Signalment:  

21-month-old spayed female border collie, Canis familiaris, dogThe dog lived near Tampa, Florida and was maintained in a fenced yard containing a small area of marshy terrain. The presenting history included progressive lameness, pain, and subcutaneous edema of the right forelimb. Over an eight-week period, the dog developed worsening fever, dyspnea, mature neutrophilia, and hypoproteinemia that did not respond to symptomatic treatment or antibiotic therapy. The skin of the right axilla and forelimb contained several well defined areas of deep red discoloration overlying 1-3 cm diameter, fluctuant subcutaneous nodules that extended into subjacent soft tissues. Radiographs revealed linear areas of radiolucency in the soft tissue of the right shoulder region. Surgical pathology of a nodule revealed fibroplasia and chronic panniculitis. Later, a surgical incision into a nodule of the right axilla revealed a 2-cm diameter cystic cavity containing coiled aggregates of many (>10) intact and fragmented white worms ranging from 10-30 mm in length and 2-4 mm in width. The dog was treated with praziquantel (generic, Phoenix Scientific, Vedco, 20mg/kg PO SID x 5 days) and fenbendazole (Panacur-�, DPT Laboratories, Intervet, 50 mg/kg PO SID x 3 days), in addition to antibiotics. Upon identification of the worms as plerocercoids (spargana) of a pseudophyllidian tapeworm, anthelmentic therapy was changed to cefpodoxime proxetil (Simplicef-�, Pfizer, 2.5 mg/kg PO SID x 10 days), metronidazole (generic, PLIVA, Inc, 24 mg/kg PO BID x 7 days), and fenbendazole (100 mg/kg, PO, BID). Praziquantel (Praziject, IVX Animal Health, Inc., 50 mg/kg SQ divided among six sites) was given once a week for 3 weeks. After two weeks of clinical improvement, new nodules developed over the ventral chest, neck, right axillary region, and these encompassed cystic spaces containing many spargana. A right pleural cavity effusion developed, and approximately 500 ml of cloudy serosanguinous fluid were removed by thoracocentesis. Complete blood count and serum biochemical profile revealed mild anemia, normal WBC with mild monocytosis, and moderate hypoalbuminemia. Bacterial culture and sensitivity of the fluid identified Pseudomonas aeruginosa, and enrofloxacin therapy (Baytril-�, Bayer, 3.5 mg/kg PO BID) was initiated. Praziquantel (Biltricide-�, Bayer) was administered at 30 mg/kg PO SID for 8 days. Within two weeks, the dog developed a peritoneal exudate. The dogs overall condition continued to deteriorate and the owners authorized euthanasia and necropsy.

Gross Description:  

The subcutis and intermuscular fascia of the right forelimb, right axilla, ventral thoracic midline, and ventral cervical region contained many inflammatory tissue cysts filled with nodules of entangled intact and fragmented ribbon-shaped white larval cestodes (spargana) surrounded by red, cloudy, thick fluid (Fig. 4-1). There was severe atelectasis of the right lung, and the right pleural cavity contained about 150 ml of thick, cloudy, tan fluid with two larval cestodes and scattered white, friable fragments. There was partial atelectasis of the left lung, and the left pleural cavity contained about 100 ml of cloudy tan fluid with several free-floating larval cestodes. Microscopic examination of the pleural fluid after Wright-Giemsa staining revealed many bacteria both extracellularly and within neutrophils. The peritoneal cavity contained about 250 ml of red cloudy fluid in the caudoventral region containing many bacteria and segmented neutrophils. There were many fibrous adhesions between the omentum and serosal surfaces of the small intestine, spleen, and stomach. At least two larval cestodes were present in the peritoneal fluid.

Histopathologic Description:

Tissues from the skin and soft tissues of the right axilla are submitted. The deep dermis and subcutis of haired skin contain a parasitic cyst with a wall comprised of fibrous connective tissue and a lumen partially filled with larval cestodes, blood, fibrin, and proteinaceous fluid (Fig. 4-2). Macrophages and neutrophils are rare in the region of the cyst, and there is congestion of surrounding vasculature. The larval cestodes lack discernible scolices or suckers and have shallow invaginations of the deeply eosinophilic tegument, resulting in segmentation and formation of tortuous parenchymal cavities (excretory ducts) filled with intensely eosinophilic granular substance. Microtriches occasionally project from the surface of the tegument. Columnar cells (subtegumentary cells) are often located in a parallel row beneath the tegument. The larval body is comprised of a fine fibrillar stroma with many calcareous corpuscles and a few striated muscle fibers, sometimes arranged as loose bundles beneath the tegument. The overlying skin is characterized by hyperkeratosis, epidermal atrophy, follicular keratosis, dermal edema, and venous congestion.

Morphologic Diagnosis:  

Tissue from right axilla: Subcutaneous parasitic cyst, with intralesional larval cestodes and mild focal granulomatous panniculitis

Lab Results:  

Samples of the parasites were submitted to the Diagnostic Parasitology Service, Department of Pathobiology, College of Veterinary Medicine, Auburn University for identification. The worms were identified as larval cestodes (plerocercoids or spargana) of a pseudophyllidian tapeworm, most likely, Spirometra sp. Nucleic acids were extracted from intact, frozen spargana with a robotic extractor (Maxwell-� 16, Promega Corporation) and used as template in PCR of an 18S rDNA fragment employing eucestode primers 84 and 90 as previously described.(7) Amplicons were sequenced (courtesy of Dr. Susan E. Little and M.D. West, Oklahoma State University) using an ABI3730 capillary sequencer and the sequence compared to those previously reported from Spirometra erinacei (D64072), Diphyllobothrium latum (AM778553), Mesocestoides corti (AF286984), and Taenia solium (DQ157224). Sequence of the spargana from this dog (EU392209) most closely resembled (99.4% identical) that previously reported from Spirometra erinacei, a pseudophyllidian cestode

Condition:  

Sparganum proliferum

Contributor Comment:  

The progressive disease in this young adult dog was attributed to proliferative sparganosis, caused by proliferating larval cestodes (spargana) of the organism Sparganum proliferum.(9,12) The spargana were widely distributed throughout the subcutis and intermuscular fascia of the cranial half of the body, the pleural cavities, and the peritoneal cavity. Morbidity resulted from widespread parasitism and septic pleuritis and peritonitis due to Pseudomonas aeruginosa infection. Bacteria were presumably introduced through tracts established by the encysted parasites.

Sparganosis is a disease characterized by the presence of larval pseudophyllidian cestodes in the hosts tissues.(13) Tapeworms may be characterized in tissue sections by the absence of a digestive tract, the presence of a thick layered cuticle with a basement membrane, the presence of calcareous corpuscles, and evidence of a segmented body (4) Plerocercoid larvae are usually solid, club-shaped forms in which scolices and suckers are absent.

Spargana were located in tissue cysts. In histologic sections, there is abundant space around individual spargana (arrows) and the discernible capsule (C) is comprised of eosinophilic amorphous material and relatively few inflammatory cells. Spargana are characterized by invaginations of the tegument resulting in segmentation. Columnar subtegumentary cells form a row beneath the densely eosinophilic tegumentary syncytium, which is covered by a row of dense microtriches. The body is comprised of evenly distributed loose parenchyma with calcareous corpuscles (arrowheads), muscle fibers (M), and excretory ducts (E). Muscle fibers are loosely arranged in a discontinuous row that is oriented parallel to the tegument. Scolices or suckers are not evident. 

There are two forms of sparganosis: non-proliferative and proliferative.(7,10) Most infections are of the non-proliferative type associated with the presence of a single larva of either Spirometra erinaceieuropaei or Spirometra mansonoides. Proliferative sparganosis is caused by the asexual replication of larvae of Sparganum proliferum in host tissues and the migration of these larvae to new tissues where they grow and repeat the process, ultimately resulting in the death of the host.(3) In 2001, Sparganum proliferum was identified phylogenetically as a new species in the order Pseudophyllidea.(9) The first human infection by S. proliferum in the United States was reported in 1908.(14) Infection by S. proliferum has been reported in cats, dogs, and feral hogs, but this appears to be the first case of canine proliferative sparganosis in North America.(1-3,6)

The life cycle of S. proliferum has not yet been confirmed (12) but probably resembles that of other members of a related pseudophyllidian tapeworm, Spirometra spp. Adult tapeworms reside in the intestinal tract of a carnivorous definitive host, where they shed operculated eggs in the feces following discharge from the uterine pore of adult tapeworms. The operculated eggs then hatch in water, releasing a ciliated intermediate form (coracidium). The coracidium is ingested by the first intermediate host, a copepod crustacean (Cyclops sp.), where it develops into the procercoid stage. After the infected copepod is ingested by any one of a broad array of possible second intermediate hosts (any vertebrate other than a fish), the procercoids develop into plerocercoids (spargana) and migrate throughout the soft tissues of the body. If the second intermediate host is eaten by another non-fish vertebrate serving as a transport host, the plerocercoids migrate through the tissues but may remain as plerocercoids. The larval Spirometra can infect and survive in a series of transport hosts until finally consumed by a carnivore definitive host.(7) The ova are released from the uterine pore and are evident in the hosts feces 10-30 days after infection.(1,6,7,11) Infection of the dog can occur through three different ways: ingestion of contaminated water, direct infection of open wounds with plerocercoids, or ingestion of plerocercoids in intermediate vertebrate hosts (11,12) Due to its requirement for an aquatic primary intermediate host, clinical disease is usually associated with exposure to aquatic environments. Sparganosis is zoonotic; thus, precautions should be made to block human infection by preventing consumption of infected water and insufficiently cooked fish or game, or the application of infected medicinal poultices to wounds. It is interesting to note that the first human case of proliferative sparganosis in North America was reported in 1908 in a Florida resident living in the same geographic region as the current canine case.(14)

Currently, there are no products labeled for treatment of Spirometra spp infections.(7) The lack of treatment options for proliferative sparganosis warrants a poor prognosis for survival. Infection of dogs is best controlled by preventing the consumption of infected water or the ingestion of vertebrates that could serve as secondary intermediate hosts.

JPC Diagnosis:  

Skeletal muscle: Rhabdomyositis and panniculitis, pyogranulomatous and eosinophilic, focally extensive, mild with encysted larval cestodes

Conference Comment:  

The contributor did an outstanding job of describing this parasite in depth and in full, so this comment will focus on distinguishing trematodes from cestodes and some common larval forms of cestodes found in domestic animals. 

Adult cestodes are normally present in the intestine of the final host with larval forms present in tissue or body cavities of unfortunate intermediate hosts. Cestodes are split into segmented sections called proglottids that contain both female and male reproductive organs. Both larval and adult cestodes have suckers on their anterior end that may also have hooks depending on the species of cestode.(5)

Several types of cystic larval cestodes are often seen in tissue sections, and these include cysticercoids, cysticercus, coenurus, and the hydatid cyst. Cysticercoids are tiny larvae with a very small bladder and scolex that is encircled by parenchymous tissue. Cysticercus can be identified by a bladder with an inverted neck and scolex that always has four suckers. Coenurus is very similar in appearance to cysticercus but has more than one scolex. Hydatid cysts have a bladder with large numbers of very small scolices. (5)

In tissue section trematodes and cestodes look very similar, but to the trained eye they can be differentiated by a few key features. Both cestodes and trematodes are described as having a spongy parenchyma with no body cavity. Cestodes lack a digestive tract in contrast to trematodes which are endowed with one. Cestodes have calcareous corpuscles which are basophilic clear corpuscles of unknown function. Trematodes are devoid of calcareous corpuscles.(5) These features can help to delineate these two similar appearing parasites. 

References:

1 Bengtson SD, Rogers F: Prevalence of sparganosis by county of origin in Florida feral swine. Vet Parasitol
97:239-242, 2001
2 Beveridge I, Friend SC, Jeganathan N, Charles J: Proliferative sparganosis in Australian dogs. Aust Vet J 76:757-759, 1998
3 Buergelt CD, Greiner EC, Senior DF: Proliferative sparganosis in a cat. J Parasitol 70:121-125, 1984
4 Chitwood M, Lichtenfels J: Parasitological Review: Identification of Parasitic Metazoa in Tissue Sections. Experimental Parasitology 32:407-519, 1972
5 Gardiner CH, Poynton SL: An Atlas of Metazoan Parasites in Animal Tissues. Armed Forces Institute of Pathology, Washington DC, 1999
6 Gray ML, Rogers F, Little S, Puette M, Ambrose D, Hoberg EP: Sparganosis in feral hogs (Sus scrofa) from Florida. J Am Vet Med Assoc 215:204-208, 1999
7 Little S, D A: Spirometra Infection in Cats and Dogs. Compendium on continuing education for the practicing veterinarian 22:299-306, 2000
8 Mariaux J: A molecular phylogeny of the eucestoda. J Parasitol 84:114-124, 1998
9 Miyadera H, Kokaze A, Kuramochi T, Kita K, Machinami R, Noya O, Alarcon de Noya B, Okamoto M, Kojima S: Phylogenetic identification of sparganum proliferum as a pseudophyllidean cestode by the sequence analyses on mitcochondrial COI and nuclear sdhB genes. Parasitology International 50:93-104, 2001
10 Moulinier R, Martinez E, Torres J, Noya O, de NBA, Reyes O: Human proliferative sparganosis in Venezuela: report of a case. Am J Trop Med Hyg 31:358-363, 1982
11 Mueller JF: The biology of Spirometra. J Parasitol 60:3-14, 1974
12 Nakamura T, Hara M, Matsuoka M, Kawabata M, Tsuji M: Human proliferative sparganosis. A new Japanese case. Am J Clin Pathol 94:224-228, 1990
13 Noya O, Alarcon de Noya B, Arrechedera H, Torres J, Arguello C: Sparganum proliferum: an overview of its structure and ultrastructure. Int J Parasitol 22:631-640, 1992
14. Stiles W: The occurance of a proliferating cestode larva (sparganum proliferum) in a man in Florida. Bulletin of the Hygienic Laboratory 40:7-18, 1908

Click the slide to view.

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4-1. Skeletal muscle, dog.

4-2. Skeletal muscle and subcutis, dog.

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