• 1.

    Mas-Coma S, Valero MA, Bargues MD, 2009. Chapter 2. Fasciola, lymnaeids and human fascioliasis, with a global overview on disease transmission, epidemiology, evolutionary genetics, molecular epidemiology and control. Adv Parasitol 69: 41146.

    • Search Google Scholar
    • Export Citation
  • 2.

    Lean I, Westwood C, Playford M, 2008. Livestock disease threats associated with intensification of pastoral dairy farming. N Z Vet J 56: 261269.

    • Search Google Scholar
    • Export Citation
  • 3.

    Parkinson M, O’Neill SM, Dalton JP, 2007. Endemic human fasciolosis in the Bolivian Altiplano. Epidemiol Infect 135: 669674.

  • 4.

    Marcos LA, Terashima A, Leguia G, Canales M, Espinoza JR, Gotuzzo E, 2007. Fasciola hepatica infection in Peru: an emergent disease. Rev Gastroenterol Peru 27: 389396.

    • Search Google Scholar
    • Export Citation
  • 5.

    Espinoza JR, Terashima A, Herrera-Velit P, Marcos LA, 2010. Human and animal fascioliasis in Peru: impact in the economy of endemic zones. Rev Peru Med Exp Salud Publica 27: 604612.

    • Search Google Scholar
    • Export Citation
  • 6.

    Keiser J, Duthaler U, Utzinger J, 2010. Update on the diagnosis and treatment of food-borne trematode infections. Curr Opin Infect Dis 23: 513520.

    • Search Google Scholar
    • Export Citation
  • 7.

    Fairweather I, 2009. Triclabendazole progress report, 2005–2009: an advancement of learning? J Helminthol 83: 139150.

  • 8.

    Brennan GP, Fairweather I, Trudgett A, Hoey E, McCoy, McConville M, Meaney M, Robinson M, McFerran N, Ryan L, Lanusse C, Mottier L, Alvarez L, Solana H, Virkel G, Brophy PM, 2007. Understanding triclabendazole resistance. Exp Mol Pathol 82: 104109.

    • Search Google Scholar
    • Export Citation
  • 9.

    Alvarez-Sanchez MA, Mainar-Jaime RC, Perez-Garcia J, Rojo-Vazquez FA, 2006. Resistance of Fasciola hepatica to triclabendazole and albendazole in sheep in Spain. Vet Rec 159: 424425.

    • Search Google Scholar
    • Export Citation
  • 10.

    Overend DJ, Bowen FL, 1995. Resistance of Fasciola hepatica to triclabendazole. Aust Vet J 72: 275276.

  • 11.

    Olaechea F, Lovera V, Larroza M, Raffo F, Cabrera R, 2011. Resistance of Fasciola hepatica against triclabendazole in cattle in Patagonia (Argentina). Vet Parasitol 178: 364366.

    • Search Google Scholar
    • Export Citation
  • 12.

    Oliveira DR, Ferreira DM, Stival CC, Romero F, Cavagnolli F, Kloss A, Araujo FB, Molento MB, 2008. Triclabendazole resistance involving Fasciola hepatica in sheep and goats during an outbreak in Almirante Tamandare, Parana, Brazil. Rev Bras Parasitol Vet 17 17 (Suppl 1): 149153.

    • Search Google Scholar
    • Export Citation
  • 13.

    Rojas M, 1990. Parasitismo de los Rumiantes Domésticos. Lima, Peru: Maijosa.

  • 14.

    Snedecor GW, Cochran WG, 1989. Statistical Methods. Ames, IA: Iowa State University Press.

  • 15.

    Gavidia CM, Gonzalez AE, Barron EA, Ninaquispe B, Llamosas M, Verastegui MR, Robinson C, Gilman RH, 2010. Evaluation of oxfendazole, praziquantel and albendazole against cystic echinococcosis: a randomized clinical trial in naturally infected sheep. PLoS Negl Trop Dis 4: e616.

    • Search Google Scholar
    • Export Citation
  • 16.

    Gonzalez AE, Gavidia C, Falcon N, Bernal T, Verastegui M, Garcia HH, Gilman RH, Tsang VC, 2001. Protection of pigs with cysticercosis from further infections after treatment with oxfendazole. Am J Trop Med Hyg 65: 1518.

    • Search Google Scholar
    • Export Citation
  • 17.

    Alvarez L, Moreno G, Moreno L, Ceballos L, Shaw L, Fairweather I, Lanusse C, 2009. Comparative assessment of albendazole and triclabendazole ovicidal activity on Fasciola hepatica eggs. Vet Parasitol 164: 211216.

    • Search Google Scholar
    • Export Citation
  • 18.

    McKellar QA, Scott EW, 1990. The benzimidazole anthelmintic agents–a review. J Vet Pharmacol Ther 13: 223247.

  • 19.

    Bogan J, Armour J, 1987. Anthelmintics for ruminants. Int J Parasitol 17: 483491.

  • 20.

    Boray JC, Crowfoot PD, Strong MB, Allison JR, Schellenbaum M, Von Orelli M, Sarasin G, 1983. Treatment of immature and mature Fasciola hepatica infections in sheep with triclabendazole. Vet Rec 113: 315317.

    • Search Google Scholar
    • Export Citation
  • 21.

    Fairweather I, 2005. Triclabendazole: new skills to unravel an old(ish) enigma. J Helminthol 79: 227234.

  • 22.

    Keiser J, Engels D, Buscher G, Utzinger J, 2005. Triclabendazole for the treatment of fascioliasis and paragonimiasis. Expert Opin Investig Drugs 14: 15131526.

    • Search Google Scholar
    • Export Citation
  • 23.

    Keiser J, Utzinger J, 2004. Chemotherapy for major food-borne trematodes: a review. Expert Opin Pharmacother 5: 17111726.

  • 24.

    Fairweather I, 2011. Raising the bar on reporting ‘triclabendazole resistance’. Vet Rec 168: 514515.

  • 25.

    Fraser DE, Hunt PJ, Skinner RJ, Coles GC, 2006. Survey of parasite control on sheep farms in south-west England. Vet Rec 158: 5557.

  • 26.

    Furmaga S, Gundalach JL, Sadzikowski A, Paciejewski S, 1982. (Systamex (oxfendazole) in the treatment of parasitoses of sheep). Med Weter 38: 269271.

    • Search Google Scholar
    • Export Citation
  • 27.

    Lanusse CE, Gascon LH, Prichard RK, 1995. Comparative plasma disposition kinetics of albendazole, fenbendazole, oxfendazole and their metabolites in adult sheep. J Vet Pharmacol Ther 18: 196203.

    • Search Google Scholar
    • Export Citation
  • 28.

    Soraci AL, Mestorino N, Errecalde JO, 1997. Some pharmacokinetic parameters of oxfendazole in sheep. Vet Res Commun 21: 283287.

  • 29.

    Blanton RE, Wachira TM, Zeyhle EE, Njoroge EM, Magambo JK, Schantz PM, 1998. Oxfendazole treatment for cystic hydatid disease in naturally infected animals. Antimicrob Agents Chemother 42: 601605.

    • Search Google Scholar
    • Export Citation
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Efficacy of a Single Oral Dose of Oxfendazole against Fasciola hepatica in Naturally Infected Sheep

Luis A. Gomez-PuertaSchool of Veterinary Medicine, Universidad Nacional Mayor de San Marcos, Lima, Peru; Department of Microbiology, School of Sciences, Universidad Peruana Cayetano Heredia, Lima, Peru

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Cesar GavidiaSchool of Veterinary Medicine, Universidad Nacional Mayor de San Marcos, Lima, Peru; Department of Microbiology, School of Sciences, Universidad Peruana Cayetano Heredia, Lima, Peru

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Maria T. Lopez-UrbinaSchool of Veterinary Medicine, Universidad Nacional Mayor de San Marcos, Lima, Peru; Department of Microbiology, School of Sciences, Universidad Peruana Cayetano Heredia, Lima, Peru

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Hector H. GarciaSchool of Veterinary Medicine, Universidad Nacional Mayor de San Marcos, Lima, Peru; Department of Microbiology, School of Sciences, Universidad Peruana Cayetano Heredia, Lima, Peru

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Armando E. GonzalezSchool of Veterinary Medicine, Universidad Nacional Mayor de San Marcos, Lima, Peru; Department of Microbiology, School of Sciences, Universidad Peruana Cayetano Heredia, Lima, Peru

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for The Cysticercosis Working Group in PeruSchool of Veterinary Medicine, Universidad Nacional Mayor de San Marcos, Lima, Peru; Department of Microbiology, School of Sciences, Universidad Peruana Cayetano Heredia, Lima, Peru

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The efficacy of a single oral dose of 30 mg/kg of oxfendazole against Fasciola hepatica was evaluated in a controlled study in naturally infected sheep. Sheep were diagnosed by stool microscopy after sedimentation, and positive animals were randomized to oxfendazole (N = 20) or no treatment (N = 20). A new stool exam was performed 10 days after treatment. All stool microscopies were performed masked to the treatment group. No side effects were noticed. All sheep in the control group remained infected with similar counts of eggs per gram of stools. None of the animals in the treatment group showed Fasciola eggs in stools after 10 days of treatment. A single dose of oxfendazole is highly effective against F. hepatica, providing a new drug alternative for the control of fascioliasis or integrated zoonosis control.

Introduction

Fascioliasis is an infection caused by the trematode Fasciola hepatica, commonly found in the liver and biliary system of farmed ruminants.1 This infection has a cosmopolitan distribution and it is the main parasitic disease of livestock in terms of economic losses. Fascioliasis causes chronic human liver disease and is an emerging public health problem.2,3 Fascioliasis is endemic in the Peruvian highlands, with infection rates up to 100% in sheep and cattle, and prevalence in humans ranging from 9% to 16%.4,5 Control of fascioliasis is crucial for animal and human health, and rests solely on chemotherapy.6,7 Triclabendazole (TCBZ) is the current drug of choice; however, TCBZ resistance has already been reported in livestock farms across Europe, Australia, and some countries of South America.812 Our group has extensive experience using a single oral dose of 30 mg/kg of oxfendazole to treat porcine cysticercosis (Taenia solium). To the best of our knowledge, this scheme has not been tested for trematode infections in field conditions. We evaluated the efficacy of 30 mg/kg of oxfendazole against F. hepatica in naturally infected sheep.

Materials and Methods

Study area and animals.

The study was conducted in two sheep farms (A and B) located in Occobamba community, an endemic area to F. hepatica. Both farms were similar in terms of environmental settings and animal handling conditions. Occobamba is an agricultural and pecuary community located in the Andes at 4,000 m above the sea level in Cusco, Peru. Animal husbandry is based on raising sheep, cattle, and South American camelids.

Study design and treatment.

The sheep farms had a total of 50 and 60 sheep up to 1 year of age. All animals from the farms had a stool sample collected for coproparasitological and screened for Fasciola one day before the beginning of the study (Day 0). Stool samples were collected directly from the rectum of each sheep, placed into labeled new polyethylene bags, transported to the local laboratory, and processed for microscopy examination after sedimentation13 to detect Fasciola-positive animals and determine their baseline fecal egg output. Only animals with fecal Fasciola egg counts equal or higher than two eggs per gram (epg) were included in the study. All included sheep also showed parasite eggs compatible with nematode and cestode infections in their baseline stool samples. The sample size was calculated using the Snedecor and Cochran14 formula to estimate a difference between proportions, considering a minimal difference between groups of at least 30% to justify treatment of infected animals.

After screening, 20 sheep from each farm were randomly selected; 20 sheep (14 females and 6 males) from farm A were considered as the control group, and 20 sheep (15 females and 5 males) from farm B were considered as the treatment group. The control group did not receive treatment, whereas the treatment group was treated orally with a single dose of 30 mg/kg of body weight of oxfendazole (Synanthic, Fort Dodge, Mexico), adapted from the studies from Gavidia and others15 and Gonzalez and others.16 A drench dosing gun was used for oxfendazole administration, with the animal in standing position. After treatment the animals were released and allowed to continue grazing in the area. The median was used to express the parasite burden (number of eggs per gram of feces) on each group. The data were analyzed using a non-parametric approach with two-sample Mann-Whitney test.

Sampling and sample processing.

Fecal samples were taken from each animal 1 day before treatment and 10 days after treatment. The samples were analyzed individually with a sedimentation method. An original sieve technique was used for the quantitative assessment of the presence of eggs of F. hepatica in the feces. For this technique, 3 g of fecal samples were homogenized with 15 mL of tap water, slowly passed through a sieve, and then slowly washed under running water. Material filtered on the sieve was transferred to an edged Petri dish and examined under microscope at 100×. The sensitivity of this method is very high allowing counting one egg per gram.13

Ethical Approval.

This study was approved by the ethical committee of animal welfare of the Veterinary School from San Marcos University.

Results

At Day 0 the sheep had a median of 4 (range 2–28) epg, with similar egg counts between groups (Table 1). Ten days after treatment, we observed a statistical difference between control and treatment; the stool samples from all animals in the control group were positive for Fasciola eggs (median = 2), whereas none of the samples from treated animals had eggs (P < 0.01) (Table 1). Likewise, at baseline all sheep were positive for nematode eggs (median 450, range 100–2,800 epg), and three sheep from the control group and seven sheep from the treatment group were also positive for cestode eggs. On post-treatment follow-up the control group had a median of 400 (range 0–1,700) nematode epg and 5 sheep from the control group were positive for cestode eggs. In the treatment group all animals were negative for helminth parasites.

Table 1

Median and range of eggs before and after treatment with oxfendazole in sheep

ControlTreatment
N = 20N = 20
Male65
Age (in year)3.5 (1–5)3.8 (2–5)
Weight (kg)35.6 (28–40)36.6 (29–41)
Median baseline egg count5 (2–28)*4 (2–22)*
Post treatment egg count2 (1–37)0

Mann-Whitney test demonstrated no difference between control and treatment at baseline.

Significant difference between control and treatment (Mann-Whitney test, P < 0.01).

Discussion

This study provides proof of concept of feasibility and efficacy of treating F. hepatica and other gastrointestinal helminthes in sheep, with a single oral dose of 30 mg/kg of oxfendazole, under field conditions.

Benzimidazoles are a group of broad-spectrum anthelmintic drugs with good efficacy against nematode, cestode, and trematode, commonly used in human and veterinary medicine.17 For fascioliasis the most used benzimidazoles are albendazole and TCBZ. Albendazole is recommended for the control of F. hepatica in domestic animals18; however, its anthelmintic effect is only for chronic fascioliasis (adult stages) and is not effective to acute and sub-acute fascioliasis (immature stages).19,20 Currently, fascioliasis is mainly treated using the TCBZ because of its ability to act in both stages, immature and mature F. hepatica.20 This drug has been used since the 80s and it has shown good activity against liver fluke for many years.2123 However, in recent years F. hepatica has been reported to present resistance to TCBZ in various countries.812,24 This study demonstrated that oxfendazole at 30 mg/kg acts efficaciously against F. hepatica in naturally infected sheep. Although the study was not designed to evaluate the safety or pharmacokinetics of this dosage of oxfendazole in sheep, the animals did not show any signs of toxicity.

Oxfendazole has been previously evaluated against other important zoonotic tissue helminths. Gonzalez and others16 showed that oxfendazole is effective against T. solium cysticercosis in naturally infected pigs. Likewise, Gavidia and others15 showed that oxfendazole in combination with praziquantel is effective against hydatid disease (Echinococcus granulosus) in naturally infected sheep. Oxfendazole has also been previously used for the treatment of fascioliasis. Faser and others25 realized a survey about antiparasitic drug used in a sheep farm from England, and found that a farm used oxfendazole in the treatment of fascioliasis, but no mention of the dose or efficacy of oxfendazole are provided. Likewise, Furmaga and others26 evaluated oxfendazole against sheep parasitosis at doses of 5 and 15 mg/kg of body weight, reporting an efficacy for fascioliasis of 14% to 20%.

Oxfendazole is stored in the rumen of ruminants and it is detectable for up to 7 days after administration.27,28 Therefore, it is not necessary to dose the animals twice a week.29 We selected 30 mg/kg based on the literature and our experience in sheep, and also in pigs that are monogastric. Whether higher or lower doses could be used with similar efficacy and no toxicity remains to be studied.

Our study could have potentially overestimated cure rates if the coproparasitological examination was insensitive, although there is no reason to assume lack of sensitivity in the diagnosis. Follow-up egg counts in the controls were always positive and the egg counts were in similar ranges (Mann-Whitney test, P = 0.11). On the other hand, we cannot exclude the possibility of a temporary effect, if Fasciola infections were only partially damaged and surviving larvae begin to produce eggs again after 2 or 3 weeks. For logistical reasons, we could not prolong our stay in the region for more time.

The data presented here shows that a single dose of oxfendazole is safe and effective against F. hepatica in sheep. Oxfendazole is not expensive, effective in a single dose, and available worldwide. It should be considered as a new alternative drug for the control of fascioliasis, and eventually for integrated zoonosis control.

  • 1.

    Mas-Coma S, Valero MA, Bargues MD, 2009. Chapter 2. Fasciola, lymnaeids and human fascioliasis, with a global overview on disease transmission, epidemiology, evolutionary genetics, molecular epidemiology and control. Adv Parasitol 69: 41146.

    • Search Google Scholar
    • Export Citation
  • 2.

    Lean I, Westwood C, Playford M, 2008. Livestock disease threats associated with intensification of pastoral dairy farming. N Z Vet J 56: 261269.

    • Search Google Scholar
    • Export Citation
  • 3.

    Parkinson M, O’Neill SM, Dalton JP, 2007. Endemic human fasciolosis in the Bolivian Altiplano. Epidemiol Infect 135: 669674.

  • 4.

    Marcos LA, Terashima A, Leguia G, Canales M, Espinoza JR, Gotuzzo E, 2007. Fasciola hepatica infection in Peru: an emergent disease. Rev Gastroenterol Peru 27: 389396.

    • Search Google Scholar
    • Export Citation
  • 5.

    Espinoza JR, Terashima A, Herrera-Velit P, Marcos LA, 2010. Human and animal fascioliasis in Peru: impact in the economy of endemic zones. Rev Peru Med Exp Salud Publica 27: 604612.

    • Search Google Scholar
    • Export Citation
  • 6.

    Keiser J, Duthaler U, Utzinger J, 2010. Update on the diagnosis and treatment of food-borne trematode infections. Curr Opin Infect Dis 23: 513520.

    • Search Google Scholar
    • Export Citation
  • 7.

    Fairweather I, 2009. Triclabendazole progress report, 2005–2009: an advancement of learning? J Helminthol 83: 139150.

  • 8.

    Brennan GP, Fairweather I, Trudgett A, Hoey E, McCoy, McConville M, Meaney M, Robinson M, McFerran N, Ryan L, Lanusse C, Mottier L, Alvarez L, Solana H, Virkel G, Brophy PM, 2007. Understanding triclabendazole resistance. Exp Mol Pathol 82: 104109.

    • Search Google Scholar
    • Export Citation
  • 9.

    Alvarez-Sanchez MA, Mainar-Jaime RC, Perez-Garcia J, Rojo-Vazquez FA, 2006. Resistance of Fasciola hepatica to triclabendazole and albendazole in sheep in Spain. Vet Rec 159: 424425.

    • Search Google Scholar
    • Export Citation
  • 10.

    Overend DJ, Bowen FL, 1995. Resistance of Fasciola hepatica to triclabendazole. Aust Vet J 72: 275276.

  • 11.

    Olaechea F, Lovera V, Larroza M, Raffo F, Cabrera R, 2011. Resistance of Fasciola hepatica against triclabendazole in cattle in Patagonia (Argentina). Vet Parasitol 178: 364366.

    • Search Google Scholar
    • Export Citation
  • 12.

    Oliveira DR, Ferreira DM, Stival CC, Romero F, Cavagnolli F, Kloss A, Araujo FB, Molento MB, 2008. Triclabendazole resistance involving Fasciola hepatica in sheep and goats during an outbreak in Almirante Tamandare, Parana, Brazil. Rev Bras Parasitol Vet 17 17 (Suppl 1): 149153.

    • Search Google Scholar
    • Export Citation
  • 13.

    Rojas M, 1990. Parasitismo de los Rumiantes Domésticos. Lima, Peru: Maijosa.

  • 14.

    Snedecor GW, Cochran WG, 1989. Statistical Methods. Ames, IA: Iowa State University Press.

  • 15.

    Gavidia CM, Gonzalez AE, Barron EA, Ninaquispe B, Llamosas M, Verastegui MR, Robinson C, Gilman RH, 2010. Evaluation of oxfendazole, praziquantel and albendazole against cystic echinococcosis: a randomized clinical trial in naturally infected sheep. PLoS Negl Trop Dis 4: e616.

    • Search Google Scholar
    • Export Citation
  • 16.

    Gonzalez AE, Gavidia C, Falcon N, Bernal T, Verastegui M, Garcia HH, Gilman RH, Tsang VC, 2001. Protection of pigs with cysticercosis from further infections after treatment with oxfendazole. Am J Trop Med Hyg 65: 1518.

    • Search Google Scholar
    • Export Citation
  • 17.

    Alvarez L, Moreno G, Moreno L, Ceballos L, Shaw L, Fairweather I, Lanusse C, 2009. Comparative assessment of albendazole and triclabendazole ovicidal activity on Fasciola hepatica eggs. Vet Parasitol 164: 211216.

    • Search Google Scholar
    • Export Citation
  • 18.

    McKellar QA, Scott EW, 1990. The benzimidazole anthelmintic agents–a review. J Vet Pharmacol Ther 13: 223247.

  • 19.

    Bogan J, Armour J, 1987. Anthelmintics for ruminants. Int J Parasitol 17: 483491.

  • 20.

    Boray JC, Crowfoot PD, Strong MB, Allison JR, Schellenbaum M, Von Orelli M, Sarasin G, 1983. Treatment of immature and mature Fasciola hepatica infections in sheep with triclabendazole. Vet Rec 113: 315317.

    • Search Google Scholar
    • Export Citation
  • 21.

    Fairweather I, 2005. Triclabendazole: new skills to unravel an old(ish) enigma. J Helminthol 79: 227234.

  • 22.

    Keiser J, Engels D, Buscher G, Utzinger J, 2005. Triclabendazole for the treatment of fascioliasis and paragonimiasis. Expert Opin Investig Drugs 14: 15131526.

    • Search Google Scholar
    • Export Citation
  • 23.

    Keiser J, Utzinger J, 2004. Chemotherapy for major food-borne trematodes: a review. Expert Opin Pharmacother 5: 17111726.

  • 24.

    Fairweather I, 2011. Raising the bar on reporting ‘triclabendazole resistance’. Vet Rec 168: 514515.

  • 25.

    Fraser DE, Hunt PJ, Skinner RJ, Coles GC, 2006. Survey of parasite control on sheep farms in south-west England. Vet Rec 158: 5557.

  • 26.

    Furmaga S, Gundalach JL, Sadzikowski A, Paciejewski S, 1982. (Systamex (oxfendazole) in the treatment of parasitoses of sheep). Med Weter 38: 269271.

    • Search Google Scholar
    • Export Citation
  • 27.

    Lanusse CE, Gascon LH, Prichard RK, 1995. Comparative plasma disposition kinetics of albendazole, fenbendazole, oxfendazole and their metabolites in adult sheep. J Vet Pharmacol Ther 18: 196203.

    • Search Google Scholar
    • Export Citation
  • 28.

    Soraci AL, Mestorino N, Errecalde JO, 1997. Some pharmacokinetic parameters of oxfendazole in sheep. Vet Res Commun 21: 283287.

  • 29.

    Blanton RE, Wachira TM, Zeyhle EE, Njoroge EM, Magambo JK, Schantz PM, 1998. Oxfendazole treatment for cystic hydatid disease in naturally infected animals. Antimicrob Agents Chemother 42: 601605.

    • Search Google Scholar
    • Export Citation

Author Notes

*Address correspondence to Luis A. Gomez-Puerta, School of Veterinary Medicine, Universidad Nacional Mayor de San Marcos, Av. Circunvalación 2800, Lima 41, Peru. E-mail: lucho92@yahoo.com

Financial support: This work was supported by Fogarty/NIH (grants D43TW008273 and D43TW001140). HG is supported by a Wellcome Trust International Senior Research Fellowship.

Authors’ addresses: Luis A. Gomez-Puerta, Cesar Gavidia, Maria T. Lopez-Urbina, and Armando E. Gonzalez, School of Veterinary Medicine, Universidad Nacional Mayor de San Marcos, Lima, Peru, E-mails: lucho92@yahoo.com, cgavidia@jhsph.edu,mtlu@terra.com.pe, and agonzale@jhsph.edu. Hector H. Garcia, Department of Microbiology, School of Sciences, Universidad Peruana Cayetano Heredia, Lima, Peru, E-mail: hgarcia@jhsph.edu.

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