Environmental contamination with infectious stages of gastrointestinal helminths is widespread, and the risk of reinfection of pets, particularly those allowed to roam freely outside, is great.
Despite the widespread availability of affordable and highly efficacious anthelmintics, gastrointestinal helminths remain a common finding in dogs and cats.1 Environmental contamination with infectious stages of gastrointestinal helminths is widespread, and the risk of reinfection of pets, particularly those allowed to roam freely outside, is great. Infection with gastrointestinal helminths can adversely affect the health of dogs and cats, and the presence of infectious stages in the environment also poses a zoonotic health risk to people. Ensuring that pets stay free of infection with these parasites requires instituting a parasite control program that focuses on both regular deworming and stringent flea control, together with routine monitoring for worms by performing fecal examinations.
Ascarid infections are one of the most common nematode infections diagnosed in pet dogs and cats. Surveys have shown that virtually all pups are born infected with Toxocara canis, the common ascarid of dogs.2 A recent survey of samples collected from dogs in shelters across the United States found that more than 30% of dogs less than 6 months old were shedding T. canis eggs.1 Toxocara canis infection is much less common in adult dogs but still occurs.1 Toxocara cati, the common ascarid of cats, is also routinely found; these worms are present in more than 25% of cats in some surveys.3,4 Unlike dogs, in which age-related resistance to intestinal infection is seen, cats remain susceptible to adult T. cati infection throughout their lives.5 Veterinarians, veterinary technicians, and knowledgeable clients commonly refer to ascarids of dogs and cats as roundworms, although this term refers to any nematode.
Fetal pups acquire T. canis in utero when larvae from the dam's somatic tissue stores are activated late in pregnancy to migrate across the placenta. The pups are then born with developing ascarids in the liver and lungs. These larval stages complete a liver-lung migration in the neonates. This migration results in larvae breaking across the alveoli, traveling up the respiratory tree, and then being swallowed to develop to egg-producing adults in the small intestine within three or four weeks of birth. A small number of larvae may also be transmitted to nursing pups through the milk.5 Because somatic infection is common in adult dogs, even in those receiving routine monthly intestinal parasite control, veterinarians should assume that essentially every pup is likely to harbor developing ascarids in the small intestine and, thus, should routinely deworm pups for T. canis. 6
Dogs and cats of any age may acquire infection with Toxocara species by ingesting infective larvae in eggs from a contaminated environment or by ingesting larvae in the tissues of paratenic hosts. In adult dogs, ingesting infectious larvae of T. canis results primarily in the formation of quiescent larval tissue stores rather than patent, egg-producing intestinal infections with adult worms. If a dog infected with tissue stores of quiescent larvae is an intact female, the larvae may later be transmitted to pups in utero.7 However, in adult cats, both somatic tissue stores and patent intestinal infections commonly develop; somatic stores of T. cati larvae in intact female cats may be transmitted to future litters of kittens through a transmammary but not a transplacental route. Cats allowed to roam outside where they are likely to consume infected paratenic hosts are at greatest risk of infection.5
Disease due to T. canis and T. cati is most severe in young animals. Clinical signs may develop in response to migrating larvae or because of large numbers of adult ascarids in the small intestine. Larvae migrating through the lungs induce pulmonary inflammation; affected animals may develop a mild to moderate cough accompanied by a mucopurulent discharge. Large numbers of larvae migrating through the lungs of young pups may result in severe pulmonary edema, hemorrhage, and even death just a few days after birth.7
Adult ascarids in the small intestine of pups and kittens can induce a mucoid enteritis, which may be associated with a mild diarrhea. A characteristic potbelly appearance may develop in heavily infected animals. Intussusception and intestinal obstruction due to large numbers of ascarids in the small intestine of young animals have been reported but are relatively rare. Adult ascarids may migrate from the small intestine to the stomach where they irritate the gastric mucosa and induce vomiting. Intact, live ascarids are often found in vomit or feces from infected animals.7 Older pups may vomit a large mass of live ascarids either spontaneously or after treatment with an ant helmintic, a phenomenon that can cause great distress to clients. Older kittens and adult cats will often vomit one or two intact adult T. cati, which can be readily distinguished from Physaloptera species, another stout stomach worm of dogs and cats occasionally found in vomit, by the presence of prominent cervical alae that give the anterior end of T. cati a characteristic arrowhead shape (Figures 1A & 1B).5
Figure 1A: The prominent cervical alÃ¦ of Toxocara cati, a nematode of cats that is occasionally found in vomitus.
Ascarid infection in dogs and cats must be controlled not only to protect the health of the pets but also because both T. canis and T. cati can induce severe disease in people, particularly children, who consume eggs containing infective larvae from a fecal-contaminated environment. Eggs containing infective larvae of Toxocara species are commonly found in soil samples from public areas such as parks and playgrounds, and the eggs survive and remain infectious for many years.2 When geophagia leads to ingestion of eggs containing infective larvae, the larvae emerge and migrate aberrantly in the child, resulting in disease syndromes. Different syndromes of toxocariasis include visceral larva migrans, in which hepatomegaly and eosinophilia develop because of the inflammatory reaction to larvae migrating in the liver; covert toxocariasis, in which chronic or recurrent abdominal pain and eosinophilia are associated with infection; and ocular larva migrans, in which the larvae induce a unilateral granulomatous retinitis. Asymptomatic infections also commonly occur.8
Figure 1B: The cervical collar of Physaloptera species, a stomach worm that can infect cats and dogs.
Other ascarids are occasionally found in small animals, including Toxascaris leonina, an ascarid of dogs and cats that migrates only in the gastrointestinal tract, and Baylisascaris species, ascarids of wildlife that have occasionally been reported in domestic dogs.5 Toxascaris leonina is not known to be zoonotic. However, the finding of patent Baylisascaris species infections in dogs is particularly troubling because larvae of some Baylisascaris species migrate in the central nervous system of paratenic hosts, including people, and can cause severe neurologic disease. A number of cases of severe Baylisascaris species-induced neurologic disease and death have been reported in children who consumed eggs containing infective larvae from a fecal-contaminated environment.9,10
Infection with the hookworms Ancylostoma caninum and Ancylostoma tubaeforme is also commonly diagnosed in dogs and cats, respectively. Infection with A. caninum is common throughout the United States, with 19.2% of dogs found to be shedding eggs, and is even more common (> 35% prevalence) in the southeastern United States, where warm, humid climates support the development and survival of infectious larvae in contaminated environments.1 Dogs become infected with A. caninum upon skin penetration by or ingestion of infectious third-stage larvae from a contaminated environment. Larvae that penetrate the skin migrate in the bloodstream to the lungs, cross the pulmonary parenchyma to migrate up the respiratory tree, and are then swallowed to develop in the small intestine. Ingested larvae may penetrate the oral mucosa and migrate through the lungs, or they may pass directly to the small intestine and begin development to the adult stage.5
Some of the larvae that migrate to the lungs remain in circulation and develop into quiescent forms in the musculature of dogs. If a dog is an intact female, these quiescent larvae will become active late in pregnancy, migrate to the mammary glands, and be transmitted to nursing pups. Such transmammary infections can result in large numbers of larvae being passed directly to neonatal pups. These quiescent larvae may also be reactivated in adult dogs in the absence of pregnancy or lactation, migrating to the small intestine to reestablish a patent infection even in the absence of exposure to infectious stages in a contaminated environment.7 Referred to as larval leak, this phenomenon can be frustrating to both veterinarians and clients attempting to clear a dog of infection. Ancylostoma tubaeforme follows a similar life history pattern as A. caninum does except transmammary transmission has not been demonstrated.7
Ancylostoma caninum infection in pups and young dogs causes an acute anemia because of the blood loss induced by the feeding worms in the small intestine. This anemia is most severe, and may be fatal, in neonatal pups that acquire large numbers of larvae by transmammary transmission. Because the developing hookworms begin feeding on the small intestinal mucosa as early as eight days after infection, but the worms themselves do not begin producing eggs until two or three weeks after infection, pups that receive large numbers of larvae can become moribund and die even though their fecal examination results are negative. Anemic pups less than 3 weeks old should be presumptively dewormed for A. caninum regardless of the results of any fecal examination. Adult dogs may also be infected with A. caninum, but because adult dogs are larger and have greater iron reserves, disease is generally less acute. In a contaminated environment, larvae can penetrate the skin and may cause dermatitis.7 Disease in cats due to A. tubaeforme is similar to, but generally less severe than, that caused by A. caninum in dogs.
People can become infected with A. caninum when they contact the infectious larvae in a contaminated environment. Larval penetration of the skin of the aberrant human host results in cutaneous larva migrans, a pruritic dermatitis associated with tortuous tracts of erythema characteristically arising on the hands, feet, or other areas of the body that have contacted soil containing A. caninum larvae. Intestinal infection of people with adults of A. caninum has been reported as a cause of eosinophilic enteritis and abdominal pain in affected individuals.11 The related hookworm Ancylostoma braziliense, which infects both dogs and cats, is another well-known cause of cutaneous larva migrans in people; this parasite is considered to be more common in sandy, coastal areas and warm climates. Uncinaria stenocephala is another canine and feline hookworm found throughout the United States. However, the northern hookworm, so named because of the ability of the larval stages to survive lower temperatures than Ancylostoma species, is not thought to cause severe disease in infected animals or zoonotic infections.5
Trichuris vulpis, the whipworm of dogs, is a common parasite in older pups and adult dogs. In some surveys, up to 10% of dogs are shedding whipworm eggs in their feces.12,13 The eggs are persistent in the environment and remain infectious for many years. No reasonable, effective means of removing or killing eggs in a contaminated yard exists, although completely removing the topsoil or paving the contaminated area, when possible, may be effective.5
Dogs acquire T. vulpis infection by ingesting eggs containing infective larvae from a contaminated environment. The larvae then emerge from the eggs, penetrate the glandular epithelium of the cecum, and develop to adults. Adult worms embed their anterior ends into the cecal or colonic mucosa, disrupting the integrity of the epithelium and causing a watery diarrhea that may contain blood. Disease may be chronic, and elimination of infection can be difficult.7 Although most cases of whipworms in people are due to infection with the human whipworm, Trichuris trichiura, zoonotic gastrointestinal T. vulpis infections are occasionally reported.14-16
Dipylidium caninum is often referred to as the flea tapeworm because dogs and cats become infected when they ingest fleas and, less commonly, lice containing the infectious immature cestodes. The prevalence of D. caninum in shelter animals in some studies is reported to be as high as 52.7% in cats and 60% in dogs, likely reflecting the high prevalence of flea infestations and lack of care the population considered received.4,17 Although the prevalence is probably lower in well-cared-for animals in more temperate climates, D. caninum infection is almost certainly underappreciated when evaluated by fecal examination alone, as proglottids are intermittently shed and may not be present in the sample examined.1
Infection of dogs and cats with Taenia species is also frequently encountered by veterinarians. Ingesting infected prey animals is necessary to establish an infection with adults of Taenia species, as well as Echinococcus species in areas where the latter cestode occurs. Infection with Spirometra species, a primitive cestode of cats and, less commonly, dogs, is routinely diagnosed in many areas of the southeastern United States. Again, cats and dogs become infected when they ingest infected prey containing the immature cestode larvae. Although aesthetically unpleasant because of the shedding of motile proglottids into pets' environments, the common adult cestodes of dogs and cats do not cause clinical disease in their hosts.5 However, infection with Spirometra species may cause weight loss, vomiting, and diarrhea in infected animals; this primitive cestode passes eggs rather than proglottids in the feces of the dog or cat host.18
Like their nematode counterparts, some cestodes of dogs and cats can infect people. Children who accidentally ingest an infected flea from an infested environment may develop D. caninum adults in their small intestine. Infections are recognized when motile proglottids are found in the diaper or on the perianal area of the infected child.19 Although disease is usually absent or mild, and anthelmintic treatment prescribed by a pediatrician readily clears the infection,19 parents may still experience distress at the diagnosis and the source of infection. Echinococcus species infection poses a very serious potential health risk to anyone who ingests eggs from feces or a fecal-contaminated environment; Echinococcus species eggs are immediately infectious when shed.20 Spirometra species infection also presents a zoonotic risk, but people acquire infection from consuming water containing copepod intermediate hosts or consuming or coming into contact with infected prey species serving as second intermediate hosts; direct contact with Spirometra species-infected dogs or cats does not pose a public health risk.18
As mentioned above, several of the gastrointestinal helminths commonly found in dogs and cats are zoonotic and may cause disease in children or adults who are exposed to or ingest the infectious stages. Infection with these parasites is usually acquired from a contaminated environment rather than directly from an infected dog or cat. For most of these parasites, time in the environment is needed for the infectious stages to develop. Preventing infection in people requires not only treating dogs and cats to eliminate the source of the parasites but also paying careful attention to basic hygiene measures. Such measures include washing hands frequently, washing fruits and vegetables carefully before consumption, promptly removing pet feces from the yard, avoiding contact with fecal-contaminated soil, covering sandboxes when not in use, discouraging dogs and cats from roaming (by enforcing leash laws and other pet confinement legislation), and supervising young children to prevent geophagia and other forms of pica. Direct contact with well-cared-for dogs and cats is not considered a major risk factor in most of these diseases.
Open communication between veterinarians and physicians is essential to prevent zoonotic disease from gastrointestinal helminths of dogs and cats. Physicians should encourage patients to seek routine veterinary care for their pets to ensure that contamination of the home environment is kept to a minimum. Similarly, veterinarians who encounter clients with signs consistent with a zoonotic parasitic disease should refer them to their physicians. When zoonotic diseases are diagnosed in people, the attending physician should ensure that all dogs and cats that might serve as a source of the infection are promptly examined by a veterinarian and treated with effective ant helmintics. Veterinarians also serve as an excellent source of management recommendations to prevent future infection of pets and to remove infectious stages from the environment, when possible.
Because dogs and cats can serve as a source of infection of zoonotic gastrointestinal helminths to people, some physicians erroneously think that other nonzoonotic helminths are also acquired from dogs and cats. The most common of these misunderstandings involves the human pinworm, Enterobius vermicularis. Pinworms are common in children, but people and nonhuman primates are the only hosts of E. vermicularis. Dogs and cats do not become infected with pinworms and cannot serve as a source of pinworm infection to children. Likewise, dogs and cats are not involved in the life cycle of and do not serve as a source of infection for the human ascarid Ascaris lumbricoides, the human hookworms Ancylostoma duodenale and Necator americanus, or the human whipworm Trichuris trichiura. The primary source of all of these parasites is other infected people.
Regular fecal examinations should be performed at least annually as part of the routine physical examination of every adult dog and cat. Pups and kittens, which are more likely to harbor intestinal parasites, should have at least two and as many as four fecal examinations performed in the first year of life. However, young pups and kittens should be presumptively dewormed; it is inappropriate to wait for a positive fecal examination result before treating a newborn dog or cat.
To ensure that you reach an accurate diagnosis, include gross inspection of the feces as part of the fecal examination, noting blood, mucus, intact worms, or the presence of cestode proglottids. Be sure not to mistake fibrous material commonly found in feces for a parasite. Next, perform a centrifugal flotation procedure. This concentrates any eggs present and allows their detection by microscopic examination. A direct smear may also be prepared from fluid diarrheic fecal samples and examined microscopically to detect motile protozoa or nematode larvae. To be effective, the fecal flotation must evaluate an adequate amount of material, which may be as little as 1 g of formed feces or as much as 6 g of fluid feces. The small samples collected by a fecal wand are not appropriate for diagnosis because they do not provide enough material to allow the detection of a low number of eggs and, thus, may yield false negative results.
Centrifugal flotation is a more sensitive and accurate means of detecting parasite eggs in fecal samples than the commonly used passive tabletop flotation method. Veterinary clinics that switch from passive to active fecal flotation protocols often note increased detection of eggs in fecal samples. Centrifugation of feces suspended in a solution (1.18 to 1.2 g/ml) of appropriate specific gravity to float nematode eggs forces the eggs to the top of the solution and the debris to the bottom. Both Sheather's sugar solution and zinc sulfate solution are commonly used in centrifugal fecal flotation techniques.21 The sugar solution is viscous, and frequent cleaning of laboratory areas where it is used is required. It also collapses some protozoal cysts (e.g. Giardia species), altering their morphology. However, Sheather's sugar solution allows efficient flotation of eggs, and slides can be stored for examination for longer periods. Zinc sulfate is not as viscous and also allows efficient flotation of all common gastrointestinal parasites, but the salt crystallizes on the slides fairly quickly, thereby obscuring examination of a slide at a later time. Disposal of zinc sulfate solution may be problematic in some areas.
Regardless of the solution used, the preparation of a sample for centrifugal flotation requires suspending about 1 g of feces in 20 to 30 ml of flotation solution, straining that slurry through a sieve or cheesecloth, and then pouring the strained fluid into a centrifuge tube. If you use a centrifuge with a swinging bucket rotor, you can fill the tubes to form a reverse meniscus on top, add a coverslip, and spin the tubes with the coverslip in place. When using a fixed-rotor centrifuge, fill the tubes to just below the top to avoid spillage, spin the tubes without a coverslip, and then add more solution to form a reverse meniscus. You can then add a coverslip and allow the tube to stand for another five minutes so that the eggs can passively float to the top of the solution. Then remove the coverslip and examine the entire area microscopically (Figure 2).21
Figure 2: Ova of Toxocara canis (lower right) and Ancylostoma caninum (upper left), gastrointestinal helminths commonly found on canine fecal examination.
Historically, efforts to control gastrointestinal helminths in dogs and cats have focused on early effective deworming of pups and kittens. At present, the joint recommendations of the Centers for Disease Control and Prevention and the American Association of Veterinary Parasitologists are that pups should be dewormed at 2, 4, 6, and 8 weeks of age with an anthelmintic effective against both ascarids and hookworms, and that kittens, which do not become infected with gastrointestinal helminths until after birth, should be dewormed at 3, 5, 7, and 9 weeks of age. Nursing dams should be dewormed along with their young. All pets should begin receiving a monthly heartworm preventive that also controls intestinal parasites at the earliest age possible (6 to 8 weeks), and they should undergo regular fecal examinations and receive treatment as needed.
Such an approach makes sense because younger animals consistently harbor larger numbers of parasites and pass more eggs in their feces to contaminate the environment. However, pups and kittens often are not brought to a veterinarian until 6 or 8 weeks of age; by that time, the environment probably has been contaminated with ascarid and hookworm eggs. To dramatically reduce infection of pups with ascarids and hookworms, dams can be treated late in pregnancy after the larvae have been activated and, thus, are susceptible to anthelmintics.22 Regardless of the approach taken, every effort should be made to ensure that all pups and kittens are cleared of gastrointestinal helminths.
In recent years, many veterinary parasitologists and internists have begun to recommend that all dogs and cats be treated for gastrointestinal parasites year-round. This approach may, at first, seem overly aggressive to veterinarians who are more comfortable with simply performing annual fecal examinations and treating any parasite infections that are detected. Annual fecal examinations followed by appropriate treatment are certainly an important part of veterinary preventive care. However, waiting for an annual fecal examination to indicate that gastrointestinal parasites are present allows the environment to become contaminated, sometimes over many months, with eggs that may then serve as a source of reinfection to that pet, other animals, and people. Treating pets routinely year-round with ant helmintics effective against gastrointestinal parasites will help eliminate patent gastrointestinal parasite infections and reduce environmental burdens of parasite stages infectious to pets and people.
Several safe effective anthelmintics are available for use in a year-round program to control gastrointestinal parasite infections in dogs and cats. Veterinarians are often comfortable with using heartworm preventives that are also effective against gastrointestinal parasites because they already use these products in their practices. In the southeastern United States, where heartworm is actively transmitted most of the year, many veterinarians already routinely prescribe year-round heartworm preventives that are also effective against intestinal parasites. The seasonality of heartworm transmission in more temperate areas depends on varying climatic factors, and the onset of mosquito activity is somewhat unpredictable. Considering how many pets travel with their owners to heartworm-endemic areas and how frequently pets encounter infectious stages of intestinal parasites in the environment, year-round administration of a heartworm preventive that also controls intestinal parasites may be warranted throughout the United States.
None of the currently available combination heartworm and intestinal parasite control products is effective against cestodes. To also eliminate infections with D. caninum and Taenia and Echinococcus species in dogs and cats, a product containing either praziquantel or epsiprantel must be used. Fenbendazole has efficacy against Taenia species but not the more frequently encountered flea tapeworm D. caninum. In addition to anthelmintics, effective control of tapeworms also requires owners to stringently adhere to a veterinarian-prescribed flea control program to eliminate reinfection with D. caninum and to prevent their pets from roaming and consuming prey to avoid reinfection with Taenia and Echinococcus species. Keeping dogs in a fenced yard or on a leash, keeping cats indoors, and feeding pets only cooked canned or dry commercial food are all excellent means of preventing parasitic infection.
Susan E. Little, DVM, PhD, DEVPC
Department of Infectious Diseases
College of Veterinary Medicine
University of Georgia
Athens, GA 30602
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