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ARS Home » Northeast Area » Beltsville, Maryland (BARC) » Beltsville Agricultural Research Center » Animal Parasitic Diseases Laboratory » Research » Research Project #421090

Research Project: INTEGRATED APPROACH TO THE DETECTION AND CONTROL OF FOODBORNE PARASITES AND THE IMPACT ON FOOD SAFETY

Location: Animal Parasitic Diseases Laboratory

2016 Annual Report


1a. Objectives (from AD-416):
Objective 1: Evaluate the impact of changing management and production practices (e.g. free range, confined, organic) on the incidence of Toxoplasmosis and Trichinella in swine, as it relates to foodborne risk. Objective 2: Assess the effectiveness of on-farm interventions (such as passive immunization therapy as a feed supplement) to prevent enteric Toxoplasma infection in swine, consequent foodborne risk, and potential interaction with Salmonella foodborne infections in swine. C.1., PS 1B, and PS 1.D, Section 4.1. Objective 3: Evaluate the impact of anthelminthic and antiprotozoal treatments on parasitic foodborne infections in swine and the potential foodborne risk. Evaluate the impact of anthelminthic and antiprotozoal treatments on the interaction between foodborne pathogen and foodborne parasitic infections, specficially coinfections of Toxoplasma, Trichinella with Salmonaella and Campylobacter in swine, and changes following treatments. C.1., P.S., 1.A, and P.S., 1.D.


1b. Approach (from AD-416):
Toxoplasma gondii infects 11-20% of the U.S. population, causing birth defects in exposed pregnant women, devastating disease in immunocompromised individuals, and illness and loss of vision in otherwise healthy adults. Consumption of infected pork may be a significant source of infection for consumers in the U.S. Meat derived from pasture-raised pigs is of particular concern, since prevalence in these pigs may exceed 50%. Reducing the risk of foodborne human infection from meat requires adherence to livestock production practices that prevent exposure of animals to the parasite at the farm level, and the development of new treatments which can be used in pasture-raised pigs to prevent infection. Trichinella spiralis is a serious zoonotic pathogen with an unusually broad host and geographic range. Trichinella species infecting game animals pose a risk to humans consuming these meat products as well as a risk to domestic pigs that feed on their carcasses. Understanding the risk to pigs that have access to infected wildlife is an important component of on-farm certification efforts. In addition, the safety of meat from pasture-raised swine needs to be assessed in light of increasing consumer demand for organically-raised meat products. We will evaluate the impact of different management and production practices (e.g., free range, confinement, organically-raised pigs) on the incidence of Toxoplasma and Trichinella in swine, as it relates to foodborne risk, and assess the effectiveness of on-farm interventions (such as passive immunization therapy as a feed supplement) to prevent enteric Toxoplasma infection in swine, consequent foodborne risk, and potential interaction with Salmonella foodborne infections in swine.


3. Progress Report:
This is the final report for the project 8042-32000-090-00D terminated in September 2016. Substantial and impactful results were obtained over the 5 years of the project. Essentially all milestones were “Met” or “Substantially Met.” During this period, we conducted standardization trials for proficiency sample preparation for Trichinella infected pork in support of the Agricultural Marketing Service (AMS) Analyst Training and Check Sample Program. Due to the labor intensive nature of producing standardized proficiency samples, many international reference laboratories do not have a quality assurance program in place. This lack of quality assurance calls into question the reliability of analyst competence for performing required testing to assure negligible risk from Trichinella in pork. We determined optimal worm burdens, mixing times, and test sensitivity at 3 infection levels. Results showed that using an optimal larval density of 5 larvae per gram (lpg) with a 2 hour mixing time, the test sensitivity is 100% when performed according to recommendations from the International Commission on Trichinellosis. The simplified and economical method for production of standardized proficiency samples allows for the establishment of robust quality assurance programs in reference laboratories worldwide. Proficiency sample preparation for the AMS Program was modified to reflect these findings. These efforts support certification and export marketing efforts as requested by USDA regulatory agencies through determination of risk to domestic pigs from Trichinella. A cross-sectional serological survey was conducted in collaboration with APHIS to estimate the seroprevalence of Trichinella spp. and Toxoplasma gondii, and risk factors associated with infection in feral pigs in the U.S. Serum samples were tested from 3247 feral pigs from 32 states. The overall seroprevalence of antibodies to Trichinella spp. and T. gondii, indicating infection, was 3.0% and 17.7%, respectively. A small proportion of feral pigs (0.7 %) was seropositive for both parasites. Toxoplasma seropositive feral pigs were widespread across the South and Midwest, and more restricted in the arid West. Trichinella infection was significantly higher in the South than in the Midwest, and higher in the Midwest than in the West (p<0.05). Species distribution modeling indicated that the most probable distribution areas for both parasites are similar, and concentrated mostly in the Southern and the Midwestern U.S. For acceptance of pork produced in negligible risk compartments in the U.S., recent legislation in the European Union endorses surveillance of wildlife indicator populations; this project provides data to establish feral pigs as an indicator population for Trichinella in support of export marketing efforts to answer this requirement from our trading partners. During this period, we expanded a U.S. State Department funded Biosecurity Engagement Program on T. spiralis in the Republic of the Philippines. In collaboration with the Bureau of Animal Industry, Philippine Animal Health Center (PAHC), Republic of the Philippines, a validated Trichinella testing facility at PAHC, Quezon City, Luzon was established and a nationwide prevalence study for T. spiralis in market hogs was conducted. Also, the sample storage capacity of PAHC for establishment of a swine serum bank was expanded for prevalence studies on other swine pathogens of interest. This project improved the disease surveillance capacity for a trading partner which in turn reduces risks to U.S. consumers from foodborne pathogens, and to U.S. agriculture from importation of foreign animal diseases. We developed and conducted an international ring trial with National Reference Laboratories from Canada, France, Italy, and Germany for production parameters of T. spiralis excretory/secretory (E/S) proteins used for serological detection of infection in pigs. Codex and World Organization for Animal Health (OIE) regulations on establishing risk for Trichinella infection in pigs is expected to develop guidelines for surveillance testing for documenting low or negligible risk of acquiring trichinellosis from pork. Surveillance testing using serological methods, though sensitive, economical, and amenable to high throughput procedures, is currently not in use because reagents have not been internationally normalized to reduce false positive results. This research 1)identified variations in methodologies that lead to high false positives, 2) developed methods for eliminating cross reacting components, and 3) demonstrated the suitability of serology as a tool for surveillance testing and assessing risk. Results were presented at an Organization for Economic Cooperation and Development (OECD) sponsored workshop, “Best Practices in Documenting Negligible Risk for Trichinella in Pork” in Berlin, Germany. Our lab provided examples of serological surveillance protocols that can achieve various levels of statistical confidence to identify compartments with negligible risk for infection. These data were used to inform a new OIE Code Chapter on Trichinella, to establish a framework for classifying the public health risk of pork and pork products from defined compartments using serological surveillance, and serves as a reference for regulatory authorities when developing legislation or interpreting food safety requirements. These efforts improve standardization of international protocols for surveillance, and provide a basis for increased U.S. market share. We determined the minimal effective dose of mebendazole on encysted T.spiralis muscle larvae (ML)in pigs and showed that mebendazole treatment with 5, 50, or 100 mg/kg every other day for 3 days was not effective in reducing numbers of recovered ML or inactivating ML, while 50 mg/kg for 5 days or 83 mg/kg for 3 days were both effective. Mebendazole treatment of pigs with 250mg/kg over 3 days or 5 days reduced numbers of recovered ML and rendered ML non-infective to mice, whereas treatment with 250mg/kg in a single dose was not effective. Mature nurse cells and older larvae may have reduced exposure to anthelmintics, while circulating larvae and younger nurse cells may be impacted differently by anthelmintic exposure, therefore studies of the effect of mebendazole on shorter and longer term infections (< and > 45 days) were conducted. Analysis revealed that mebendazole (50mg/kg, daily, 5 days) rendered all ML non-viable regardless of age of the nurse cell (45, 60, or 100 days post infection). These data permit evaluation of the efficacy of anthelmintic treatment on the viability of Trichinella ML in pig tissues and provide a framework for eliminating Trichinella risk in pigs raised in uncontrolled management systems. The National Animal Health Monitoring System (NAHMS) 2012 swine serological survey for Trichinella and Toxoplasma was completed. Samples (5688) were collected in collaboration with APHIS-Center for Epidemiology and Animal Health. Seroprevalence for Toxoplasma was 3.79%; a single Trichinella positive sample was found from a pig with outdoor access on a poorly managed farm. This is the first Trichinella positive pig found during the NAHMS survey since 1995. This survey determined the seroprevalence of Trichinella and Toxoplasma in the national swine herd, and provided data on farm management practices that impact pathogen prevalence. These data serve to demonstrate the extremely low prevalence of Trichinella in the national swine herd and assure trading partners of the safety of U.S. pork. An oocyst-specific antigen (TgERP) was identified from T. gondii and a serological assay was developed which allows attributing parasite transmission to the oocyst (found in cat feces) rather than the tissue cyst (found in meat). A study was completed examining transmission in mothers and children from an endemic region in Brazil using serum, and to expand the sampling which could be used for testing, including saliva, breast milk, and fecal extracts using a bead-based assay. In addition, we analyzed Toxoplasma prevalence considering groundwater vulnerability information assessed at a regional scale. Results suggest that water is an important vehicle for disseminating human toxoplasmosis via oocysts in endemic settings and during outbreaks; nearly 80% of acutely infected mothers were positive for exposure to oocysts. Similar results were seen in human serum collected from the U.S. National Health and Nutrition Examination Survey (NHANES), Columbia, France, and Chile. These studies increased our understanding of Toxoplasma epidemiology, and provided clues as to what types of controls are needed to reduce transmission to humans via oocysts. Research showed that a primary infection with North American sylvatic genotypes of Trichinella (which do not infect pigs) could protect pigs against a challenge infection with T. spiralis (T1),(which is highly infectious for pigs). Protection was examined by first exposing animals to T. nativa (T2), T. pseudospiralis (T4), or T. murrelli (T5), then challenging with T1. Pigs exposed to encapsulated genotypes (T2 and T5) were protected against a challenge infection with T1. Exposure to the unencapsulated genotype (T4) provided little protection, and both T1 and T4 were recovered from pig tissues after challenge. Antibody isotypes and cytokine gene expression analyses in blood and intestinal tissues were conducted in protected vs unprotected animals. A Th-2 immune response was elevated in early infection in protected pigs, but not in unprotected animals. These data demonstrate that pigs can be rendered resistant to T. spiralis infection by immunization, and provides a basis for protecting pigs raised in uncontrolled environments against T. spiralis, while reducing risk to consumers.


4. Accomplishments
1. A framework to qualitatively estimate the exposure risk to Toxoplasma gondii from various meat products consumed in the U.S. Consuming raw or undercooked meat products exposes people to contracting toxoplasmosis. Scientists at the Beltsville Agricultural Research Center, Beltsville, Maryland, and the University of Maryland developed a framework to qualitatively estimate the exposure risk to Toxoplasma from various meat products consumed in the U.S. Risk estimates of various meats were analyzed by a farm-to-retail qualitative assessment which included evaluation of farm, abattoir, storage and transportation, meat processing, packaging and retail modules. Exposure risks associated with meats from free-range chickens, non-confinement raised pigs, goats and lambs were found to be higher than those from confinement-raised pigs, cattle, and caged-chickens. For fresh meat products, risk at the retail level was similar to that at the farm level unless meats had been frozen or moisture-enhanced. Meat processing such as salting, freezing, commercial hot air drying, long term fermentation, hot smoking, and cooking reduce T. gondii levels, whereas nitrite/nitrate, spice, low pH, and cold storage have no effect on the viability of T. gondii tissue cysts. Raw-fermented sausage, cured raw meat, non-hot air dried meat and fresh processed meat conferred higher exposure risks as compared with cooked meat. This study provides a reference for meat management programs to determine critical control points, and is the foundation for future quantitative risk assessments.

2. Estimation of T. gondii prevalence in meat animals using meta-analysis. The Centers for Disease Control and Prevention (CDC) reported that T. gondii is one of three pathogens (along with Salmonella and Listeria), which collectively account for >70% of all deaths due to foodborne illness in the U.S. and meat animals act as sources for parasite transmission to humans. Based on limited population-based data, the Food and Agriculture Organization (FAO) /World Health Organization (WHO) estimated that approximately 22% of human T. gondii infections are meat borne. Scientists at the Beltsville Agricultural Research Center, Beltsville, Maryland, and the University of Maryland, College Park, Maryland conducted a systematic meta-analysis to provide an estimation of T. gondii prevalence in meat animals, using studies published between 1960 and 2015. Animals raised outdoors or that have outdoor access were found more often infected compared to animals raised indoors. T. gondii prevalence in non-confinement raised pigs ranked the highest (31.0%) followed by goats (30.7%), non-confinement raised chickens (24.1%), lambs (22.0%), confinement raised sows (17.0%), and confinement raised market pigs (5.6%). These results demonstrate that T. gondii-infected animals are a food safety concern. Further, computed prevalence can be used as an important input in quantitative microbial risk assessment models to predict public health burden.

3. The use of free-range chickens as indicators of Toxoplasma. Free-range chickens are good indicators of soil contamination with oocysts because they feed from the ground and they are also an important source of infection for cats that in turn shed oocysts after eating tissues of intermediate hosts, butlittle is known of the epidemiology of toxoplasmosis in chickens. Scientists at the Beltsville Agricultural Research Center, Beltsville, Maryland, placed sentinel chickens on farms and bioassayed those that developed antibody responses. The density of T. gondii in poultry muscle was found to be low, but heart muscle was found best for isolating viable parasites from chickens. These data demonstrate that free range chickens are highly susceptible to Toxoplasma infection, and are a suitable surveillance tool for environmental sampling of Toxoplasma on animal pasturage where free range management is practiced.

4. Prevalence of T. gondii antibodies in seagull chicks. Wild birds are involved in the maintenance and spread of Toxoplasma. Understanding the spread of T. gondii in wild birds, particularly in those with opportunistic feeding behavior, is of interest for elucidating their epidemiological involvement in the maintenance and dissemination of the parasite. Scientists from the Beltsville Agricultural Research Center, Beltsville, Maryland, and from Spain collected sera from several sources of gulls. The results suggested that freshwater and sewage are important routes of parasite dispersion. This study is the first to report T. gondii antibodies in Yellow-legged and Audouin´s gulls. It extends the range of intermediate hosts for this parasite and underscores the complexity of its epidemiology.


5. Significant Activities that Support Special Target Populations:
Service on the National Committee on Neglected Infections of Poverty in the United States, Centers for Disease Control. Member, Working Group on Data collection, surveillance, epidemiology, and mapping, and Working Group, Outreach: Mobilizing Communities/Messaging.


Review Publications
Dubey, J.P., Kwok, O.C., Gardner, I. 2015. Bayesian estimation of sensitivity and specificity of the modified agglutination test and bioassay for detection of Toxoplasma gondii in free-range chickens. Parasitology. 143:314-319.
Caler-Bernal, R., Van Wilpe, E., White, K., Verma, S., Cerqueira-Cezar, C., Dubey, J.P. 2015. Sarcocystis oreamni n. sp. from the mountain goat (oreamnos americanus). Parasitology Research. 114:4135-4141.
Guo, M., Buchanan, R., Dubey, J.P., Hill, D.E., Lambertini, E., Ying, Y., Gamble, R., Jones, J., Pradhan, A. 2015. Qualitative assessment for Toxoplasma gondii exposure risk associated with consumption of meat products in the United States. Journal of Food Protection. 78(12):2207-2219.
Dubey, J.P. 2015. Foodborne and waterborne zoonotic sarcocystosis. Foodborne Pathogens and Disease. 1:2-11.
Guo, M., Mishra, A., Buchanan, R., Dubey, J.P., Hill, D.E., Gamble, R., Jones, J., Pradhan, A. 2016. A systematic meta-analysis of Toxoplasma gondii prevalence in meat animals in the United States. Journal of Food Protection. 13(3):109-118.
Dubey, J.P., Lehmann, T., Lautner, F., Kwok, O.C., Gamble, R. 2015. Toxoplasmosis in sentinel chickens (Gallus domesticus) in New England farms: seroconversion, distribution of tissue cysts in brain, heart, and skeletal muscle by bioassay in mice and cats. Veterinary Parasitology. 214:55-58.
Verma, S., Carstensen, M., Calero-Bernal, R., Moore, S., Jiang, T., Su, C., Dubey, J.P. 2015. Seroprevalence, isolation, first genetic characterization of Toxoplasma gondii, and possible congenital transmission in wild moose from Minnesota, USA. Parasitology Research. 115:687-690.
Cabezon, O., Cerda, C., Morera, V., Bocanegra, I., Gonzalez-Solis, J., Ribas, M.P., Blanch-Lazaro, B., Fernandez-Aguilar, X., Antilles, N., Lopez-Soria, S., Lorca-Oro, C., Dubey, J.P., Almeria, S. 2016. Study of the relationship between Toxoplasma gondii infection and food source in seagull chicks from breeding areas from Spain. PLoS One. 11(30):1-11.
Shwab, E.K., Jiang, T., Pena, H.F., Gennari, S.M., Dubey, J.P., Su, C. 2015. The ROP18 and ROP5 allele types are highly predictive of mouse-virulence across globally distributed strains of Toxoplasma gondii. International Journal for Parasitology. 46:141-146.
Dubey, J.P., Houk, A., Verma, S., Humphreys, J., Lindsay, D. 2015. Experimental transmission of Cystoisospora felis- like coccidium from bobcat (Lynx rufus) to the domestic cat (Felis catus). Veterinary Parasitology. 221(2015):35-39.
Ballash, G., Dubey, J.P., Kwok, O.C., Shoben, A., Terry, R., Kraft, T., Dennis, P. 2014. Seroprevalence of toxoplasma gondii in white-tailed deer and free-roaming cats across a suburban to urban gradient in northeastern Ohio. EcoHealth. doi: 10.1007/s10393-014-0975-2.
Blazejewski, B., Nursimulu, N., Pszenny, V., Dangoudoubiyam, S., Namasivayam, S., Chiasson, M., Chessman, K., Tonkin, M., Seshadri, S., Hung, S., Bridgers, J., Ricklefs, S., Boulanger, M., Dubey, J.P. 2015. Systems based analysis of the Sarcocystis neurona genome identifies pathways that contribute to a heteroxenous life cycle. mBio. 6(1):e02445-14.
Dryburgh, E., Marsh, A., Dubey, J.P., Howe, D., Reed, S., Bolten, K., Pei, W., Saville, W. 2015. Sarcocyst development in raccoons (Procyon lotor) inoculated with different strains of Sarcosytis neurona culture-derived merozoites. Journal of Parasitology. 101(4):462-467.
Yang, Y., Ying, Y., Verma, S., Cassinelli, A., Kwok, O.C., Liang, H., Pradhan, A., Su, C., Zhu, X., Dubey, J.P. 2015. Isolation and genetic characterization of viable Toxoplasma gondii from tissues and feces of cats from the central region of China. Veterinary Parasitology. 211(3-4):283-288.
Sanders, J., Moulton, H., Mcleod, R., Dubey, J.P., Weiss, L., Zhou, Y., Kent, M. 2015. The zebrafish, Danio rerio, as a model for Toxoplasma gondii: an initial description of infection in fish. Biology Letters. 38:675-679.
Mason, S., Dubey, J.P., Smith, J., Boag, B. 2015. Toxoplasma gondii coinfection with diseases and parasites in wild rabbits in Scotland. Parasitology. doi: 10.1017/S003118201500075X.
Jenkins, M.C., Fetterer, R.H., Miska, K.B., Tuo, W., Kwok, O.C., Dubey, J.P. 2015. Characterization of the Eimeria maxima sporozoite surface protein IMP1. Veterinary Parasitology. doi: 10.1016/jvetpar2015.05.009.
Gennarri, S., Ogrzewalska, M., Soares, H., Saraiva, D., Saraiva, A., Pinter, A., Labruna, M., Dubey, J.P. 2014. Occurrence of Toxoplasma gondii antibodies in wild rodents and marsupials from the Atlantic forest, State of Sao Paulo, Brazil. Journal of Zoo and Wildlife Medicine. 200:193-197.
Calero-Bernal, R., Verma, S., Cerqueira-Cezar, C., Schafer, L., Van Wilpe, E., Dubey, J.P. 2015. Sarcocystis mehlhorni n. sp. (Apicomplexa: Sarcocystidae) from the black-tailed deer (Odocoileus hemionus columbianus). Parasitology Research. 114:4397-4403.
Dubey, J.P., Hilali, M., Van Wilpe, E., Calero-Bernal, R., Verma, S., Abbas, I. 2015. A review of sarcocystosis in camels and redescription of Sarcocystis cameli and Sarcocystis ippeni sarcocysts from the one-humped camel (Camelus dromedarius). Parasitology. doi: 10.1017/S0031182015000852.
Verma, S., Calero-Bernal, R., Lovallo, M., Sweeny, A., Grigg, M., Dubey, J.P. 2015. Bobcat (Lynx rufus) as a new natural intermediate host for Sarcocystis neurona. Veterinary Parasitology. doi: 10.1016/j.vetpar.2015.06.007.
Dubey, J.P., Dunams, D.B., Caler-Bernal, R., Verma, S., Rosenthal, B.M. 2015. Molecular characterization and development of Sarcocystis speeri sarcocysts in gamma interferon gene knockout mice. Parasitology. 142:1555-1562.
Dubey, J.P., Van Wilpe, E., Hilali, M. 2015. Ultrastructure of Sarcocystis bertrami sarcocysts from naturally infected donkey (Equus asinus) from Egypt. Parasitology. 143(01):18-23.
Trupkiewicz, J.G., Calero-Bernal, R., Verma, S., Mowery, J.D., Davison, S., Habecker, P., Georoff, T.A., Ialeggio, D.M., Dubey, J.P. 2015. Acute, fatal Sarcocystis calchasi-associated hepatitis in Roller pigeons (Columbia livia f. dom.) at Philadelphia Zoo. Veterinary Parasitology. 216:52-58.
Hohweywe, J., Cazeaux, C., Travaile, E., Dumetre, A., Aubert, D., Languet, E., Terryn, C., Dubey, J.P., Azas, N., Houssin, M., Loic, F., Villena, I., La Carbona, S. 2016. Strategy for simultaneous molecular detection of the protozoan parasites Toxoplasma, Cryptosporidium and Giardia in food matrices and persistence on leaves of vegetables during storage at 4°C. Food Microbiology. 57:36-44.
Gondim, P., Wolf, P., Vrhovec, M., Pantechev, N., Bauer, C., Langenmeyer, M., Bohne, W., Teifke, J., Dubey, J.P., Conraths, F., Schares, G. 2016. Characterization of IgG monoclonal antibody targeted to both tissue cyst and sporocyst walls of Toxoplasma gondii. Experimental Parasitology. 163:46-56.
Frey, C.F., Regidor-Cerrillo, J., Marreros, N., Garcia-Lunar, P., Gutierrez-Exposito, D., Schares, G., Dubey, J.P., Gentile, A., Jacquiet, P., Shkap, V., Cortes, H., Ortega-Mora, L.M., Alvarez-Garcia, G. 2016. Besnoitia besnoti lytic cycle in vitro and differences in invasion and intracellular proliferation among isolates. Parasites & Vectors. 29:115.
Sa, S., Lima, D., Silva, L., Pinheiro, J., Dubey, J.P., Da Silva, J., Mota, R. 2016. Seroprevalence of Toxoplasma gondii among turkeys on family farms in the state of Northeastern Brazil. Acta Parasitologica. 61:401-5.
Parker, M.L., Penarete-Vargas, D.M., Hamilton, P.T., Guerin, A., Dubey, J.P., Perlman, S.J., Spano, F., Lebrun, M., Boulanger, M.J. 2016. Dissecting the interface between apicomplexan parasite and host cell: Insights from a divergent AMARON2 pair. Proceedings of the National Academy of Sciences. 113(2):398-403.
Vieira, F.P., Alves, M.G., Martins, L.M., Rangel, A.L., Dubey, J.P., Hill, D.E., Bahia-Oliveira, L.M. 2015. Waterborne toxoplasmosis investigated and analyzed under hydrogeological assessment: new data and perspectives for further research. Memorias Do Instituto Oswaldo Cruz. 113(2):398-403.
Dubey, J.P., Verma, S.K., Villena, I., Aubert, D., Geers, R., Su, C., Lee, E., Forde, M.S., Krecek, R. 2016. Toxoplasmosis in Caribbean islands: Seroprevalence in pregnant women in ten countries, and isolation and report of new genetic types of Toxoplasma gondii from dogs from St. Kitts, West Indies. Parasitology Research. 115:1627-34.
More, G., Regensburger, C., Gos, L.M., Pardini, L., Verma, S.K., Ctibor, J., Serrano-Martinez, E., Dubey, J.P., Venturini, C. 2016. Sarcocystis masoni, n. sp. (Apicomplexa: Sarcocystidae), and redescription of Sarcocystis aucheniae from llama (Lama glama), guanaco (Lama guanicoe) and alpaca (Vicugna pacos). Parasitology. 143(5):617-26.
Gennari, S., Nieymeyer, C., Catao-Dias, J., Soares, H., Acousta, I., Dias, R., Ribeiro, J., Lassalvia, C., Kolesnikovas, C., Mayorga, L., Dubey, J.P. 2016. Survey of Toxoplasma gondii antibodies in magellanic penguins (Spheniscus magellanicus Forster, 1781). Journal of Zoo and Wildlife Medicine. 47:364-6.
Guo, M., Mishra, A., Buchanan, R., Dubey, J.P., Hill, D.E., Gamble, R., Jones, J., Du, X., Pradhan, A. 2015. Development of the dose-response relationship for human toxoplasma gondii infection associated with meat consumption. Journal of Risk Assessment. 36(5):926-38.
Dubey, J.P., Mcconkey, G.A., Ferreira, L., Alsaad, M., Verma, S.K., Alves, D.A., Holland, G.N. 2016. Experimental toxoplasmosis in rats induced orally with eleven strains of Toxoplasma gondii of seven genotypes: Tissue tropism, tissue cyst size, neural lesions, tissue cyst rupture without reactivation, and ocular lesions. PLoS One. doi: 10.1371/journal.pone.0156255.
Dubey, J.P., Calero-Bernal, R., Verma, S.K., Mowery, J. 2016. Pathology, immunohistochemistry, and ultrastructural findings associated with neurological sarcocystosis in cattle. Veterinary Parasitology. 223:147–152.
Dubey, J.P., More, G., Van Wilpe, E., Calero-Bernal, R., Verma, S.K., Schares, G. 2015. Sarcocystis rommeli, n. sp. (Apicomplexa: Sarcocystidae) from cattle (Bos taurus) and its differentiation from Sarcocystis hominis. Journal of Eukaryotic Microbiology. 63:62-68.
Dubey, J.P., Van Wilpe, E., Caler-Bernal, R., Verma, S., Fayer, R. 2015. Sarcocystis heydorni, n. sp. (Apicomplexa: Protozoa) with cattle (Bos taurus) and human (Homo sapiens) cycle. Parasitology Research. doi: 10.1007/s00436-015-4645-2.
Guo, M., Dubey, J.P., Hill, D.E., Buchanan, R., Gamble, R., Jones, J., Pradhan, A. 2015. Prevalence and risk factors of Toxoplasma gondii infection in meat products destined for human consumption. Journal of Food Protection. 78(2):457-76.
Ochiai, E., Brogli, M., Kudo, T., Wang, X., Dubey, J.P., Suzuki, Y. 2015. CXCL9 Is Important for Recruiting Immune T Cells into the Brain and Inducing an accumulation of the T Cells to the areas of tachyzoite proliferation to prevent reactivation of chronic cerebral infection with Toxoplasma gondii. American Journal of Pathology. 185(2):314-24.
Staggs, S., Scot, K., Ware, M., Schable, N., See, M., Gregorio, D., Zou, X., Su, C., Dubey, J.P., Villegas, E. 2015. Using blue mussels (Mytilus spp.) as biosentinels of Cryptosporidium spp. and Toxoplasma gondii contamination in marine aquatic environments. Parasitology Research. 114(12):4655-67.
Lorenzi, H., Khan, A., Behnke, M.S., Liu, L., Namasivayam, S., Seshadri, S., Hadjithomas, M., Karamycheva, S., Pinney, D., Brunk, B., Ajioka, J., Azjenberg, D., Boothroyd, J.C., Boyle, J., Darde, M.L., Dubey, J.P., Grigg, M., Howe, D., Kim, K., Rosenthal, B.M., Saeij, J., Su, C.L., White, M., Zhu, X.Q., Parkinson, J., Kissinger, J.C., Roos, D.S., Sibley, L.D. 2016. Comparative genomic sequence variation of Toxoplasma gondii reveals local admixture drives concerted expansion and diversification of secreted pathogenesis determinants. Nature Genetics. 7:10147.
Canon-Franco, W.A., Lopez-Orozco, N., Christoff, A.U., De Castilho, C.S., Pacheco De Araujo, F., Verma, S.K., Dubey, J.P., Soares, R.S., Gennari, S.M. 2016. Detection of Sarcocystis felis-like protozoon in South American wild felids from Brazil. Veterinary Parasitology. 217:15-20.
Work, T.M., Verma, S., Su, C., Medeiros, J., Kaiakapu, T., Dubey, J.P. 2016. Serology and genetics of Toxoplasma gondii in endangered Hawaiian (Nene) geese (Branta sandvicensis). Journal of Wildlife Diseases. 52(2):253-7.
Verma, S.K., Calero-Bernal, R., Cerqueira-Cezar, C.K., Kwok, O.C., Dudley, M.R., Su, C., Hill, D.E., Dubey, J.P. 2016. Isolation and genetic characterization of Toxoplasma gondii from naturally infected Canada goose (Branta canadensis) detected two new atypical strains. Parasitology Research. 115(5):1767-72.
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