Forgotten People, Forgotten Diseases. Peter J. Hotez
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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 and stunting!
Moreover, the unholy trinity also adversely affects the neuropsychiatric activities of children, in turn damaging school performance and reducing school attendance.10,11 The mechanisms by which school performance is impaired are not well established, but a number of clinical studies have shown that STHs can adversely affect cognition and memory and in some cases possibly lower intelligence. 11 Therefore, chronic infections with STHs destroy the lives of children not by shortening their lives but instead by impairing their physical growth, mental development, and ability to learn in school. Each of the NTDs not only occurs in the setting of poverty but also promotes poverty. In the case of STH infections, roundworms, whipworms, and hookworms promote poverty primarily through their impact on overall child development. Presumably, these processes account for the observation that chronic infection with hookworm during childhood is associated with a 43% reduction in future wage-earning capacity (similar studies for ascariasis and trichuriasis are not yet available).12 Therefore, STH infections have a huge impact not only on health but also on education, and like other NTDs they are economic threats.
As suggested by the opening quotation from the late Norman Stoll, hookworm is probably the most significant STH. New Global Burden of Disease 2010 information (published at the end of 2012) confirms this observation, with preliminary indications that hookworm is responsible for almost two-thirds of the disability-adjusted life years (DALYs) lost from all of the STH infections.13 Hookworms are 1-cm-long parasites that live in the small intestine, where they suck blood from the small blood vessels lining the gut mucosa and submucosa. Approximately 700 million people, about one-half of the world’s poorest people, are infected with hookworm. The greatest concentration of cases occurs in rural areas of sub-Saharan Africa, East Asia and the Pacific region, the Indian subcontinent, and tropical regions of the Americas, especially Brazil and Central America (Fig. 2.5).2,14 Infection rates are often particularly high in coastal areas, an observation that most likely reflects the unique requirements of the soil-dwelling environmental stages of these parasites.
Figure 2.5 Global distribution of human hookworm infection. (From Hotez et al., 2005.)
Nearly as striking as the high prevalence of hookworm in developing countries is the almost complete absence of hookworm in highly developed countries, including the United States. However, up until the 1930s, hookworm infection (as well as many other NTDs, such as malaria and typhoid fever) was endemic in the southern United States.15 Shown in Fig. 2.6 is a map of the distribution of hookworm in the American South during the first decades of the 20th century, when high rates of hookworm infection occurred along the Gulf Coast and the