Review article: Biomedical intelligence
Vol. 142 No. 4748 (2012)
Neglected tropical diseases: diagnosis, clinical management, treatment and control
- Jürg Utzinger
- Sören L. Becker
- Stefanie Knopp
- Johannes Blum
- Andreas L. Neumayr
- Jennifer Keiser
- Christoph F. Hatz
Summary
Branded in 2005, “neglected tropical diseases” have gained traction in terms of advocacy, interest for research, enhanced funding and political will for their control and eventual elimination. Starting with an initial set of 13 neglected tropical diseases – seven helminth, three bacterial and three protozoal infections – the list considerably expanded to more than 40 diseases that now also includes viral, fungal and ectoparasitic infections. In this review, we provide a comprehensive overview of the neglected tropical diseases, their causative agents and the current geographical distribution, including their importance for the general practitioners seeing returning travellers and migrants in Switzerland. We characterise the most important of the neglected tropical diseases in terms of at-risk population, estimated number of infections, annual mortality rates and global burden, including current knowledge gaps. With an emphasis on neglected tropical diseases due to helminths, protozoa and ectoparasites, we review common diagnostic methods and current recommendations for treatment at the population level and the individual patient, thereby juxtaposing the situation in highly endemic countries on one side, with Switzerland on the other. We highlight the clinical presentation and management of the neglected tropical diseases in general and then elaborate on two examples, strongyloidiasis and leptospirosis. Our review provides a global perspective of neglected tropical diseases and we hope that it will prove useful for the general practitioner and clinician in Switzerland and elsewhere to enhance their suspicion index, differential diagnosis, clinical management and treatment, including referral to specialised clinics and laboratories when need be.
References
- WHO. Macroeconomics and health: investing in health for economic development. Geneva: World Health Organization 2001.
- Jha P, Mills A, Hanson K, Kumaranayake L, Conteh L, Kurowski C, et al. Improving the health of the global poor. Science. 2002;295:2036–9.
- Vitoria M, Granich R, Gilks CF, Gunneberg C, Hosseini M, Were W, et al. The global fight against HIV/AIDS, tuberculosis, and malaria: current status and future perspectives. Am J Clin Pathol. 2009;131:844–8.
- Alonso PL, Brown G, Arevalo-Herrera M, Binka F, Chitnis C, Collins F, et al. A research agenda to underpin malaria eradication. PLoS Med. 2011;8:e1000406.
- Sachs J, Malaney P. The economic and social burden of malaria. Nature. 2002;415:680–5.
- Lopez AD, Mathers CD, Ezzati M, Jamison DT, Murray CJL. Global and regional burden of disease and risk factors, 2001: systematic analysis of population health data. Lancet. 2006;367:1747–57.
- Howitt P, Darzi A, Yang GZ, Ashrafian H, Atun R, Barlow J, et al. Technologies for global health. Lancet. 2012;380:507–35.
- Murray CJL, Rosenfeld LC, Lim SS, Andrews KG, Foreman KJ, Haring D, et al. Global malaria mortality between 1980 and 2010: a systematic analysis. Lancet. 2012;379:413–31.
- Nelson K. Stimulating research in the most neglected diseases. Lancet. 2002;359:1042.
- Trouiller P, Olliaro P, Torreele E, Orbinski J, Laing R, Ford N. Drug development for neglected diseases: a deficient market and a public-health policy failure. Lancet. 2002;359:2188–94.
- Morel CM. Neglected diseases: under-funded research and inadequate health interventions. Can we change this reality? EMBO Rep. 2003;4 Spec No:S35–8.
- Komatsu R, Korenromp EL, Low-Beer D, Watt C, Dye C, Steketee RW, et al. Lives saved by Global Fund-supported HIV/AIDS, tuberculosis and malaria programs: estimation approach and results between 2003 and end-2007. BMC Infect Dis. 2010;10:109.
- The Global Fund to Fight AIDS Tuberculosis and Malaria. The Global Fund 2010: Innovation and Impact. Geneva: The Global Fund to Fight AIDS, Tuberculosis and Malaria 2010.
- Katz I, Komatsu R, Low-Beer D, Atun R. Scaling up towards international targets for AIDS, tuberculosis, and malaria: contribution of Global Fund-supported programs in 2011–2015. PLoS One. 2011;6:e17166.
- Molyneux DH, Hotez PJ, Fenwick A. “Rapid-impact interventions”: how a policy of integrated control for Africa's neglected tropical diseases could benefit the poor. PLoS Med. 2005;2:e336.
- Hotez PJ, Molyneux DH, Fenwick A, Ottesen E, Ehrlich Sachs S, Sachs JD. Incorporating a rapid-impact package for neglected tropical diseases with programs for HIV/AIDS, tuberculosis, and malaria. PLoS Med. 2006;3:e102.
- Lammie PJ, Fenwick A, Utzinger J. A blueprint for success: integration of neglected tropical disease control programmes. Trends Parasitol. 2006;22:313–21.
- Utzinger J, Raso G, Brooker S, de Savigny D, Tanner M, Ørnbjerg N, et al. Schistosomiasis and neglected tropical diseases: towards integrated and sustainable control and a word of caution. Parasitology. 2009;136:1859–74.
- Molyneux DH. Combating the “other diseases“ of MDG 6: changing the paradigm to achieve equity and poverty reduction? Trans R Soc Trop Med Hyg. 2008;102:509–19.
- Weiss MG. Stigma and the social burden of neglected tropical diseases. PLoS Negl Trop Dis. 2008;2:e237.
- Hotez PJ, Fenwick A, Savioli L, Molyneux DH. Rescuing the bottom billion through control of neglected tropical diseases. Lancet. 2009;373:1570–5.
- Allotey P, Reidpath DD, Pokhrel S. Social sciences research in neglected tropical diseases 1: the ongoing neglect in the neglected tropical diseases. Health Res Policy Syst. 2010;8:32.
- Kettler HE, Modi R. Building local research and development capacity for the prevention and cure of neglected diseases: the case of India. Bull World Health Organ. 2001;79:742–7.
- Frankish H. Initiative launched to develop drugs for neglected diseases. Lancet. 2003;362:135.
- Steverding D. A new initiative for the development of new diagnostic tests for human African trypanosomiasis. Kinetoplastid Biol Dis. 2006;5:1.
- Ndung'u JM, Bieler S, Roscigno G. “Piggy-backing” on diagnostic platforms brings hope to neglected diseases: the case of sleeping sickness. PLoS Negl Trop Dis. 2010;4:e715.
- Utzinger J, de Savigny D. Control of neglected tropical diseases: integrated chemotherapy and beyond. PLoS Med. 2006;3:e112.
- Hotez PJ, Molyneux DH, Fenwick A, Kumaresan J, Ehrlich Sachs S, Sachs JD, et al. Control of neglected tropical diseases. N Engl J Med. 2007;357:1018–27.
- Hotez P. A new voice for the poor. PLoS Negl Trop Dis. 2007;1:e77.
- Probst-Hensch N, Tanner M, Kessler C, Burri C, Künzli N. Prevention – a cost-effective way to fight the non-communicable disease epidemic: an academic perspective of the United Nations High-level NCD Meeting. Swiss Med Wkly. 2011;141:w13266.
- WHO. Working to overcome the global impact of neglected tropical diseases. First WHO report on neglected tropical diseases. Geneva: World Health Organization. 2010.
- Hotez PJ. The four horsemen of the apocalypse: tropical medicine in the fight against plague, death, famine, and war. Am J Trop Med Hyg. 2012;87:3–10.
- Litt E, Baker MC, Molyneux D. Neglected tropical diseases and mental health: a perspective on comorbidity. Trends Parasitol. 2012;28:195–201.
- King CH. Parasites and poverty: the case of schistosomiasis. Acta Trop. 2010;113:95–104.
- Utzinger J, N’Goran EK, Caffrey CR, Keiser J. From innovation to application: social-ecological context, diagnostics, drugs and integrated control of schistosomiasis. Acta Trop. 2011;120(Suppl.1):S121–37.
- WHO. Preventive chemotherapy in human helminthiasis: coordinated use of anthelminthic drugs in control interventions: a manual for health professionals and programme managers. Geneva: World Health Organization 2006.
- WHO. Neglected tropical diseases: hidden successes, emerging opportunities. Geneva, World Health Organization 2006.
- Hotez PJ, Yamey G. The evolving scope of PLoS Neglected Tropical Diseases. PLoS Negl Trop Dis. 2009;3:e379.
- Brady MA, Hooper PJ, Ottesen EA. Projected benefits from integrating NTD programs in sub-Saharan Africa. Trends Parasitol. 2006;22:285–91.
- Fenwick A. New initiatives against Africa's worms. Trans R Soc Trop Med Hyg. 2006;100:200–7.
- King CH, Dickman K, Tisch DJ. Reassessment of the cost of chronic helmintic infection: a meta-analysis of disability-related outcomes in endemic schistosomiasis. Lancet. 2005;365:1561–9.
- Mathers CD, Ezzati M, Lopez AD. Measuring the burden of neglected tropical diseases: the global burden of disease framework. PLoS Negl Trop Dis. 2007;1:e114.
- Fürst T, Keiser J, Utzinger J. Global burden of human food-borne trematodiasis: a systematic review and meta-analysis. Lancet Infect Dis. 2012;12:210–21.
- WHO. The world health report 2004: changing history. Geneva: World Health Organization 2004.
- WHO. Prevention and control of schistosomiasis and soil-transmitted helminthiasis: report of a WHO expert committee. WHO Tech Rep Ser. 2002;912:1–57.
- Murray CJL, Lopez AD, Black R, Mathers CD, Shibuya K, Ezzati M, et al. Global burden of disease 2005: call for collaborators. Lancet. 2007;370:109–10.
- Bergquist R, Johansen MV, Utzinger J. Diagnostic dilemmas in helminthology: what tools to use and when? Trends Parasitol. 2009;25:151–6.
- Johansen MV, Sithithaworn P, Bergquist R, Utzinger J. Towards improved diagnosis of zoonotic trematode infections in Southeast Asia. Adv Parasitol. 2010;73:171–95.
- Tchuem Tchuenté LA. Control of soil-transmitted helminths in sub-Saharan Africa: diagnosis, drug efficacy concerns and challenges. Acta Trop. 2011;120(Suppl. 1):S4–11.
- Becker SL, Vogt J, Knopp S, Panning M, Warhurst DC, Polman K, et al. Persistent digestive disorders in the tropics: causative infectious pathogens and reference diagnostic tests. BMC Infect Dis. 2012 (submitted for publication).
- Yansouni CP, Bottieau E, Lutumba P, Winkler AS, Lynen L, Büscher P, et al. Rapid diagnostic tests for neurological infections in Central Africa. Lancet Infect Dis. 2012;(submitted for publication).
- Adam RD. The biology of Giardia spp. Microbiol Rev. 1991;55:706–32.
- Stanley SL, Jr. Amoebiasis. Lancet. 2003;361:1025–34.
- Knopp S, Steinmann P, Keiser J, Utzinger J. Nematode infections: soil-transmitted helminths and Trichinella. Infect Dis Clin North Am. 2012;26:341–58.
- Molyneux DH. Filaria control and elimination: diagnostic, monitoring and surveillance needs. Trans R Soc Trop Med Hyg. 2009;103:338–41.
- Rassi A, Jr., Rassi A, Marin-Neto JA. Chagas disease. Lancet. 2010;375:1388–402.
- Wastling SL, Welburn SC. Diagnosis of human sleeping sickness: sense and sensitivity. Trends Parasitol. 2011;27:394–402.
- Brun R, Blum J. Human African trypanosomiasis. Infect Dis Clin North Am. 2012;26:261–73.
- Knopp S, Steinmann P, Hatz C, Keiser J, Utzinger J. Nematode infections: filariases. Infect Dis Clin North Am. 2012;26:359–81.
- Rassi A, Jr., Rassi A, Rezende JD. American trypanosomiasis (Chagas disease). Infect Dis Clin North Am. 2012;26:275–91.
- Murray HW, Berman JD, Davies CR, Saravia NG. Advances in leishmaniasis. Lancet. 2005;366:1561–77.
- Goto H, Lauletta Lindoso JA. Cutaneous and mucocutaneous leishmaniasis. Infect Dis Clin North Am. 2012;26:293–307.
- van Griensven J, Diro E. Visceral leishmaniasis. Infect Dis Clin North Am. 2012;26:309–22.
- Booth M, Vounatsou P, N'Goran EK, Tanner M, Utzinger J. The influence of sampling effort and the performance of the Kato-Katz technique in diagnosing Schistosoma mansoni and hookworm co-infections in rural Côte d’Ivoire. Parasitology. 2003;127:525–31.
- Cringoli G, Rinaldi L, Maurelli MP, Utzinger J. FLOTAC: new multivalent techniques for qualitative and quantitative copromicroscopic diagnosis of parasites in animals and humans. Nat Protoc. 2010;5:503–15.
- Zhang W, McManus DP. Recent advances in the immunology and diagnosis of echinococcosis. FEMS Immunol Med Microbiol. 2006;47:24–41.
- Gottstein B, Pozio E, Nöckler K. Epidemiology, diagnosis, treatment, and control of trichinellosis. Clin Microbiol Rev. 2009;22:127–45.
- Rubinsky-Elefant G, Hirata CE, Yamamoto JH, Ferreira MU. Human toxocariasis: diagnosis, worldwide seroprevalences and clinical expression of the systemic and ocular forms. Ann Trop Med Parasitol. 2010;104:3–23.
- Keiser J, Duthaler U, Utzinger J. Update on the diagnosis and treatment of food-borne trematode infections. Curr Opin Infect Dis. 2010;23:513–20.
- van Lieshout L, Polderman AM, Deelder AM. Immunodiagnosis of schistosomiasis by determination of the circulating antigens CAA and CCA, in particular in individuals with recent or light infections. Acta Trop. 2000;77:69–80.
- Ross AGP, Bartley PM, Sleigh AC, Olds GR, Li YS, Williams GM, et al. Schistosomiasis. N Engl J Med. 2002;346:1212–20.
- Tanyuksel M, Petri WA, Jr. Laboratory diagnosis of amebiasis. Clin Microbiol Rev. 2003;16:713–29.
- Doenhoff MJ, Chiodini PL, Hamilton JV. Specific and sensitive diagnosis of schistosome infection: can it be done with antibodies? Trends Parasitol. 2004;20:35–9.
- WHO. Report of the WHO expert consultation on foodborne trematode infections and taeniasis/cysticercosis. Vientiane. World Health Organization Wester Pacific Regional Office 2011 (WHO/HTM/NTD/PCT/2011.3 WHO/HTM/NTD/PCT/2011.3).
- Verweij JJ, Blange RA, Templeton K, Schinkel J, Brienen EA, van Rooyen MA, et al. Simultaneous detection of Entamoeba histolytica, Giardia lamblia, and Cryptosporidium parvum in fecal samples by using multiplex real-time PCR. J Clin Microbiol. 2004;42:1220–3.
- Verweij JJ, Brienen EA, Ziem J, Yelifari L, Polderman AM, Van Lieshout L. Simultaneous detection and quantification of Ancylostoma duodenale, Necator americanus, and Oesophagostomum bifurcum in fecal samples using multiplex real-time PCR. Am J Trop Med Hyg. 2007;77:685–90.
- ten Hove RJ, Verweij JJ, Vereecken K, Polman K, Dieye L, van Lieshout L. Multiplex real-time PCR for the detection and quantification of Schistosoma mansoni and S. haematobium infection in stool samples collected in northern Senegal. Trans R Soc Trop Med Hyg. 2008;102:179–85.
- ten Hove RJ, van Esbroeck M, Vervoort T, van den Ende J, van Lieshout L, Verweij JJ. Molecular diagnostics of intestinal parasites in returning travellers. Eur J Clin Microbiol Infect Dis. 2009;28:1045–53.
- Steinmann P, Zhou XN, Du ZW, Jiang JY, Wang LB, Wang XZ, et al. Occurrence of Strongyloides stercoralis in Yunnan province, China, and comparison of diagnostic methods. PLoS Negl Trop Dis. 2007;1:e75.
- Knopp S, Mgeni AF, Khamis IS, Steinmann P, Stothard JR, Rollinson D, et al. Diagnosis of soil-transmitted helminths in the era of preventive chemotherapy: effect of multiple stool sampling and use of different diagnostic techniques. PLoS Negl Trop Dis. 2008;2:e331.
- Hotez PJ. New antipoverty drugs, vaccines, and diagnostics: a research agenda for the US President's Global Health Initiative (GHI). PLoS Negl Trop Dis. 2011;5:e1133.
- Jackson Y, Chappuis F. Chagas disease in Switzerland: history and challenges. Euro Surveill. 2011;16.
- Bethony J, Brooker S, Albonico M, Geiger SM, Loukas A, Diemert D, et al. Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet. 2006;367:1521–32.
- Montes M, Sawhney C, Barros N. Strongyloides stercoralis: there but not seen. Curr Opin Infect Dis. 2010;23:500–4.
- Olsen A, van Lieshout L, Marti H, Polderman T, Polman K, Steinmann P, et al. Strongyloidiasis – the most neglected of the neglected tropical diseases? Trans R Soc Trop Med Hyg. 2009;103:967–72.
- Feely NM, Waghorn DJ, Dexter T, Gallen I, Chiodini P. Strongyloides stercoralis hyperinfection: difficulties in diagnosis and treatment. Anaesthesia. 2010;65:298–301.
- Stothard JR, Pleasant J, Oguttu D, Adriko M, Galimaka R, Ruggiana A, et al. Strongyloides stercoralis: a field-based survey of mothers and their preschool children using ELISA, Baermann and Koga plate methods reveals low endemicity in western Uganda. J Helminthol. 2008;82:263–9.
- Krolewiecki AJ, Ramanathan R, Fink V, McAuliffe I, Cajal SP, Won K, et al. Improved diagnosis of Strongyloides stercoralis using recombinant antigen-based serologies in a community-wide study in northern Argentina. Clin Vaccine Immunol. 2010;17:1624–30.
- Verweij JJ, Canales M, Polman K, Ziem J, Brienen EA, Polderman AM, et al. Molecular diagnosis of Strongyloides stercoralis in faecal samples using real-time PCR. Trans R Soc Trop Med Hyg. 2009;103:342–6.
- Marques CC, Zago-Gomes MP, Gonçalves CS, Pereira FEL. Alcoholism and Strongyloides stercoralis: daily ethanol ingestion has a positive correlation with the frequency of Strongyloides larvae in the stools. PLoS Negl Trop Dis. 2010;4:e717.
- Carvalho EM, Da Fonseca Porto A. Epidemiological and clinical interaction between HTLV-1 and Strongyloides stercoralis. Parasite Immunol. 2004;26:487–97.
- Segarra-Newnham M. Manifestations, diagnosis, and treatment of Strongyloides stercoralis infection. Ann Pharmacother. 2007;41:1992–2001.
- Roxby AC, Gottlieb GS, Limaye AP. Strongyloidiasis in transplant patients. Clin Infect Dis. 2009;49:1411–23.
- WHO. Leptospirosis worldwide, 1999. Wkly Epidemiol Rec. 1999;74:237–42.
- Lau CL, Smythe LD, Craig SB, Weinstein P. Climate change, flooding, urbanisation and leptospirosis: fuelling the fire? Trans R Soc Trop Med Hyg. 2010;104:631–8.
- Leshem E, Meltzer E, Schwartz E. Travel-associated zoonotic bacterial diseases. Curr Opin Infect Dis. 2011;24:457–63.
- Keenan J, Ervin G, Aung M, McGwin G, Jr., Jolly P. Risk factors for clinical leptospirosis from Western Jamaica. Am J Trop Med Hyg. 2010;83:633–6.
- Hartskeerl RA, Collares-Pereira M, Ellis WA. Emergence, control and re-emerging leptospirosis: dynamics of infection in the changing world. Clin Microbiol Infect. 2011;17:494–501.
- Daher EF, Abreu KLS, Silva Junior GB. Leptospirosis-associated acute kidney injury. J Bras Nefrol. 2010;32:400–7.
- Toyokawa T, Ohnishi M, Koizumi N. Diagnosis of acute leptospirosis. Expert Rev Anti Infect Ther. 2011;9:111–21.
- Desakorn V, Wuthiekanun V, Thanachartwet V, Sahassananda D, Chierakul W, Apiwattanaporn A, et al. Accuracy of a commercial IgM ELISA for the diagnosis of human leptospirosis in Thailand. Am J Trop Med Hyg. 2012;86:524–7.
- Yang HY, Yen TH, Lin CY, Chen YC, Pan MJ, Lee CH, et al. Early identification of leptospirosis as an ignored cause of multiple organ dysfunction syndrome. Shock. 2012;38:24–9.
- Brett-Major DM, Coldren R. Antibiotics for leptospirosis. Cochrane Database Syst Rev. 2012;2:CD008264.
- Keiser J, Utzinger J. The drugs we have and the drugs we need against major helminth infections. Adv Parasitol. 2010;73:197–230.
- Savioli L, Gabrielli AF, Montresor A, Chitsulo L, Engels D. Schistosomiasis control in Africa: 8 years after World Health Assembly Resolution 54.19. Parasitology. 2009;136:1677–81.
- WHO. Global programme to eliminate lymphatic filariasis: progress report on mass drug administration, 2010. Wkly Epidemiol Rec. 2011;86:377–88.
- WHO. Soil-transmitted helminthiases: estimates of the number of children needing preventive chemotherapy and number treated, 2009. Wkly Epidemiol Rec. 2011;86:257–67.
- WHO. Schistosomiasis: population requiring preventive chemotherapy and number of people treated in 2010. Wkly Epidemiol Rec. 2012;87:37–44.
- Brun R, Blum J, Chappuis F, Burri C. Human African trypanosomiasis. Lancet. 2010;375:148–59.
- Jia TW, Melville S, Utzinger J, King CH, Zhou XN. Soil-transmitted helminth reinfection after drug treatment: a systematic review and meta-analysis. PLoS Negl Trop Dis. 2012;6:e1621.
- Bartram J, Cairncross S. Hygiene, sanitation, and water: forgotten foundations of health. PLoS Med. 2010;7:e1000367.
- Ziegelbauer K, Speich B, Mäusezahl D, Bos R, Keiser J, Utzinger J. Effect of sanitation on soil-transmitted helminth infection: systematic review and meta-analysis. PLoS Med. 2012;9:e1001162.
- Schwitz FM, Haley TJ, Stat C, Hatz CF. Health information given by Swiss travel agencies. J Travel Med. 2006;13:294–9.
- Schlagenhauf P, Santos-O’Connor F, Parola P. The practice of travel medicine in Europe. Clin Microbiol Infect. 2010;16:203–8.
- Willingham AL, 3rd, Engels D. Control of Taenia solium cysticercosis/taeniosis. Adv Parasitol. 2006;61:509–66.
- Brunetti E, White AC, Jr. Cestode infestations: hydatid disease and cysticercosis. Infect Dis Clin North Am. 2012;26:421–35.
- Torgerson PR, Macpherson CN. The socioeconomic burden of parasitic zoonoses: global trends. Vet Parasitol. 2011;182:79–95.
- Scholz T, Garcia HH, Kuchta R, Wicht B. Update on the human broad tapeworm (genus Diphyllobothrium), including clinical relevance. Clin Microbiol Rev. 2009;22:146–60.
- Richards FO, Ruiz-Tiben E, Hopkins DR. Dracunculiasis eradication and the legacy of the smallpox campaign: What's new and innovative? What's old and principled? [Presented at the Symposium on Smallpox Eradication: Lessons, Legacies & Innovations]. Vaccine. 2011;29(Suppl 4):D86–90.
- WHO. Monthly report on dracunculiasis cases, January-May 2012. Wkly Epidemiol Rec. 2012;87:315–6.
- McManus DP. Echinococcosis with particular reference to Southeast Asia. Adv Parasitol. 2010;72:267–303.
- Brunetti E, Kern P, Vuitton DA, WHO-IWGE. WPf. Expert consensus for the diagnosis and treatment of cystic and alveolar echinococcosis in humans. Acta Trop. 2010;114:1–16.
- Cook GC. Enterobius vermicularis infection. Gut. 1994;35:1159–62.
- Keiser J, Utzinger J. Food-borne trematodiases. Clin Microbiol Rev. 2009;22:466–83.
- Fürst T, Duthaler U, Sripa B, Utzinger J, Keiser J. Trematode infections: liver and lung flukes. Infect Dis Clin North Am. 2012;26:399–419.
- Padgett JJ, Jacobsen KH. Loiasis: African eye worm. Trans R Soc Trop Med Hyg. 2008;102:983–9.
- Taylor MJ, Hoerauf A, Bockarie M. Lymphatic filariasis and onchocerciasis. Lancet. 2010;376:1175–85.
- Gryseels B, Polman K, Clerinx J, Kestens L. Human schistosomiasis. Lancet. 2006;368:1106–18.
- Keiser J, Utzinger J. Foodborne trematodiasis and schistosomiasis. In: Rudolph CD, Rudolph AM, Lister GE, First LR, Gershon AA, editors. Rudolph’s Pediatrics. 22nd ed. New York: The McGraw-Hill Companies, Inc.,. 2011, pp. 1200–3.
- Pullan RL, Brooker SJ. The global limits and population at risk of soil-transmitted helminth infections in 2010. Parasit Vectors. 2012;5:81.
- Despommier D. Toxocariasis: clinical aspects, epidemiology, medical ecology, and molecular aspects. Clin Microbiol Rev. 2003;16:265–72.
- Schuster FL, Ramirez-Avila L. Current world status of Balantidium coli. Clin Microbiol Rev. 2008;21:626–38.
- Urech K, Neumayr A, Blum J. Sleeping sickness in travelers – do they really sleep? PLoS Negl Trop Dis. 2011;5:e1358.
- Ximénez C, Morán P, Rojas L, Valadez A, Gómez A, Ramiro M, et al. Novelties on amoebiasis: a neglected tropical disease. J Glob Infect Dis. 2011;3:166–74.
- Escobedo AA, Almirall P, Robertson LJ, Franco RMB, Hanevik K, Morch K, et al. Giardiasis: the ever-present threat of a neglected disease. Infect Disord Drug Targets. 2010;10:329–48.
- Florin TA, Zaoutis TE, Zaoutis LB. Beyond cat scratch disease: widening spectrum of Bartonella henselae infection. Pediatrics. 2008;121:e1413–25.
- Ayele WY, Neill SD, Zinsstag J, Weiss MG, Pavlik I. Bovine tuberculosis: an old disease but a new threat to Africa. Int J Tuberc Lung Dis. 2004;8:924–37.
- van der Werf TS, Stinear T, Stienstra Y, van der Graaf WTA, Small PL. Mycolactones and Mycobacterium ulcerans disease. Lancet. 2003;362:1062–4.
- Wansbrough-Jones M, Phillips R. Buruli ulcer: emerging from obscurity. Lancet. 2006;367:1849–58.
- Kelvin AA. Outbreak of cholera in the Republic of Congo and the Democratic Republic of Congo, and cholera worldwide. J Infect Dev Ctries. 2011;5:688–91.
- Gupta SK, Keck J, Ram PK, Crump JA, Miller MA, Mintz ED. Part III. Analysis of data gaps pertaining to enterotoxigenic Escherichia coli infections in low and medium human development index countries, 1984–2005. Epidemiol Infect. 2008;136:721–38.
- Crump JA, Ram PK, Gupta SK, Miller MA, Mintz ED. Part I. Analysis of data gaps pertaining to Salmonella enterica serotype Typhi infections in low and medium human development index countries, 1984-2005. Epidemiol Infect. 2008;136:436–48.
- Ram PK, Crump JA, Gupta SK, Miller MA, Mintz ED. Part II. Analysis of data gaps pertaining to Shigella infections in low and medium human development index countries, 1984–2005. Epidemiol Infect. 2008;136:577–603.
- Britton WJ, Lockwood DNJ. Leprosy. Lancet. 2004;363:1209-19.
- Cutler SJ. Possibilities for relapsing fever reemergence. Emerg Infect Dis. 2006;12:369–74.
- Burton MJ, Mabey DCW. The global burden of trachoma: a review. PLoS Negl Trop Dis. 2009;3:e460.
- Meheus A, Antal GM. The endemic treponematoses: not yet eradicated. World Health Stat Q. 1992;45:228–37.
- Fahal AH. Mycetoma: a thorn in the flesh. Trans R Soc Trop Med Hyg. 2004;98:3–11.
- Lupi O, Tyring SK, McGinnis MR. Tropical dermatology: fungal tropical diseases. J Am Acad Dermatol. 2005;53:931–51, quiz 52–4.
- Brummer E, Castaneda E, Restrepo A. Paracoccidioidomycosis: an update. Clin Microbiol Rev. 1993;6:89–117.
- Rogers DJ, Wilson AJ, Hay SI, Graham AJ. The global distribution of yellow fever and dengue. Adv Parasitol. 2006;62:181–220.
- Erlanger TE, Weiss S, Keiser J, Utzinger J, Wiedenmayer K. Past, present, and future of Japanese encephalitis. Emerg Infect Dis. 2009;15:1–7.
- Campbell GL, Hills SL, Fischer M, Jacobson JA, Hoke CH, Hombach JM, et al. Estimated global incidence of Japanese encephalitis: a systematic review. Bull World Health Organ. 2011;89:766–74, 74A–74E.
- Barnett ED. Yellow fever: epidemiology and prevention. Clin Infect Dis. 2007;44:850–6.
- Wilde H, Briggs DJ, Meslin FX, Hemachudha T, Sitprija V. Rabies update for travel medicine advisors. Clin Infect Dis. 2003;37:96–100.
- Chevalier V, Pépin M, Plée L, Lancelot R. Rift Valley fever – a threat for Europe? Euro Surveill. 2010;15:19506.
- Cajimat MNB, Milazzo ML, Rollin PE, Nichol ST, Bowen MD, Ksiazek TG, et al. Genetic diversity among Bolivian arenaviruses. Virus Res. 2009;140:24–31.
- Ogbu O, Ajuluchukwu E, Uneke CJ. Lassa fever in West African sub-region: an overview. J Vector Borne Dis. 2007;44:1–11.
- Ergönül Ö. Crimean-Congo haemorrhagic fever. Lancet Infect Dis. 2006;6:203–14.
- Jonsson CB, Figueiredo LT, Vapalahti O. A global perspective on hantavirus ecology, epidemiology, and disease. Clin Microbiol Rev. 2010;23:412–41.
- Leroy EM, Gonzalez JP, Baize S. Ebola and Marburg haemorrhagic fever viruses: major scientific advances, but a relatively minor public health threat for Africa. Clin Microbiol Infect. 2011;17:964–76.
- Gould EA, Solomon T. Pathogenic flaviviruses. Lancet. 2008;371:500–9.
- Francesconi F, Lupi O. Myiasis. Clin Microbiol Rev. 2012;25:79–105.
- Hengge UR, Currie BJ, Jäger G, Lupi O, Schwartz RA. Scabies: a ubiquitous neglected skin disease. Lancet Infect Dis. 2006;6:769–79.
- Steinmann P, Keiser J, Bos R, Tanner M, Utzinger J. Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk. Lancet Infect Dis. 2006;6:411–25.
- Little MP, Breitling LP, Basáñez MG, Alley ES, Boatin BA. Association between microfilarial load and excess mortality in onchocerciasis: an epidemiological study. Lancet. 2004;363:1514–21.
- Zouré HGM, Wanji S, Noma M, Amazigo UV, Diggle PJ, Tekle AH, et al. The geographic distribution of Loa loa in Africa: results of large-scale implementation of the Rapid Assessment Procedure for Loiasis (RAPLOA). PLoS Negl Trop Dis. 2011;5:e1210.
- Watkins BM. Drugs for the control of parasitic diseases: current status and development. Trends Parasitol. 2003;19:477–8.
- Simarro PP, Diarra A, Ruiz Postigo JA, Franco JR, Jannin JG. The human African trypanosomiasis control and surveillance programme of the World Health Organization 2000–2009: the way forward. PLoS Negl Trop Dis. 2011;5:e1007.
- Snow RW, Guerra CA, Noor AM, Myint HY, Hay SI. The global distribution of clinical episodes of Plasmodium falciparum malaria. Nature. 2005;434:214–7.
- WHO. The global burden of disease, 2004 update. Geneva: World Health Organization 2008.
- UNAIDS. UNAIDS report on the global AIDS epidemic. Geneva 2010.
- WHO. Global tuberculosis control 2011. Geneva: World Health Organization 2011.
- Utzinger J. A research and development agenda for the control and elimination of human helminthiases. PLoS Negl Trop Dis. 2012;6:e1646.
- Cairncross S, Muller R, Zagaria N. Dracunculiasis (Guinea worm disease) and the eradication initiative. Clin Microbiol Rev. 2002;15:223–46.
- Parija SC, Sheeladevi C, Shivaprakash MR, Biswal N. Evaluation of lactophenol cotton blue stain for detection of eggs of Enterobius vermicularis in perianal surface samples. Trop Doct. 2001;31:214–5.
- Burkhart CN, Burkhart CG. Assessment of frequency, transmission, and genitourinary complications of enterobiasis (pinworms). Int J Dermatol. 2005;44:837–40.
- Viyanant V, Brockelman WY, Lee P, Ardsungnoen S, Upatham ES. A comparison of a modified quick-Kato technique and the Stoll dilution method for field examination for Opisthorchis viverrini eggs. J Helminthol. 1983;57:191–5.
- Touré FS, Mavoungou E, Kassambara L, Williams T, Wahl G, Millet P, et al. Human occult loiasis: field evaluation of a nested polymerase chain reaction assay for the detection of occult infection. Trop Med Int Health. 1998;3:505–11.
- Boussinesq M. Loiasis. Ann Trop Med Parasitol. 2006;100:715–31.
- Weil GJ, Lammie PJ, Weiss N. The ICT Filariasis Test: a rapid-format antigen test for diagnosis of bancroftian filariasis. Parasitol Today. 1997;13:401–4.
- Weil GJ, Ramzy RM. Diagnostic tools for filariasis elimination programs. Trends Parasitol. 2007;23:78–82.
- Stingl P. Onchocerciasis: developments in diagnosis, treatment and control. Int J Dermatol. 2009;48:393–6.
- Lambertucci JR, dos Santos Silva LC, Andrade LM, de Queiroz LC, Carvalho VT, Voieta I, et al. Imaging techniques in the evaluation of morbidity in schistosomiasis mansoni. Acta Trop. 2008;108:209–17.
- Coulibaly JT, Knopp S, N’Guessan NA, Silué KD, Fürst T, Lohourignon LK, et al. Accuracy of urine circulating cathodic antigen (CCA) test for Schistosoma mansoni diagnosis in different settings of Côte d’Ivoire. PLoS Negl Trop Dis. 2011;5:e1384.
- Peters PA, Mahmoud AA, Warren KS, Ouma JH, Siongok TK. Field studies of a rapid, accurate means of quantifying Schistosoma haematobium eggs in urine samples. Bull World Health Organ. 1976;54:159–62.
- Katz N, Chaves A, Pellegrino J. A simple device for quantitative stool thick-smear technique in schistosomiasis mansoni. Rev Inst Med Trop São Paulo. 1972;14:397–400.
- WHO. Bench aids for the diagnosis of intestinal parasites. Geneva: World Health Organization 1994.
- Glinz D, Silué KD, Knopp S, Lohourignon LK, Yao KP, Steinmann P, et al. Comparing diagnostic accuracy of Kato-Katz, Koga agar plate, ether-concentration, and FLOTAC for Schistosoma mansoni and soil-transmitted helminths. PLoS Negl Trop Dis. 2010;4:e754.
- Marti H, Escher E. SAF – an alternative fixation solution for parasitological stool specimens. Schweiz Med Wochenschr. 1990;120:1473–6 (in German).
- Levecke B, Behnke JM, Ajjampur SS, Albonico M, Ame SM, Charlier J, et al. A comparison of the sensitivity and fecal egg counts of the McMaster egg counting and Kato-Katz thick smear methods for soil-transmitted helminths. PLoS Negl Trop Dis. 2011;5:e1201.
- Koga K, Kasuya S, Khamboonruang C, Sukhavat K, Ieda M, Takatsuka N, et al. A modified agar plate method for detection of Strongyloides stercoralis. Am J Trop Med Hyg. 1991;45:518–21.
- García LS, Bruckner DA Diagnostic medical parasitology. Washington, DC: American Society for Microbiology 2001.
- Gónzalez MT, Ibañez O, Balcarce N, Nanfito G, Kozubsky L, Radman N, et al. Toxocariasis with liver involvement. Acta Gastroenterol Latinoam. 2000;30:187–90 (in Spanish).
- Smith H, Holland C, Taylor M, Magnaval JF, Schantz P, Maizels R. How common is human toxocariasis? Towards standardizing our knowledge. Trends Parasitol. 2009;25:182–8.
- Kociecka W. Trichinellosis: human disease, diagnosis and treatment. Vet Parasitol. 2000;93:365–83.
- Dupouy-Camet J, Kociecka W, Bruschi F, Bolas-Fernandez F, Pozio E. Opinion on the diagnosis and treatment of human trichinellosis. Expert Opin Pharmacother. 2002;3:1117–30.
- Miles MA. Culturing and biological cloning of Trypanosoma cruzi. Methods Mol Biol. 1993;21:15–28.
- Chappuis F, Loutan L, Simarro P, Lejon V, Büscher P. Options for field diagnosis of human african trypanosomiasis. Clin Microbiol Rev. 2005;18:133–46.
- Guerin PJ, Olliaro P, Sundar S, Boelaert M, Croft SL, Desjeux P, et al. Visceral leishmaniasis: current status of control, diagnosis, and treatment, and a proposed research and development agenda. Lancet Infect Dis. 2002;2:494–501.
- Chappuis F, Sundar S, Hailu A, Ghalib H, Rijal S, Peeling RW, et al. Visceral leishmaniasis: what are the needs for diagnosis, treatment and control? Nat Rev Microbiol. 2007;5:873–82.
- Reithinger R, Dujardin JC. Molecular diagnosis of leishmaniasis: current status and future applications. J Clin Microbiol. 2007;45:21–5.
- Johnston G, Sladden M. Scabies: diagnosis and treatment. BMJ. 2005;331:619–22.
- Chosidow O. Scabies. N Engl J Med. 2006;354:1718–27.
- Heukelbach J, Feldmeier H. Scabies. Lancet. 2006;367:1767–74.
- Simarro PP, Franco JR, Cecchi G, Paone M, Diarra A, Ruiz Postigo JA, et al. Human African trypanosomiasis in non-endemic countries (2000–2010). J Travel Med. 2012;19:44–53.
- Blum JA, Hatz CF. Treatment of cuaneous leishmaniasis in travelers 2009. J Travel Med. 2009;16.123–31.