PeeR ReVIeWeD PARASITE PROTOCOLS

PARASITE PROTOCOLS FOR YOUR PRACTICE CANINE INTESTINAL HELMINTHS Recommendations from the Companion Parasite Council

Dwight D. Bowman, MS, PhD, Diplomate ACVM The mission of the Companion Animal Parasite (, Hon) Council (CAPC) is to foster animal and human health, Cornell University while preserving the human–animal bond, through recommendations for the diagnosis, treatment, Tom Nelson, DVM prevention, and control of parasitic infections. For more information, including detailed parasite control Animal Medical Center, Anniston, Alabama recommendations, please visit capcvet.org.

Table 1. National Prevalence of Common Canine Parasites A NATIONAL POSITIVE/ DIAGNOSTIC HelmintH PREVALENCE TESTED STAGE C 2.23% 1/43 Figure A Roundworm 1.86% 1/54 Figure B () Whipworm 1.23% 1/81 Figure C (Trichuris vulpis) B

elminth parasites are regularly diagnosed in dogs in the U.S (Table 1). Despite approximately 2 Clinical Signs. In puppies infected via transmamma- Hdecades of excellent therapeutics, ry transmission, sometimes fatal may develop as large numbers of dogs are still infected with common early as 2 to 3 weeks of age, usually occurring before , roundworms, whipworms, and tapeworms.1 appear in the feces. Affected puppies may present with Many dogs are also affected by helminths that occur locally pale mucous membranes, anemia, ill thrift, failure to gain or sporadically in the U.S. These helminths may not be con- weight, poor haircoat, dehydration, and melena. Puppies trolled by the different products available for prescribed harboring many worms develop an acute normocytic, nor- broad-spectrum parasite control, which highlights the mochromic anemia, followed by hypochromic, microcytic importance of an annual fecal examination. anemia due to iron deficiency. While helminths can affect many different systems and organs, such as the and , this article will focus on those that affect the gastrointestinal (GI) system.

HOOKWORMS caninum, , & Uncinaria stenocephala Distribution. Hookworms are found in dogs throughout the U.S. (Figure 1). Prevalence in the southeast is about twice the national prevalence; numbers are lower than the national average in the southwest and upper Midwest. • A caninum is the most significant agent of hookworm- induced anemia,2 and its eggs account for the prepon- derance of positive samples represented in Figure 1. • U stenocephala is thought to occur more commonly in northern climates. • A braziliense is found in the Caribbean and southeast- Figure 1. map from the CAPC website showing the prevalence of ern U.S., and along the Gulf and Atlantic coasts. hookworm eggs in submitted fecal specimens.

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Table 2. U.S. Canine Intestinal Helminths: Transmission, Diagnostics, Treatment, & Prevention Helminth TRANSMISSION DIAGNOSIS TREATMENT Prevention HOOKWORMS Ancylostoma of paratenic Fecal flotation Bayer: Advantage Multi, Drontal Plus Bayer: Advantage Multi caninum hosts or infective Elanco: Trifexis Elanco: Trifexis larvae, transcutaneous, Merck: Panacur C, Tri-Heart Plus Merck: Tri-Heart Plus transmammary Merial: Heartgard Plus Merial: Heartgard Plus Novartis: Sentinel Novartis: Sentinel Virbac: Iverhart Plus, Virbantel Virbac: Iverhart Plus Zoetis: Nemex, Nemex 2, ProHeart 6 Ancylostoma Ingestion of paratenic Fecal flotation Merial: Heartgard Plus Merial: Heartgard Plus braziliense hosts or infective larvae, Virbac: Iverhart Max, Iverhart Plus, Virbac: Iverhart Max, Iverhart transcutaneous Virbantel Plus Uncinaria Ingestion of infective larvae Fecal flotation Bayer: Advantage Multi, Drontal Plus Bayer: Advantage Multi, stenocephala Merck: Panacur C, Tri-Heart Plus Drontal Plus Merial: Heartgard Plus Merck: Tri-Heart Plus Virbac: Iverhart Plus, Virbantel Merial: Heartgard Plus Zoetis: Nemex, Nemex 2, ProHeart 6 Virbac: Iverhart Plus ROUNDWORMS Toxocara canis Ingestion of parasite Fecal flotation Bayer: Advantage Multi, Drontal Plus Bayer: Advantage Multi hosts or infective , Elanco: Trifexis Elanco: Trifexis transplacental Merck: Panacur C, Tri-Heart Plus Merck: Tri-Heart Plus Toxascaris Ingestion of egg or paratenic Fecal flotation Merial: Heartgard Plus Merial: Heartgard Plus leonina hosts Novartis: Sentinel Novartis: Sentinel Virbac: Virbantel Zoetis: Nemex, Nemex 2 Ingestion of egg or paratenic Fecal flotation Most drugs used to treat Toxocara and Toxascaris are likely to be procyonis hosts effective* WHIPWORMS Trichuris vulpis Ingestion of infective egg Fecal flotation Bayer: Advantage Multi, Drontal Plus Bayer: Advantage Multi Elanco: Trifexis Elanco: Trifexis Merck: Panacur C Novartis: Sentinel Novartis: Sentinel TAPEWORMS Dipylidium Ingestion of intermediate Finding worm Bayer: Droncit, Drontal Plus Novartis: Sentinel Spectrum caninum () segments, Novartis: Sentinel Spectrum is a possible choice for fecal flotation Virbac: Iverhart Max, Virbantel prevention Zoetis: Cestex Virbac: Iverhart Max Taenia Ingestion of intermediate Finding worm Bayer: Droncit, Drontal Plus Novartis: Sentinel Spectrum host (mammalian) segments, Merck: Panacur C Virbac: Iverhart Max fecal flotation Novartis: Sentinel Spectrum Virbac: Iverhart Max, Virbantel Zoetis: Cestex Echinococcus Ingestion of intermediate Fecal flotation Bayer: Droncit, Drontal Plus Novartis: Sentinel Spectrum multilocularis host () Novartis: Sentinel Spectrum Virbac: Iverhart Max is Echinococcus Ingestion of intermediate Fecal flotation a possible choice for granulosus host (ungulate) prevention* Ingestion of intermediate Fecal flotation , 25 mg/kg for 2 None latum host (piscine) consecutive days* Spirometra Ingestion of intermediate Fecal flotation mansonoides host (terrestrial ) TREMATODES Alaria species Ingestion of intermediate Fecal flotation Bayer: Droncit,* Drontal Plus* Novartis: Sentinel Spectrum host (vertebrate) Merck: Panacur C* is a possible choice for pre- Virbac: Iverhart Max,* Virbantel* vention* Zoetis: Cestex* Virbac: Iverhart Max is a pos- Nanophyetus Ingestion of intermediate Fecal flotation Bayer: Droncit,* Drontal Plus* sible choice for prevention* salmincola host () * Not approved product for control of this helminth

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death at a few days of age because the large numbers of lar- vae acquired in utero cross the alveoli en route to the . Adult dogs—even those infected in utero—can be repeatedly infected with adult T canis if the is oral- ly exposed to even a few (25–100) in- fective eggs. Diagnosis. Eggs

are identified in C anine I ntestinal H el m inths the feces of dogs by centrifugal fecal flotation. The eggs of all 3 species can Figure 3. Eggs of Baylisascaris be readily observed in a procyonis (left) and Toxocara fecal sample; the eggs of Figure 2. Map from the CAPC website showing the prevalence of canis (right) from a canine fecal roundworm eggs in submitted fecal specimens. B procyonis are smaller specimen; magnification, 40×. and darker than eggs from Without immediate intervention, these may die. other roundworm species (Figure 3). Those that survive usually continue as “poor doers,” with Treatment & Prevention. See Table 2. chronic anemia. Respiratory disease and may occur in puppies when large numbers of larvae migrate WHIPWORMS through the lungs. Trichuris vulpis Diagnosis. Eggs are found in the feces of dogs, and are Distribution. T vulpis eggs are found throughout the best identified by centrifugal fecal flotation. The eggs of U.S. (Table 1). Prevalence rates are lower in the north U stenocephala are larger than those of Ancylostoma spe- central and mountain states, but T vulpis is present in cies; most laboratories can now distinguish the eggs on more than 1% of canine fecal samples from Washington fecal examination. and Michigan (Figure 4). Treatment & Prevention. See Table 2. Clinical Signs. Some T vulpis infections result in hem- orrhagic typhilitis or colitis, characterized by ROUNDWORMS streaked with mucus and fresh .2 Severe infections Toxocara canis, , & Baylisascaris due to the presence of thousands of worms may occur procyonis when a dog lives in a highly contaminated area, resulting in bloody diarrhea, weight loss, dehydration, anemia and, Distribution. As shown in Figure 2, T canis is found in in the most extreme cases, death. dogs throughout the U.S., with areas in the northeastern and western U.S. above the national average. T leonina is Diagnosis. Eggs are identified in the feces of dogs by cen- less common, but considered to be more common in the trifugal fecal flotation, and require a flotation solution of colder areas of the U.S. B procyonis is commonly found in higher specific gravity than hookworms and roundworms throughout much of the U.S. but, fortunately, in- to insure maximal recovery. 3 fections in dogs are rare. Treatment & Prevention. See Table 2. Transmission. Puppies are often infected with T canis in utero via transplacental transmission.2 After , dogs primarily become infected with ascarids via ingestion of: • Larvated eggs from a contaminated environment (all ascarid species) • Other vertebrate hosts that have consumed larvated eggs and, thus, have larvae in their tissue. Clinical Signs. Disease caused by infection with T canis is most severe in young puppies, and can occur before eggs are present in the feces. Puppies infected in utero may present with ill thrift, failure to gain weight, and a poor haircoat; a pot-bellied appearance is also common. Those with heavy infections may expel a large mass of worms in vomitus at 4 to 6 months of age, causing the owner distress as the worms are large and usually alive. Severe infections in neonatal pups can result in acute Figure 4. Map from the CAPC website showing the prevalence of whipworm eggs in submitted fecal specimens. tvpjournal.com January/February 2014 Today’s Veterinary Practice 75 | PARASITE PROTOCOLS

TAPEWORMS Cyclophyllidean Zoonotic Disease Risk Posed by Helminths • Dipylidium caninum • Taenia species Toxocara canis: Of the zoonotic helminth parasites • Echinococcus species discussed, T canis is considered the most common infectious agent in humans. Diphyllobothriidean In the 1950s, it was realized that, if children ingest- • Diphyllobothrium latum ed the embryonated eggs of T canis, they could de- • Spirometra species velop severe systemic disease caused by larval mi- Distribution & Transmission. CAPC does not collect gration into their and lungs. A small percentage data on tapeworm prevalence because the common spe- of children and young adults also developed retinal cies found in dogs are unlikely to be diagnosed by simple lesions from the larvae entering their eyes after mi- fecal examination, and fecal flotation alone almost cer- gration through the body. tainly underestimates the frequency of infection. This dif- When these larvae enter human hosts, they persist in the tissues for years. Ingestion of these embryo- ficulty is due to the focal distribution of proglottids (and, nated eggs appears to be fairly common in the U.S. thus, eggs) in fecal material and the eggs’ weight, which because approximately 14% of the U.S. population keeps them from readily floating. Even in the presence of demonstrate to larvae. This statistic sug- infection, a fecal sample may be negative for tapeworm gests that humans, like dogs, have larvae seques- segments—called proglottids—or eggs. Based on various tered in their tissues, although overt human disease published studies, prevalence of canine tapeworms varies is less commonly seen. 4 from 4% to 60%. : The round- D caninum & Taenia species. The 2 most common worm, B procyonis, can develop into adults within tapeworms in U.S. dogs and are D caninum (associ- dogs, and is much more worrisome than T canis. ated with ) and T pisiformis (acquired from rabbits). When B procyonis larvae infect warm-blooded Other Taenia species are found throughout North America hosts (birds or ), the results can be devas- 4 and may infect dogs that ingest sheep or wild ungulates. tating. Since this disease was first recognized in the All Taenia species in North America utilize mammals as 1950s, B procyonis has killed over 100 different spe- intermediate hosts, and dogs as final hosts. cies of animals,9 and 18 human deaths have been as- Intermediate hosts of tapeworms become infected from cribed to this infection. Death results from migration eggs in a dog’s feces. of the larvae into tissues of the body, including the • D caninum: The egg is eaten by a flea larvae; the dog brain. Unlike T canis larvae, these larvae mature and becomes infected when it eats an adult flea contain- cause significant neurologic disease. ing the fully mature larval stage. After a dog ingests an Raccoons routinely deposit their feces in similar infected flea, it begins shedding proglottids in its feces places called latrines. While this precludes most hu- approximately 3 weeks later. mans from contact with B procyonis eggs, dogs, with • Taenia species: The rabbit or ungulate intermediate their indiscriminate defecation habits, are much more host becomes infected by ingesting eggs while graz- worrisome hosts. The seroprevalence of larval toxo- ing; then the dog becomes infected when it ingests the cariasis in humans demonstrates that other animals viscera (or muscles) that contains larval stages of the and humans are at risk if dogs are shedding Baylisas- tapeworm. Taenia species need 6 to 8 weeks to mature caris eggs. before they begin shedding segments in the dog’s feces. & Ancylostoma brazil- E multilocularis & E granulosus. These parasites are iense. In the U.S., dogs can be infected with the zoo- found in the northern U.S. and Canada. E multilocularis notic hookworms, A caninum and A braziliense. The cycles through small and ; E granulosus cycles larvae of A caninum and A braziliense can penetrate through large, wild ruminants, such as moose and . human , migrating around for weeks to months The ranges of both are expanding, and concern exists that if left untreated; this disease is known as cutaneous these dangerous zoonotic agents may begin affecting do- migrans. It is critical that all dogs be treated mestic dog populations. routinely to control hookworm infections and prevent D latum & Spirometra species. Infections with D contamination of areas frequented by people. latum are acquired from ingestion of freshwater fish and Echinococcus multilocularis & . The ranges of the tapeworms E mul- tend to sporadically occur in the northern U.S. and Canada. tilocularis and E granulosus are expanding, rais- S mansonoides occur in the eastern U.S. and are acquired ing concerns that these dangerous zoonotic agents from ingestion of larvae in tissues of a variety of vertebrate may move into local dog populations. Thus, in areas intermediate hosts. where this worm is present in canids—the northern Clinical Signs. Disease resulting from adult tapeworms is U.S. and Canada—products effective against this probably underappreciated. agent need to be considered when planning helminth Humans with adult Taenia infections may report vague preventive strategies. abdominal discomfort, hunger pains, loss of appetite,

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chronic indigestion, persis- pecially those new to or visiting tent diarrhea, or alternating endemic areas of Oregon and diarrhea and constipation.5 Washington, may present with However, dogs are infected fever, diarrhea, and thrombocy- with different Taenia spe- topenia, which results from the cies than humans. rickettsial agent, Neorickettsia Tapeworms cause marked helminthoeca. thickening of the intestinal mu- Diagnosis. Dogs become infect- cosa in dogs, and cases of fatal

Figure 5. Segments of Di- ed with N salmincola by ingesting Figure 7. Egg of C anine I ntestinal H el m inths pylidium caninum (left) and impaction have been reported metacercariae in salmonid fish; Taenia pisiformis (right); in young puppies with fleas these flukes often begin shedding in canine fecal specimen. these specimens are Courtesy Dr. J. Stewart, and massive tapeworm infec- eggs within a short time after in- backlit. The D caninum tions. When examined at nec- Aumsville Animal Clinic, segment has 2 genital fection, and a fecal examination Aumsville, Oregon pores on the left and ropsy, the intestines of a dog with a direct smear revealing eggs right and contains egg with 50 T pisiformis are usu- in a dog with clinical signs of neorickettsiosis will help packets; the T pisiformis ally packed to the intestinal lu- verify the clinical diagnosis. segment has a single men’s full capacity. pore on the right, and left N salmincola (Figure 7) eggs are small and heavy (they and right branching uter- Infections with S mansonoi- float best in a saturated sugar solution and centrifugal ine segments with eggs, des have been associated with flotation), while Alaria eggs are larger. which are fairly indistinct. GI disease in dogs and cats.4 Re- ported clinical signs include di- Treatment. See Table 2. Tetracyclines are considered arrhea, weight loss, and vomiting, which usually resolve the treatment of choice for neorickettsial disease as- following appropriate anthelmintic therapy. sociated with N helminthoeca. Short-acting corticoste- roids may be used supportively. Diagnosis. A D caninum egg packet or taeniid egg in a fecal sample is diagnostic of tapeworm infection, and Prevention. See Table 2. proglottids can be readily identified as either Dipylid- ium or Taenia (Figure 5). However, the chances of finding an egg in the feces are minimized because eggs Are Intestinal Helminths Developing Resistance? are intermittently shed in segments and are usually too Concern has been raised about development of resis- dense to float in common flotation solutions. tance of intestinal helminths to the active ingredients Because Echinococcus and Taenia are morphologically of various preventives included in broad-spectrum similar, and Echinococcus is a significant and dangerous year-round parasite control. zoonotic agent, there is cause for concern if a taeniid egg, While the concern about resistance is real, the but no proglottids, is identified in the feces of a dog locat- chance of resistance developing is minimal—as long ed where Echinococcus is also found. as success of prevention/treatment is monitored. Mon- Tests are available in Europe that itoring includes annual fecal examinations and con- distinguish Echinococcus eggs firming worm burden removal post treatment. If a dog from Taenia eggs, but these returns to the clinic and tests positive, deworm it again tests are not yet available in with a different product and follow up to confirm treat- the U.S. ment success. The eggs of D latum and The veterinary practice team has a responsibility to Spirometra species are also the pet and the public to make certain that treatments are efficacious. found in the feces, and resem- Figure 6. Egg of a Diphyllobothriidean ble a trematode egg (Figure tapeworm in canine fecal 6). These eggs are shed from specimen. Courtesy CAPC the tapeworm strobila within APPLICATION TO CLINICAL PRACTICE the dog’s intestine rather than being passed in termi- Few things are as disruptive to the human–animal nal segments. bond as a puppy or adult dog passing a worm in its stool, vomiting a wad of worms, or depositing a tape- Treatment. See Table 2. worm proglottid on the owner’s lap. Since some intesti- nal helminths also have zoonotic potential, control and TREMATODES prevention of these parasites are imperative to preserve Alaria canis, Alaria marcianae, & Nanophyetus this bond. salmincola Prevalence. Intestinal helminths are common in all Distribution. Alaria species are found throughout the dogs, especially stray dogs and dogs found in shelters. 6 7 U.S, while N salmincola is found in the coastal northwest. Surveys of shelter dogs in the U.S. demonstrate higher Clinical Signs. Alaria alone does not cause signs in numbers of helminths than the numbers seen in the dogs. However, dogs that contract N salmincola, es- general canine population.8 (Continued on page 56.) tvpjournal.com January/February 2014 Today’s Veterinary Practice 77 | PARASITE PROTOCOLS

• In the northeast, 1 or more of every 10 dogs has round- References 1. little SE, Johnson EM, Lewis D, et al. Prevalence of intestinal worms, hookworms, and whipworms. parasites in pet dogs in the United States. Vet Parasitol 2009; • These numbers are higher in the Midwest, approaching 166:144-152. 1 in every 5 dogs, and highest in the South, ranging 2. epe C. Intestinal : Biology and control. Vet Clin N Am Sm Anim Pract 2009; 39(6):1091-1107. from 1 in 5 to 1 in every 2 dogs. 3. Kazacos KR. Unusual faecal parasite in a dog. NAVC Clin Brief 2006; • Even in western states, 1 in 10 to 1 in 20 dogs sampled 4(6):37-39. are positive for these parasites. 4. Conboy G. Cestodes of dogs and cats in North America. Vet Clin N Am Sm Anim Pract 2009; 39(6):1075-1090. Because roundworm and whipworm eggs can per- 5. beaver PC, Jung RC, Cupp EW. Cyclophyllidean tapeworms. sist in the environment for several years, clients Clinical Parasitology. Philadelphia: Lea & Febiger, 1984, pp 505-543. need to understand that their pets are at risk for in- 6. Gaunt MC, Carr AP. A survey of intestinal parasites in dogs from Saskatoon, Saskatchewan. Can Vet J 2011; 52(5):497-500. fection when outside. In addition, stray dogs defecat- 7. Headley SA, Scorpio DG, Vidotto O, et al. Neorickettsia ing in the yard or park are not receiving treatment and helminthoeca and poisoning disease: A review. Vet J 2011; 187:165-173. likely infected. 8. blagburn BL. National parasite prevalence survey: An interim report. Diagnosis. Dogs should have fecal examinations per- Proc NAVC Conference 2009; pp 1168-1171. 9. Kazacos KR, Jelicks LA, Tanowitz HB. Baylisascaris larva migrans. formed 2 to 4 times during their first year of life and 1 to Handb Clin Neurol 2013; 114:251-262. 2 times per year as adults, depending on patient health and lifestyle factors. Treatment & Prevention. • Routinely deworm puppies beginning at 2 weeks of age, with repeated every 2 weeks. • Begin administering a monthly control product with ef- ficacy against intestinal helminths when puppies reach 4 to 8 weeks of age (Table 2). • Broad spectrum parasite control products should be administered monthly year round. Inform clients that routine parasite control typical- ly results in negative fecal examinations, confirming the efficacy of routine parasite prevention. Other pre- ventive measures they can implement include: • Keeping dogs on a leash or in a fenced yard to prevent predation and scavenging activities; this limits the op- portunity for dogs to acquire infection via ingestion of vertebrate hosts (ascarids) or from a feces-contaminat- ed environment. • Promptly removing feces from the yard to prevent eggs from being released from fecal material or dispersing into the environment. • Preventing contamination with eggs of B procyonis by not keeping raccoons as pets and avoiding areas fre- quented by dogs and wildlife. n

GI = gastrointestinal

Dwight Bowman, MS, PhD ,is pro- fessor of parasitology at Cornell Univer- sity College of Veterinary Medicine. He received his MS and PhD in parasitol- ogy from Tulane University. Tom Nelson, DVM, is co-owner of the Animal Medical Center, Anniston, Al. He received his DVM from the College of Veterinary Medicine at Texas A&M University.

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