Abstract
Human hookworm infection is linked to a variety of factors, such as poverty, inadequate living conditions, absence of adequate sanitary facilities, cultural habits, and ineffective prevention programs/health systems. Zoonotic hookworm infection, leading to cutaneous larva migrans in humans, is related to the presence of animals (dogs and cats) serving as reservoirs. Climate and soil structure are also important determinants for larval development in the environment, and consequently for both human and animal hookworm infections. Health systems usually focus on individual medicalization, leading eventually to antiparasitic overuse and development of drug resistances. Given the reduced sustainability and effectiveness of the community interventions observed over the last decades, there is a need for more comprehensive approaches. In this chapter, we discuss the One Health Approach as a multidisciplinary measure to control hookworm disease. Integrated control programs would reduce transmission sustainably, for example, by combining mass drug administration aiming at the entire population rather than only schoolchildren or other defined target groups, and expansion of sanitary improvement programs. Once available, widespread application of a hookworm vaccine will be an additional tool to further boost control efforts. Health professionals involved in specific control programs should integrate into an interdisciplinary manner differing disciplines and departments. Existing overlapping disease control programs should be integrated, to achieve sustainable and cost-effective control on the long run, of both human and animal hookworm infection, and hookworm-related cutaneous larva migrans, in addition to other neglected tropical diseases.
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12.1 Human Hookworm Infection and Cutaneous Larva Migrans
About 470 million people are estimated to be infected with hookworms worldwide. In Latin America, the predominant human hookworm species is Necator americanus. The parasites may survive for many years in the human intestine, and chronic disease can cause cognitive deficits, growth retardation, as well as reduced school and work performance. Continuous intestinal blood loss may lead to iron-deficiency anemia. Despite intensive mass drug administration efforts during the past decades, the disease burden continues being high, both in low and middle-income settings (Loukas et al. 2016). In fact, due to the tremendous burden, human hookworm infection has been considered the most important neglected tropical disease (Haldeman et al. 2020).
On the other hand, infestation with animal hookworm larvae, mainly from dogs and cats, leads to a self-limiting condition in humans: hookworm-related cutaneous larva migrans. The adult hookworms living in the intestine of dogs and cats expel eggs, which hatch in the excreted animal feces and develop into infective larvae in the environment. Similar to human hookworms, the animal hookworm larvae penetrate into the upper layer of the epidermis, after the host’s direct contact with the contaminated feces. If this new host is a dog or a cat, the larvae migrate further into the lymphatic and blood systems, finally reaching the intestine, and cause animal hookworm disease. If the host is a human being, larvae will penetrate into the skin, but will not be able to penetrate the basal membrane, and migrate within the epidermis, without completing their life cycle. Larvae may survive for months in the epidermis, and while creeping around cause unbearable itching (Heukelbach and Feldmeier 2008). The prevalences of hookworm infections in dogs are usually high in both urban and rural areas, and soil samples from public parks, streets, playgrounds, and beaches are often contaminated with dog and cat feces containing animal hookworm larvae (Heukelbach and Feldmeier 2008). In tropical regions, especially in resource-poor communities, people often walk barefooted. Walking barefooted and inadequate housing have been described as risk factors for cutaneous larva migrans in these settings (Heukelbach et al. 2008). Humans usually are also infested while sitting on the floor or at the beach where animals have deposited their feces.
Anthelminthic drugs against human and animal hookworm infections are usually effective, but in endemic areas reinfection is common, and control strategies should include improved water quality, sanitation, and hygiene (Loukas et al. 2016).
12.2 Hookworm Control and One Health
Already in the nineteenth century, the German physician Rudolf Virchow recognized the link between humans and animals within the realm of infectious diseases and formed the term zoonosis. Later, in the twentieth century, medical disciplines were more and more specialized, with increasing separation and silo thinking. This is partly a result of specific human and animal disease management, and individualized treatment (Rushton et al. 2018).
Human hookworm disease control programs are usually based on regular mass administration of anthelminthic drugs every 6–12 months (mostly albendazole or mebendazole), to school-aged children in endemic regions. These widespread deworming programs are targeted at soil-transmitted helminth infections in general, but usually have a focus on specific target groups. Annual deworming with albendazole or mebendazole has been discussed to be less effective for hookworms than for other soil-transmitted helminth infections, and in fact prevalences did not decrease considerably on the long run, even after 20 years of mass-treatment programs (Loukas et al. 2016). There are growing concerns about drug resistance, and a need for long-term interventions, given the long lifespan of adult worms in the human intestine. Vaccines currently under development may prevent moderate and severe infections, leading to more sustainable control than being achieved via mass drug administration programs (Haldeman et al. 2020).
Given the reduced sustainability and effectiveness of the interventions observed over the last decades, there is a need for more comprehensive multidisciplinary approaches. Integrated control programs would reduce transmission sustainably, for example, by combining mass drug administration aiming at the entire population rather than only schoolchildren or other defined target groups, and expansion of sanitary improvement programs. Once available, widespread application of a hookworm vaccine will an additional tool to further boost control efforts. These approaches should consider the multi-faceted characteristics of hookworm transmission dynamics and integrate several disciplines.
Hookworm infection is clearly linked to poverty, inadequate living conditions, absence of adequate sanitary facilities and sewage systems, cultural habits and human behavior, poor health systems, and ineffective prevention programs. In addition, zoonotic hookworm infection, leading to cutaneous larva migrans in humans, is related to the presence of animals (dogs and cats) serving as reservoirs. Climate and soil structure are other important determinants for larval development outside the host, and consequently both human and animal hookworm infections.
Similar to other neglected tropical diseases, the determinants leading to human and animal hookworm infections and respective diseases are linked with each other, and related to a variety of factors, including the human health, animal health, and the environment (Heukelbach 2021). Despite increasing advocacy for integrated approaches during the recent years, human, animal, and environmental health are still today often highly separated into different sectors, within guidelines, policy frameworks, management structures, and governance (Kock et al. 2018). In addition, classical health systems are based on individual medicalization, leading eventually to antibiotic and anthelminthic overuse and development of antimicrobial resistances. A paradigm shift towards to a fully integrated One Health approach covering a broad array of disciplines and considering humans, animals, and plants is needed, to overcome the current and future public health problems (Kock et al. 2018).
The integrated and sustainable control of hookworm infection requires not only mass drug administration, but also sanitary improvements (Water—Sanitation and Hygiene [WASH] programs). Integrated WASH interventions including improved sanitary facilities and sewage management, access to clean water, promotion of handwashing, health education, and use of shoes will also prevent infections with other soil-transmitted helminths, diarrhea and other diseases. While there is some evidence that shoe wearing reduces the chance of hookworm infection, the effectiveness of shoes has been discussed, and depending on the cultural context, compliance to shoe use may be low. WASH activities should be embedded in community engagement and awareness campaigns. These measures would increase the general health situation of the population, and it seems obvious that WASH programs will be an important tool for soil-transmitted control efforts in general, but its effectiveness for reduction of human hookworm infection is still a matter of debate, and the results of available studies are mixed (Haldeman et al. 2020).
Effective control measures of both human hookworm infection and cutaneous larva migrans will necessarily include infection control not only in humans, but also in dogs and cats. Clearly, mass drug interventions will have an effect on transmission dynamics of human hookworm infection, but not on cutaneous larva migrans. This can only be achieved by systematic anthelminthic treatment of dogs and cats, reduction of the free-ranging and stray dog population, and environmental measures. However, in resource-poor settings and in areas with a deficient public veterinary health system and a high number of stray dogs, this is a difficult endeavor, and the community will have to be involved in addition to public health professionals and veterinarians. Despite the lack of interdisciplinary thinking, a control program based on communication campaigns, community involvement, and treatment of animals has been effective in an endemic area in South Africa (McCrindle et al. 1996).
One Health is a multidisciplinary approach considering all these different factors, areas, and interactions, to effectively and sustainably control diseases (Heukelbach 2021). Ideally, a group of diseases should be targeted in collaboration with differing disease control programs, as control measures and treatments often overlap. Treatments of choice for severe cutaneous larva migrans are oral ivermectin and albendazole. Singular lesions can easily be treated with topical thiabendazole (Heukelbach and Hengge 2009). Interestingly, ivermectin is also effective against human hookworm disease, other soil-transmitted helminths, lice infestations, and scabies. In addition, ivermectin has been used extensively for the control of lymphatic filariasis and onchocerciasis. Interventions, for example, based on mass-drug administration with ivermectin and additional focus on animal diseases will also reduce an array of other parasitic diseases.
In conclusion, health professionals involved in specific control programs should think out of the box, and integrate into an interdisciplinary manner differing disciplines and departments. The differing somehow overlapping disease control programs should be integrated, to achieve sustainable and cost-effective control on the long run, of both human and animal hookworm infection, and hookworm-related cutaneous larva migrans, in addition to other neglected tropical diseases.
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Heukelbach, J. (2022). One Health Approach to Control Human and Zoonotic Hookworm Infections. In: Mehlhorn, H., Heukelbach, J. (eds) Infectious Tropical Diseases and One Health in Latin America. Parasitology Research Monographs, vol 16. Springer, Cham. https://doi.org/10.1007/978-3-030-99712-0_12
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