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Why are intestinal parasities a reason for concern in shleter?
Which intestinal parasites should we be concerned about?
What tools are available to diagnose intestinal parasites
How can a shelter treat & control intestinal parasites
A suggested basic parasite control protocol for shelters
Frequently asked questions about intestinal parasite control
Intestinal parasites (worms and protozoans) are common in animal shelters in the US. For dogs, this fact was clearly demonstrated in a comprehensive survey of nearly 6,500 fecal samples from dogs housed in animal shelters in all 50 U.S. states.In another study, 40 out of 50 fecal samples from shelter dogs tested positive for hookworms, roundworms, whipworms, and/or Giardia. A third study showed that intestinal disease (possibly due to parasites) is more common in puppies adopted from shelters than in puppies purchased from breeders. While a comprehensive national survey on parasites in shelter cats has not been conducted, there have been several reports of the prevalence of intestinal parasites in shelter cats and feral cats.
Intestinal parasites often cause illness in the animals they infect. 7 Diarrhea is most common, but anemia, coughing and even death can occur. On the other hand, many parasites may cause sub-clinical infections. This means that some animals that appear perfectly healthy may be causing significant spread of infections and environmental contamination.
Several intestinal parasites of dogs & cats are zoonotic – that is, they can also cause disease in human beings, including shelter staff, adopters, or even just members of the general public who visit animal shelters. Shelter workers, with their constant exposure to animals and their feces, are at particularly high risk.
Significant contamination of the environment by worm eggs or protozoan oocysts can be a major problem that is difficult to resolve. Many of these eggs or oocysts are extremely resistant to cleaning and disinfection. This can be particularly problematic in a shelter environment, where there is often a dense population of animals and/or a constant influx of new animals.
Hookworms (Ancyclostoma, Uncinaria). The national shelter parasite study1 showed that 20% of shelter dogs were shedding hookworm eggs, making hookworms the most common intestinal parasite of dogs in the U.S. It has often been thought that dogs develop considerable resistance to hookworms as they grow older, but this study showed that hookworms are just as common in older dogs as they are in puppies. Hookworms are nearly twice as common in the Southeastern U.S.See our Infectious Disease: Profiles of Common shelter Diseases page for more information
Roundworms (Toxacara, Toxascaris). The national shelter parasite study1 showed that 15% of shelter dogs were shedding roundworms. Roundworms are more common in the Southeastern U.S., and much more prevalent in puppies less than 6 months old. A study of shelter cats found that fully a third of cats were shedding roundworms.5 The clinical signs of roundworms infection may be somewhat less severe in kittens than puppies. However, roundworms are probably nearly as common in adult cats as they are in kittens. Roundworms can be treated with pyrantel, piperazine, or fenbendazole. See our Infectious Disease: Profiles of Common shelter Diseases page for more information.
Whipworms (Trichuris vulpis). The national shelter parasite study1 showed that 14.3% of shelter dogs were shedding whipworms. It has traditionally been assumed that whipworms are less common than other intestinal worms, but the prevalence of whipworms in this study was nearly equal to that of roundworms. Whipworms are just as common in older dogs as they are in puppies. Whipworms are particularly common in the Southeastern and Midwestern regions of the U.S. See our Infectious Disease: Profiles of Common shelter Diseases page for more information.
Tapeworms. The most common species of tapeworms in dogs and cats in North America is Diplydium caninum. Infection with this tapeworm is acquired by eating infected fleas. In populations with high flea burdens, nearly all animals may be infected with D. caninum. Infected animals may intermittently shed egg-containing worm segments (called ‘proglottids’) in their feces. The pre-patent period is usually around 2-3 weeks. The second most common type of tapeworm in dogs and cats are various Taenia species. Dogs and cats may become infected with these types of tapeworms by feeding on smaller mammals, such as mice or rabbits. There are also a few other kinds of tapeworms that are much less common, such as Echinococcus, Diphyllobothrium and Spirometra. These tapeworms are generally limited to certain regions of the country. For example, in Florida, Spirometra is the second most common tapeworm in cats.
Most tapeworm infections in dogs and cats are sub-clinical (i.e. they do not usually cause clinical signs, such as diarrhea). They do sometimes cause peri-anal irritation, resulting in an animal scooting its rear end along the ground. Heavy infections can sometimes result in abdominal pain, vomiting, weight loss, and possible intestinal blockage. However, several tapeworm species are zoonotic – they can also infect humans. Humans (most often children) can become infected with Diplydium caninum the same way dogs and cats do - by eating infected fleas. As in dogs and cats, these infections are usually asymptomatic and not serious, and are usually only recognized when proglottids are passed in the stool. However, the larval forms of Echinococcus tapeworms pose a serious zoonotic threat. While this type of tapeworm is uncommon in most areas of the US, humans can become infected through contact with the feces of dogs harboring the tapeworm.
Tapeworms are often diagnosed when proglottids are seen on the feces or near the anus of an animal. These proglottids resemble grains of rice or cucumber seeds. For some tapeworm species, individual eggs rather than proglottids are shed, and these eggs may occasionally be detected on fecal float exams. However, fecal flotation exams are generally unreliable for detection of tapeworm infections.
Praziquantel is the drug most commonly used to treat tapeworm infections in dogs and cats. Epsiprantel is also effective against most tapeworms, and fenbendazole is effective against a few types of tapeworms. Eliminating and preventing fleas is also extremely important in controlling Diplydium caninum infections.
Strongyloides stercoralis: Strongyloides stercoralis infection in dogs may be asymptomatic, or may cause bronchopneumonia or severe diarrhea. S. stercoralis is potentially zoonotic, but transmission of S. stercoralis from dogs to humans is probably relatively rare. Nevertheless, the potential human health hazard should always be taken into account, and infected dogs should be handled with caution. S. stercoralis is diagnosed by observing larvae in fecal culture, and is typically treated with ivermectin.
Coccidia (Isospora spp.) The national shelter canine parasite study showed that about 8% of shelter dogs less than 6 months old were shedding coccidian oocysts. Coccidia are less common in dogs over 1 year of age, and very uncommon in dogs over 7 years old. The prevalence of Coccidia is fairly consistent across various regions of the country. Drugs used to treat Coccidia include ponazuril (Marquis Paste), toltrazuril, and sulfadimethoxine (Albon). In shelters in which Coccidia is a common problem, prophylactic treatment of all puppies and kittens with ponazuril is recommended. See our Infectious Disease: Profiles of Common Shelter Diseases page for more information.
Giardia (multiple species). The prevalence of Giardia in shelter dogs and cats is probably underestimated. Giardia is potentially zoonotic, but the risk of humans contracting Giardia infection from dogs and cats is low. Giardia cysts are difficult to detect on fecal floats. If fecal flotation is relied upon, a zinc sulfate centrifugation method be used, and that at least three samples should be examined over a period of about a week. Direct smears are about 50% sensitive for detecting Giardia in diarrheic fecal samples. In cats, Giardia may be mistaken for Tritrichomonas on a fecal direct smear. The most sensitive method for diagnosis of Giardia in shelters is a SNAP ELISA test, but this test is not intended for screening of asymptomatic dogs. Vaccination for Giardia is available, but not recommended for use in shelters. Giardia can be treated with metronidazole, fenbendazole, or febantel (Drontal Plus) See our Infectious Disease: Profiles of Common shelter Diseases page for more information.
Tritrichomonas foetus. This is a recently recognized intestinal protozoal pathogen in cats. Although its prevalence in shelters is unknown, one study found that approximately 1/3 of cats at cat shows and breeding catteries were infected with Tritichomonas. Tritrichomonas infection is most common in kittens and young adult cats and in crowded environments, so it may be an important problem in shelter cats. In addition, it is not detected by standard diagnostic methods (e.g. fecal float) and does not respond to routinely used anti-parasite medications. Tritrichomonas tends to cause chronic, mucoid diarrhea, with fecal incontinence and anal swelling, pain and redness. Tritrichomonas can be detected by a direct fecal smear, although more sensitive diagnostic tests are available. Fecal protozoal culture using the “InPouch” test is most practical for shelters. Co-infection of cats with Tritrichomonas and Giardia is not uncommon, and the two parasites may be confused when seen on a direct fecal smear. Cats thought to have Giardia but not improving with treatment may have Tritrichomonas. Ronidazole is the only drug that has shown to be effective for treatment of Tritrichomonas. See our Infectious Disease: Profiles of Common shelter Diseases page for more information.
Cryptosporidium (C. parvum, C. felis). The prevalence of Cryptosporidium in shelter dogs and cats in unknown. In studies that included shelter cats and ferals, 4-7% of cats were shedding Cryptosporidium oocysts. Cryptosporidium can also infect guinea pigs, cattle, humans, and other species. Infections in dogs and cats are usually mild, with only self-limiting diarrhea, but may cause more severe diarrhea in kittens and puppies. Cryptosporidium presents a potential zoonotic risk, and the infective dose (number of oocysts needed to cause infection) is very low, especially in immunocompromised people. However, most human infections are not obtained from animals, and the risk of infections from pets is generally low. Oocysts are often shed only intermittently and in small numbers from infected animals, but prolonged shedding from infected dogs and cats may occur. Oocysts are difficult to detect on fecal flotation exams because they are extremely small. Using sucrose solution and repeating flotation exams may increase the chances of detecting Cryptosporidium. There are several other tests for Cryptosporidium available; most require sending samples out to a diagnostic lab, and there is little consensus about which test is the most accurate. Cryptosporidium does not respond to any anti-parasitic medications. Cryptosporidium oocysts are resistant to most disinfectants, and can remain viable in the environment for months.
Toxoplasma. Exposure to this parasite is common in cats. Studies of antibody titers in cats suggest that nearly half of cats in the U.S. have been exposed to Toxoplasma. Cats are the only “definitive” host, meaning that they are the only animals that can shed infective forms of the parasite (‘oocysts’) in their feces. Although previous exposure is common, it is quite uncommon for cats to be actively shedding Toxoplasma oocysts. In one study of 77 shelter cats, none were shedding Toxoplasma. Studies indicate that at any point in time, less than 1% of cats in the U.S. have a patent intestinal infection and are shedding oocysts, but shedding is more likely in kittens and young cats. Cats typically become infected through exposure to the feces of other cats, or by eating undercooked meat or rodents. Shortly after their first exposure to Toxoplasma, cats usually shed oocysts for 1 to 3 weeks. This is typically followed by the development of significant immunity. Subsequent re-infections are uncommon, and generally do not result in shedding. Toxoplasma infections are usually sub-clinical in cats; diarrhea is not generally seen. Occasionally, the parasite causes systemic inflammation, affecting the brain, eye and other tissues, but these manifestations are not necessarily associated with active shedding of oocysts.
Serum antibodies titers can be measured to determine whether a cat has ever been exposed to toxoplasmosis, but this is of little practical value. The vast majority of cats with positive antibody titers are not shedding oocysts. If present, oocysts can usually be detected on fecal floatation, but it can be challenging to distinguish Toxoplasma oocysts from those of other protozoans. Toxoplasma oocysts are smaller than those of Coccidia.
While cats are the only species that can shed Toxoplasma oocysts, many other species can be infected with Toxoplasma, including dogs, pigs, sheep, goats, rodents and humans. Exposure to toxoplasmosis is common in humans, with 30-40% of people having positive antibody titers. Toxoplasma infections can also be obtained through the ingestion of intermediate forms of the parasite in the tissues of other animals, such as pigs or rodents. Most human Toxoplasma infections result from ingestion of undercooked meat, but humans may also become infected by ingestion of oocysts from soil contaminated with cat feces, usually following gardening or ingestion of raw vegetables from such soil, or through exposure to cat feces, usually when cleaning litter boxes. Toxoplasma infections in humans are usually asymptomatic, but can be serious in immunosuppressed people and in pregnant women.
Shelters commonly contain a large, non-immune population of young cats with the potential to experience initial Toxoplasma infection and shed the Toxoplasma oocysts in large quantities. This could increase the risk of spread by ingestion of oocysts. Therefore, screening cats through fecal floatation is recommended, especially for cats less than 1 year old, and for cats being introduced into group housing. Cats found to be actively shedding toxoplasma oocysts should not be made available for adoption. If possible, they should be isolated during the 3 week potential shedding period, until oocysts are no longer detected on fecal floatation. Careful measures to prevent human exposure should also be taken during this period.
After this period, and once oocysts are no longer detected on fecal floatation, the cat need not be considered a particular zoonotic risk. Oocysts in fresh feces are not immediately infective; the oocysts require at least 24 hours after being passed to “mature” to a form that can cause infection in humans. Therefore, removal of feces from litterboxes at least once daily, followed by proper disposal of feces, will reduce the risk of exposure. Use of disposable litterboxes can also be helpful.
Toxoplasma oocysts are resistant to most disinfectants. Cleaning with scalding hot water or steam is most effective for environments contaminated by Toxoplasma oocysts, but obviously, must be done carefully to avoid burns.
Treatment of Toxoplasma infections should not be undertaken based solely on detection of Toxoplasma oocysts in the feces. Diarrhea in kittens or cats is much more likely to be due to other parasites or to other non-parasitic causes. Most cats who are shedding Toxoplasma oocysts do not experience clinical signs from this infection and do not require treatment.
Shelters may want to consider offering antibody testing for female employees of child-bearing age at the start of employment. Employees testing negative should be warned of the risk of contracting toxoplasmosis during pregnancy. Pregnant women should not handle cat litter, particularly if the woman does not already have antibody titers to Toxoplasma.
Education of adopters about Toxoplasma is important. Since most human infections with Toxoplasma are not transmitted by direct contact with cats or cat feces, the best prevention for the general public is to cook meat properly, wash vegetables thoroughly or peel before eating, and wear gloves when gardening. To prevent Toxoplasma infection in their cats, adopters should prevent hunting activity by cats (e.g. keep cats indoors) and avoid feeding raw or undercooked meat or viscera to cats (e.g. feed cats only commercially prepared diets.) Because oocysts require at least 24 hours to become infective, remove fecal material from litter boxes daily, especially when introducing a new cat to a household with other cats.
Adopters of cats in which Toxoplasma shedding has been documented need not be overly concerned about zoonotic risk, as long as the cat has been isolated through the potential shedding period and cessation of shedding has been confirmed by serial negative fecal floatation exams. As stated above, after the initial infection has ceased, cats are unlikely to become re-infected and shed oocysts again in the future. Thus, cats that have a previous history of shedding Toxoplasma oocysts and/or have positive antibody titers could actually be considered lower risk than cats that have never been exposed to the organism.
For more information, visit the following links:
Protocols should be based on known prevelance of parasites for the region. The Companion Animal Parasite Council is one resource for such information, as are local practitioners, veterinary schools, diagnostic laboratories and the scientific literature. Diagnostic testing for parasites may provide additional information specific to the shelter either to refine general treatment protocols or direct the response to an increase in symptomatic animals. Additionally, diagnostic tests are sometimes indicated to direct treatment in an individual.
Tests to identify and diagnose intestinal parasites differ in their accuracy. There are two main aspects of a test's “accuracy:” sensitivity and specificity. Sensitivity is the likelihood that the test will correctly identify infected animals (i.e. a very sensitive test has few false negatives, it doesn't "miss" very many infections). Specificity is the likelihood that the test will correctly identify animals that are NOT infected (i.e. a very specific test has few false positives, it is unlikely to identify an animal as infected if it’s not).
Note that several of the available tests are prone to false positives or false negatives. In addition, due to the parasites life cycle (e.g. intermittent shedding or a long prepatent period) the test may be negative even in an infected animal. Finally, many internal parasites can be found in clinically normal animals. Simply identifying a parasite does not mean it is the cause of the animal's symptoms, nor does it necessarily require treatment. In some cases, it is more appropriate to simply treat likely infections based on the animal's history, signalment (species, age, etc.), symptoms, and known risks in the population. Additional testing is indicated in severely ill animals, those that fail to respond to empirical treatment, or in the event of an outbreak.
Fecal flotation (fecal float). In this procedure, feces are suspended in a solution with a specific density, so that parasite eggs and cysts will float, while other fecal debris will sink. This method can be used to detect roundworm, hookworm, and tapeworm eggs, and Coccidia and Toxoplasma oocysts. A fecal float is relatively insensitive for detecting Giardia cysts and tapeworm eggs, and cannot be used to detect Tritrichomonas.
There are many different types of fecal flotation methods, and they can be categorized in two main ways: by the type of solution that is used (Fecasol®, sucrose, zinc sulfate), and by the type of force that is used to separate the floating eggs & cysts from the sinking debris (standing / gravitational vs. centrifugation techniques).
Solution type. Solutions that may be used include sucrose (sugar), sodium nitrate (Fecasol) and zinc sulfate. Zinc sulfate is generally preferred for the detection of most common parasite eggs and oocysts, because it is less likely to cause distortion of cysts. However, sucrose solution is better for detection of certain parasites, such as Cyrptosporidium oocysts. The recommended concentration and specific gravity and concentration for the solutions depend on which solution is used (for zinc sulfate, 33%, specific gravity 1.18 to 1.20; for sucrose, specific gravity 1.25 to 1.33)
Gravitational/standing vs. centrifugation techniques. The commonly used Fecalyzer® system is probably the most familiar standing fecal float technique. While standing methods are easier and quicker, and do not require a centrifuge, centrifugation techniques are more sensitive for detection of certain parasites, particularly Giardia cysts. Giardia will very likely be missed if only a standing technique is used.Centrifugation may also improve detection of whipworm eggs. A centrifuge with free-swinging buckets is recommended.
Instructions for performing a fecal flotation with centrifugation:
Modification for fixed-angle centrifuges: Instead of completely filling the tube to the top, only fill it to within a few centimeters of the top, and do not place the coverslip on top of the tube before centrifugation. When the centrifugation is complete, carefully set the tube upright in a test-tube rack, and use a pipette to very slowly drizzle additional solution down the inside of the tube until the tube is completely full and a positive meniscus is formed. Try to avoid disturbing the contents of the tube when adding the additional solution. Then set a coverslip on top of the tube and let it stand for 5 minutes. Remove coverslip, place on slide, and examine as described above.
Direct fecal smear (wet preparation). This is made by breaking up a small particle of fresh feces in a drop of saline solution on a microscope slide. The sample can be obtained by introducing a cotton swab or thermometer into the rectum and gently rotating it several times. Placement of a coverslip over the sample is recommended. Be careful not to make the smear too thick. This method is more sensitive than a fecal float for detecting Giardia trophozoites and can also be used to detect Tritrichomonas. Detection of Giardia is more efficient if the sample is diarrhea rather than formed stool. The slide should be scanned at 10X, with 40X used to confirm identity of parasites.
Idexx SNAP ELISA tests (for Giardia). Very sensitive. Not recommended for screening of non-diarrheic shelter dogs, or for use to test recovered dogs post-treatment to verify cure, as its high sensitivity may detect clinically unimportant infections.
Fecal protozoal culture (InPouch TF test). This is a practical, affordable in-house test for detection of Tritrichomonas. It was designed for use in cattle, but it can easily be used with a peppercorn-size amount of fresh cat feces. Test kits are available at http://biomeddiagnostics.com/tfoetus The cost is approximately $50 for 20-test-kit.
Other diagnostic tests available from laboratories:
Treatment of intestinal parasites
Ideally, we would like to be able to treat all shelter animals with a single all-purpose dewormer that is inexpensive, safe, convenient to administer, highly effective against a broad spectrum of parasites, and appropriately labeled for our intended use. Unfortunately, such an ideal product does not exist! Listed below are various deworming medications that may be useful in a shelter.
Ideally, a shelter’s deworming program should be based on a knowledge of which parasites are present in the particular shelter population. However, there are some general guidelines that apply to nearly all shelter populations. All dogs, cats, puppies and kittens entering shelters should be treated for certain parasites in order to protect the rest of the shelter population, prevent environmental contamination or infestation, and minimize zoonotic threats to shelter staff and the public.
A minimum shelter parasite control protocol should consist of prophylactic treatment of all shelter dogs and cats for the most common parasites at the time of intake. This should consist at least of a dewormer effective against roundworms and hookworms, and flea preventive (+ tick preventive for dogs). All of these parasites are common in dogs and cats, all can potentially cause problems in people, and environmental contamination of these parasites can be difficult to eradicate once it occurs. The most straightforward products to use for this basic internal and external parasite control protocol are an oral dewormer containing pyrantel pamoate (Nemex® and Strongid® are the most commonly used products), and topical products such as imidacloprid (Advantage) and/or fipronil (Frontline).
In addition to deworming on intake, puppies and kittens should also be dewormed repeatedly with pyrantel every 2 weeks from 2 weeks to 16 weeks of age. Re-treatment is very important!
All pregnant and nursing dogs and cats should also be dewormed with pyrantel every 2 weeks while housed in the shelter or foster care.
For all other adult dogs and cats, a second dose of pyrantel is recommended 2-3 weeks after intake, if still in the shelter.
If whipworms, tapeworms, Giardia, coccidia, ear mites, or other parasites are common in the shelter population, the protocol can be modified as needed. For example:
If coccidia is a problem in your puppies and kittens, we recommend giving Ponazuril (Marquis Paste) to all puppies and kittens starting at 2-3 weeks of age, repeated in 7-14 days, and then as needed based on clinical signs/ fecal exams.
Which intestinal parasites should we treat?
Ideally, a shelter’s deworming program should be based on a knowledge of which
parasites are present in your particular shelter population. However, there are some general guidelines for deworming that could apply to nearly all shelter populations. For example, in puppies and kittens, roundworms and hookworms are ubiquitous. These are particularly important because they can be transmitted from mothers to puppies or kittens through the placenta and/or the mammary gland, so infections are extremely common in young animals, and can be severe. Up to 80% of puppies are infected with roundworms, but typically only about 20% of these infections are detected on fecal exam, so they should be treated regardless of fecal exam results. Also, rounds and hooks are both zoonotic, another reason that great care should be taken to control them. Lastly, environmental contamination with roundworm eggs is practically impossible to get rid of,
another reason to treat animals prophylactically to prevent shedding. Whipworms are less common than rounds or hooks, and are also generally less of a concern in a shelter environment. So, it may not be necessary to treat whipworms unless whipworm eggs are found on a fecal exam. However, like roundworm eggs, whipworm eggs are also very resistant to disinfection, so it is not a bad idea to treat all dogs over 3 months of age for whipworms too. Many shelters only treat for tapeworms if worm segments are noted, tapeworm eggs are seen on a fecal exam, or if the animal has fleas. Treating all animals for fleas on intake is probably more important than treating all animals for tapeworms.
If coccidia is a problem in your puppies and kittens, we recommend giving Ponazuril (Marquis Paste) to all puppies and kittens starting at 2-3 weeks of age, repeated in 7-14 days, and then as needed based on clinical signs/ fecal exams. Dosing details are available on the Veterinarian Log-In section of our website.
Which animals should be treated for intestinal parasites?
The Companion Animal Parasite Council (CAPC) recommends that all companion animals be treated year-round with broad-spectrum heartworm antihelminthics that have activity against parasites with zoonotic potential. Therefore, it would be ideal to make treatment for common parasites as widely available for all shelter animals as possible. However, limited shelter resources often necessitate compromises that are less than ideal.
However, some general guidelines for parasite treatment should apply to nearly all shelter populations. As stated above, roundworms and hookworms are extremely common in puppies and kittens, so it may be particularly important to prophylactically deworm all animals under the age of 3 or 4 months.
However, the national study of intestinal parasites in shelter dogsfound parasites in dogs of all age groups. In this study, hookworms and whipworms were just as common in older dogs as they were in puppies, although roundworms and coccidia were less common in adults than in puppies.
What is the suggested basic deworming protocol?
The most practical dewormer to use for treatment of roundworms and hookworms
is pyrantel (Strongid® or Nemex®). Puppies and kittens should be treated immediately on intake (as early as 2 weeks of age), and again every 2-3 weeks until 8-12 weeks of age. Re-treatment is very important!
For deworming of adults, two doses of pyrantel are recommended: one immediately on intake, another 3 weeks later if still in the shelter.
If whipworms, tapeworms, Giardia, or coccidia are diagnosed, or other parasites are a common problem, the protocol can be changed as needed.
What about environmental contamination?
The eggs or cysts of some parasites are very resistant to disinfection and will persist in the environment for a very long time. Examples of these are roundworms and coccidian. Other parasites, such as Giardia and Tritrichomonas, are quite fragile in the environment and easily destroyed by most disinfectants as well as by drying.
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Nutter FB, Dubey JP, Levine JF, et al. Seroprevalences of antibodies against Bartonella henselae and Toxoplasma gondii and fecal shedding of Cryptosporidium spp, Giardia spp, and Toxocara cati in feral and pet domestic cats. Journal of the American Veterinary Medical Association 2004;225:1394-1398.
Marks SL. Demystifying infectious diarrhea: An update on the diagnosis, management and prevention of common causes of parasitic and bacterial causes of diarrhea. Shelter Medicine Symposium: Building Community Health 2006.
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