Ancylostomiasis, or hookworm disease, is caused by hookworm infection and is characterized by progres­sive anemia.

In 1989, it was estimated that perhaps as many as one billion people, most of them living in tropical and subtropical regions, are afflicted to some extent with hookworm infection, although it is not known how many thus infected can be said to be victims of hookworm disease.

Two species of intestinal nematode, Ancylostoma duodenale and Necator americanus, are the parasites that cause ancylostomiasis. Although they appar­ently cause the same disease, there are important differences between the two species. A. duodenale is slightly larger, sickle-shaped, with hooks or teeth; N. americanus is smaller, “S” shaped, with shell-like semilunar cutting plates instead of teeth. Despite being named the “American killer,” N. americanus is less pathogenic than A. duodenale, as measured by comparative blood loss. A. duodenale has a higher reproductive rate and a shorter life-span. It is also able to infect the host in more ways than can N. americanus. Hookworm disease has been called by nearly 150 different names, taxonomic as well as colloquial. Many, such as geophagia and langue blanche, describe physical symptoms, clinical fea­tures, or unusual behavior associated with the afflic­tion.

Etiology and Epidemiology

Although A. duodenale can be ingested in contami­nated food, water, or possibly breast milk, the more common route of infection, and the only one for N. americanus, is through penetration of the skin. Lar­vae in the soil typically enter through the skin of the feet, frequently causing dermatitis, once called “ground itch” or “dew poison” in the southern United States, and “water itch” or “coolie itch” in India. Then the parasites travel through the bloodstream to the alveoli of the lungs, climb the respiratory tree, and make their way into the esophagus. During their migration through the airways into the esophagus, the host sometimes develops a cough, wheeziness, or temporary hoarseness. The hookworms are then swal­lowed and pass into the gut, where some will success­fully attach themselves to the small intestinal mucosa and begin nourishing themselves on their host’s blood. In the small intestine, hookworms will grow to a length of about 1 centimeter and mature in 6 to 8 weeks after initial infection. Depending on the species, hookworms generally live from 1 to 5 years, although a few apparently live longer. The adult fe­male may produce thousands of ova per day, which pass out of the body with the host’s feces. Egg produc­tion varies with the species, the age of the worm, the number of worms in the gut, and the degree of the host’s resistance. If deposited on warm, moist soil, the eggs will produce larvae that will molt twice over 2 weeks before becoming infective and can survive in a free-living state for over a month before finding a host.

Hookworms thrive on human ignorance and pov­erty. If the billions of people living in areas of hook­worm infestation were able to eat moderately well, wear good shoes, and defecate in latrines, hookworm disease would soon no longer pose a serious threat to human health.

Distribution and Incidence

The earliest global survey of hookworm distribution was conducted in 1910, in preparation for a cam­paign against hookworm disease carried out by the Rockefeller Foundation. Responses from 54 coun­tries led to a preliminary description of a “hookworm belt” girdling the Earth between 30^o south latitude and 36^o north. Another survey conducted at the same time estimated that 40 percent of the inhabit­ants of the southern United States suffered in vary­ing degrees from hookworm infection. The larvae prefer shade, and light sand or loam soils. They thrive in the southeastern coastal plains of the United States, but not in the Piedmont clays. Al­though infection has not been eliminated in the United States, the public health menace of hook­worm disease has disappeared, only in part because of the earlier treatment and control programs, but largely as an incidental consequence of the concen­tration of the population in cities and towns with sewer systems, and the general improvement in sani­tary conditions and the standard of living for those remaining on the farms.

It is still, however, a chronic fact of life in most of the rest of the regions within the old “hookworm belt.” In the Caribbean, Central and South America, Africa, China, India, Southeast Asia, and Oceania, endemic hookworm infection remains widespread and largely untreated. After a flurry of activity in the first three decades of the twentieth century, hook­worm prevention and treatment programs have been sporadic and uncoordinated. This recent his­tory of neglect has made it difficult even to estimate the incidence of hookworm disease in areas of the world where hookworm infection is known to be prevalent. A combination of factors helps to explain why hookworm lost the attention it once received from philanthropic organizations and public health agencies. The failure of earlier intensive efforts to make quick, dramatic reductions in the incidence of hookworm infection and hookworm disease led pub­lic health officials with limited budgets to conclude that a concentration of resources elsewhere would produce better results. Hookworm infection came to be regarded as a stubborn condition of rural poverty in developing nations. The campaigns of the 1910s and 1920s seemed to demonstrate the futility of treating the condition in a systematic way without major improvements in the general standard of liv­ing. Other diseases such as smallpox and malaria were both deadlier and less obviously the conse­quences of social and economic circumstances be­yond the control of public health workers.

Other parasitic diseases for which there are no effective anthelmintics were given research priority and funding, thus distracting workers in developed countries and signaling public health officials in de­veloping countries that hookworms and other soil- transmitted parasites were no longer as important as they once had seemed.

Clinical Manifestations and Pathology

Theoretically, the presence of a single parasite is detrimental in some way to the host. In reality, how­ever, adequately nourished persons with light infec­tions are not likely to suffer discernible ill effects or to exhibit the clinical features associated with hook­worm anemia. Children and pregnant women will begin to manifest symptoms of hookworm disease at lower levels of infection, as greater demands on their normal iron stores already exist. Efforts to establish a threshold of infection above which the host might be expected to begin to show signs of hookworm anemia have been frustrated by the inability to con­trol other significant variables such as nutrition and general health in a population large enough to be statistically valid. An otherwise healthy person with a normal daily intake of iron can apparently tolerate several hundred hookworms without patently ad­verse effects. The likelihood of hookworm disease in an individual varies in direct proportion to the worm burden and in inverse proportion to iron intake.

Hookworm disease shares many of the same clini­cal symptoms accompanying other kinds of anemia. Persons suffering from severe hookworm infection often have a pale and wan appearance, a tell-tale yellow-green pallor to the skin that helps to explain why the disease was sometimes called “Egyptian chlorosis” or “tropical chlorosis” in the years before the parasite was discovered and described in the medical literature. In children, growth may be sig­nificantly retarded. A distended abdomen and pro­nounced, sharply pointed shoulder blades (“pot belly” and “angel wings” in the American South) were once thought to identify children with hook­worm disease, although the same features often ac­company malnutrition as well.

A diagnosis of hookworm infection can be made easily if ova are detected during a microscopic exami­nation of a fecal smear. Quantitative methods have made it possible to estimate both the total number of eggs based on a quick count in the area under the cover slip and the quantity of hookworms lodged in the intestine. Since the nineteenth century, dozens of anthelmintic drugs have been tried, including thymol, oil of chenopodium, carbon tetrachloride, and tetrachloroethylene. More recently developed hookworm vermifuges include bephenium, mebenda­zole, pyrantel, and thiabendazole. A regimen combin­ing chemotherapy with the simultaneous adminis­tration of iron tablets now seems to be the most effective way to eliminate the parasites and at the same time to restore the hemoglobin to a normal level quickly.

The probability of reinfection is high, however, if a person thus treated continues to walk barefooted on ground contaminated with hookworm larvae. This discouraging realization has bedeviled public health workers since the days of the massive early control programs. Numerous designs for sanitary latrines have come and gone over the years; their construc­tion costs placed them beyond the means of impover­ished agricultural workers. Cheaper and less sani­tary latrines were often worse than no latrines at all, as they tended to concentrate the locus of infec­tion in a small area where people habitually went to defecate. Reinfection would occur rapidly in such instances, although it would take somewhat longer to reach pretreatment worm burdens.

The problems posed by unsanitary latrines were universal. Other difficulties were specific to certain regions or cultures, though no less imposing for that.

For example, an extensive treatment and control campaign in China in the early 1920s foundered on the age-old practice of fertilizing mulberry trees with human feces, often infested with hookworm ova, acquired in massive quantities from brokers who collected it for that purpose in nearby villages. For centuries, then, the Chinese silk industry had sustained a disease afflicting its workers whose con­taminated feces nourished the crop on which their livelihoods depended.

History and Geography

From Ancient Times Through the Nineteenth Century

Hieroglyphic entries on the Ebers Papyrus (c. 1550 B.C.) describe a mysterious affliction, a-a-a disease, thought by some to be hookworm anemia, but by others, schistosomiasis. In the fifth century B.C., Hippocrates described a pathological condition marked by dirt eating, intestinal distress, and a yellowish complexion. A handful of other sketchy descriptions from the Mediterranean basin in the ancient and early medieval periods now appear to be reports of hookworm disease. From the Western Hemisphere in the centuries after European coloni­zation came scattered accounts from English, French, Spanish, and Portuguese settlers of epidem­ics among their slaves, called by a rich variety of colloquial names and now thought to be descriptions of widespread hookworm infestation.

The Italian physician Angelo Dubini was the first to report the discovery of hookworms in a human. He detected them first during an autopsy in 1838 and again in 1842. His interest aroused, Dubini exam­ined 100 cadavers for hookworms and found them in more than 20. His 1843 article provided a detailed description of the parasite, which he named “Agchy- lostoma” (a faulty transliteration of the Greek words for “hook” and “mouth”) duodenale. Dubini did not believe that hookworms had caused the deaths of any of the people he had examined, although he did detect a slight inflammation of the intestinal mucosa at the point of attachment. By 1846, Dubini’s parasites had been found in Egypt and, by 1865, in Brazil. In 1878, a trio of Italian scientists - Giovanni Battista Grassi, Corrado Parona, and Er­nesto Parona - announced that they had detected hookworm ova in the feces of anemic patients, thus making it possible for anyone with access to a micro­scope to diagnose hookworm infection.

In 1880, an outbreak of anemia among the miners digging the St. Gotthard tunnel in the Alps gener­ated a wave of public concern in Italy. Within weeks, hundreds of miners were examined and found to be infected with hookworms. Edoardo Perroncito, a pa­thologist at the University of Turin who had found over 1,500 hookworms in a postmortem examination of a miner, argued that the presence of hookworms in large numbers and the epidemic of anemia were causally related. In 1881, Camillo BozzoIo reported that he had had success using thymol to treat the infection. For the next 35 years, thymol remained the most widely used drug in the treatment of hook­worm disease.

Twentieth-Century Writings

In 1898, Arthur Looss in Cairo first suggested that hookworm larvae could penetrate the skin. He had accidentally infected himself by spilling water con­taminated with hookworm larvae on his hand. Shortly afterward, the spot on his hand where the water had spilled began to burn and turned red. He surmised that the hookworm larvae were responsi­ble. Two to three months later, he found hookworm ova in his feces. Although Looss’s announcement was initially greeted with considerable skepticism, further experimentation by himself and others had by 1901 confirmed beyond doubt the percutaneous route of infection. Looss was later to describe the migratory path of the hookworm within the host.

While Looss was developing his theory of skin penetration in Egypt, a U.S. Army physician sta­tioned in Puerto Rico, Bailey K. Ashford, discovered in 1899 that hookworm infection was rampant among the agricultural workers in the sugar cane fields (Ashford 1900). In 1903, Ashford persuaded the governor to budget funds for the creation of the Anemia Commission of Puerto Rico, the first large antihookworm program of its kind in the world.

Ashford had believed that the hookworms he found in Puerto Rico were A. duodenale. At the time of his discovery, no other species was known to infect humans. Charles W. Stiles, a zoologist trained in Germany working for the U.S. Department of Agri­culture, examined a sample of Ashford’s hookworms and others sent to him from different parts of the United States. He compared them with samples of A. duodenale and concluded in 1902 that these hook­worms were indigenous to the Western Hemisphere and were a different species, which he named Necator americanus. In 1905, Looss found N. ameri­canus in six Central African pygmies brought to Cairo for a music hall exhibition. He speculated that N. americanus originated in the Eastern Hemi­sphere and was brought to the Americas by African slaves. Within 2 years, N. americanus had been found extensively not only in Afnca but also in India and Australia. Whether A. duodenale might also have been introduced into the Americas at about the same time by the first Spanish explorers and the conquistadors has been the subject of some disagree­ment. The theory that A. duodenale existed in pre­Columbian America seems to have been bolstered by the discovery in 1974 of what appears to be an A. duodenale in the intestine of a Peruvian mummy dating from about A.D. 900. Both species are wide­spread in both hemispheres, although their origins remain murky.

In 1909, John D. Rockefeller created an organiza­tion to eradicate hookworm disease in the southern United States. Stiles, who maintained that eradica­tion was an unrealistic goal, had nevertheless per­suaded Rockefeller’s principal philanthropic advisor, Frederick T Gates, that hookworm infection was a serious problem. With $1 million at its disposal, the Rockefeller Sanitary Commission established opera­tions in 11 American states. Over its 5-year exis­tence, the Rockefeller Sanitary Commission awak­ened the public to the nature and extent of the threat, stimulated widespread concern for improved sanitation, treated almost 700,000 people suffering from hookworm infection, and invigorated long- moribund state boards of health. It failed, however, to eradicate hookworm infection anywhere.

At the invitation of the British Colonial Office, the Rockefeller Foundation in 1914 undertook a world­wide campaign modeled on the experience of the Rockefeller Sanitary Coipmission. They opened op­erations in the British possessions in the West Indies before extending the work into British Guiana, Egypt, Ceylon, and Malaya. By the end of the First World War, Rockefeller programs were underway or ready to begin in Central America, Brazil, and China. Shortly thereafter, Rockefeller-sponsored campaigns were in place in most of the countries in the tropics. Their earlier experience in the southern United States had led administrators of the Rockefel­ler Foundation programs to employ a combination of two approaches to the problem of hookworm infec­tion. The dispensary method attracted people from the surrounding area to a day-long demonstration conducted by a Rockefeller physician assisted by mi­croscopists during which examinations were carried out and treatments dispensed, while the crowd heard lectures on prevention and improved sanita­tion. The intensive method was based on a different approach to the problem of hookworm infection. A clearly delimited area was selected for a saturation campaign of aggressive hookworm treatment and latrine construction.

Beginning in the early 1920s, the Rockefeller Foun­dation had begun to rethink its basic approach to hookworm work. The early days of extensive, pro­tracted campaigns had produced negligible results. The incidence of hookworm infection in Puerto Rico, for example, was as high in 1920 as it had been in 1903, just before Ashford’s Anemia Commission be­gan to go to work. Not yet prepared to abandon hook­worm work altogether, the Rockefeller Foundation gradually withdrew from massive treatment cam­paigns and began to redirect its efforts toward labora­tory research, with field work restricted to the gather­ing of data and the testing of hypotheses and drugs. By the mid-1920s, disillusionment had set in and the days of the antihookworm crusades were over. Since then, although laboratory work has revealed much more about the relationship between humans and hookworms, little has been done in a practical way to rid the former of the latter, except where there have been improvements in living conditions.

John Ettling

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