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Case report: Protein-losing enteropathy caused by Mesocestoides vogae (syn. M. corti) in a dog
Veterinary Parasitology 205 (2014) 412–415
Contents lists available at ScienceDirect
Veterinary Parasitology journal homepage: www.elsevier.com/locate/vetpar
Short Communication
Case report: Protein-losing enteropathy caused by Mesocestoides vogae (syn. M. corti) in a dog Yu Tamura a , Hiroshi Ohta a,∗ , Takuya Kashiide b , Jun Matsumoto b , Tatsuya Sakurai c , Nozomu Yokoyama a , Keitaro Morishita d , Kensuke Nakamura d , Masahiro Yamasaki a , Mitsuyoshi Takiguchi a a Laboratory of Veterinary Internal Medicine, Department of Veterinary Clinical Sciences, Graduate School of Veterinary Medicine, Hokkaido University, Sapporo 060-0818, Japan b Laboratory of Medical Zoology, Department of Veterinary Medicine, Faculty of Bioresource Sciences, Nihon University, 1866 Kameino, Fujisawa, Kanagawa 252-0880, Japan c Laboratory Animal Facilities, Jikei University School of Medicine, Tokyo 105-8461, Japan d Veterinary Teaching Hospital, Department of Veterinary Clinical Sciences, Graduate School of Veterinary Medicine, Hokkaido University, Sapporo 060-0818, Japan
a r t i c l e
i n f o
Article history: Received 20 March 2014 Received in revised form 22 July 2014 Accepted 23 July 2014 Keywords: Mesocestoides vogae (syn. M. corti) Dog Protein-losing enteropathy
a b s t r a c t An eight-year-old, neutered, female Shetland Sheepdog presented with a 6-week history of small intestinal diarrhea. Regenerative anemia, hypoproteinemia, and an increased plasma C-reactive protein concentration were detected on blood examination. Fecal examination and abdominal radiography were unremarkable. Abdominal ultrasonography showed diffusely hyperechoic mucosa in the small intestine. Gastroduodenoscopy, performed under general anesthesia, revealed mucosal edema and increased granularity in the duodenum and jejunum. Histopathological examination of the endoscopically biopsied small intestinal mucosa revealed tapeworm infection. A single administration of a combined anthelmintic drug (5 mg/kg praziquantel, 14.4 mg/kg pyrantel pamoate, and 15 mg/kg febantel) was successful for deworming, and the dog fully recovered. The parasites were removed from stored frozen duodenal mucosa and morphologically identified as Mesocestoides sp. immature adult worms. Mitochondrial (mt) 12S rDNA and mt cytochrome c oxide subunit 1 genes were amplified from the parasites. DNA sequence analysis showed that the genes shared 100% identity with those of reported M. vogae (syn. M. corti). This is the first reported case of protein-losing enteropathy caused by M. vogae in a dog. © 2014 Elsevier B.V. All rights reserved.
1. Introduction Mesocestoides sp. is a cestode, which belongs to tapeworms. The lifecycle of Mesocestoides sp. has yet to be fully clarified, but it is known that two intermediate hosts are required for its completion, and carnivores and birds are
∗ Corresponding author. Tel.: +81 11 706 5223; fax: +81 11 706 5223. E-mail address: [email protected] (H. Ohta). http://dx.doi.org/10.1016/j.vetpar.2014.07.027 0304-4017/© 2014 Elsevier B.V. All rights reserved.
considered to be definitive hosts (Bowman, 1997; Toplu et al., 2004). Coprophagous arthropods such as oribatid mites may serve as the first intermediate host. In the first intermediate host, oncospheres (first larval stage) develop into cysticercoids (second larval stage). A tetrathyridium (third larval stage) is formed when an infected mite is eaten by a second intermediate host, such as rodents, amphibians, reptiles, and birds. The final adult form develops when the second intermediate host is ingested by the definitive host. The adult form of Mesocestoides sp. develops within
Y. Tamura et al. / Veterinary Parasitology 205 (2014) 412–415
the intestines of the definitive host, such as dogs, cats, and wild carnivores, approximately 2–3 weeks after ingestion of the second intermediate host (Caruso et al., 2003; Tennant, 2001). Dogs can harbor both the intermediate stage and adult tapeworm at the same time (Papini et al., 2010; Toplu et al., 2004). Canine peritoneal larval cestodiasis (CPLC) is caused by tetrathyridium and is known as life-threatening peritonitis with severe peritoneal effusion in dogs (Bonfanti et al., 2004; Patten et al., 2013; Venco et al., 2005; Wirtherle et al., 2007). Recently, the first reported case of CPLC caused by M. vogae (syn. M. corti) was published in Japan (Kashiide et al., 2014). This finding indicated that the lifecycle of M. vogae is maintained in Japan. In contrast to CPLC caused by tetrathyridium, adult worm infection in the intestinal tract of their final hosts is usually asymptomatic. Adult Mesocestoides sp. tapeworms are intestinal parasites of domestic and wild carnivores and are found globally, with the exception of Australia, and are typically non-pathogenic (Boyce et al., 2011). Intestinal Mesocestoides sp. adult worm infection has been found in stray dogs in western parts of Iran (22/83 dogs), Jordan (3/340 dogs), and Mexico City (2/120 dogs) (Dalimi et al., 2006; Eguía-Aguilar et al., 2005; El-Shehabi et al., 1999), in farm dogs in Heilongjiang Province, China (36/178 dogs) (Wang et al., 2006), and in gun dogs in Japan (10 dogs) (Kugi, 1983), but is considered to be rare in practice (Michael, 2012; Williams et al., 1975). It was reported that the percentage of Mesocestides sp. infection was 0.2% in 8438 dogs from the Veterinary Laboratory Freiburg in Germany, and that there were no Mesocestides sp. infection from 239 pet dogs in Italy (Barutzki and Schaper, 2003; Riggio et al., 2013). To the best of our knowledge, all previous studies describing intestinal Mesocestoides sp. infection were postmortem or fecal examinations with no clinical signs. Therefore, there have been no reports of a clinical case of intestinal Mesocestoides sp. infection. This report describes protein-losing enteropathy caused by M. vogae infection in a dog. 2. Case report An eight-year-old, neutered, female Shetland Sheepdog, weighing 10 kg, was referred to Hokkaido University Veterinary Teaching Hospital for detailed examination of a 6-week history of small intestinal diarrhea and hypoproteinemia. Before referral, the dog had been treated with a homemade elimination diet composed of chicken, rice, and potato for 1 week, and metronidazole (10 mg/kg q12 h) for 1 week, but showed no recovery. The dog’s clinical signs were temporarily improved when an anti-inflammatory dose of prednisolone was administered. At presentation, the physical examination findings were unremarkable. Hematology showed mild regenerative anemia (red blood cells [RBC]: 5.63 × 106 /l, packed cell volume [PCV]: 33%, reticulocytes: 90 × 103 /l). Serum biochemistry revealed mild hypoalbuminemia (2.2 g/dl) and increased C-reactive protein (CRP) concentration (5.2 mg/dl). Fecal examination, urinalysis (urinary proteinto-creatinine ratio: 0.09), and abdominal radiography were unremarkable. Abdominal ultrasonography showed
413
Fig. 1. Photomicrograph of the duodenal mucosa. Tapeworm infection on the surface of the duodenal mucosa was confirmed. Tapeworms are attached to villi by their suckers (arrow). Hematoxylin and eosin (H&E) 200×.
diffusely hyperechoic mucosa in the small intestine, indicating mucosal inflammation. Gastroduodenoscopy, performed under general anesthesia, revealed edema and increased granularity in the duodenal and jejunal mucosa. Multiple mucosal biopsy specimens were obtained from the duodenum and jejunum. The samples were placed in neutral-buffered 10% formalin and embedded in paraffin, and hematoxylin and eosin (HE)-stained sections were prepared. In addition, two mucosal biopsy specimens were stored at −80 ◦ C for the study on canine inflammatory bowel disease (IBD). Histopathological examination of the specimen obtained by endoscopic biopsy revealed tapeworm infection in the intestinal mucosa with moderate lymphocytic-plasmacytic enteritis and mild intestinal lymphangiectasia (Fig. 1). The dog was treated with a combined anthelmintic agent (50 mg praziquantel, 144 mg pyrantel pamoate, and 150 mg febantel; Drontal® Plus, Bayer Yakuhin, Ltd., Osaka, Japan). Two days after single oral administration of combined anthelmintic agent, the diarrhea had completely disappeared. Within 3 weeks after treatment, anemia, hypoalbuminemia, and the serum CRP concentration were normalized (RBC: 6.51 × 106 /l, PCV: 41%, albumin: 2.8 g/dl, CRP: 0.15 mg/dl) without the additional use of anthelmintic agents. Because histopathological examination revealed tapeworm infection in the intestinal mucosa, we thawed and examined the stored frozen intestinal mucosa under a stereomicroscope, and removed the parasites from the intestinal mucosa. The parasites appeared whitish and were less than 1 mm. Some of the parasites were stored in 70% ethanol at room temperature and identified by the Laboratory of Medical Zoology, Nihon University. The parasites were observed under an optical microscope and morphologically identified as an early stage of an adult worm without segments. Such parasites were characterized by the presence of four suckers and the absence of a rostellum or hooks (Fig. 2). Molecular identification of the adult worm was conducted by targeting both the mitochondrial (mt) 12S rDNA and mt cytochrome c oxidase subunit 1 (CO1)
414
Y. Tamura et al. / Veterinary Parasitology 205 (2014) 412–415
Fig. 2. Close-up appearance of immature M. vogae (syn. M. corti). Four suckers are present (arrowhead).
genes, as previously described (Kashiide et al., 2014). DNA sequence analysis showed that those genes shared 100% identity with those of M. vogae (syn. M. corti). Based on these results, the parasites collected from the patient were confirmed to be M. vogae. 3. Discussion To the best of our knowledge, this is the first reported case of clinically confirmed protein-losing enteropathy caused by Mesocestoides sp. in a dog. Moreover, this is also the first reported case of canine intestinal cestodiasis caused by Mesocestoides sp. in a pet dog in Japan. In humans, several clinical cases of intestinal Mesocestoides sp. infection have been reported. In Korea, a patient infected with Mesocestoides lineatus complained of abdominal pain and the massive discharge of sesame-like proglottids in his stools for several months before diagnosis (Eom et al., 1992). In the United States, a 19-month-old boy was infected with Mesocestoides variabilis, and the only symptom was diarrhea (Fuentes et al., 2003). Based on these previous reports, intestinal infection by Mesocestoides sp. is unlikely to cause a life-threatening condition in humans. In contrast, the present dog infected with M. vogae exhibited severe clinical signs, although the pathogenicity of M. vogae remains unclear. In this case, fecal examination showed no other parasites which can cause small intestinal diarrhea, such as hookworms, roundworms, Giardia, or Isospora. Therefore, the dog’s clinical signs seemed to have been caused by M. vogae (syn. M. corti). The whole proglottid is the diagnostic stage; however, it is seldom seen in feces (Barutzki and Schaper, 2011; Tassi and Widenhorn, 1977). Therefore, we cannot eliminate Mesocestoides infection based on negative fecal examinations. Moreover, we could not find M. vogae during the gastroduodenoscopy, possibly because of the small size of the parasites. In the present case, a combined anthelmintic agent (50 mg praziquantel, 144 mg pyrantel pamoate, and 150 mg febantel) was used and effectively improved the clinical
signs with a single oral administration. It has been reported that praziquantel (Papini et al., 2010; Kashiide et al., 2014) and fenbendazole (Caruso et al., 2003; Crosble et al., 1998) are effective drugs for the treatment of CPLC. Praziquantel is the drug most commonly used against cestode infection, and it displays marked anthelmintic activity against a wide range of adult and larval cestodes (Miró et al., 2007). In addition, the effectiveness of a single dose of praziquantel (10 mg/kg) for the treatment of intestinal Mesocestoides variabilis infection in humans was also reported (Fuentes et al., 2003). Febantel is a prodrug that is metabolized to fenbendazole (Miró et al., 2007). However, it was reported that febantel alone was ineffective in dogs with intestinal cestodiasis (Sharp and McCurdy, 1985). Therefore, praziquantel administration seemed to be effective against intestinal Mesocestoides sp. adult worm infection in dogs. The present case had previously been treated with prednisolone based on a tentative diagnosis of canine IBD. According to a previous report, the administration of prednisolone might be a predisposing factor for atypical infiltration of the liver and lymph nodes by Mesocestoides sp. larvae in dogs with CPLC due to its immunosuppressive effect (Patten et al., 2013). Therefore, the use of prednisolone might have exacerbated the intestinal Mesocestoides sp. infection in this case. Thus, prednisolone should be administered after excluding the possibility of Mesocestoides sp. infection, because there is a chance of latent infection. In this study, Mesocestoides sp. was confirmed as M. vogae using molecular identification by targeting both the mt 12S rDNA and mt CO1 genes. Recently, Kashiide et al. described the first reported case of CPLC caused by M. vogae in Japan (Kashiide et al., 2014) in Kanagawa Prefecture, located about 800 km south of Sapporo City. Therefore, the lifecycle of M. vogae suggested that it is maintained widely in Japan. However, the source of M. vogae infection was not clear in this study. Further investigation is needed to clarify the distribution and lifecycle of M. vogae in Japan. In conclusion, this is the first reported case of proteinlosing enteropathy caused by M. vogae (syn. M. corti) in a dog. Praziquantel may be effective for the treatment of intestinal Mesocestoides sp. adult worm infection in dogs.
Conflict of interest The authors have no financial conflicts of interest.
References Barutzki, D., Schaper, R., 2003. Endoparasites in dogs and cats in Germany 1999–2002. Parasitol. Res. 90 (suppl 3), S148–S150. Barutzki, D., Schaper, R., 2011. Results of parasitological examinations of faecal samples from cats and dogs in Germany between 2003 and 2010. Parasitol. Res. 109 (suppl. 1), S45–S60. Bonfanti, U., Bertazzolo, W., Pagliaro, L., Demarco, B., Venco, L., Casiraghi, M., Bandi, C., 2004. Clinical, cytological and molecular evidence of Mesocestoides sp. infection in a dog from Italy. J. Vet. Med. A: Physiol. Pathol. Clin. Med. 51, 435–438. Bowman, D.D., 1997. Cestodes. In: Bowman, D.D., Lynn, R.C. (Eds.), Georgi’s Parasitology for Veterinarians. , 6th ed. W.B. Saunders, Philadelphia, pp. 129–150. Boyce, W., Shender, L., Schultz, L., Vickers, W., Johnson, C., Ziccardi, M., Beckett, L., Padgett, K., Crosbie, P., Sykes, J., 2011. Survival analysis
Y. Tamura et al. / Veterinary Parasitology 205 (2014) 412–415 of dogs diagnosed with canine peritoneal larval cestodiasis (Mesocestoides spp.). Vet. Parasitol. 180, 256–261. Caruso, K.J., James, M.P., Fisher, D., Paulson, R.L., Christopher, M.M., 2003. Cytologic diagnosis of peritoneal cestodiasis in dogs caused by Mesocestoides sp. Vet. Clin. Pathol. 32, 50–60. Crosble, P.R., Boyce, W.M., Platzer, E.G., Nadler, S.A., Kerner, C., 1998. Diagnostic procedures and treatment of eleven dogs with peritoneal infections caused by Mesocestoides spp. J. Am. Vet. Med. Assoc. 213, 1578–1583. Dalimi, A., Sattari, A., Motamedi, G., 2006. A study on intestinal helminthes of dogs, foxes and jackals in the western part of Iran. Vet. Parasitol. 142, 129–133. Eguía-Aguilar, P., Cruz-Reyes, A., Martínez-Maya, J.J., 2005. Ecological analysis and description of the intestinal helminths present in dogs in Mexico City. Vet. Parasitol. 127, 139–146. El-Shehabi, F.S., Abdel-Hafez, S.K., Kamhawi, S.A., 1999. Prevalence of intestinal helminths of dogs and foxes from Jordan. Parasitol. Res. 85, 928–934. Eom, K.S., Kim, S.H., Rim, H.J., 1992. Second case of human infection with Mesocestoides lineatus in Korea. Kisaengchunghak Chapchi 30, 147–150. Fuentes, M.V., Galán-Puchades, M.T., Malone, J.B., 2003. Short report: a new case report of human Mesocestoides infection in the United States. Am. J. Trop. Med. Hyg. 68, 566–567. Kashiide, T., Matsumoto, J., Yamaya, Y., Uwasawa, A., Miyoshi, A., Yamada, K., Watari, T., Nogami, S., 2014. Case report: First confirmed caseof canine peritoneal larval cestodiasis caused by Mesocestoides vogae (syn. M. corti) in Japan. Vet. Parasitol. 201, 154–157. Kugi, G., 1983. Morphological studies on the Cestode, Mesocestiodes paucitesticulus. J. Jpn. Vet. Med. Assoc. 36, 464–468 (written in Japanese with English summary). Michael, R.L., 2012. Infection. In: Washabau, R.J., Day, M.J. (Eds.), Canine and Feline Gastroenterology. W.B. Saunders, Philadelphia, pp. 683–695.
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Miró, G., Mateo, M., Montoya, A., Vela, E., Calonge, R., 2007. Survey of intestinal parasites in stray dogs in the Madrid area and comparison of the efficacy of three anthelmintics in naturally infected dogs. Parasitol. Res. 100, 317–320. Papini, R., Matteini, A., Bandinelli, P., Pampurini, F., Mancianti, F., 2010. Effectiveness of praziquantel for treatment of peritoneal larval cestodiasis in dogs: a case report. Vet. Parasitol. 170, 158–161. Patten, P.K., Rich, L.J., Zaks, K., Blauvelt, M., 2013. Cestode infection in 2 dogs: cytologic findings in liver and a mesenteric lymph node. Vet. Clin. Pathol. 42, 103–108. Riggio, F., Mannella, R., Ariti, G., Perrucci, S., 2013. Intestinal and lung parasites in owned dogs and cats from central Italy. Vet. Parasitol. 193, 78–84. Sharp, M.L., McCurdy, H.D., 1985. Anthelmintic efficacy of febantel combined with praziquantel in dogs. J. Am. Vet. Med. Assoc. 187, 254–255. Tassi, P., Widenhorn, O., 1977. Research on intestinal parasitic diseases in dogs of the city of Rome. Parassitologia 19, 43–57. Tennant, B.J., 2001. Intestine. In: Ramsey, K., Tennant, B.J. (Eds.), Mannual of Canine and Feline Infectious Diseases. British Small Animal Veterinary Association, Gloucester, pp. 128–145. Toplu, N., Yildiz, K., Tunay, R., 2004. Massive cystic tetrathyridiosis in a dog. J. Small Anim. Pract. 45, 410–412. Venco, L., Kramer, L., Pagliaro, L., Genchi, C., 2005. Ultrasonographic features of peritoneal cestodiasis caused by Mesocestoides sp. in a dog and in a cat. Vet. Radiol. Ultrasound 46, 417–422. Wang, C.R., Qiu, J.H., Zhao, J.P., Xu, L.M., Yu, W.C., Zhu, X.Q., 2006. Prevalence of helminthes in adult dogs in Heilongjiang Province, the People’s Republic of China. Parasitol. Res. 99, 627–630. Williams, J.F., Westherimer, J., Banman, W.R., 1975. Mesocestoides infection in the dog. J. Am. Vet. Med. Assoc. 166, 996–998. Wirtherle, N., Wiemann, A., Ottenjann, M., Linzmann, H., van der Grinten, E., Kohn, B., Gruber, A.D., Clausen, P.H., 2007. First case of canine peritoneal larval cestodosis caused by Mesocestoides lineatus in Germany. Parasitol. Int. 56, 317–320.
Contents lists available at ScienceDirect
Veterinary Parasitology journal homepage: www.elsevier.com/locate/vetpar
Short Communication
Case report: Protein-losing enteropathy caused by Mesocestoides vogae (syn. M. corti) in a dog Yu Tamura a , Hiroshi Ohta a,∗ , Takuya Kashiide b , Jun Matsumoto b , Tatsuya Sakurai c , Nozomu Yokoyama a , Keitaro Morishita d , Kensuke Nakamura d , Masahiro Yamasaki a , Mitsuyoshi Takiguchi a a Laboratory of Veterinary Internal Medicine, Department of Veterinary Clinical Sciences, Graduate School of Veterinary Medicine, Hokkaido University, Sapporo 060-0818, Japan b Laboratory of Medical Zoology, Department of Veterinary Medicine, Faculty of Bioresource Sciences, Nihon University, 1866 Kameino, Fujisawa, Kanagawa 252-0880, Japan c Laboratory Animal Facilities, Jikei University School of Medicine, Tokyo 105-8461, Japan d Veterinary Teaching Hospital, Department of Veterinary Clinical Sciences, Graduate School of Veterinary Medicine, Hokkaido University, Sapporo 060-0818, Japan
a r t i c l e
i n f o
Article history: Received 20 March 2014 Received in revised form 22 July 2014 Accepted 23 July 2014 Keywords: Mesocestoides vogae (syn. M. corti) Dog Protein-losing enteropathy
a b s t r a c t An eight-year-old, neutered, female Shetland Sheepdog presented with a 6-week history of small intestinal diarrhea. Regenerative anemia, hypoproteinemia, and an increased plasma C-reactive protein concentration were detected on blood examination. Fecal examination and abdominal radiography were unremarkable. Abdominal ultrasonography showed diffusely hyperechoic mucosa in the small intestine. Gastroduodenoscopy, performed under general anesthesia, revealed mucosal edema and increased granularity in the duodenum and jejunum. Histopathological examination of the endoscopically biopsied small intestinal mucosa revealed tapeworm infection. A single administration of a combined anthelmintic drug (5 mg/kg praziquantel, 14.4 mg/kg pyrantel pamoate, and 15 mg/kg febantel) was successful for deworming, and the dog fully recovered. The parasites were removed from stored frozen duodenal mucosa and morphologically identified as Mesocestoides sp. immature adult worms. Mitochondrial (mt) 12S rDNA and mt cytochrome c oxide subunit 1 genes were amplified from the parasites. DNA sequence analysis showed that the genes shared 100% identity with those of reported M. vogae (syn. M. corti). This is the first reported case of protein-losing enteropathy caused by M. vogae in a dog. © 2014 Elsevier B.V. All rights reserved.
1. Introduction Mesocestoides sp. is a cestode, which belongs to tapeworms. The lifecycle of Mesocestoides sp. has yet to be fully clarified, but it is known that two intermediate hosts are required for its completion, and carnivores and birds are
∗ Corresponding author. Tel.: +81 11 706 5223; fax: +81 11 706 5223. E-mail address: [email protected] (H. Ohta). http://dx.doi.org/10.1016/j.vetpar.2014.07.027 0304-4017/© 2014 Elsevier B.V. All rights reserved.
considered to be definitive hosts (Bowman, 1997; Toplu et al., 2004). Coprophagous arthropods such as oribatid mites may serve as the first intermediate host. In the first intermediate host, oncospheres (first larval stage) develop into cysticercoids (second larval stage). A tetrathyridium (third larval stage) is formed when an infected mite is eaten by a second intermediate host, such as rodents, amphibians, reptiles, and birds. The final adult form develops when the second intermediate host is ingested by the definitive host. The adult form of Mesocestoides sp. develops within
Y. Tamura et al. / Veterinary Parasitology 205 (2014) 412–415
the intestines of the definitive host, such as dogs, cats, and wild carnivores, approximately 2–3 weeks after ingestion of the second intermediate host (Caruso et al., 2003; Tennant, 2001). Dogs can harbor both the intermediate stage and adult tapeworm at the same time (Papini et al., 2010; Toplu et al., 2004). Canine peritoneal larval cestodiasis (CPLC) is caused by tetrathyridium and is known as life-threatening peritonitis with severe peritoneal effusion in dogs (Bonfanti et al., 2004; Patten et al., 2013; Venco et al., 2005; Wirtherle et al., 2007). Recently, the first reported case of CPLC caused by M. vogae (syn. M. corti) was published in Japan (Kashiide et al., 2014). This finding indicated that the lifecycle of M. vogae is maintained in Japan. In contrast to CPLC caused by tetrathyridium, adult worm infection in the intestinal tract of their final hosts is usually asymptomatic. Adult Mesocestoides sp. tapeworms are intestinal parasites of domestic and wild carnivores and are found globally, with the exception of Australia, and are typically non-pathogenic (Boyce et al., 2011). Intestinal Mesocestoides sp. adult worm infection has been found in stray dogs in western parts of Iran (22/83 dogs), Jordan (3/340 dogs), and Mexico City (2/120 dogs) (Dalimi et al., 2006; Eguía-Aguilar et al., 2005; El-Shehabi et al., 1999), in farm dogs in Heilongjiang Province, China (36/178 dogs) (Wang et al., 2006), and in gun dogs in Japan (10 dogs) (Kugi, 1983), but is considered to be rare in practice (Michael, 2012; Williams et al., 1975). It was reported that the percentage of Mesocestides sp. infection was 0.2% in 8438 dogs from the Veterinary Laboratory Freiburg in Germany, and that there were no Mesocestides sp. infection from 239 pet dogs in Italy (Barutzki and Schaper, 2003; Riggio et al., 2013). To the best of our knowledge, all previous studies describing intestinal Mesocestoides sp. infection were postmortem or fecal examinations with no clinical signs. Therefore, there have been no reports of a clinical case of intestinal Mesocestoides sp. infection. This report describes protein-losing enteropathy caused by M. vogae infection in a dog. 2. Case report An eight-year-old, neutered, female Shetland Sheepdog, weighing 10 kg, was referred to Hokkaido University Veterinary Teaching Hospital for detailed examination of a 6-week history of small intestinal diarrhea and hypoproteinemia. Before referral, the dog had been treated with a homemade elimination diet composed of chicken, rice, and potato for 1 week, and metronidazole (10 mg/kg q12 h) for 1 week, but showed no recovery. The dog’s clinical signs were temporarily improved when an anti-inflammatory dose of prednisolone was administered. At presentation, the physical examination findings were unremarkable. Hematology showed mild regenerative anemia (red blood cells [RBC]: 5.63 × 106 /l, packed cell volume [PCV]: 33%, reticulocytes: 90 × 103 /l). Serum biochemistry revealed mild hypoalbuminemia (2.2 g/dl) and increased C-reactive protein (CRP) concentration (5.2 mg/dl). Fecal examination, urinalysis (urinary proteinto-creatinine ratio: 0.09), and abdominal radiography were unremarkable. Abdominal ultrasonography showed
413
Fig. 1. Photomicrograph of the duodenal mucosa. Tapeworm infection on the surface of the duodenal mucosa was confirmed. Tapeworms are attached to villi by their suckers (arrow). Hematoxylin and eosin (H&E) 200×.
diffusely hyperechoic mucosa in the small intestine, indicating mucosal inflammation. Gastroduodenoscopy, performed under general anesthesia, revealed edema and increased granularity in the duodenal and jejunal mucosa. Multiple mucosal biopsy specimens were obtained from the duodenum and jejunum. The samples were placed in neutral-buffered 10% formalin and embedded in paraffin, and hematoxylin and eosin (HE)-stained sections were prepared. In addition, two mucosal biopsy specimens were stored at −80 ◦ C for the study on canine inflammatory bowel disease (IBD). Histopathological examination of the specimen obtained by endoscopic biopsy revealed tapeworm infection in the intestinal mucosa with moderate lymphocytic-plasmacytic enteritis and mild intestinal lymphangiectasia (Fig. 1). The dog was treated with a combined anthelmintic agent (50 mg praziquantel, 144 mg pyrantel pamoate, and 150 mg febantel; Drontal® Plus, Bayer Yakuhin, Ltd., Osaka, Japan). Two days after single oral administration of combined anthelmintic agent, the diarrhea had completely disappeared. Within 3 weeks after treatment, anemia, hypoalbuminemia, and the serum CRP concentration were normalized (RBC: 6.51 × 106 /l, PCV: 41%, albumin: 2.8 g/dl, CRP: 0.15 mg/dl) without the additional use of anthelmintic agents. Because histopathological examination revealed tapeworm infection in the intestinal mucosa, we thawed and examined the stored frozen intestinal mucosa under a stereomicroscope, and removed the parasites from the intestinal mucosa. The parasites appeared whitish and were less than 1 mm. Some of the parasites were stored in 70% ethanol at room temperature and identified by the Laboratory of Medical Zoology, Nihon University. The parasites were observed under an optical microscope and morphologically identified as an early stage of an adult worm without segments. Such parasites were characterized by the presence of four suckers and the absence of a rostellum or hooks (Fig. 2). Molecular identification of the adult worm was conducted by targeting both the mitochondrial (mt) 12S rDNA and mt cytochrome c oxidase subunit 1 (CO1)
414
Y. Tamura et al. / Veterinary Parasitology 205 (2014) 412–415
Fig. 2. Close-up appearance of immature M. vogae (syn. M. corti). Four suckers are present (arrowhead).
genes, as previously described (Kashiide et al., 2014). DNA sequence analysis showed that those genes shared 100% identity with those of M. vogae (syn. M. corti). Based on these results, the parasites collected from the patient were confirmed to be M. vogae. 3. Discussion To the best of our knowledge, this is the first reported case of clinically confirmed protein-losing enteropathy caused by Mesocestoides sp. in a dog. Moreover, this is also the first reported case of canine intestinal cestodiasis caused by Mesocestoides sp. in a pet dog in Japan. In humans, several clinical cases of intestinal Mesocestoides sp. infection have been reported. In Korea, a patient infected with Mesocestoides lineatus complained of abdominal pain and the massive discharge of sesame-like proglottids in his stools for several months before diagnosis (Eom et al., 1992). In the United States, a 19-month-old boy was infected with Mesocestoides variabilis, and the only symptom was diarrhea (Fuentes et al., 2003). Based on these previous reports, intestinal infection by Mesocestoides sp. is unlikely to cause a life-threatening condition in humans. In contrast, the present dog infected with M. vogae exhibited severe clinical signs, although the pathogenicity of M. vogae remains unclear. In this case, fecal examination showed no other parasites which can cause small intestinal diarrhea, such as hookworms, roundworms, Giardia, or Isospora. Therefore, the dog’s clinical signs seemed to have been caused by M. vogae (syn. M. corti). The whole proglottid is the diagnostic stage; however, it is seldom seen in feces (Barutzki and Schaper, 2011; Tassi and Widenhorn, 1977). Therefore, we cannot eliminate Mesocestoides infection based on negative fecal examinations. Moreover, we could not find M. vogae during the gastroduodenoscopy, possibly because of the small size of the parasites. In the present case, a combined anthelmintic agent (50 mg praziquantel, 144 mg pyrantel pamoate, and 150 mg febantel) was used and effectively improved the clinical
signs with a single oral administration. It has been reported that praziquantel (Papini et al., 2010; Kashiide et al., 2014) and fenbendazole (Caruso et al., 2003; Crosble et al., 1998) are effective drugs for the treatment of CPLC. Praziquantel is the drug most commonly used against cestode infection, and it displays marked anthelmintic activity against a wide range of adult and larval cestodes (Miró et al., 2007). In addition, the effectiveness of a single dose of praziquantel (10 mg/kg) for the treatment of intestinal Mesocestoides variabilis infection in humans was also reported (Fuentes et al., 2003). Febantel is a prodrug that is metabolized to fenbendazole (Miró et al., 2007). However, it was reported that febantel alone was ineffective in dogs with intestinal cestodiasis (Sharp and McCurdy, 1985). Therefore, praziquantel administration seemed to be effective against intestinal Mesocestoides sp. adult worm infection in dogs. The present case had previously been treated with prednisolone based on a tentative diagnosis of canine IBD. According to a previous report, the administration of prednisolone might be a predisposing factor for atypical infiltration of the liver and lymph nodes by Mesocestoides sp. larvae in dogs with CPLC due to its immunosuppressive effect (Patten et al., 2013). Therefore, the use of prednisolone might have exacerbated the intestinal Mesocestoides sp. infection in this case. Thus, prednisolone should be administered after excluding the possibility of Mesocestoides sp. infection, because there is a chance of latent infection. In this study, Mesocestoides sp. was confirmed as M. vogae using molecular identification by targeting both the mt 12S rDNA and mt CO1 genes. Recently, Kashiide et al. described the first reported case of CPLC caused by M. vogae in Japan (Kashiide et al., 2014) in Kanagawa Prefecture, located about 800 km south of Sapporo City. Therefore, the lifecycle of M. vogae suggested that it is maintained widely in Japan. However, the source of M. vogae infection was not clear in this study. Further investigation is needed to clarify the distribution and lifecycle of M. vogae in Japan. In conclusion, this is the first reported case of proteinlosing enteropathy caused by M. vogae (syn. M. corti) in a dog. Praziquantel may be effective for the treatment of intestinal Mesocestoides sp. adult worm infection in dogs.
Conflict of interest The authors have no financial conflicts of interest.
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