A. W., Badger, C. and Sitzia, J. (2000). Non-invasive assessment of the lymphedematous limb. Lymphology 33, 122135.Google ScholarPubMed
Stephenson, L. S., Latham, M. C., Adams, E. J., Kinoti, S. N. and Pertet, A. (1993). Physical fitness, growth and appetite of Kenyan school boys with hookworm, Trichuris trichiura and Ascaris lumbricoides infections are improved four months after a single dose of albendazole. Journal of Nutrition 123, 10361046.Google ScholarPubMed
Suma, T. K., Shenoy, R. K. and Kumaraswami, V. (2002). Efficacy and sustainability of a footcare programme in preventing acute attacks of adenolymphangitis in Brugian filariasis. Tropical Medicine and International health 7, 763766. doi: 914 [pii].CrossRefGoogle ScholarPubMed
Sunish, I. P., Rajendran, R., Mani, T. R., Munirathinam, A., Tewari, S. C., Hiriyan, J., Gajanana, A. and Satyanarayana, K. (2002). Resurgence in filarial transmission after withdrawal of mass drug administration and the relationship between antigenaemia and microfilaraemia – a longitudinal study. Tropical Medicine and International Health 7, 5969. doi: _828 [pii].CrossRefGoogle ScholarPubMed
Taylor, M. J., Hoerauf, A. and Bockarie, M. (2010). Lymphatic filariasis and onchocerciasis. Lancet 376, 11751185. doi: S0140-6736(10)60586-7 [pii] 10.1016/S0140-6736(10)60586-7.CrossRefGoogle ScholarPubMed
Vanamail, P., Ramaiah, K. D., Krishnamoorthy, K., Pani, S. P. and Das, P. K. (1992). Distribution oif microfilaria carriers and clinical cases of bancroftian filariasis in relation to family size in an urban situation. Tropical Biomedicine 9, 9198.Google Scholar
Vanamail, P., Subramanian, S., Das, P. K., Pani, S. P. and Bundy, D. A. P. (1989). Familial clusttering in Wuchereria bancrofti infection. Tropical Biomedicine 6, 6771.Google Scholar
Weil, G. J. and Ramzy, R. M. (2007). Diagnostic tools for filariasis elimination programs. Trends in Parasitology 23, 7882. doi: S1471-4922(06)00293-5 [pii] 10.1016/j.pt.2006.12.001.CrossRefGoogle ScholarPubMed
World Health Organization (2000). Preparing and implementing a national plan to eliminate lymphatic filariasis. WHO/CDS/CPE/CEE/2000.15, 29 pp.Google Scholar
World Health Organization (2010 a). Global programme to eliminate lymphatic filariasis. Weekly Epidemiological Record 85, 365372.Google Scholar
World Health Organization (2010 b). Working to overcome the global impact of neglected tropical diseases. First WHO Report on Neglected Tropical Diseases, WHO/HTM/NTD/2010.1, 172 pp.Google Scholar
World Health Organization (2010 c). World Health Organization Global Programme to Eliminate Lymphatic Filariasis: Progress report 2000–2009 and strategic plan 2010–2020 of the global programme to eliminate lymphatic filariasis: halfway towards eliminating lymphatic filariasis. WHO/HTM/NTD/PCT/2010.6, 79 pp.Google Scholar
Witt, C. and Ottesen, E. A. (2001). Lymphatic filariasis: an infection of childhood. Tropical Medicine and International Health 6, 582606. doi: tmi765 [pii].CrossRefGoogle ScholarPubMed
Witte, M. H., Jamal, S., Williams, W. H., Witte, C. L., Kumaraswami, V., McNeill, G. C., Case, T. C. and Panicker, T. M. (1993). Lymphatic abnormalities in human filariasis as depicted by lymphangioscintigraphy. Archives of Internal Medicine 153, 737744.CrossRefGoogle ScholarPubMed