Parasitic zoonoses in perspective

OOZO-7519:91 53.00 + 0.00 Pergamon Press pi& Ausrralian Society for Parasifolopy

t~f~~~fi~l Jaurmdfor Parasitofogy Vol. 21, No. 2,pp. 161-170, 1991 Printed in Great Mm&

RVVITEDREVIEWARTICLE PARASITIC ZOONOSES IN PERSPECTIVE PETER M. SCHANTZ Division of Parasitic Diseases, Center for Infectious Diseases, Centers for Disease Control, Public Health Service, U.S. Dept of Health and Human Services,Atlanta, GA 30333,U.S.A. (Received 22 November

1990)

CONTENTS INTRODUCTION LYME BORRELIOSIS AND OTHER TICK-BORNE TRICHINELLOSIS TOXOCARIASIS AND ANCYLOSTOMIASIS ECHINOCOCCOSIS/HYDATIDOSIS TAENIA SOLIUA4 TAENIASIS/CYSTICERCOSIS GIARDIASIS CRY~OS~RIDIOSIS OPPORTUNISTIC INFECTIONS CONCLUSIONS REFERENCES

INFECTIONS

I61 162 163 164 165 I66 167 168 168 168 168

INDEX KEY WORDS: Zoonoses; helminth and protozoa; Lyme borreliosis; trichinellosis; toxocariasis; ancylostomiasis; echinococcosis; cysticercosis; giardiasis.

INTRODUCTION ZOONOTICdiseases can be viewed from many perspectives. The more than 150 currently recognized zoonotic diseases represent all known classes of infectious agents (Acha & Szyfres, 1987). The variety of animal hosts varies greatly, as do modes of transmission from animals to humans. Zoonotic diseases can also be ranked according to their impact on public health or the economy. This can be taken further by comparing the different factors which contribute to the perpetuation or the impact of zoonotic diseases in different socioeconomic systems. In this regard, the spectrum of zoonotic diseases and the imposed public health burden are vastly different in developing countries than in modern industrialized countries (McKeown, 1988). Diseases of animal origin remain of greatest importance in rural areas of developing countries, where most people live. In such regions people commonly share their home environments with a variety of animal species under conditions of poor sanitation and hygiene that inevitably lead to frequent exposure to each other’s pathogens. Since veterinary services are often lacking, and human medical care is usually inadequate, zoonoses are often among the diseases of major economic and public heahh importance. In Latin America, for example, zoonotic diseases, including those of parasitic origin, rank high among diagnosed diseases (Acha & Arambulo, 1985). Although none of these are major causes of mortality, they take a heavy burden in terms of human

morbidity. They also result in direct economic losses by reducing the productivity and value of animal hosts. In Latin America and other developing countries, zoonotic diseases interact with other causes of morbidity and mortality and with relentless population increase to aggravate poverty and to constrain efforts to spur economic growth and human welfare. They serve as reminders that much of the Third World has not yet benefited from what has been referred to as the “first public health revolution,” that is, the massive improvements in environmental sanitation, housing, and nut~tion in modem, industrialized countries that have resulted in conditions that severely limit the transmission of most infectious diseases (United States Department of Health, Education and Welfare, 1979). In Western industrialized countries, prevailing demographic, economic, and social conditions produce patterns of morbidity and mortality quite distinct from those in the developing world (United States Department of Health and Human Services, 1989). The strengthening of this trend is seen very dramatically by comparing the 10 leading causes of death in the United States in 1900 and 1985. At the turn of this century, four of the leading causes of mortality were infectious diseases. Today the only infectious disease ranked among the top 10 is the pneumonia/influenza complex, which kills mainly persons >75 years of age and thus causes relatively little premature mortality. Today’s top killers are heart disease, stroke, cancer, accidents and violence. 161

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Recognition of these current public health realities has led to new public health goals and priorities in most developed countries. My organization, for example, the Centers for Disease Control (CDC), reorganized in 198 1 and significantly broadened its programmatic scope to include diseases related to the environment, occupational health hazards, and promotion of health. Such significant changes required major commitments of funds, personnel, and other resources. Unfortunately, these decisions and reorganizational plans were made in a time of increasing restrictions on funds to the public sector. Furthermore, at about the same time, acquired immunodeficiency syndrome (AIDS) emerged as the most urgent public health concern in the U.S. These two events have limited the response to the changing public health priorities mentioned above and have had an unfortunate retrogressive effect on research and control of most infectious diseases other than AIDS. The effect of these events can be seen in budgetary terms: all the increases in the CDC budget since 1980 were accounted for by funding for AIDS and new programs and grants. The funding for core activities, which includes most research and control of zoonotic diseases, has actually decreased if inflation is taken into consideration. These facts reflect a reality with which all of us who work on parasitic diseases are familiar. However, I believe that the situation has descended to a critical point where it is becoming difficult to attract students and to obtain funding for training and research on parasitic zoonoses. Zoonotic diseases are epidemiologically complex, and adequate research capability requires scientists representing multiple specialties in biology, medicine, veterinary medicine, and environmental sciences. If current trends continue, we may lose our capacity to prevent and control this group of infections. Fortunately, the lack of generous funding for research on parasitic zoonoses is partially compensated for by the talent of the scientists already dedicated to this field and by the international networks that have been created to foster exchange of information and collaboration between workers. Thus, despite limited and inconsistent funding, significant progress has been made. We have learned more about host-parasite relationships at the individual and populations levels. We are also seeing the fruits of the revolution in molecular biology: new tools for clinical and epidemiologic studies and better methods of treatment and prevention. Presented below are some examples of parasitic zoonoses from the United States that serve to illustrate the perspective on these diseases from one industrialized country. They represent newly emerging and rapidly changing diseases as well as old ones that just won’t go away. They represent the indigenous and the imported. Some of these diseases are reflections of old cultural traditions or existing poverty, while others owe much of their current status to society’s modern technology.

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LYME BORRELIOSIS AND OTHER TICK-BORNE INFECTIONS

Many infections have only recently been discovered or have become recognized as more important after having been known for a long time. Among such infections are babesiosis, Legionnaires’ disease, toxic shock syndrome, Lyme disease, AIDS, cryptosporidiosis, and microsporidiosis. The emergence of these diseases reminds us of our continued vulnerability to infectious and parasitic diseases. Lyme disease, or Lyme borreliosis, has been present for many centuries if not forever. However, its tickborne zoonotic agent, Borrelia b~rgdor~F~,and its full clinical syndrome have only been characterized in the United States since 1976 (Steere, 1989). Were Lyme disease not overshadowed by the more serious AIDS, it would be the most serious public health crisis currently faced in the United States. Typically, the earliest manifestations of Lyme borreliosis are a bulls-eye type e~thematous rash at the site of the tick bite, accompanied by fever, stiffness, and other flu-like symptoms. Weeks or months later, more serious signs related to involvement of the joints, the neurologic system, and the heart may develop. Although the illness responds favorably to antibiotic therapy in its early stages, relapses are not uncommon and subacute and chronic neurologic complications may persist for years in some patients. The principal vector is a three-host tick, Ixodes dczmmini. The adult tick feeds on deer, but in its larval and nymphal stages the tick parasitizes mice, which carry the spirochaete. The disease spreads to people when infected tick larvae develop into nymphs and the tick nymph bites a human being (Mad&an & Teitler, 1988). These are very small ticks, and tick bites are, therefore, often unnoticed. About half of patients do not give a history of tick bites (Steere, 1989). Unknown in the United States 1.5years ago, Lyme disease has increased 15-fold in the 7 years since nationwide reporting began in 1982. Preliminary 1989 reports indicate approximately 7402 cases (Centers for Disease Control, 1989a). Although most intense transmission occurs in the northeastern, middle Atlantic, and north central states, the disease is now reported from 46 states. In some areas, particularly in the northeast, agricultural lands have been allowed to revert to woodland, and deer have been encouraged to repopulate these areas. The proximity of deer and rodent populations to households permits high tick populations, high rates of infection, and frequent opportunities for exposure of humans (Madigan & Teitler, 1988). Current data suggest that the parasite may have spread throughout the continental United States. One reason postulated for the recent geographic spread of the disease is that the vector ticks are being carried by birds to new geographic areas. The parasite becomes a problem to humans when a critical threshold of spirochaetes, reservoir hosts, and the number of competent vector ticks is exceeded. Most tick-borne

Parasitic zoonoses in Perspective diseases are diseases of place; people are exposed when they enter into the tick life cycle as a result of occupational or recreational pursuits. However, in certain parts of the country, exposure to Lyme disease is primarily peridomestic. There is public concern that dogs may bring home infected ticks and expose their owners; however, epidemiologic studies do not suggest this to be common. Increased research on Lyme disease is imperative to reduce the further spread of this disease. Research priorities include specific diagnostic tests, improved treatment, and effective prevention strategies. Lyme disease is now the most common vector-borne disease in the United States. However, three other tick-borne diseases, Rocky Mountain spotted fever (RMSF), tularemia, and Colorado tick fever follow Lyme disease on this list. A fifth tick-borne disease, ehrlichiosis, has only recently been described in human beings. The agent, Ehrlichia canis, a type of Rickettsia, is known to cause a severe infection in dogs characterized by parasitism of white blood cells. In humans the disease is an acute febrile illness. More than 100 cases of human ehrlichiosis have been reported since the disease was recognized in 1986 (Centers for Disease Control, 1990). Although substantially fewer cases of ehrlichiosis than RMSF are reported, two recent studies indicate that in some geographic areas the incidence of human ehrlichiosis may equal or exceed that of RMSF. The vast majority of cases have been reported from the same south central and southeastern states as RMSF. We know little of the means by which this infection is transmitted to humans or the role of wild and domestic animals as reservoirs in human ehrlichiosis. Still another tick-borne infection of public health importance in the United States is babesiosis due to the protozoan Babesia microti. The reservoirs of B. microti are the same rodents that are hosts to Borrelia burgdorferi. The principal tick vector is also the same. Human infection is no longer a rarity in the coastal areas and islands of Massachusetts, Rhode Island, and New York (Centers for Disease Control, 1989b). The emergence of Lyme borreliosis and, more recently, human ehrlichiosis, has dramatically increased the awareness and importance of tick-borne zoonoses as public health problems. TRICHINELLOSIS

The United States is infamous for the occurrence of trichinellosis. Although the incidence has declined markedly during the past 50 years (Bailey & Schantz, 1990), the United States remains in the unenviable position of being one of the few developed countries where trichinellosis is still perceived as a public health problem. The history of this disease is of interest from both a public health and a political perspective. About 110 years ago, Germany, recognizing that pork from the U.S. contained Trichinella and was a danger to public health, banned the importation of the product. This action was repeated by other European

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countries, and the ban, with certain exceptions, continues today. Public concern about trichinellosis probably reached its peak in the 1940s when outbreaks were common and an average of about lO15 deaths per year were recorded. A study of human cadavers at that time showed 16% were infected (Wright, Jacobs & Walton, 1944). Although the United States has never had a specific trichinellosis control program, multiple events, some government sponsored, have contributed to significant declines in transmission of infection between pigs and from pigs to humans (Leighty, 1983). The prohibition of feeding raw garbage to pigs was an important factor. More recent control measures include preventing pigs from scavenging on dead pigs and eliminating rats, which contain Trichinella in a commensal cycle. Another important factor in the prevention of trichinellosis has been consumer education. At present, virtually every U.S. citizen knows that pork should be cooked well, even though they may not know why. The U.S. Department of Agriculture further legislates that all pork marketed as a ready-to-eat product must be processed to destroy TrichineIIa. Low-dose ionizing radiation (30-50 krad) is effective for preventing Trichinella infection and recently has been approved by the government for processing pork and other foods. The industry, however, has shown limited interest in this safe and effective technology because of widespread consumer fear and mistrust of radiation (Sun, 1984). In the United States, routine post-mortem detection of Trichinella-infected pigs has never been employed. Tbis may remain true even though the sensitivity and cost-effectiveness of the diagnostic technology has increased significantly. A highly sensitive and specific antibody test based on first-stage larval metabolic antigens has been shown to be capable of detecting infections as low as one larva per 100 g of meat (Madden & Murrell, 1990). The test is currently under consideration for approval as an ante-mortem test for trichinosis and, if approved and applied, could further reduce the pubiic health problem of trichinosis in the United States, as has been achieved so effectively in several European countries. The number of reported cases of human trichinellosis continues to decline. In the last 5 years, an average of about 57 cases were reported each year (Bailey & Schantz, 1990). Most of this decline was the result of a reduction in the number of cases acquired from domestic pork products. The number of cases of trichinellosis acquired from wild animal meat has always been relatively low, but has recently increased as a proportion of total cases. Trichinella is enzootic in scavenging carnivores throughout North America. Transmission of infection in humans occurs regularly from these sylvatic sources through ingestion of bear meat and, more rarely, from other wild animal sources such as walrus and seal meat in Arctic regions. That these sylvatic reservoirs of Trichinella represent an important source for re-establishing the infection in

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domestic swine populations has long been suspected. Recent studies have shown, however, that the strain or strains indigenous to sylvatic animals represent gene pools distinct from those of the parasite in domestic swine (Zarlenga & Barta, 1990). The sylvatic strains do not readily infect domestic pigs. Similarly, recent studies using repetitive DNA probes have shown that only rarely is the pig-adapted strain recovered from wildlife (Minchella, Branstetter & Kazacos, 1989). In rare cases, wild animals appeared to acquire the pigtype parasite from scavenging or being fed garbage. The United States has reached a critical juncture in trichinellosis control. The low number of human cases prevents this disease from being ranked as a public health priority and lowers the level of public concern. New technology that could be applied to detect or inactivate infected carcasses as routine processing methods are now available and could be applied to finally eliminate this public health problem. However, whether the public and the regulators have the political will to implement the technology remains to be seen. TOXOCARIASIS

AND ANCYLOSTOMIASIS

Although in most industrialized countries the percentage of persons in contact with livestock animals has decreased greatly, the number of animals kept as pets has increased, at least in the United States. Some 52 million dogs are currently distributed in 38% of all households, as are nearly 55 million cats (Anon, 1988). Nearly 60% of households have either a dog or a cat. Consequently, potential exposure to zoonotic disease agents of pet animals is greater than ever before. Among these diseases, larva migrans due to the common roundworms of dogs and cats, Toxocara spp., is probably the most common. The frequency of dog and cat ownership, the high prevalence of Toxocara infection, the widespread environmental contamination with Toxocara eggs, and the play habits of children all combine to result in frequent opportunities for zoonotic transmission of the nematode. CDC receives thousands of serum specimens each year from patients with a presumptive diagnosis of Toxocara infection, and we estimate that a minimum of 1000 cases of ocular larva migrans syndrome are diagnosed every year (Schantz, 1989a). This past decade has seen a virtual explosion of knowledge about Toxocara infection and disease. The mean annual number of scientific publications on Toxocara larva migrans cited in the National Library of Medicine’s Medline file has doubled in the past 10 years, primarily as a consequence of the development of improved serodiagnostic procedures that have been used widely for clinical and experimental studies (Schantz, 1989a). Although much remains to be done to improve serologic tests, enzyme immunoassays using Toxocara excretory-secretory antigens have been a major asset for clinical diagnosis and a useful tool for epidemiologic surveys that were previously impossible (Glickman, Schantz & Grieve, 1986).

In the United States, we have used these tests for seroepidemiologic studies of toxocariasis on representative samples of the population (Glickman & Schantz, 198 1; Herrmann, Glickman & Schantz 1985). Seroprevalence varied from 4.6 to 7.3% in different geographic regions and was strongly associated with the black race, rural residence, and low socioeconomic status. The rate approached 30% among black children aged 6-11 of low socioeconomic status. Similar findings have been reported from numerous other countries (Nicholas, Stewart & Walker, 1986; Clemett, Williamson, Hidajat, Allardyce & Stewart, 1987; Kenny & Allwright, 1987; Embil, Tanner, Pereira, Staudt, Morrison & Gualazzi, 1988). Such findings are usually described as reflecting the prevalence of asymptomatic toxocariasis; however, Toxocara infection may cause neurological deficits or behaviour disorders in children who may not show obvious signs of infection. In experimentally infected animals, larvae clear the liver in the first few days and accumulate progressively within the central nervous system (Dunsmore, Thompson & Bates, 1983). This occurs in humans as well, but little is known about the possible consequences of these parasites accumulating in the CNS. Whether so-called asymptomatic Toxocara infection might cause epilepsy or other subtle neurobehavioral alterations is an important question. Several studies have shown that children with epilepsy are more likely to be infected with Toxocara infection (Glickman, Cypress, Crumrine & Gitlin, 1979; Arpino, CastelliGattinara, Piergilli & Curatolo, 1990). Still other studies have shown hyperactivity, neuropsychological deficits and lack of motor coordination in infected children (Worley, Green, Frothingham, Sturner, Walls, Pakalnis & Ellis, 1984; Marmot-, Glickman, Shofer, Faith, Rosenberg, Cornblatt & Friedman, 1987). However, methodological problems inherent in the design of these studies prevented the establishment of clear cause-and-effect relationships. These questions cannot be resolved by retrospective, nonblinded studies; they require a prospective design with adequate sample size and periods of observation. Given the widespread occurrence of this environment contaminant, such studies would seem to be warranted. Hookworms are other common parasites of dogs and cats that are capable of producing larva migrans syndromes in humans (Kalkofen, 1987). Cutaneous larva migrans, characterized by progressive linear eruptive lesions caused by the prolonged migration of the larvae in the skin, is the most common manifestation of zoonotic hookworm infection. In the United States, this condition is mainly due to Ancylostoma braziliense, which is common in dogs and cats in the Atlantic and Gulf coastal areas in the southeastern United States (Beaver, 1956). Infections are seen in electricians, plumbers, and other persons who have to crawl beneath a raised house or building, in children and in sun bathers who recline on wet sand

Parasitic zoonoses in perspective contaminated by hookworm larvae (Centers for Disease Control, 198 1). Ordinarily the lesions are self-limiting, and the intense pruritis subsides in a few days or weeks (Enander & Adam, 1989); however, in some cases the larvae may penetrate into deeper tissues and produce symptoms of visceral larva migrans (Little, Halsey, Cline & Katz, 1983). Of great concern regarding the zoonotic potential of another species of hookworm, A. caninum, is a recent report (Prociv & Croese, 1990) of epidemic eosinophilic enteritis in Townsville, Australia. The patients experienced severe abdominal pain, diarrhea, weight loss, and melena. Colonoscopic examination and resection of the ileum was done in several patients, and in two of them hookworms recovered from the ileum were identified as A. caninum. The observed syndrome was interpreted as a local allergic reaction to the feeding hookworms. Many questions remain to be answered; however, the potential implications of this report are quite astounding. A. caninum is a nematode with worldwide distribution, and the expense and invasive nature of the required diagnostic procedures make it quite plausible that the condition may be more widespread but misdiagnosed. Most cases of human toxocariasis and zoonotic hookworm infection are preventable by simple measures such as careful personal hygiene, eliminating intestinal parasites from pets, and not allowing children to play in potentially contaminated environments. Unfortunately, at least in the United States, few people are aware of the health hazards associated with pets. Surveys of families of patients with larva migrans and of pet owners in general reveal a remarkable ignorance of potential zoonoses (Fontaine & Schantz, 1989). Therefore, pet owners lack the incentives to ask the right questions or to take simple precautions. Veterinarians could be effective in reversing this lack of knowledge by systematically providing pet owners with sound advice. Veterinarians are uniquely suited for this role because of their special knowledge and their rapport with clients and because a high proportion of pet owners use veterinary services. However, we know from recent surveys that about a third of U.S. veterinarians either never discuss potential zoonotic hazards with clients or do so only when asked (Harvey, Roberts & Schantz, submitted for publication). Another one-third say they discuss these potential hazards whenever worms are diagnosed; however, since many pups and kittens are not brought to veterinarians until they are 6 or more weeks old, extensive contamination with roundworm or hookworm eggs may have already occurred. Our survey suggested that only about half of veterinarians recommended that pups first be treated for intestinal worms prior to 1 month of age, when morbidity to the animals and contamination of the environment with potentially infectious eggs could be prevented.

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ECHINOCOCCOSIS/HYDATIDOSIS Echinococcus granulosus, the cause of classic cystic hydatid disease, remains widely dispersed through the world. Several successful control programs, pioneered in New Zealand and Tasmania, have demonstrated that this zoonosis can be controlled, but the results have produced only minor modifications in the global distribution and the public health impact ofthe disease (Schantz, 1989b). In some regions the disease has been almost totally neglected and continues to exact great suffering and mortality. Surveillance studies only recently initiated in China have determined that the disease exists in 20 provinces and autonomous regions involving more than 85% of the country (Chi, Fan, Zhang, Hasyet, Zhang, Tuerhon, Ha-jang, Li, Tian, Liu, Jia, Ye, Chen, Ming & Sung, 1989). It is classified as hyperendemic in areas with a population of more than 50 million people. The most severe problem appears to exist in Xinjiang Uighur Autonomous Region, which has a population of 13 million people (Chi, Zhang, Zhang, Hasyet, Lie, Ding, Andersen, Tolley & Schantz, 1990); in 1986 there were nearly 3000 surgical procedures for hydatid disease performed in hospitals in Xinjiang alone, and the zoonosis was listed as the most important infectious disease in this region. A National Hydatid Disease Control Center has been established in Xinjiang, and research and control programs are being planned and implemented. Although cystic hydatid disease is not considered an important public health problem in the United States, sporadic cases occur in several transmission foci. At least two separate strains of Echinococcus granulosus exist. At higher latitudes, the northern sylvatic strain of E. granulosus occurs in wolf, moose, and caribou (Rausch, 1986). In some western states, a strain adapted to dogs and sheep occurs. Until recently, cycles involving pigs and dogs occurred in the Mississippi delta region; however, the disease has not recently been reported in this region. The confinement of the northern sylvatic strain to wild animal intermediate hosts limits the risk of human exposure. In Arctic and sub-Arctic regions, however, where indigenous people subsist mainly by hunting wild reindeer, dogs kept as a means of transportation may be fed the lungs of infected deer or, if unrestrained, may scavenge on viscera left by the hunters (Rausch, 1986). The risk of transmission to nomadic hunters is usually low if habitations are moved before the environment becomes grossly contaminated by dog feces. In permanent settlements, the risk is much higher. E. granulosus life cycles involving dogs and sheep are reported from several western states. Evidence exists that the parasite may have been introduced into California or another western state around 1938 in sheep dogs imported from Australia (Crellin, Andersen, Schantz & Condie, 1982). Movement of infected dogs or sheep to other states probably resulted in spread. Maintenance of the parasite and

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transmission to humans in these states are associated with a variety of unique cultural or occupational practices. In California, the parasite is maintained in sheep herds, which are allowed to graze harvested fields. Transmission to humans occurs among the shepherds, who are usually young men of Basque origin; however, movement of infected dogs to the residences of the owners of the animals also creates a risk (Araujo, Schwabe & Sawyer, 1975). Transmission also occurs on Navajo lands and in the flocks of some of the other native American groups (Schantz, 1977). Sheep are regularly butchered, usually by women, and parts of the sheep considered unfit for human consumption are given to the dogs, an excellent means of perpetuating transmission. In central Utah, sheep herders hire local people as herders and often permit their dogs to consume the viscera of butchered sheep (Crellin et al., 1982). In this region, a control program based on health education and dog-testing carried out by local and state groups reduced infection in sheep from 6-13% in 1971-1972 to less than 0.1% in 1984 (Andersen, Crellin, Nichols & Schantz, 1983). Echinococcus multilocularis, the cause of the alveolar form of hydatid disease, also occurs in North America. Growth of Echinococcus multilocularis is very different from that of E. granulosus, and the disease in humans has similarities to malignant tumors in that it is an insidious and progressive growth with occasional metastases to the lungs and brain. By the time most cases become clinically manifest, too much of the liver is involved to be completely resectable by surgery. In Alaska until 1980, only about one in four cases was resectable at the time of diagnosis (Wilson & Rausch, 1980). Despite the extensive occurrence of the foxes and rodent species infected by this parasite in Arctic and sub-Arctic zones of North America, nearly all human cases of the disease have been limited to a few Eskimo communities on islands and in northwestern coastal areas of Alaska. There are multiple potential sources of infection for people in these villages (Rausch & Schiller, 1956). Trapping foxes is a traditional economic pursuit, and women and children assist in skinning these animals. Dogs that prey on commensal rodents living in the village serve as a source of infection for the residents. Since fox feces are scattered widely on the tundra, gathering of greens, roots, and berries can also act as a source of Echinococcus eggs when these foods are eaten without cooking. In addition, surface water has been suspected as a potential source of infection. A recent retrospective epidemiologic study of 19 cases and 38 controls, however, showed that the most likely primary sources of infection were the dogs living in the villages (Stehr-Green, Stehr-Green, Schantz, Wilson & Lanier, 1988). Patients were more likely than control persons to have owned dogs for their entire lives, tethered their dogs near their house, and lived in houses built directly on the tundra rather than on

SCHANTZ

gravel or a permanent foundation. Local environmental conditions permitted accumulations of infected dog feces, representing a constant potential danger to people living in adjacent houses. A control intervention based on monthly treatment of dogs with praziquantel was recently undertaken in one of the villages (Rausch, Wilson & Schantz, 1990). The intervention resulted in progressive decline of infection rates in voles captured within the village, which presumably reflected a decline in the potential exposure to humans as well. Continued treatments and dog control will probably be necessary to maintain this effect. Of increasing concern is the apparent spread of E. mdtilocularis infection in the lower 48 states. Since the 1960s infection has been reported in red foxes and a variety of rodents in the north central states. Only two human cases have yet been diagnosed in association with this focus; however, the potential for human exposure seems much greater (Gamble, Segal, Schantz & Rausch, 1979). Furthermore, foxes are translocated, both legally and illegally, from the north central states into the southeastern states to meet the needs of local hunting clubs. The parasite could thus become established in local populations of foxes and susceptible rodents in this region, with consequent exposure of even larger human populations. TAENIA SOLICJM TAENIASIS/CYSTICERCOSIS

Neurocysticercosis has long been known as a potentially devastating disease, however, the dimensions of the global problem have only recently become apparent as a result of improvements in diagnostic imaging techniques such as computerized tomography and magnetic resonance (Thomson, 1990). This new technology has projected the condition into prominence not only in areas where the disease is traditionally endemic, but also in many other countries with immigrants or refugees from these areas. The disease is found throughout the world. Although incidence and prevalence figures are still very limited, some recent studies in South Africa and Mexico have shown that neurocysticercosis is the most common cause of late-onset epilepsy (Medina, Rosas, Rubio-Donnadieu & Sotelo, 1990). Just north of Australia, in Irian Jaya, where the disease was introduced less than 20 years ago, neurocysticercosis now ranks as one of the most common causes of mortality (Bending & Catford, 1983). Although imported human neurocysticercosis has been seen for many decades in the United States, the visibility of the problem has increased greatly. A fourfold increase in annual numbers of cases diagnosed in four Los Angeles hospitals occurred between 1973 and 1983. This increase was associated with the introduction of CT scans (Richards, Schantz, Ruiz-Tiben & Sorvillo, 1985). The same phenomenon has been experienced in other major U.S. cities and many other industrialized countries (Crimmins, Collignon, Dwyer & Danta, 1990; McDowell & Harper, 1990). When we

Parasitic zoonoses in perspective

reviewed the histories of the patients in Los Angeles, we found that less than 3% were persons who had been born and resided continuously in the United States. About 75% of patients were from Mexico; the others originated from other Latin American countries, Asia, and Africa. No evidence exists that the proportion of locally acquired cases is increasing, and swine husbandry practices in the United States are not conducive to transmission of the parasite in the pig/human cycle; however, patients with neurocysticercosis, many of whom require repeated hospitalizations, expensive surgery, and chemotherapy, have a significant impact on medical care expenditures (Richards et al., 1985). Although new imaging procedures have greatly increased the ability to diagnose neurocysticercosis, many cases, especially those with few lesions, require a confirmatory diagnostic test. Increased demand for these services made us aware of the non-sensitivity and lack of specificity of serologic tests using crude Taenia solium antigens (Schantz, Tsang & Maddison, 1988). The development of specific purified antigens by lectin-affinity chromatography has provided an improved, highly sensitive, and specific cysticercosis diagnostic assay for Taenia solium cysticercosis (Tsang, Brand & Boyer, 1989). The solution to this imported disease cannot come from measures taken in the United States. Rather, control measures must be implemented in the diseaseendemic areas. Although some regional differences exist in the complex patterns of transmission, the basic factors that permit transmission of Taenia solium are swine-rearing practices that allow pigs to run loose and scavenge human feces, absence of effective latrines, and poor hygiene. Allowing pigs to run loose is not simply a question of ignorance. Pigs are often counted upon to scavenge human feces, thus keeping the village clean and obviating the need for special feeding. In most communities, some individuals make a business of clandestine marketing of infected meat. Therefore, eliminating cysticercosis transmission is not just a question of educating the population. Rather some incentives must be provided to change traditional practices that are popular with local residents. Although comprehensive control requires multiple measures targeted against tapeworm carriers, infected pigs, and the environment, it is recognized that health education is a long term goal and improvement of sanitary infrastructure is far too expensive for the budgets of most of these communities. Several community-wide control projects have recently been initiated to achieve rapid interruption of transmission by periodic mass chemotherapy integrated into primary health care (Cruz, Davis, Dixon, Pawlowski & Proano, 1989; Pawlowski, 1990). GIARDIASIS Giardia is the most common parasitic infection in the United States, and its prevalence is increasing: in 1987 it was found in 7% of stool specimens examined

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by state diagnostic laboratories, up from 4% in 1977-1979 (Kappus, Lundgren, Juranek, Roberts & Spencer, in preparation). Many states have made giardiasis a reportable condition; in Vermont in 1985, giardiasis was the most common reportable disease, with an average annual incidence rate of 45.9 cases per 100,000 population per year (Birkhead & Vogt, 1989). Transmission occurs by diverse modes. Giardia is the most common cause of waterborne outbreaks of disease in the United States (Levine, Stephenson & Craun, 1990). The largest outbreak occurred in 1984 in Pittsfield, MA where an estimated 3800 people were infected (Kent, Greenspan, Herndon, Moferson, Harris, Eng & Waskin, 1988). That same year, about 250,000 people in Pennsylvania were advised to boil their drinking water for 6 months because of Giardiacontaminated water. Waterborne transmission most often occurs because of ineffective filtration or inadequate pretreatment of surface water by municipal utilities. Filtration is necessary to remove Giardiu from water; chlorination alone is insufficient without high concentrations and long contact times. To prevent waterborne transmission of Giardia and other infectious agents, the Environmental Protection Agency prepared criteria for filtration and disinfection of all public water systems using surface-water sources (Levine et al., 1990). Giurdia is a common cause of outbreaks of diarrhea in day-care centers (Crawford & Vermund, 1987; Steketee, Reid, Cheng, Stoebig, Harrington & Davis, 1989). The infection easily spreads outward to the children’s families, and many family contacts develop symptomatic disease. Although fecal-oral and waterborne transmission are most common, a few instances of foodborne transmission have been recorded. The frequency of zoonotic transmission is controversial and remains unknown. Giardia is undoubtedly a zoonosis in the sense that humans and a variety of lower animals naturally share this parasite. Giurdiu is not hostspecific, and at least some strains are transmitted from animals to human beings. This is evident from crosstransmission studies and investigation of numerous waterborne outbreaks in the United States in which evidence was found of infected animal hosts, particularly aquatic rodents, in the surface-water source (Craun, 1984). Recent studies using molecular techniques have shown similarities of strains of Giardia isolated from humans and animals (Meloni, Lymbery & Thompson, 1989; Thompson, Lymbery & Meloni, 1990). It seems clear that Giardia isolates from humans represent multiple gene pools, and that some strains differ from others in many ways, including host specificity and pathogenicity. The more important questions are how often direct transmission occurs from lower animals to humans and how often such zoonotic transmission results in clinical disease in humans. The experience in the United States suggests that person-to-person transmission through fecal-oral

168

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routes and water contamination is far more common than direct zoonotic transmission. Answering these questions will be facilitated by the application of molecular techniques as epidemiologic tools to show the similarities between Giardia strains in human beings and associated animals (Thompson et al., 1990). CRYI’TOSPORIDIOSIS In the decade or so that Cryptosporidium has been recognized as a common cause of human disease, we have learned some interesting facts about this protozoan genus. In normal hosts, the diarrhea produced by Cryp~osporidi~ is self-limiting. However, in immunocomprom~sed individuals, the organisms can cause life-threatening disease for which there is no satisfactory chemotherapy (Soave & Johnson, 1988). Cryp~osporidi~m is clearly a zoonotic disease agent. Most initial reports of the disease in immunocompetent hosts indicated that infected animals were the source of human infections. Direct transmission through the fecal-oral route is also common among members of the same household, children in day-care centers, or homosexual men. Because of the circumstances of outbreaks acquired by tourists to Leningrad and several areas of the tropics, it is not surprising that Cryptosporidium is now recognized as being spread also by cont~inated water (Smith & Rose, 1990). More recently, community water-source outbreaks have occurred. A cryptosporidiosis outbreak in Georgia in 1987 was the largest outbreak ever reported to the CDC waterborne outbreaks surveillance system (Hayes, Matte, O’Brien, McKinley, Logsdon, Rose, Ungar, Word, Pinsky, Cummings, Wilson, Long, Hurwitz & Juranek, 1989). An estimated 13,000 people became ill with gastroenteritis after consuming water from a filtered, chlorinated public water supply. Cryptosporidium oocysts were isolated from patients’ stool specimens, from samples of public water, and from cattle grazing in the watershed area. The most unique and disconcerting aspect of this outbreak was that this water system met current state and federal drinking water standards. These standards may not be sufficient to prevent outbreaks due to this pathogen; the investigation showed that although treated water met turbidity standards, filters allowed passage of particulate matter likely accompanied by oocysts. Recommended improvement in chemical flocculation and filtration practices resulted in clearance of oocysts from the water. Recognizing this potential problem of surface-water contamination, the Environmental Protection Agency (EPA) has funded studies in many states to survey surface waters for Crypfosporidium. These studies have found that surface-water contamination with this ubiquitous pathogen is more frequent than contamination with Giardiu. Since we know that oocysts can gain access to drinking water systems by a variety of routes, research into the origin, fate, and survival of oocysts in the environment is urgently needed.

SCHANTZ

OPPORTUNISTIC INFECTIONS Cryptosporidium, and Toxoplasma are major causes of morbidity and mortality in AIDS patients (Selik, Starcher & Curran, 1987). Pneamocystiscontinues to be most common. Cryptosporidium~ Toxoplasma, and others are much less frequent; however, prevalence of these inf~tions at the time of initial diagnosis is probably underestimated. For example, clinicians who manage patients with AIDS suggest that the actual incidence of Cryptosporidium infection during the course of a case of AIDS may be as high as 20%. Although these infections are considered to be zoonoses, evidence of direct transmission from animab is usually lacking. In fact, despite the marked increase in frequency of diagnosis of these infections associated with the AIDS epidemic, remarkably little new epidemiologic information has been collected about risk factors for opportunistic infections. Since effective therapy for these infections has not been identified, information on risk factors is crucial in order to develop effective preventive strategies. The Parasitic Diseases Branch at CDC is currently initiating a collaborative effort to obtain such information by a longitudinal study of opportunistic enteric infections in HIV-infected patients in two cities in the tinited States. Pneumocystis,

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Inter-