Jeba Jesudoss Chelladurai
BVSc, MS, PhD, DACVM (Parasitology, Immunology)
Dr. Jesudoss Chelladurai is an ACVM board-certified veterinary parasitologist and assistant professor in the Department of Diagnostic Medicine/Pathobiology at Kansas State University. She heads a research lab that focuses on helminth parasites, anthelmintic resistance, and epidemiology. She is involved with teaching parasitology to veterinary students. She also serves as a diagnostic parasitologist for the Kansas State Veterinary Diagnostic Lab and provides consultation to practicing veterinarians on challenging cases.
Read Articles Written by Jeba Jesudoss ChelladuraiSeveral species of tapeworms can live as adults in the small intestines of dogs. In the United States, infections with tapeworms such as Dipylidium caninum and Taenia pisiformis are very common, while infections with tapeworms in the genera Mesocestoides, Echinococcus, Dibothriocephalus, and Spirometra are less common. This article discusses D. caninum and T. pisiformis in detail, with a brief mention of the rarer tapeworms.
The Parasitology series is brought to you by Merck Animal Health, the makers of Bravecto® (fluralaner) and Sentinel® (milbemycin oxime/lufenuron).
D. caninum—known as the flea tapeworm, double-pored tapeworm, or cucumber-seed tapeworm—is found in dogs and cats in the United States. Two distinct host-associated genotypes of D. caninum have been demonstrated: the “feline genotype” and the “canine genotype.”1
Several species of Taenia tapeworms can be found as adults in the small intestines of dogs. They are acquired when dogs ingest the infective stages in intermediate-host “prey” animals. The most common Taenia species in dogs in the United States is T. pisiformis, which uses rabbits as the intermediate host.
Tapeworm Life Cycle and Transmission
Canine tapeworms typically use a predator and prey to complete their life cycle. Adult tapeworms are chains of flattened, progressively maturing segments (called proglottids) beginning anteriorly at the scolex and ending terminally as mature, gravid proglottids. Both Dipylidium and Taenia tapeworms shed segments into the intestines that are passed out in the feces of dogs. The segments are white and resemble rice grains. They may show motility on the dog’s perineum, feces, or bedding or house furniture where the dog has been resting. This can cause disgust and severe distress to pet owners.
In the case of D. caninum, terminal proglottids passed into the feces break down to release egg packets into the environment (FIGURE 1). The egg packets are ingested by flea larvae or immature stages of lice developing in the same environment and mature to infectious cysticercoids in these intermediate hosts. Dogs become infected by ingesting fleas or lice containing infectious cysticercoids. D. caninum obligately uses fleas (Ctenocephalides felis, Pulex irritans) or lice (Trichodectes canis) in its life cycle. In the absence of arthropods, the life cycle cannot be completed. Oral transmission through the ingestion of infected insects is the only recorded route of infection in dogs and humans, primarily children. The prepatent period (i.e., the time from ingestion of infected fleas to the time that Dipylidium segments or egg packets can be detected in feces) can be as short as 17 to 18 days.2
In the case of T. pisiformis, terminal proglottids that are shed into feces break down to release single taeniid-type eggs (FIGURE 2). Eggs in contaminated yards, parks, or wildernesses may be ingested by rabbits, in which the intermediate stages, called cysticerci, develop in the visceral organs. Cysticerci in rabbit viscera must be ingested by a dog for the life cycle to be completed. T. pisiformis is not zoonotic; however, other Taenia species that infect dogs, such as Taenia serialis and Taenia multiceps, may cause human infections. The prepatent period is 42 to 56 days.
Tapeworm Distribution and Prevalence
Both D. caninum and Taenia species are found globally and infect all age groups of dogs.3 D. caninum is the most common tapeworm found in dogs in the United States, and Taenia species are the second most common. No seasonality has been observed with either infection. A survey of nontreated shelter dogs in Oklahoma revealed that 49.5% were infected with D. caninum while 7.2% were infected with Taenia species.4 Client-owned dogs in a different study had a lower prevalence, with 0.84% having D. caninum proglottids or egg packets and 0.47% having Taenia proglottids or eggs.3
The prevalence of T. pisiformis cysticerci in rabbit populations is unknown, as studies to evaluate prevalence of infection in intermediate hosts is lacking. One study in Kentucky found 53% of rabbits to be harboring cysticerci.5
Clinical Presentation of Canine Tapeworm
Canine tapeworms are generally well tolerated by the infected animal, with few or no clinical signs. Released tapeworm segments may be actively motile and cause anal pruritus and scooting behavior in a few infected animals. Adult D. caninum and Taenia tapeworms in the intestine are well tolerated even in large numbers.4
Very rarely, companion animals may become intermediate hosts for Taenia species. Taenia crassiceps has been reported to be the cause of subcutaneous cysticercosis in a dog.6
Diagnosis of Canine Tapeworm
The life stages of tapeworms that are useful in diagnosing infection are (a) the proglottids shed into the intestines by adult worms, which can be recovered from feces or the perineal regions of the infected dog, and (b) eggs or egg packets that are released by degrading proglottids.
Examination of Tapeworm Segments
Segments (proglottids) recovered from the perineal regions of the dog or from furniture/bedding are frequently brought to veterinarians for identification. They typically look like small, white, cooked rice grains when fresh but may be submitted dehydrated. If dehydrated, they may be soaked in water or saline prior to examination. Examination of morphological characteristics of proglottids is facilitated using a microscope.
D. caninum segments may be oval to cucumber-seed shaped and have distinctive bilateral genital pores (FIGURE 3). Crushing the proglottids between 2 glass slides with a few drops of saline releases characteristic egg packets that measure 120 to 200 microns and contain 2 to 30 eggs.
Figure 3. Terminal segment of Dipylidium caninum stained with acetocarmine, which renders the proglottid pink. Arrows point to the bilateral pores.
Taenia segments are roughly rectangular and have a single lateral pore (FIGURE 4). Crushing Taenia proglottids releases “taeniid-type” eggs (also known as “taeniid” eggs). The eggs are brown and thick-shelled with radial striations, measure 25 to 40 microns, and contain a hexacanth embryo. Taeniid-type eggs are produced by both Taenia and Echinococcus species and cannot be differentiated morphologically.
Figure 4. Terminal segment of Taenia species stained with acetocarmine, which renders the proglottid pink. Arrow points to the lateral genital pore.
If all the eggs or egg packets have been completely released by the proglottid, the finding of single or double laterally placed genital pores should provide clues to the identification of the proglottid as Taenia or Dipylidium, respectively.
Fecal Examination for Tapeworm Segments
D. caninum egg packets can sometimes be demonstrated using centrifugal fecal flotation. However, the sensitivity of fecal flotation is extremely low because the proglottids must break down in the fecal sample for egg packets to become detectable on flotation or sedimentation.4
Taeniid eggs have a high specific gravity (1.2251) and cannot be easily recovered in fecal flotation.7 Centrifugal fecal flotation techniques have more sensitivity than passive fecal flotation for taeniid egg diagnosis, but are not 100% sensitive.4 Fecal sedimentation techniques may also be used to identify taeniid eggs in infected animal feces. A slide scanning algorithmic system that has recently been made available can also identify taeniid eggs (VETSCAN IMAGYST; Zoetis, zoetisus.com).8
Since eggs of Taenia cannot be differentiated from zoonotic Echinococcus species eggs, gloves must be worn while handling feces of infected animals and slides, cups, and coverslips used in the diagnostic procedure, which all must be properly disposed of with other biohazardous materials.
Polymerase Chain Reaction
A multiplex polymerase chain reaction (PCR) test to simultaneously detect and differentiate Dipylidium from Taenia species found in dogs has been developed.9 PCR tests to distinguish Taenia from Echinococcus species are also available.
Treatment of Canine Tapeworm
Praziquantel given orally or by subcutaneous or intramuscular injection is approved by the U.S. Food and Drug Administration (FDA) for use against D. caninum and T. pisiformis in dogs. Since several products and combinations are available, veterinarians should refer to the label of the product before prescribing.
Praziquantel resistance in D. caninum has been reported.10 However, practitioners should make every effort to rule out reinfection before declaring an infection praziquantel resistant.
Epsiprantel is FDA approved for oral use against D. caninum and T. pisiformis in dogs. Fenbendazole is FDA approved for oral use against T. pisiformis in dogs.
Prevention and Control of Canine Tapeworm
Flea control must be instituted to prevent reinfections and break the life cycle of D. caninum. Fleas can be killed using products approved by the FDA or Environmental Protection Agency. Hunting of rabbits and/or scavenging rabbit carcasses by dogs must be prevented to break the life cycle of T. pisiformis.
Rarer Tapeworms and Emerging Infections
Echinococcus
Known for many years to exist in wild canids,11,12 Echinococcus multilocularis has been recently recorded in dogs in the contiguous United States.13 Adult worms are less than 1 cm in length and consist of 3 to 5 proglottids (FIGURE 5). Terminal proglottids are shed and contain infective taeniid-type eggs. Typically, rodents serve as intermediate hosts, but humans can accidentally acquire the infection through ingestion of the eggs. Alveolar echinococcosis results in proliferative invasion of tissues of the intermediate host that can lead to death.
Coproantigen enzyme-linked immunosorbent assays (ELISAs) and copro-PCR tests are useful diagnostic tests to help differentiate Echinococcus from Taenia.14,15 Praziquantel is FDA approved for use in dogs against Echinococcus adults. Since taeniid-type eggs cannot be differentiated, veterinarians must be aware of the exposure risk they pose to clients, clinic staff, and the general public and advocate for the safe handling of dog feces.
Mesocestoides
Mesocestoides species may use dogs as definitive hosts or as second intermediate hosts. Adult worms live in the small intestine. Terminal proglottids are shed and contain a characteristic, medially located parauterine organ (FIGURE 6). Eggs do not possess the thick shell seen in taeniid-type eggs, are colorless with a hexacanth embryo, and are 30 to 40 microns in size. Mesocestoides species use an insect as the first intermediate host and a vertebrate as the second intermediate host. Dogs may become accidental second intermediate hosts and suffer from peritoneal and/or pleural infections with larval stages of the parasite (tetrathyridia).
Treatment of the larval infection in dogs requires prolonged use of high doses of fenbendazole. Treatment of adult infections should be treatable with either praziquantel or epsiprantel.
Figure 6. Nonterminal segment of Mesocestoides species stained with acetocarmine, which renders the proglottid pink. Arrow points to the parauterine organ, which is larger, rounded, and well developed in terminal gravid segments.
Dibothriocephalus and Spirometra
Dibothriocephalus (formerly Diphyllobothrium) and Spirometra tapeworms, which are associated with aquatic intermediate hosts, can infect dogs, humans, and other mammals. In the United States, Dibothriocephalus is found in the Great Lakes region, while Spirometra is found in eastern and Gulf Coast states. Dibothriocephalus is acquired when dogs and humans ingest larval tapeworm stages (plerocercoids) found in fish tissue. Adult Spirometra are acquired when hosts ingest larval tapeworm stages found in the tissues of frogs, snakes, birds, or mammals. Adult tapeworms develop in the small intestines and may be passed out as complete worms in the vomitus or feces. Single eggs, not proglottids, are released and are detectable in fecal sedimentations. Infection is tolerated with minimal gastrointestinal signs of diarrhea, vomiting, weight loss and, in the case of Dibothriocephalus, pernicious anemia.
Although not FDA approved, praziquantel has been successfully used in treatment. Repeated treatments at higher doses may be necessary to achieve complete cure. Additionally, dogs may experience sparganosis should they become intermediate hosts of Spirometra by ingesting copepods with larval stages (procercoids) or through the entry of larvae via open wounds. These may cause nonpainful swellings or even death depending on the organ involved.
References
1. Beugnet F, Labuschagne M, Vos C, et al. Analysis of Dipylidium caninum tapeworms from dogs and cats, or their respective fleas – Part 2. Distinct canine and feline host association with two different Dipylidium caninum genotypes. Parasite. 2018;25:31.
2. Fourie JJ, Crafford D, Horak IG, Stanneck D. Prophylactic treatment of flea-infested dogs with an imidacloprid/flumethrin collar (Seresto®, Bayer) to preempt infection with Dipylidium caninum. Parasitol Res. 2013;112(suppl 1):33-46.
3. Nagamori Y, Payton ME, Looper E, et al. Retrospective survey of endoparasitism identified in feces of client-owned dogs in North America from 2007 through 2018. Vet Parasitol. 2020;282:109137.
4. Adolph C, Barnett S, Beall M, et al. Diagnostic strategies to reveal covert infections with intestinal helminths in dogs. Vet Parasitol. 2017;247:108-112.
5. Strohlein DA, Christensen BM. Metazoan parasites of the eastern cottontail rabbit in western Kentucky. J Wildl Dis. 1983;19(1):20-23.
6. Ballweber LR. Taenia crassiceps subcutaneous cysticercosis in an adult dog. Vet Rec. 2009;165(23):693-694.
7. David ED, Lindquist WD. Determination of the specific gravity of certain helminth eggs using sucrose density gradient centrifugation. J Parasitol. 1982;68(5):916-919.
8. Nagamori Y, Hall Sedlak R, DeRosa A, et al. Evaluation of the VETSCAN IMAGYST: an in-clinic canine and feline fecal parasite detection system integrated with a deep learning algorithm. Parasit Vectors. 2020;13(1):346.
9. Zhu GQ, Li L, Ohiolei JA, et al. A multiplex PCR assay for the simultaneous detection of Taenia hydatigena, T. multiceps, T. pisiformis, and Dipylidium caninum infections. BMC Infect Dis. 2019;19(1):854.
10. Jesudoss Chelladurai J, Kifleyohannes T, Scott J, Bewer MT. Praziquantel resistance in the zoonotic cestode. Am J Trop Med Hyg.
2018;99(5):1201-1205.
11. Storandt ST, Kazacos KR. Echinococcus multilocularis identified in Indiana, Ohio, and east-central Illinois. J Parasitol. 1993;79(2):301-305.
12. Storandt ST, Virchow DR, Dryden MW, et al. Distribution and prevalence of Echinococcus multilocularis in wild predators in Nebraska, Kansas, and Wyoming. J Parasitol. 2002;88(2):420-422.
13. Kuroki K, Morishima Y, Neil J, et al. Intestinal echinococcosis in a dog from Missouri. JAVMA. 2020;256(9):1041-1046.
14. Deplazes P, Gottstein B, Eckert J, et al. Detection of Echinococcus coproantigens by enzyme-linked immunosorbent assay in dogs, dingoes and foxes. Parasitol Res. 1992;78(4):303-308.
15. Abbasi I, Branzburg A, Campos-Ponce M, et al. Copro-diagnosis of Echinococcus granulosus infection in dogs by amplification of a newly identified repeated DNA sequence. Am J Trop Med Hyg. 2003;69(3):324-330.