Seminar Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm Jeff rey Bethony, Simon Brooker, Marco Albonico, Stefan M Geiger, Alex Loukas, David Diemert, Peter J Hotez The three main soil-transmitted helminth infections, ascariasis, trichuriasis, and hookworm, are common clinical Lancet 2006; 367: 1521–32 disorders in man. The gastrointestinal tract of a child living in poverty in a less developed country is likely to be Department of Microbiology, parasitised with at least one, and in many cases all three soil-transmitted helminths, with resultant impairments in Immunology, and Tropical physical, intellectual, and cognitive development. The benzimidazole anthelmintics, mebendazole and albendazole, Medicine, The George Washington University, are commonly used to remove these infections. The use of these drugs is not limited to treatment of symptomatic Washington DC, 20037 USA soil-transmitted helminth infections, but also for large-scale prevention of morbidity in children living in endemic (J Bethony PhD, S M Geiger PhD, areas. As a result of data showing improvements in child health and education after deworming, and the burden of Prof P J Hotez MD); Department disease attributed to soil-transmitted helminths, the worldwide community is awakening to the importance of these of Infectious and Tropical Diseases, London School of infections. Concerns about the sustainability of periodic deworming with benzimidazole anthelmintics and the Hygiene and Tropical Medicine, emergence of resistance have prompted eff orts to develop and test new control tools. London, UK (S Brooker DPhil); Fondazione Ivo de Carneri, Introduction of the eff ect of soil-transmitted helminth infections on Torino, Italy (M Albonico MD); Fundação Oswaldo Cruz, Centro The soil-transmitted helminths are a group of parasitic economic development and education is diffi cult. Over the de Pesquisa René Rachou, Belo nematode worms causing human infection through past 5 years, however, the worldwide community has Horizonte, Brazil (J Bethony, contact with parasite eggs or larvae that thrive in the warm begun to recognise the importance of these infections after S Geiger); Queensland Institute and moist soil of the world’s tropical and subtropical revised estimates showed that their combined disease of Medical Research, Brisbane, Australia (A Loukas PhD); and countries. As adult worms, the soil-transmitted helminths burden might be as great as those of malaria or Albert B Sabin Vaccine live for years in the human gastrointestinal tract. More tuberculosis.2 Studies have also highlighted the profound Institute, Washington DC, USA than a billion people are infected with at least one species eff ect of soil-transmitted helminth infection on school (D Diemert MD, Prof P J Hotez) (table 1).1 Of particular worldwide importance are the performance and attendance and future economic Correspondence to: roundworms (Ascaris lumbricoides), whipworms (Trichuris productivity.3,4 Such infections might also increase host Prof Peter J Hotez [email protected] trichiura), and hookworms (Necator americanus or susceptibility to other important illnesses such as malaria, Ancylostoma duodenale). They are considered together tuberculosis, and HIV infection.5,6 In 2001, the World because it is common for a single individual, especially a Health Assembly passed a resolution urging member child living in a less developed country, to be chronically states to control the morbidity of soil-transmitted helminth infected with all three worms. Such children have infections through large-scale use of anthelmintic drugs malnutrition, growth stunting, intellectual retardation, for school-aged children in less developed countries. A and cognitive and educational defi cits.1 response to this resolution could establish one of the The soil-transmitted helminths are one of the world’s most important causes of physical and intellectual growth Disease Estimated population Geographic region retardation. Yet, despite their educational, economic, and infected (millions) public-health importance (panel), they remain largely Major worldwide pathogens neglected by the medical and international community. Ascaris lumbricoides Common roundworm 807–1221 This neglect stems from three features: fi rst, the people infection most aff ected are the world’s most impoverished, Trichuris trichiura Whipworm infection 604–795 Necator americanus and Hookworm infection 576–740 particularly those who live on less than US$2 per day; Ancylostoma duodenale second, the infections cause chronic ill health and have Strongyloides stercoralis Threadworm infection 30–100 insidious clinical presentation; and third, quantifi cation Enterobius vermicularis Pinworm infection 4–28% of children Toxocara canis and Visceral and ocular larva 2–80% of children Toxocara cati migrans Search strategy and selection criteria Pathogens of minor or local importance Data for this review were identifi ed by a search of PubMed Ancylostoma brazilienese Cutaneous larva migrans Coastal regions worldwide without date restriction for the items “geohelminth”, “soil- Uncinaria stenocephala Cutaneous larva migrans Coastal regions worldwide transmitted helminths”, “hookworms”, “Necator americanus”, Ancylostoma caninum Eosinophilia enteritis Australia “Ancylostoma duodenale”, “Ascaris lumbricoides”, and “Trichuris Ancylostoma ceylanicum Hookworm infection Asia trichiura”. We also made widespread use of WHO publications Baylisascaris procyonis Eosinophilic meningitis North America on soil-transmitted helminths and chapters of books from Oesophagostomum bifurcum Nodular worm infection West Africa the authors. When more than one paper illustrated a specifi c Strongyloides fuelleborni Swollen belly syndrome Papua New Guinea point, the most representative paper was chosen. We selected Ternidens diminutus False hookworm infection Southern Africa papers published in English. Table 1: Soil-transmitted helminth infections of human beings www.thelancet.com Vol 367 May 6, 2006 1521 Seminar N americanus and A duodenale hookworm eggs hatch in Panel: Major websites on biology and public-health eff ect soil. The larvae moult twice to become infective third-stage of soil-transmitted helminths larvae, which are non-feeding but motile organisms that WHO partners for parasite control seek out higher ground to improve the chance of contact http://www.who.int/wormcontrol with human skin. After skin penetration, they enter subcutaneous venules and lymphatic vessels to access the Focusing resources on eff ective school health host’s aff erent circulation. Ultimately, the larvae become http://www.freshschools.org trapped in pulmonary capillaries, enter the lungs, pass over 13 Soil-transmitted helminth genome-sequencing projects the epiglottis, and migrate into the gastrointestinal tract. http://www.nematode.net About 5–9 weeks are needed from skin penetration until http://www.sanger.ac.uk/Projects/Helminths/ development of egg-laying adults. A duodenale larvae are also orally infective, and lactogenic transmission during breastfeeding has been postulated. Soil-transmitted largest worldwide health initiatives ever undertaken.7 helminths do not reproduce within the host. This feature is However, such widespread and frequent use of crucial for understanding of the epidemiology and clinical anthelmintics could lead to drug resistance or at least a features of soil-transmitted helminth infections, as well as decline in eff ectiveness of these front-line drugs in the the approaches to their control. long-term battle with soil-transmitted helminths.8,9 Epidemiology and burden of disease The parasites Soil-transmitted helminth infections are widely distributed Adult hookworms of the genera Necator and Ancylostoma throughout the tropics and subtropics (table 3). Climate is parasitise the upper part of the human small intestine, an important determinant of transmission of these whereas ascaris roundworms parasitise the entire small infections, with adequate moisture and warm temperature intestine and adult trichuris whipworms live in the large 10 intestine, especially the caecum (table 2). The parasites Ascaris lumbricoides can live for several years in the human gastrointestinal tract. Human beings are regarded as the only major defi nitive host for these parasites, although in some cases ascaris infections can also be acquired from pigs.11 The soil-transmitted helminths vary greatly in size, and female worms are larger than males (fi gure 1).10 After mating, each adult female produces thousands of eggs per day (fi gure 2), which leave the body in the faeces. People become infected with T trichiura and A lumbricoides by ingesting the fully developed eggs. Female Male After ingestion of trichuris eggs, the released larvae moult and travel to the colon where they burrow into the Trichuris trichiura epithelia and develop into adult whipworms within about 12 weeks.10 Ascaris larvae penetrate the intestinal mucosa and after an obligatory extraintestinal migration, they enter the liver then the lungs, before passing over the epiglottis to re-enter the gastrointestinal tract and develop into egg-laying adult worms about 9–11 weeks after egg ingestion.12 Female Male Species Length Daily egg output Location in host Lifespan (mm) per female worm (years) Hookworm Large common roundworm Ascaris lumbricoides 150–400 200 000 Small intestine 1 Whipworm Trichuris trichiura 30–50 3000–5000 Caecum and colon 1·5–2·0 Hookworms Necator americanus 7–13 9000–10 000 Upper small intestine 5–7 Ancylostoma duodenale