2.1 Children (left) living outside the Brazilian village of Americaninhas, Minas Gerais State (right). About 75% of people living in the area are infected with hookworm. The effects of the disease—malnutrition and anemia—are worse in children. (Photos of the children courtesy of Brigid McCarthy of National Public Radio [© 2005 NPR].)
The reason we know that most of the children of Americaninhas, Minas Gerais State, Brazil, harbor intestinal worms is that we can diagnose their STH infections by examining their feces under a microscope. The adult male and female roundworms, whipworms, and hookworms mate in the intestines and produce eggs that exit the body in feces. Each type of STH produces characteristically shaped eggs that are easy to identify through microscopy. If we now do this test for all children in this particular rural Brazilian village, we get a result that is shown in Fig. 2.2, in which more than 70% of the children between the ages of 5 and 11 are infected with Ascaris worms and hookworms. It turns out that we can repeat this study in almost any rural Brazilian village or indeed almost any rural village in the tropical regions of the Americas, including Central America, and probably obtain a similar result or find that just as many children are also infected with Trichuris whipworms. Indeed, if we were to conduct fecal examinations on most of the rural villages in sub-Saharan Africa, on the Indian subcontinent, or in Southeast Asia, really wherever people live in poverty and depend on subsistence agriculture and where the soil and climate are suitable for survival of the parasite eggs and immature larval stages (typically the warm and moist soil of the tropics), we would find a similar paradigm of extraordinarily high rates of STH infections. Such observations suggest how it can be that hundreds of millions of people harbor the unholy trinity in their bellies.
Figure 2.2 Prevalence of STH infections among school-age children in Americaninhas, Brazil. (Data courtesy of Jeff Bethony and David Diemert, Human Hookworm Vaccine Initiative; modified from graph prepared by Sophia Raff.)
Beginning in the late 1980s, parasitologists of the Chinese Academy of Preventive Medicine, now known as the Chinese Center for Disease Control and Prevention, conducted a 4-year study of intestinal parasites on an almost unimaginable scale by performing fecal examinations on 1,477,742 individuals in every province of China. The results were impressive and demonstrated that approximately 531 million cases of ascariasis, 212 million cases of trichuriasis, and 194 million cases of hookworm infection had occurred in that country.4 In collaboration with the Institute of Parasitic Diseases in Shanghai, I began working in China shortly after the completion of this nationwide survey of parasites. What particularly impressed me was the very tight link between high endemicity of STH infections in rural China and the level of economic underdevelopment.5 Wherever rural poverty was extreme and the villagers were engaged in subsistence agriculture, and provided there were suitable moisture and warmth, it was almost guaranteed that high levels of hookworm and other STH infections were present. Conversely, in areas of rapid economic gains, the STH infections disappeared. For instance, during the late 1990s when I visited a village in Jiangsu Province, not too far from Shanghai, there had been a steep decline in the prevalence of hookworm from just a decade previously.6 The decline coincided with the building of new factories such that fewer villagers were engaged in agricultural activities. Moreover, there was even a new Kentucky Fried Chicken franchise, as well as a pirated version with the same red-and-white logos—called KCF instead of KFC! Hookworm occurs only in the setting of poverty, and in a sense, the factory, KFC, and KCF represent indicators of economic development.
As shown in Fig. 2.3, the relationship between STH prevalence and poverty is extremely tight,7 and I believe that it is feasible to develop a “worm index” of economic development as a poverty indicator. However, a clear understanding of the specific mechanisms underlying the link between a high prevalence of STH infections and poverty is still somewhat elusive. At least three possible factors linking poverty to STH infections have been identified so far, including (i) inadequate sanitation, because survival of the environmental stages of STH parasites depends on the deposition of human feces on soil; (ii) poor housing construction, because dirt floors allow propagation of STHs in households, whereas cement floors prevent parasite transmission; and (iii) inadequate access to essential medicines, because better-off families can afford deworming drugs.8 Urbanization is also a potent factor in reducing the prevalence of STH infections. In eastern China, for example, rapid economic growth has brought with it a significant decline in prevalence, whereas in the poor and largely rural southern and southwestern provinces of China, such as Hainan, Sichuan, Yunnan, Guizhou, and Guangxi, hookworm and other STH infections remain highly endemic.5,8
Figure 2.3 The relationship between prevalence of hookworm and poverty. The socioeconomic status of 94 countries was assessed according to a number of commonly used indicators, with poverty measures divided into quartiles including the poorest (first quartile), very poor (second quartile), poor (third quartile), and least poor (fourth quartile). (Original from de Silva et al., 2003; later modified for Hotez et al., 2005.)
In addition to their enormous global prevalence and their intimate link with rural poverty, another important feature of STH infections is their predilection for affecting children more than adults. For reasons that are not well understood, children between the ages of 4 and 15 on average harbor larger numbers of STHs than do any other group; i.e., children are wormier than adults. This propensity is particularly true for Ascaris roundworms and Trichuris whipworms, less so for hookworms. For example, shown in Fig. 2.4 is a little girl from Paraguay who simultaneously is emaciated and has a distended abdomen. It is sometimes possible to gently palpate the abdomens of children like her and feel the presence of worms in their intestines. Figure 2.4 also shows the Ascaris roundworms that she expelled after treatment with an anthelmintic drug (a process often referred to as deworming). It is easy to grasp how this girl could get into medical trouble if the roundworms were allowed to remain and obstruct the intestine or in some cases migrate from the intestine and into the liver or pancreas.
Figure 2.4 (Left) Little girl from Paraguay with severe Ascaris worm infection. (Right) Worms expelled after anthelmintic treatment. (Photos courtesy of Nora Labiano; reproduced from Despommier et al., 2006.)
Although such clinical pictures are dramatic, they actually represent only a small portion of the global pediatric pathology caused by STHs. Far more important is the observation that in hundreds of millions of children the STHs stunt physical growth, physical fitness, and development. These processes probably operate at least partly through parasite-induced malnutrition, as all three major STHs can live in the intestines of children for years, where they can rob children of essential nutrients. For example, Ascaris roundworm infections most likely retard growth by impairing the digestion of protein, causing the malabsorption of fat, lactose, and vitamin A, as well as reducing appetite; Trichuris whipworm infections also result in reduced appetite, as well as in protein losses; and hookworms impair growth by causing blood loss that leads to profound protein and iron losses and ultimately to anemia.9 Through these mechanisms, it is possible that STHs represent the world’s leading cause of growth retardation
