Oxfendazole as successful treatment of Taenia hydatigena metacestodes in naturally infected pigs

Luis Antonio Gomez-Puerta，Armando Emiliano Gonzalez，Cesar Gavidia，Viterbo Ayvar，Hector Hugo Garcia，3，Maria Teresa Lopez-Urbina，for the Cysticercosis Working Group in Peru

1School of Veterinary Medicine，National University of San Marcos，Lima，Peru

2Cysticercosis Elimination Program and Center for Global Health Tumbes，Cayetano Heredia University，Tumbes，Peru

3Department of Microbiology，School of Sciences，Cayetano Heredia University，Lima，Peru

Oxfendazole as successful treatment of Taenia hydatigena metacestodes in naturally infected pigs

Luis Antonio Gomez-Puerta1*，Armando Emiliano Gonzalez1，Cesar Gavidia1，Viterbo Ayvar2，Hector Hugo Garcia2，3，Maria Teresa Lopez-Urbina1，for the Cysticercosis Working Group in Peru

1School of Veterinary Medicine，National University of San Marcos，Lima，Peru

2Cysticercosis Elimination Program and Center for Global Health Tumbes，Cayetano Heredia University，Tumbes，Peru

3Department of Microbiology，School of Sciences，Cayetano Heredia University，Lima，Peru

ARTICLE INFO

Article history：

Accepted 14 Mar 2015

Available online 22 Aug 2015

Taenia hydatigena

Cysticercus tenuicollis

Oxfendazole

Treatment

The efficacy of oxfendazole（OFZ）on Taenia hydatigena metacestodes，also called Cysticercus tenuicollis（C.tenuicollis），was studied in 648 raising pigs.This study was performed in Tumbes Department in Peru，an endemic area for cysticercosis.Pigs were randomized in two groups；untreated group（n=142）did not receive any treatment and treated group（n=506）received OFZ treatment at a single dose of 30 mg/kg body weight. Six months after treatment，the pigs were necropsied.The prevalence of infection by C.tenuicollis among the pigs was 27.5%（39/142）and 2.0%（10/506）in untreated and treated groups，respectively.Untreated group was infested only with viable cysts，whereas treated group had no viable cysts.All the cysts found in treated group presented degeneration，with a thick membrane，and they contained milky fluid and fibrous tissue.A single dose of OFZ was effective against C.tenuicollis，thus providing an alternative drug for controlling this parasite in pigs.

Short communicationhttp://dx.doi.org/10.1016/j.apjtb.2015.03.013

1.Introduction

Taenia hydatigena（T.hydatigena）is a cosmopolitan tapeworm from domestic and wild canids.This tapeworm uses domestic ruminants as an intermediate host principally sheep［1，2］. However，T.hydatigena metacestodes，also called Cysticercus tenuicollis（C.tenuicollis），have also been reported in wild ruminants and monogastric mammals such as the pig［1，3，4］. This metacestode has veterinary and economic importance，especially in pig production systems.Studies have shown that the pathogenicity of cysticerci is higher in pigs than in ruminants［1，5］.

Oxfendazole（OFZ）is a potent benzimidazole drug with high efficacyagainstimportantzoonoticdiseasessuchascysticercosis，echinococcosis and fasciolosis.This efficacy has been observed by the Cysticercosis Working Group in Peru（CWGP）using asingleoraldoseof30mg/kgofbodyweightinpigsandsheep［6-8］.In the present scientific work，the efficacy of a single dose of 30 mg/kg of OFZ against T.hydatigena metacestodes in naturally infected pigs is evaluated.

2.Materials and methods

2.1.Study area and animals

This study was conducted in Tumbes Department，Peru，an endemic area for porcine cysticercosis caused by Taenia solium and T.hydatigena.Tumbes is an agricultural and livestock region located in Northern Peru that mainly raises pigs，cattle and goats.

2.2.Study design and treatment

As part of the cysticercosis pilot control program conducted by the CWGP，a total of 648 raising pigs were selected for this study and then they were randomized in 2 groups:treated group（n=506）and control group（n=142）.Control group did notreceive any treatment，while treated group received OFZ treatment at a single dose of 30 mg/kg body weight.Six months after treatment，the pigs were acquired and necropsied at the Center forGlobalHealth-Tumbes（CayetanoHerediaUniversity，Tumbes，Peru）.The pigs used in the study were from 2 to 8 months of age.

2.3.Sampling and sample processing

After treatment，the pigs were acquired and humanely sacrificed.The thoracic and peritoneal cavities were carefully reviewed，with special attention to the mesentery for the presence of cysticerci.Parasites were classified as viable if a defined cystic structure with liquid content was still present，and as degenerated if the cyst had been replaced by semi-solid content or an inflammatory scar（calcified nodule）.

2.4.Data analysis

The Chi-square test was used to assess the association between C.tenuicollis infection status and treatment group.A twosample test of proportions was performed to evaluate the percentages of C.tenuicollis infection between the groups.The significance level was set at 0.05.The data were analyzed using the Stata 12 statistical software（v12；StataCorp LP，College Station，TX，USA）.

2.5.Ethical approvals

This study was approved by the Ethics Committee for Animal Welfare of the School of Veterinary Medicine，University of San Marcos，Lima，Peru.

3.Results

The prevalence of C.tenuicollis was 27.5% （39/142）and 2.0% （10/506）in untreated and treated groups，respectively. Untreated group was infested only with viable cysts and the parasite burden was 1-12 cysts for each animal（Figure 1）.The cyst diameter measurements were from 2.3 to 6.2 cm.No viable cysts were observed among the animals in the treated groups. All cysts found in treated group presented degeneration and their diameter measurements ranged from 1 to 5 cm.The C.tenuicollis infection rate was statistically associated with the treatment group（P＜0.05）.Furthermore，untreated group had a statistically higher infection rate than treated group（P＜0.01）.

In the treated group，degenerative cysts with an inflammatory reaction were the only finding in animals and these were mainly in pigs with high cyst infestation（Figure 1）.The cysts had a thick membrane and contained milky fluid and fibrous tissue. Occasionally，some cysts were observed adhering to the peritoneum，liver and intestines，with infiltration of fibrous tissue.

4.Discussion

The larval stage of T.hydatigena（C.tenuicollis）is responsible for causing high morbidity and mortality in livestock［9-11］. Likewise，C.tenuicollis is responsible for causing condemnation of livers in slaughterhouses［12-15］.However，there have been very few scientific studies regarding treatment of cysticercosis comprising C.tenuicollis.Heath and Lawrence evaluated the efficacy of mebendazole and praziquantel against different taeniid metacestodes，including C.tenuicollis in sheep［16］.They found that mebendazole was efficient against C.tenuicollis at a dose of 50 mg/kg in sheep for 14 consecutive days.Similarly，praziquantel injected subcutaneously at 50 mg/kg on Day 1 was effective against C.tenuicollis.Likewise，Gemmell et al.used a dose of 50 mg/kg of mebendazole for 5 days over a period of 1-3 months，in naturally infected sheep［17］.They found that sheep treated for 1-3 months had no viable cysts，while sheep treated with a single dose had viable cysts.On the other hand，a study evaluatedtheefficacyofpraziquantelinacutecasesof cysticercosis by T.hydatigena in lambs.In that study，15 mg/kg body weight of praziquantel was efficient and reduced the mortality of lambs［18］.

The CWGP has carried out different scientific studies on treatments for metacestodes of major zoonotic importance（Taenia solium and Echinococcus granulosus）.These studies have shown that a single dose of 30 mg/kg is effective for treating porcine echinococcosis and cysticercosis［6，8，19］.The present study demonstrated the same efficacy of OFZ against C.tenuicollis.

Heath and Lawrence showed that mebendazole used for 14 consecutive days was effective against C.tenuicollis［16］. However，ourresultsshowedthegreatestefficacywas achievedthroughusingasingledoseoftreatment. Furthermore，the effect of praziquantel on C.tenuicollis was similar to that of OFZ used in the present study.The cysts in the treated groups had more greatly thickened walls and greater amounts of opaque or macerated fluid than observed in the cysts of the control group.However，the treatment against echinococcosis using praziquantel was not effective at doses of 50 mg/kg for 1 day of treatment，thus contrasting with OFZ，which was effective at a single dose［6］.

Our results show that OFZ is a better antiparasitic drug than others that are used for treating metacestodes in mammals.OFZ is effective against different metacestodes using only a single dose，thus reducing the cost of treatment for farmers.

Conflict of interest statement

We declare that we have no conflict of interest.

Acknowledgments

Partial support from the Fogarty International Center/NIH（training grants D43 TW008273-03 and D43 TW001140）is acknowledged.Luis Antonio Gomez-Puerta's PhD study is supported by theFogarty InternationalCenter/NIH（D43 TW008273-03）.Hector Hugo Garcia is supported by a Welcome Trust Senior International Research Fellowship in Public Health and Tropical Medicine.

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25 Feb 2015

Luis Antonio Gomez-Puerta，Department of Veterinary Epidemiology and Economics，School of Veterinary Medicine，National University of San Marcos，Av.Circunvalacion 2800，San Borja，Lima 41，Peru.

Tel:+51 1 4368938

Fax:+51 1 4365780

E-mail:lucho92@yahoo.com

Peer review under responsibility of Hainan Medical University.

Foundation Project:Partly supported by Fogarty International Center/NIH（training grants D43 TW008273-03 and D43 TW001140），Fogarty International Center/NIH（D43 TW008273-03）.

in revised form 5 Mar 2015