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Revista Brasileira de Parasitologia Veterinária

Print version ISSN 0103-846XOn-line version ISSN 1984-2961

Rev. Bras. Parasitol. Vet. vol.26 no.3 Jaboticabal July/Sept. 2017  Epub Aug 31, 2017

https://doi.org/10.1590/s1984-29612017045 

Review Article

All about neosporosis in Brazil

Tudo sobre neosporose no Brasil

Camila Koutsodontis Cerqueira-Cézar1 

Rafael Calero-Bernal1 

Jitender Prakash Dubey1 

Solange Maria Gennari2  * 

1Animal Parasitic Diseases Laboratory, Beltsville Agricultural Research Center, United States Department of Agriculture, Agricultural Research Service, Beltsville, MD, United States of America

2Departamento de Medicina Veterinária Preventiva e Saúde Animal, Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo – USP, São Paulo, SP, Brasil


Abstract

Neospora caninum is protozoan parasite with domestic and wild dogs, coyotes and grey wolves as the definitive hosts and many warm-blooded animals as intermediate hosts. It was cultivated and named in 1988. Neosporosis is a major disease of cattle and has no public health significance. Since 1990’s N. caninum has emerged as a major cause of abortion in cattle worldwide, including in Brazil. N. caninum also causes clinical infections in several other animal species. Considerable progress has been made in understanding the biology of N. caninum and there are more than 200 papers on this subject from Brazil. However, most of the reports on neosporosis from Brazil are serological surveys. Overall, little is known of clinical neosporosis in Brazil, particularly cattle. The few reports pertain to sporadic cases of abortion with no information on epidemics or storms of abortion. The objective of the present review is to summarize all reports from Brazil and suggest topic for further research, including prevalence of N. caninum oocysts in soil or in canine feces, and determining if there are additional definitive hosts, other than the domestic dog. There is need for a national survey in cattle using defined parameters. Future researches should focus on molecular characterization of N. caninum strains, possibility of vaccine production and relationship between wildlife and livestock epidemiology.

Keywords: Neospora caninum; neosporosis; domestic animals; wild animals; Brazil

Resumo

Neospora caninum é um protozoário parasita que possui os canídeos domésticos e selvagens, coiotes e lobos cinzentos como hospedeiros definitivos e vários animais de sangue quente como hospedeiros intermediários. Foi cultivado e nomeado em 1988. A neosporose é uma das principais doenças em bovinos e não tem significância em saúde pública. Desde 1990, N. caninum tem emergido como uma das principais causas de aborto em bovinos em todo o mundo, inclusive no Brasil. N. caninum também causa infecções clínicas em várias outras espécies animais. Consideráveis avanços foram feitos na compreensão da biologia desse parasita e há mais de 200 trabalhos sobre o assunto no Brasil. No entanto, a maioria dos relatos de neosporose do Brasil são relacionados a sorologia. Em geral, pouco se sabe sobre a neosporose clínica no Brasil, particularmente em bovinos. Os poucos relatos referem-se a casos esporádicos de aborto sem informações sobre epidemias ou surtos de aborto. O objetivo da presente revisão é resumir todos os relatos sobre N. caninum no Brasil e sugerir tópicos para pesquisas futuras, incluindo a prevalência de oocistos de N. caninum no solo ou em fezes caninas e determinar se há hospedeiros definitivos adicionais, exceto o cão doméstico no país. Uma pesquisa nacional em bovinos usando parâmetros definidos seria de grande importância. Pesquisas futuras deveriam ser focadas na caracterização de cepas de N. caninum, possibilidade de produção de vacinas e a relação epidemiológica entre a vida selvagem e o gado.

Palavras-chave: Neospora caninum; neosporose; animais domésticos; animais selvagens; Brasil

Introduction

Neosporosis is relatively a newly recognized disease. In 1988, the etiologic agent of neosporosis was cultivated and named, Neospora caninum. It is ancestrally and morphologically related to Toxoplasma gondii. Since 1990’s N. caninum has emerged as a major cause of abortion in cattle worldwide, including in Brazil. N. caninum also causes clinical infections in several other animal species. Considerable progress has been made in understanding the biology of N. caninum. A recent book on neosporosis (DUBEY et al., 2017) listed more than 2100 citations and most reports (>200) from Brazil. Many of the reports from Brazil are scattered in local journals. The objective of the present review is to summarize reports from Brazil and suggest topic for further research. To minimize citations, only references from Brazil are listed in bibliography.

Basic Biology

As stated earlier, N. caninum and T. gondii are morphologically similar but biologically different coccidians. Both parasites have a wide host range but unlike T. gondii, N. caninum is not considered zoonotic. Canids (domestic and wild canids dogs, coyote, and wolf) are the definitive hosts of N. caninum whereas felids (domestic and wild Felidae) are definitive hosts for T. gondii. Neosporosis is a major disease of cattle whereas cattle are considered resistant to T. gondii. Transplacental transmission is a major route of propagation of N. caninum in cattle while, although medically important, is not the major route of transmission for T. gondii. There is only one species of Toxoplasma, T. gondii, but the genus Neospora has two species, N. caninum and N. hughesi; only horses are reported as an intermediate host for N. hughesi.

History of Neosporosis in Brazil

The in vitro cultivation of N. caninum in 1988 in USA made it possible to develop diagnostic tests for neosporosis (DUBEY et al., 2017). However, unlike T. gondii, it is difficult to culture N. caninum (see later discussion) and only one isolate (NC-1) was available initially at the USDA laboratory in Beltsville, Maryland, USA. Thus, commercial tests were not developed for the diagnosis of neosporosis for several years. Therefore, no research was performed on this subject in Brazil until mid 1990’s.

In BA, Gondim et al. (1999b, 2001) first recognized clinical neosporosis in an aborted bovine fetus and first isolated viable N. caninum (NC-Bahia) from the brain of a naturally-infected adult dog presenting incoordination and hind-limb paresis. Corbellini et al. (2002) first recognized neosporosis as an important cause of bovine abortion. They documented lesions consistent with protozoal infection in 22 (47.8%) of 46 fetuses submitted from 12 farms in RS. From those, 18 specimens of fetuses with encephalitis reacted to N. caninum antisera.

Brazilan Contributions to the General Biology of N. caninum

Viable N. caninum isolates and genetic diversity

Unlike T. gondii, little is known of genetic diversity of N. caninum mainly because there are only few viable isolates available worldwide. One reason for this is the difficulty to isolate viable N. caninum from animal tissues, especially from latently infected animals. Table 1 summarizes all viable isolates of N. caninum from animals in Brazil. The greatest success of isolating Neospora from asymptomatic animals has been achieved by feeding brain tissue from naturally-infected animals to dogs and then examining dog feces for oocyst excretion. By doing so, N. caninum was isolated from buffaloes, sheep and cattle.

Table 1 Isolation of N. caninum from naturally infected animals from Brazil. 

Host Source Bioassay Isolate designation Genetic data Remarks Reference
Animals Cell culture
Cattle Clinical, blind, neurological calf, 3-months old SW mice, Vero BCN/PR3 No Tissue cysts were found in the brains of SW mice that were immunocompetent Locatelli-Dittrich et al. (2003)
Aborted fetus, 7 months of gestation Mice, gerbils Vero BCN/PR1 Yes Initial isolation in immunosuppressed mice. Tachyzoites infective to immunocompetent mice and gerbils Locatelli-Dittrich et al. (2004)
Asymptomatic, 4 months old KO mice MARC-145 Nc-Goiás 1b Yes Not pathogenic to BALB/c mice García-Melo et al. (2009)
Adult slaughtered in abattoir Dog, SW mice, gerbils Vero NC-SP1 Yes Isolated from dog bioassay Oliveira et al. (2017)
Dog Collie, 7 years old, clinical Gerbil Vero (COS-1) NC-Bahia Yes Isolate pathogenic to gerbils Gondim et al. (2001, 2004)
Sheep Two 4 months old, clinically normal Gerbil, SW and vesper mice, dogs Vero Not stated No Mice remained healthy. Necropsied 60 dpi. Tissue cysts in brains of both gerbils. Pena et al. (2007)
Water buffalo 6 seropositive from abattoir Dogs, gerbil, KO mice CV1 NCBrBuf-1 No Both gerbils and KO remained asymptomatic Rodrigues et al. (2004)
NCBrBuf-2
NCBrBuf-3
NCBrBuf-4
NCBrBuf-5

KO=Gamma interferon gene knockout; SW=Swiss Webster.

In addition, to provide these Neospora isolates for biological and genetic studies to researchers in other countries (DUBEY et al., 2017), García-Melo in association with researchers from Spain did the first microsatellite typing data for Nc-Goiás isolated from clinically healthy cattle. Although the isolate had most of the alleles already identified, unique alleles were described for this strain at the MS5 and MS10 loci, using 12 microsatellite markers (GARCÍA-MELO et al., 2009). The recent isolate from brain tissue from a naturally-infected cattle (OLIVEIRA et al., 2017) was also found to have unique microsatellite alleles as MS5, MS6a, MS8 and MS10. A dog fed brain tissue from a naturally-infected cattle excreted N. caninum oocysts for 14 days starting seven days post infection (dpi), with an average number of 102 oocysts/g of feces. DNA isolated from cell culture derived tachyzoites was characterized using microsatellites. No new alleles were found and comparison showed closest relation to multilocus genotyping with strains from Spain and Argentina. Comparison with Brazilian strains (NC-Bahia; NC-Goiás) revealed variation in three and four of the nine markers used.

Additionally, the Brazilian NC-Bahia strain isolated from the dog was included among the N. caninum strains characterized by researchers outside Brazil (AL-QASSAB et al., 2009, 2010; REGIDOR-CERRILLO et al., 2013).

Transmission

Tachyzoites (in groups), bradyzoites (in tissue cysts) and sporozoites (in oocysts) are the three infectious stages of N. caninum. Tachyzoites and bradyzoites occur in tissues of intermediate hosts whereas oocysts are excreted in feces of certain canids. Unlike T. gondii, relatively few oocysts are excreted by canids after ingesting infected tissues. However, oocysts were excreted with a high frequency by two-three-month old dogs fed brains from six naturally infected water buffaloes (RODRIGUES et al., 2004). An other study showed that oocyst excretion is more efficient by feeding brains than other tissues to dogs (CAVALCANTE et al., 2011). The authors fed 17 two-three month old dogs with different tissues from four cattle naturally infected with N. caninum. Each group of dogs received: masseter (n=5), heart (n=5), brain (n=4), liver (n=3), and a group remaining as control (n=3), no infected. None of the control dogs excreted oocysts and three dogs that received brain, two that received masseter, two that received heart and one that received liver excreted N. caninum-like oocysts, from day seven to day 17 after ingestion of tissues. All dogs that received brain and liver excreted only N. caninum oocysts. The results were confirmed by polymerase chain reaction (PCR) using Nc5 and ITS-1 amplification and indicated that a variety of visceral, neural, and muscular tissues are infected naturally with N. caninum.

How dogs become infected with N. caninum in nature is not fully understood. Fecal transmission of N. caninum in dogs appears to be less important than carnivorism. Until the study by Bandini et al. (2011) it was unknown if the dogs could be infected via ingestion of oocysts. They fed four dogs with 1,000, 5,000 or 10,000 N. caninum oocysts; none of the four dogs excreted N. caninum–like oocysts in their feces during the observation period of 30 days. However, the two dogs fed with 10,000 oocysts seroconverted and the two dogs fed with 1,000 or 5,000 oocysts did not. Neither parasite DNA nor parasite stages were demonstrable in tissues of the seropositive dogs euthanized six months after feeding oocysts. These findings suggest that fecal transmission may not be an important mode of transmission of the parasite for the definitive host but results need confirmation.

Tachyzoites are important in transplacental transmission of N. caninum infection. Cavalcante et al. (2012) confirmed transplacental transmission of N. caninum in dogs. Six bitches in two groups were inoculated with a very high dose (108 tachyzoites). In group I, three bitches were inoculated during the third week of gestation, and in group II, three bitches were inoculated at the sixth week of gestation. The bitches were allowed to whelp naturally. Dams and their pups were tested by immunohistochemistry (IHC), serology, and PCR. In group I, six of the ten pups died within 48 hour of birth. In group II, seven of the 13 pups died between five and ten days of birth. N. caninum DNA was detected by nested PCR in two pups (hearts of both and liver of one) from group I, and one pup in central nervous system (CNS) and lymph node from group II. The dams and the pups that survived were clinically normal. N. caninum was not demonstrable in tissues of any of pups and their dams.

Studies in Brazil showed that N. caninum can be transmitted transplacentally in water buffaloes (CHRYSSAFIDIS et al., 2014, 2015). The authors conducted an important experiment in six buffaloes and seven cows inoculated intravenously with N. caninum tachyzoites at 70 day of gestation. Three buffaloes and five cows were inoculated with a Brazilian N. caninum strain (NC-Bahia); only one cow aborted but all fetuses became infected. The other two cows and three buffaloes were inoculated with the NC-1 strain; all fetuses died by 35 dpi as determined by ultrasound and N. caninum DNA was detected in fetal tissues.

Chryssafidis et al. (2011) also showed, for the first time, that N. caninum can be transmitted transplacentally in naturally infected buffaloes; they found N. caninum DNA in one brain of the nine fetuses from buffaloes slaughtered in an abattoir, aiming Nc5 and ITS-1 DNA regions. Although, viable or intact parasite has not been demonstrated in naturally infected fetuses from buffaloes, this is the first indication of transplacental transmission in this host.

In addition to bradyzoites and oocysts, tachyzoites can also be infectious orally. Four to five day old gerbils were successfully infected by oral inoculation of tachyzoites (FERREIRA et al., 2016). All 17 gerbils died of neosporosis between eight and 17 dpi (one died on each of days 8, 9, 15, 16, and 17, four died on day 12, and five died on day 15 (personal communication to JPD on October 24, 2016) with 4 x 105 NC-1 tachyzoites. N. caninum DNA was found in heart, lung, spleen, kidney, liver and CNS of gerbils.

Environmental resistance of oocysts

Oocyst is the environmentally resistant stage. Researchers in Brazil found that N. caninum oocysts were rendered noninfectious by heating to 100 °C for one minute, and 10% sodium hypochlorite for one hour but not at 60 °C for one minute, and by other commonly used disinfectants (ALVES et al., 2011). Aqueous 2% sulfuric acid has been commonly used to store N. caninum oocysts at 4 °C; how long oocysts remain viable under these conditions is not known. N. caninum oocysts remained viable for 108 days but not for 46 months when stored in 2% sulfuric acid at 4 °C (UZÊDA et al., 2007a).

Diagnostic tests

Recently, Fehlberg et al. (2017) reported on successful development of a high resolution melting PCR method to distinguish Neospora, Sarcocystis and Toxoplasma using a single pair of primers targeting 18S rDNA.

Epidemiology

More serological studies for N. caninum infection in animals have been conducted in Brazil than rest of the world.

The results, however, are not comparable because of different serological assays used different cut-offs employed, different antigens used. For example, in the indirect fluorescent antibody test (IFAT) and the Neospora agglutination test (NAT) whole tachyzoites are used detecting antibodies to surface proteins whereas in the enzyme-linked immunoabsorbent assay (ELISA) different antigens are used, some of them using crude tachyzoite extract while others used soluble antigens (Table 2a). The standardization of serological tests was based on studies in other countries and a full discussion of these is beyond the scope of this review—this subject was recently reviewed (DUBEY et al., 2017). One of the problems with serological testing is the availability of standardized sera from experimentally infected animals. Immunoblotting (IB) was employed in some studies where no such sera were available (Table 2b).

Table 2a ELISA techniques used to confirm presence of N. caninum antibodies. 

Sera source Antigen ELISA type* Results in table Reference
Dogs Antigen incorporated into iscoms A, C, I 3 Mineo et al. (2004)
NC-1 strain maintained in bovine monocytes cells; soluble antigen B, C Silva et al. (2007)
NC-1 tachyzoites strain in Vero cells A, C Raimundo et al. (2015)
Cattle NC-1 tachyzoites strain in Vero cells, lysed in SDS buffer J 4 Chahan et al. (2003)
Commercial E Andreotti et al. (2004)
Commercial F Paz et al. (2007)
Commercial E Melo et al. (2001)
Commercial E Melo et al. (2004)
Antigen incorporated into iscoms I Mineo et al. (2006)
Commercial E Locatelli-Dittrich et al. (2001)
Commercial E Locatelli-Dittrich et al. (2008)
Commercial E Marques et al. (2011)
Commercial E Nascimento et al. (2014)
NC-1 strain in Vero cells; soluble antigen B, C Ramos et al. (2016)
Commercial E Munhoz et al. (2006, 2009)
Commercial D Vogel et al. (2006)
Commercial E Sartor et al. (2003)
Commercial M Sartor et al. (2005)
Buffalo Commercial E 5 Viana et al. (2009)
Commercial D Vogel et al. (2006)
Commercial kit G, H Silva et al. (2014)
Sheep NC-1 strain in Vero cells A, L 6 Andreotti et al. (2009)
NC-1 strain in Vero cells, soluble antigen A, C Rossi et al. (2011)
Commercial D Vogel et al. (2006)
Captive deer Commercial E 11 Zimpel et al. (2015)
Horse NC-1 strain in HeLa cells A, C 12 Pivoto et al. (2014)
NC-1 strain in bovine turbinate cell monolayers C, K Hoane et al. (2006)

*A = WT= Whole tachyzoite extract; B = SA = soluble antigen; C = IH= In house; D = CHEKIT= CHEKIT Neospora, indirect ELISA, detergent lysate of tachyzoites, IDEXX Laboratories, The Netherlands; E = IDEXX = IDEXX HerdChek Neospora caninum antibody, indirect ELISA, sonicate lysate of tachyzoites, IDEXX Laboratories, USA; F = VMRD= Neospora caninum cELISA competitive ELISA GP65 surface antigen of tachyzoites VMRD, USA; G = Horse IgG = Horse IgG(T) ELISA Quantitation Set; Bethyl Laboratories; H = Horse IgM = Horse IgM ELISA, Kamiya Biomedical Company, Seattle; I = ISCOM= Detergent extracted tachyzoite antigen incorporated in immune stimulating complex particles; J = NcSAG1 = Recombinant surface antigen; K = NhSAG1 = Recombinant NhSAG1; L = rNcSRS2 = Recombinant antigen protein; M = NS/ND= not stated/ not done.

Table 2b Immunoblotting technique used to confirm presence of N. caninum antibodies. 

Sera source Antigen* Sera tested previously Results in Table Reference
Dog NC-1 tachyzoites lysed in SDDS-PAGE buffer IFAT, 1:25; indirect ELISA 3 Silva et al. (2007)
Cattle NC-1 tachyzoites lysed in SDDS-PAGE buffer NcSAG1 ELISA, 60/66 sera positive for ELISA 4 Chahan et al. (2003)
Sheep NC-1 tachyzoites lysed in 4% sodium dodecyl sulfate buffer IFAT, 1:50; discordant results 6 Rossi et al. (2011)
Cat Detergent extracted whole NC-1 tachyzoites NAT, 1:80 9 Dubey et al. (2002)
Donkey Whole NC-1 tachyzoites Sera positive by IFAT, 1:100 12 Galvão et al. (2015)
Human NC-1 tachyzoites lysed in SDDS-PAGE buffer Sera with discordant results by IFAT and ELISA - Lobato et al. (2006)

*Produced in non reducing conditions.

Little has been done in Brazil to characterize Neospora recombinant antigens for the serological diagnosis or vaccine development, except the report of Bezerra et al. (2017) who characterized one surface protein, by cloning the sequence and named it as NcSRS67, which has no orthologue with Toxoplasma gondii, only with Hammondia hammondi.

In Tables 3-12 serological reports in different hosts are summarized. We listed all reports that we found.

Table 3 Serological studies of N. caninum in dogs from Brazil. 

State Type No. tested No. positive % Positive Test Cut-off Remarks Reference
Alagoas Urban 128 5 3.8 IFAT 1:50 Age, sex, breed, area, habitat Sousa et al. (2012)
Rural 99 5 4.8 IFAT 1:50
Amazon region Indian communities 325 32 9.8 IFAT 1:50 Age, sex, T. gondii, others Minervino et al. (2012)
(MT and TO)
Bahia Stray 250 28 11.2 IFAT 1:50 Age, sex, others Jesus et al. (2006)
Owned 165 22 13.3 IFAT 1:50
Bahia Urban 156 4 2.6 IFAT 1:50 Area, contact with other dogs, feeding habits, others Sicupira et al. (2012)
Rural 41 6 14.6 IFAT 1:50 Area, contact with other dogs, feeding habits, others
Peri-urban 214 28 13.1 IFAT 1:50 Area, contact with other dogs, feeding habits, others
Espírito Santo Rural 187 22 11.7 IFAT 1:50 Sex, T. gondii Acosta et al. (2016)
Goiás Zoonosis Center 72 26 36.1 IFAT 1:50 Sex, origin Boaventura et al. (2008)
Hospital (owned) 125 39 31.2 IFAT 1:50 Sex, origin
Maranhão Stray 100 45 45.0 IFAT 1:50 Sex Teixeira et al. (2006)
Mato Grosso Clinics 60 27 45.0 IFAT 1:50 Age, sex, diet, access to streets Benetti et al. (2008)
Mato Grosso Rural 37 25 67.6 IFAT 1:50 Benetti et al. (2009)
Mato Grosso do Sul Pet 245 65 26.5 IFAT 1:50 Age, sex Oliveira et al. (2004)
Mato Grosso do Sul Rural 40 12 30.0 IFAT 1:100 Andreotti et. al. (2004)
Mato Grosso do Sul Urban 345 93 27.2 IFAT 1:50 Age, sex, Leishmania Andreotti et al. (2006)
Minas Gerais Clinical 163 11 6.7 IFAT 1:25 T. gondii Mineo et al. (2001)
Minas Gerais Urban 300 32 10.7 IFAT 1:50 Age, breed, sex, area Fernandes et al. (2004)
Peri urban 58 11 18.9 IFAT 1:50
Rural 92 20 21.7 IFAT 1:50
Minas Gerais Clinic 275 22 7.9 ELISA A,C Age, breed, sex, habitat, T. gondii, others Mineo et al. (2004)
Stray 94 12 12.8 ELISA I
Minas Gerais Clinic, stray 300 32 10.7 IFAT 1:50 Age, breed, sex, T. gondii Silva et al. (2007)
Clinic, stray 300 105 35.0 ELISA B,C
Minas Gerais Clinics 228 7 3.1 IFAT 1:50 Age, breed, sex T. gondii, Leishmania, Babesia canis Guimarães et al. (2009)
Minas Gerais Rural 240 36 15.0 IFAT 1:50 Age, breed, origin, sex, others Bruhn et al. (2012)
Minas Gerais Urban 182 15 8.2 IFAT 1:50 Age, diet, hunting, area Nogueira et al. (2013)
Rural 421 58 13.7 IFAT 1:50 Bovine abortion, area
Pará Rural 72 8 11.1 IFAT 1:50 Sex, area T. gondii, Leishmania Valadas et al. (2010b)
Urban-stray 57 8 14.0 IFAT 1:50
Paraíba Urban Domestic 286 24 8.4 IFAT 1:50 Age, sex, breed, others, habitat, T. gondii Azevedo et al. (2005)
Paraná Dairy farms 134 29 21.6 IFAT 1:50 Age, sex, breed Souza et al. (2002)
Paraná Neurological 98 0 0.0 IFAT 1:50 T. gondii Giraldi et al. (2002)
Paraná Sheep farms 24 7 29.1 IFAT 1:50 Age, sex, breed, T. gondii Romanelli et al. (2007)
Paraná Urban 181 23 12.7 IFAT 1:50 Area, habitat Plugge et al. (2008)
Peri urban 178 28 15.7 IFAT 1:50
Rural 197 50 25.3 IFAT 1:50
Paraná Rural 129 32 25.0 IFAT 1:50 Dogs and cattle Locatelli-Dittrich et al. (2008)
Paraná Owned 127 14 11.0 IFAT 1:50 T. gondii, neurologic signs Plugge et al. (2011)
Stray 20 3 15.0 IFAT 1:50
Paraná Stray 26 3 11.5 IFAT 1:25 Leishmania spp, T. gondii, Trypanosoma cruzi Constantino et al. (2016)
Pernambuco Figueredo et al. (2008)
Paulista Domiciled 289 75 26.0 IFAT 1:50 T. gondii, origin
Amaraji Domiciled 168 44 26.2 IFAT 1:50
Garanhuns Domiciled 168 58 34.5 IFAT 1:50
Pernambuco Rural villages 56 0 0 IFAT 1:50 T.gondii antibodies surveyed Arraes-Santos et al. (2016)
Piauí 530 17 3.2 IFAT 1:50 Age, sex, breed, T. gondii, Leishmania Lopes et al. (2011)
Piauí Rural villages 71 5 7.0 IFAT 1:50 T.gondii antibodies surveyed Arraes-Santos et al. (2016)
Rio de Janeiro Urban - Clinic 402 34 8.4 IFAT 1:50 Age, neurologycal signs, others Balthazar et al. (2013)
Rio Grande do Sul Rural 230 47 20.4 IFAT 1:50 Age, sex, area, type of farm, carcasses and abortions not removed, others Cunha et al. (2008)
Urban 109 6 5.5 IFAT 1:50
Rondônia Domiciled (Street access) 157 13 8.3 IFAT 1:50 Age, sex, diet, street access Cañón-Franco et al. (2003)
Rondônia Farms 174 22 12.6 IFAT 1:50 Age, diet, abortion, stillbirth, others Aguiar et al. (2006)
São Paulo Hospital 203 44 21.6 IFAT 1:50 T. gondii, neurological signs Higa et al. (2000)
São Paulo Rural and urban 295 25 8.4 IFAT 1:50 Age, sex, T. gondii, neurologic signs Varandas et al. (2001)
São Paulo Domiciled 500 49 10.0 NAT 1:25 Age, sex, breed, habitat Gennari et al. (2002)
Street 611 151 25.0 NAT 1:25
São Paulo Urban 204 36 17.6 IFAT 1:50 Age, sex, T. gondii, Leishmania spp., Gennari et al. (2006)
São Paulo Urban 108 17 15.7 IFAT 1:50 Age, sex, diet, others, T. gondii Bresciani et al. (2007b)
São Paulo Urban 865 223 25.8 IFAT 1:50 Age, sex, area Moraes et al. (2008)
Rural 65 11 16.9 IFAT 1:50
Peri urban 33 11 33.3 IFAT 1:50
São Paulo Rural (stray) 100 14 14.0 IFAT 1:25 Leishmania spp. Greca et al. (2010)
São Paulo Sheep farms 42 2 4.8 IFAT 1:25 Type of raising (chained or free), access to raw meat or offal Machado et al. (2011)
São Paulo Neurologic 50 7 14% IFAT 1:25 T. gondii Langoni et al. (2012)
São Paulo Domiciled 342 17 4.9 IFAT 1:25 Age, sex, breed, T. gondii Langoni et al. (2014)
São Paulo Rural 93 6 6.5 IFAT 1:50 Leishmania, T. gondii, Ehrlichia spp., Babesia canis Paulan et al., (2013)
São Paulo Kennel 167 37 22.1 IFAT 1:25 T. gondii, Leishmania Seabra et al. (2015)
Clinic 133 36 27.0 IFAT 1:25 T. gondii, Leishmania
Tocantins Rural 99 43 43.4 ELISA A,C Age, breed, area, T. gondii Raimundo et al. (2015)
31 31.3 IFAT 1:25
Urban 105 45 42.9 ELISA A,C
31 29.5 IFAT 1:25

Bold=statistically significant risk factor, Area = urban, peri urban, rural; Habitat=stray, domiciled.

Table 12 Detection of N. caninum antibodies in avian species from Brazil. 

Host Tested %positive DNA or Antibodies Test Cut-off / Method Reference
Chicken (Gallus gallus domesticus) 200 (outdoor) 47 (23.5) Antibodies IFAT 1:50 Costa et al. (2008)
200 (indoor) 3 (1.5) Antibodies IFAT 1:50
10 positive 6 (60.0) DNA PCR 3/4 of brain Direct PCR for Nc5
100 farm chickens 17 (17.0) Antibodies IFAT 1:50 Gonçalves et al. (2012)
6 (6.0) DNA PCR Np21/Np6
Sparrow (Passer domesticus) 40 3 (7.5) DNA PCR Heart and brain. Gondim et al. (2010)
Nested PCR of Nc5 and sequencing of ITS
Several species 294 0 (0.0) Antibodies IFAT 1:50 Mineo et al. (2011)

Salient features are commented for some of these surveys.

Dogs: Numerous surveys from different regions of Brazil are summarized in Table 3. As stated earlier results of these types of surveys are not strictly comparable. However, 45 of 49 surveys used IFAT as a diagnostic technique, and most of them employed the cut-off value of 1:50, facilitating comparisons of occurrence values. In three surveys, IFAT and ELISA were compared for serological diagnosis of N. caninum in dog sera and IFAT was superior to indirect ELISA used (SILVA et al., 2007; HIGA et al., 2000; RAIMUNDO et al., 2015).

In some studies, risk factors were evaluated (Table 3). The age of dogs was a statistically significant factor in nine reports; older dogs were more likely to be seropositive (OLIVEIRA et al., 2004; FERNANDES et al., 2004; AZEVEDO et al., 2005; ANDREOTTI et al., 2006; CUNHA et al., 2008; MINERVINO et al., 2012; NOGUEIRA et al., 2013; BALTHAZAR et al., 2013; RAIMUNDO et al., 2015). Gender and breed were not associated with presence of antibodies. In two surveys mixed breed dogs constituted a risk factor for the infection (BRUHN et al., 2012; RAIMUNDO et al., 2015). The diet in some studies was related with access to street and prevalence was higher in dogs that had outdoor access than in pets with little or no outdoor scavenging (GENNARI et al., 2002; CAÑÓN-FRANCO et al., 2003; BENETTI et al., 2008; SICUPIRA et al., 2012). However, in some studies such an association was not found (MINEO et al., 2004; JESUS et al., 2006; PLUGGE et al., 2011). Vertical transmission was also studied (TAQUES et al., 2016), with 41 stillborn puppies from 23 bitches. By PCR and IFAT, five (21.7%) bitches were positive and 22 (53.6%) stillborn were positive by PCR, utilizing ITS-1 DNA region/locus, being 17 from positive bitches and five from negative ones. Although the prevalence of positive stillborn was higher from positive bitches, no conclusions were made.

Epidemiologically, contact between cattle and dogs has been identified as a possible risk factor that deserves attention (Table 3). Dogs from peri-urban or rural areas had more chance to be infected by N. caninum (IFAT 1:50) than urban dogs in the surveys from MG (FERNANDES et al., 2004), PR (PLUGGE et al., 2008), RS (CUNHA et al., 2008), and BA (SICUPIRA et al., 2012), and this risk factor is normally associated with proximity to cattle; access and ingestion of fetal membranes, carcasses, and prey.

Leishmania infantum chagasi is an important parasite of dogs in Brazil; and immunosuppression caused by Leishmania spp. may enhance the susceptibility of dogs to N. caninum infection (CRINGOLI et al., 2002). Serological surveys correlating N. caninum and Leishmania spp., had been conducted (GENNARI et al., 2006; ANDREOTTI et al., 2006; GUIMARÃES et al., 2009; GRECA et al., 2010; VALADAS et al., 2010a; LOPES et al., 2011; PAULAN et al., 2013; SEABRA et al., 2015; CONSTANTINO et al., 2016). In dogs from endemic cities of visceral leishmaniosis such as Araçatuba, SP (GENNARI et al., 2006), Campo Grande, MS (ANDREOTTI et al., 2006), and Teresina, PI (LOPES et al., 2011), positive association was found (Table 3).

Cattle: Seroprevalence of N. caninum varied with the type of cattle (beef, dairy), different regions, within region and with the type of serological tests used (Table 4).

Table 4 Serologic studies of N. caninum antibodies in cattle from Brazil. 

State No. tested Type No. herds No. positive % positive Test Cut-off Remarksa Reference
Bahia 447 Dairy 14 63 14.0 IFAT 1:200 - Gondim et al. (1999a)
Goiás 444 Dairy 11 135 30.4 IFAT 1:250 - Melo et al. (2006)
Goiás 30 Mixed 1 13 43.3 IFAT 1:250 - Melo et al. (2006)
Goiás 456 Beef 9 135 29.6 IFAT 1:250 - Melo et al.(2006)
Maranhão 812 Dairy 27 412 50.7 IFAT 1:200 - Teixeira et al. (2010)
Mato Grosso 932 Dairy 24 farms 499 53.5 IFAT 1:200 - Benetti et al. (2009)
Mato Grosso do Sul 197 NS 6 66 33.5 ELISA J - Chahan et al. (2003)
Mato Grosso do Sul 87 Beef NS 26 29.9 IFAT 1:25 - Ragozo et al. (2003)
Mato Grosso do Sul 23 Dairy NS 5 21.7 IFAT 1:25 - Ragozo et al. (2003)
Mato Grosso do Sul 90 Beef (history of abortions) NS 38 43.0 ELISA E - Andreotti et al.(2004)
Mato Grosso do Sul 60 Heifers 18 30.0 ELISA E - Andreotti et al. (2004)
Mato Grosso do Sul 91 Healthy 7 7.7 ELISA E - Andreotti et al. (2004)
Mato Grosso do Sul 2448 NS 205 449 14.9 IFAT 1:50 Production system (Dairy/beef) Oshiro et al. (2007)
Mato Grosso do Sul 275 Beef 2 farms 81 29.5 cELISA F - Paz et al. (2007)
Mato Grosso do Sul 392 Dairy/beef 4 farms 43 9.1 IFAT 1:50 - Mello et al. (2008)
Mato Grosso do Sul 1098 Beef 1 farm 687 62.5 IFAT 1:50 Reproductive failure, 15% higher in seropositive cows. Andreotti et al. (2010)
Minas Gerais 584 Dairy 18 109 18.7 ELISA E - Melo et al. (2001)
Minas Gerais 126 Dairy 2 43 34.4 IFAT 1:25 - Ragozo et al. (2003)
Minas Gerais 36 Beef NS 4 11.1 IFAT 1:25 - Ragozo et al. (2003)
Minas Gerais 576 Dairy 18 106 18.4 ELISA E - Melo et al. (2004)
Minas Gerais 243 Dairy 2 41 16.8 ELISA I - Mineo et al. (2006)
Minas Gerais 559 Dairy 18 510 91.2 IFAT 1:200 Farm size, number of cows lactating, milk production per day Guedes et al. (2008)
Minas Gerais 575 Dairy Abattoir 559 97.2 IFAT 1:200 Farm size, number of cows lactating, milk production per day Guedes et al. (2008)
Minas Gerais 503 Dairy Abattoir (fetuses) 64 12.7 IFAT 1:25 Farm size, number of cows lactating, milk production per day Guedes et al. (2008)
Minas Gerais 1,204 Dairy 40 farms 260 21.6 IFAT 1:200 Reproductive failure Bruhn et al. (2013)
Pará 500 beef 500 260 52 IFAT 1:128 Region, T. gondii Silva et al. (2017)
Pará 40 Dairy 4 farms 7 17.5 IFAT 1:100 - Minervino et al. (2008)
Pará 120 Beef 12 23 19.2 IFAT 1:100 - Minervino et al. (2008)
Paraná 172 Dairy 1 60 34.8 ELISA E Abortion Locatelli-Dittrich et al. (2001)
Paraná 15 Beef NS 4 26.7 IFAT 1:25 - Ragozo et al. (2003)
Paraná 75 Dairy NS 16 21.3 IFAT 1:25 - Ragozo et al. (2003)
Paraná 623 Dairy 23 farms 89 14.3 IFAT 1:25 Breed, presence of dogs, age, feed Guimarães et al. (2004)
Paraná 385 Dairy 90 farms 45 12.0 IFAT 1:200 - Ogawa et al. (2005)
Paraná 1263 NS 77 farms 423 33.0 ELISA E - Locatelli-Dittrich et al. (2008)
Paraná 159 Beef Abattoir 24 15.1 ELISA E - Marques et al. (2011)
Paraná 309 Dairy 15 farms 63 20.4 IFAT 1:100 Feed, wild animal access, artificial insemination Martins et al. (2012)
Paraná 76 Beef 4 23 30.3 ELISA E - Nascimento et al.(2014)
Pernambuco 469 Dairy 20 farms 163 31.7 IFAT 1:200 Veterinary assistance, nutritional condition, presence of wetlands, manipulation of newborn calves, destination of cows that had aborted, abortion history, abortions period. Silva et al. (2008)
Pernambuco 316 Dairy 25 municipalities 31 19.6 IFAT 1:200 Transplacental transmission Ramos et al. (2016)
57 36.0 ELISA B, C
Rio Grande do Sul 223 (abortion history) Dairy 5 25 11.2 IFAT 1:200 Reproductive failure Corbellini et al. (2002)
Rio de Janeiro 75 Dairy NS 17 22.7 IFAT 1:25 - Ragozo et al. (2003)
Rio de Janeiro 75 Beef NS 5 6.7 IFAT 1:25 - Ragozo et al. (2003)
Rio de Janeiro 563 Dairy 57 farms 131 23.2 ELISA E Breed Munhoz et al. (2006, 2009)
Rio Grande do Sul 70 Dairy NS 13 18.6 IFAT 1:25 - Ragozo et al. (2003)
Rio Grande do Sul 70 Beef NS 15 21.4 IFAT 1:25 - Ragozo et al. (2003)
Rio Grande do Sul 1,549 Dairy 60 farms 276 17.8 IFAT 1:200 several Corbellini et al. (2006)
Rio Grande do Sul 781 Dairy/beef NS 89 11.4 ELISA D - Vogel et al. (2006)
Rondônia 1011 Dairy 50 114 11.2 IFAT 1:25 Farm size, number of cows Aguiar et al.(2006)
Rondônia 584 Beef 11 farms 56 9.5 IFAT 1:25 - Aguiar et al. (2006)
Rondônia 514 Mixed 25 farms 50 9.7 IFAT 1:25 - Aguiar et al. (2006)
Rondônia 621 Dairy 63 farms 66 10.6 IFAT 1:100 Abortion, birth of weak calves Boas et al. (2015)
Santa Catarina 1518 Dairy 72 farms 466 30.6 IFAT 1:100 Presence of dogs Fávero et al. (2017)
Santa Catarina 130 Dairy 29 farms 57 43.8 IFAT 1:200 Age, no. of pregnancies Klauck et al. (2016)
São Paulo and Minas Gerais 600 NS NS 101 16.8 IFAT 1:200 Area Costa et al. (2001)
São Paulo 150 NS NS 41 27.3 IFAT 1:25 - Ragozo et al. (2003)
São Paulo 521 Dairy NS 82 15.9 IFAT 1:200 - Sartor et al. (2003)
São Paulo 521 Dairy NS 159 30.5 ELISA E - Sartor et al. (2003)
São Paulo 777 Beef 8 Farms 121 15.5 IFAT 1:200 - Hasegawa et al. (2004)
São Paulo 505 Beef 11 Herds 101 20.0 ELISA M Production system Sartor et al. (2005)
São Paulo 408 Dairy 6 herds 145 35.5 ELISA M N. caninum significatively higher in dairy cattle Sartor et al. (2005)
São Paulo 1027 Dairy 3 farms 107 10.4 IFAT 1:100 High degree of association between N. caninum serological status of dams and daughter Cardoso et al. (2012a)
Tocantins 192 Dairy 10 farms 48 25.0 IFAT 1:200 Martins et al. (2011)

aStatistically significant risk factors.

In one survey, 802 serum samples of female cattle from 55 dairy and beef farms from six Brazilian states (SP, RJ, MG, PR, RS, MS) were assayed by IFAT (cut-off 1:25) and 23.6% were seropositive; association between positivity to N. caninum and state of origin, age and production purpose was analyzed using uniform methodology (RAGOZO et al., 2003). Although seroprevalence was higher in animals older than 24 months, this difference was not statistically significant. Conclusion is not definitive because of the selection of low cut-off of 1:25. Among the six states, RJ had the lowest prevalence and MG the highest and dairy cattle had higher prevalence than beef cattle. In another large study from MS, N. caninum antibodies were found in cattle from 143 of 205 herds (IFAT 1:50); the cows were older than two years (OSHIRO et al., 2007). Overall seroprevalence was 14.9% (Table 4).

Even after using a higher cut-off titer (IFAT 1:200) than used most of the surveys listed in Table 4, high prevalence were recorded from MG, where N. caninum antibodies were detected in 23 of 24 herds with individual seroprevalence of 21.6% (BRUHN et al., 2013); and MT, where antibodies to N. caninum were found in 499 (53.5%) of 932 cattle samples, with at least one positive in each farm (BENETTI et al., 2009). In another report from MG, very high (91.2%; 510/559) prevalence of antibodies to N. caninum was found among 18 farms (GUEDES et al., 2008), revealing that N. caninum is well spread in the southern region of the state. They also recorded 97.2% (559/575) prevalence in cows from an abattoir.

There is an unconfirmed report that the quality of milk might be affected by neosporosis (MELO et al., 2001); an association was reported between the type of milk, classified as A, B and C according to its quality, produced in the farms and positivity to N. caninum antibodies, with higher occurrence in farms of MG that produce milk grade A/B than grade C; and the authors discussed about the production technology used indifferent farms, animals stress and commercialization. One possible cause is that the production of types A/B milk is higher and requests more from the animals, generating stress, which could be responsible for the higher prevalence.

An association between seroprevalence and age of cattle (older animals presenting higher prevalence) was detected, while feed produced on the farm was negatively associated with N. caninum infection in PR (GUIMARÃES et al., 2004). Also in PR, production of food in the farm, absence of artificial insemination and access of domestic and wild animals to feed facilities were associated with infection (MARTINS et al., 2012).

A strong association of N. caninum infection was found in farms of RS, which had presence of dogs close to the livestock and which also fed calves with colostrum pooled from several cows (CORBELLINI et al., 2006). In this study, the size of the farm was inversely associated with the presence of positive animals.

An association between beef herds and infection by N. caninum was reported in the Amazon region, RO, while comparing beef, dairy and mixed herds (AGUIAR et al., 2006). In that region, farms with more than 25 animals were also a risk factor. However, reproductive problems, contact with forest areas and presence of dogs were not associated with the coccidian infection.

Significant association related to animal management was found in PE (SILVA et al., 2008). Veterinary assistance, nutritional status, presence of wetlands, manipulation of the newborn calves (use of gloves when handling aborted fetuses), and destination of cows that aborted (higher in the ones that were treated with antibiotics than the ones that were discarded) were risk factors for the infection.

Pure bred Holstein cows had a higher exposure rate than mixed breeds (MUNHOZ et al., 2009) and an association between reproductive abnormalities (Table 4) (repeated estrus, repeated miscarriages and temporary anestrus) and seropositivity to N. caninum has been reported (BRUHN et al., 2013).

N. caninum is considered a primary pathogen and not influenced by concurrent BHV1, BVDV infections in dairy herds (MELO et al., 2004; MINEO et al., 2006).

Antibodies can fluctuate during pregnancy as reported, and increase in titer is not always associated with abortion (CARDOSO et al., 2009). A prospective longitudinal study was carried out in three farms in SP, during two consecutive years and the reproductive parameters were analyzed in those herds (CARDOSO et al., 2012a). In only one of the three herds the relative risk of abortion between N. caninum positive and negative cows was higher in the positive animals. No difference was observed regarding gestational age at abortion, repeated abortion, number of inseminations, and calving interval. A high association between N. caninum serological status of dams and daughters were observed in a longitudinal study carried out in three farms from SP, confirming the importance of vertical transmission, but there was no difference in the culling rate between positive and negative cows (CARDOSO et al., 2012b). A significant relationship between seropositivity of cattle and their offspring was also found in PE (RAMOS et al., 2016), which had a rate of transplacental transmission of 72.2% (13/18) for adults and 69.2% (9/13) for heifers by IFAT and 43.5% (17/39) for adults and 50.0% (9/18) for heifers by ELISA, concluding that vertical transmission is the major form of infection in this region.

Buffaloes: Studies with serum samples from Brazilian buffaloes (Table 5) showed occurrence of N. caninum antibodies varying from 14.6% to 88%. However, despite the high occurrence values, no reproductive disorders were reported in those groups (FUJII et al., 2001a, b; GENNARI et al., 2005; GONDIM et al., 2007)

Table 5 Serological studies of N. caninum in buffaloes from Brazil. 

State No. of farms No. tested No. positive % positive Test Cut-off References
Bahia 4 117 42 35.9 IFAT 1:200 Gondim et al. (2007)
Pará 3 196 139 70.9 IFAT 1:25 Gennari et al. (2005)
Pará 26 500 195 39 IFAT 1:128 Silva et al. (2017)
Pará 4 212 187 88.2 ELISA E Viana et al. (2009)
Paraíba 14 136 26 19.1 IFAT 1:200 Brasil et al. (2015)
Rio Grande do Sul 164 24 14.6 ELISA D Vogel et al. (2006)
São Paulo 11 222 117 53.0 NAT 1:40 Fujii et al. (2001a, b)
142 64.0 IFAT 1:25
São Paulo 12 411 230 56.0 IFAT 1:200 Souza et al. (2001)
São Paulo 5 192 169 88.0 IFAT 1:50 Chryssafidis et al. (2015)
Northern Brazil-13 provinces 4,796 2,665 55.5 ELISA G, H Silva et al. (2014)
2,345 48.8 IFAT 1:40

Sheep: Seroprevalences ranged from 1.8% to 64.2% (Table 6). Some surveys stated as risk factors: abortion in the flock, presence of dogs, extensive husbandry systems and breed of the sheep. Great part of the studies also evaluated the presence of T. gondii infection, which usually showed a higher prevalence. In 2017, Filho et al. (2017) studied the vertical transmission rate of 50 naturally infected sheep, analysed by in house ELISA for six months. The initial prevalence of infection was 26.0% (13/50) and by the end of the study it had increased to 72% (36/50), being the vertical transmission rate 11%, which one sheep out of nine from a group gave birth to two infected ewes (IFAT 1:25).

Table 6 Serological studies of N. caninum in sheep from Brazil. 

State Type No. tested No. positive % positive Test Cut-off Remarks Reference
Alagoas 26 farms 343 33 9.6 IFAT 1:50 Small farms, water supply Faria et al. (2010)
Federal District 32 farms 1028 90 8.8 IFAT 1:50 Titers up to 51,200 Ueno et al. (2009)
Maranhão 5 farms 64 3 4.7 IFAT 1:25 Food supplement, reproductive failure Moraes et al. (2011)
Mato Grosso do Sul 1 farm 441 136 30.8 IFAT 1:50 Comparison of techniques Andreotti et al. (2009)
141 32.0 ELISA A, L
Minas Gerais 12 farms 334 27 8.1 IFAT 1:50 Abortion history Salaberry et al. (2010)
Minas Gerais 2 farms 155 73 47.1 IFAT 1:50 Age Rossi et al. (2011)
41 26.4 ELISA A, C
Minas Gerais 63 farms 488 64 13.1 IFAT 1:50 Age, area Andrade et al. (2012)
Paraná 9 farms 305 29 9.5 IFAT 1:50 Sex, age, breed, reproductive fails, presence of dogs Romanelli et al. (2007)
Pernambuco 23 farms 81 52 64.2 IFAT 1:50 Age Tembue et al. (2011)
Pernambuco Rural villages 179 39 21.8 IFAT 1:50 Region, age, sex, breed Arraes-Santos et al. (2016)
Piauí Rural villages 153 8 5.2 IFAT 1:50 Region, age, sex, breed Arraes-Santos et al. (2016)
Rio Grande do Norte 35 farms 409 7 1.8 IFAT 1:50 Sex, presence of dogs, reproductive fails Soares et al. (2009a)
Rio Grande do Sul 4 counties 62 2 3.2 ELISA D Vogel et al. (2006)
Rondônia 15 farms 141 41 29.0 IFAT 1:50 Titers up to 1:25,600; Reproductive problems, presence of dogs, source of water Aguiar et al. (2004)
São Paulo Meat breeds 597 55 9.2 IFAT 1:50 Age and presence of dogs Figliuolo et al. (2004a)
São Paulo 16 farms 1497 120 8.0 IFAT 1:25 Water supply, presence of dogs, reproductive problems Machado et al. (2011)
São Paulo 8 farms 382 49 12.8 IFAT 1:25 Tested for T. gondii Langoni et al. (2011)
São Paulo/ Rio Grande do Sul Abattoir 596 353 59.2 IFAT 1:25 Sex, breeding system, breed, area, age Paiz et al. (2015)

Bold=statistically significant risk factors.

Goats: In goats, serological surveys found rates between 1.0% (LIMA et al., 2008) to 26.6% (TEMBUE et al., 2011) of prevalence (Table 7). A study to evaluate infections by T. gondii, N. caninum and caprine arthritis-encephalitis virus (CAEV) was conducted, finding a prevalence of 37.81%, 23.62% and 17.23%, respectively (COSTA et al., 2012). The results indicate that CAEV does not predispose goats to infection by T. gondii or N. caninum. However, when CAEV/T. gondii or CAEV/ N. caninum infection were detected, occurrence of reproductive failure was higher, maybe related to poor husbandry conditions. Differential diagnosis in cases of abortions in small ruminants is highly desirable.

Table 7 Serological studies of antibodies to N. caninum in goats from Brazil. 

State Type No. tested No. positive % positive Test Cut-off Remarks Reference
Bahia 9 herds 384 58 15.1 IFAT 1:100 Breed Uzêda et al. (2007b)
Maranhão 5 farms 46 8 17.4 IFAT 1:25 Reproductive failure Moraes et al. (2011)
Minas Gerais 90 herds 667 71 10.7 IFAT 1:50 Maximum titer 1:3,200 Andrade et al. (2013)
Paraíba Abattoir 306 10 3.3 IFAT 1:50 Gender Faria et al. (2007)
Pernambuco 23 farms 319 85 26.6 IFAT 1:50 Age Tembue et al. (2011)
Pernambuco Rural Villages 174 5 2.9 IFAT 1:50 Region, breed, age, sex Arraes-Santos et al. (2016)
Piauí Rural Villages 202 4 2.0 IFAT 1:50 Region, breed, age, sex Arraes-Santos et al. (2016)
Rio Grande do Norte 14 farms 381 4 1.0 IFAT 1:50 Gender, reproductive fails, presence of dogs Lima et al. (2008)
Santa Catarina 57 cities 654 30 4.6 IFAT 1:50 Age, abortion, diet Topazio et al. (2014)
São Paulo 19 farms 394 25 6.4 IFAT 1:50 Maximum titer 1:12,800; Age, presence of dogs Figliuolo et al. (2004b)
São Paulo 17 farms 923 161 17.7 NAT 1:25 Presence of dogs, Age, gender, reproductive problems Modolo et al. (2008)

Bold=statistically significant risk factors.

Also, N. caninum DNA was found in brains of goats from BA. Silva et al. (2009) analyzed brains, hearts and tongues of 102 goats from slaughterhouses, and found a frequency of 1, 96% (2/102), using primers for ITS-1 region (JS4/CT2b; CT1/CT2).

Pigs: The prevalence of anti-N. caninum antibodies is low in pigs, and further studies are needed to evaluate the role of this species in the epidemiology of the parasite, including attempts to isolate viable parasites. Table 8 summarizes the studies with pigs from Brazil.

Table 8 Serological studies of N. caninum antibodies in swine from Brazil. 

State Type No. tested No. positive % positive Test Cut-off Remarks Reference
Paraíba Abattoir 130 4 3.1 IFAT 1:50 Sex, Also tested for T. gondii Azevedo et al. (2010)
Paraíba Abattoir 190 6 3.2 IFAT 1:50 Also tested for T. gondii Feitosa et al. (2014b)
Mato Grosso do Sul Free living, wild 83 9 10.8 IFAT 1:50 Sex, age Soares et al. (2016)

Bold=statistically significant risk factor.

N. caninum antibodies were also found in feral pigs (Sus scrofa) in 10.8% (9/83) of samples from Pantanal, MS, with titers up to 1:800 by IFAT (SOARES et al., 2016).

Cats: In Brazil, studies determining the prevalence of antibodies in serum of cats (Table 9) found results that range from 0%, in cats from Andradina, SP, and Patos, PB (COELHO et al., 2011; FEITOSA et al., 2014a) to 27% in cats from MA (BRAGA et al., 2012). In animals from SP, NAT antibodies were found in 60 of 502 (12%) (DUBEY et al., 2002). The samples with titers greater than 1:80 were also examined by IB, as a confirmatory test, being ten of the 24 cats (41.6%) positive for both tests.

Table 9 Serological studies of N. caninum in cats from Brazil. 

State Type No. tested No. positive % positive Test Cut-off Remarks Reference
Bahia Indoor, outdoor 272 8 2.9 IFAT 1:50 Also tested Sarcocystis neurona Meneses et al. (2014)
Maranhão Outdoor access 200 54 27.0 IFAT 1:25 Also tested T. gondii Braga et al. (2012)
Mato Grosso do Sul Free roaming and domiciled 151 10 6.6 IFAT 1:50 Also tested T. gondii and L. infantum Sousa et al. (2014)
Paraíba Free roaming and domiciled 201 0 0.0 IFAT 1:50 - Feitosa et al. (2014a)
Pernambuco Rural villages 32 2 6.2 IFAT 1:50 Region, breed, age, sex Arraes-Santos et al. (2016)
Piauí Rural villages 3 0 0.0 IFAT 1:50 Region, breed, age, sex Arraes-Santos et al. (2016)
São Paulo Free roaming and domiciled 502 60 11.9 NAT 1:40 NAT + (1+ at 1:800) Dubey et al. (2002)
10 IB +
IB B, C Also tested S. neurona
São Paulo Domiciled 400 98 24.5 IFAT 1:16 4 IFAT +
1:256
Bresciani et al. (2007a)
São Paulo Domiciled 70 0 0.0 IFAT 1:16 - Coelho et al. (2011)

Wild animals: N. caninum antibodies were detected in sera of wild animals kept in captivity or trapped in the wild of the Families: Canidae, Felidae, Didelphidae, Bovidae, Caviidae and Cervidae (Table 10).

Table 10 Serological studies of N. caninum in wild animals from Brazil. 

Host species Type No. tested No. positive % positive Test Cut-off Reference
Fam. Felidae
Caracal (Caracal caracal) Zoo 1 1 100.0 IFAT 1:25 André et al. (2010)
Fishing cat (Prionailurus viverrinus) Zoo 1 1 100.0 IFAT 1:25 André et al. (2010)
Jaguar (Panthera onca) Wild 11 7 63.6 IFAT 1:25 Onuma et al. (2014)
Zoo 13 8 61.5 IFAT 1:25 André et al. (2010)
Jaguarundi (Puma yagouaroundi syn. Herpailurus yagouaroundi) Zoo 25 5 20.0 IFAT 1:25 André et al. (2010)
Lion (Panthera leo) Zoo 9 1 11.1 IFAT 1:25 André et al. (2010)
Little-spotted-cat (Leopardus tigrinus) Zoo 35 11 31.4 IFAT 1:25 André et al. (2010)
Ocelot (Leopardus pardalis) Zoo 42 30 71.4 IFAT 1:25 André et al. (2010)
Pampas cat (Oncifelis colocolo) Zoo 3 3 100.0 IFAT 1:25 André et al. (2010)
Puma-cougar (Puma concolor) Zoo 18 5 27.8 IFAT 1:25 André et al. (2010)
Serval (Leptailurus serval) Zoo 1 1 100.0 IFAT 1:25 André et al. (2010)
Tiger (Panthera tigris) Zoo 6 4 66.7 IFAT 1:25 André et al. (2010)
Fam. Canidae
Crab-eating fox (Cerdocyon thous) Wild 15 4 26.6 IFAT 1:50 Cañón -Franco et al. (2004)
1 6.6 NAT 1:40
Captivity 2 0 0.0 IFAT 1:50 Melo et al. (2002)
Hoary fox(Pseudalopex vetulus) Wild 30 0 0.0 IFAT 1:50 Cañón-Franco et al. (2004)
NAT 1:40
Maned wolf (Chrysocyon brachyurus) Captivity and wild 48 0 0.0 IFAT 1:50 Melo et al. (2002)
Zoo and preserves 59 5 8.5 IFAT 1:25 Vitaliano et al. (2004)
Pampas fox (Lycalopex gymnocercus) Wild 12 5 41.6 IFAT 1:50 Cañón-Franco et al. (2004)
NAT 1:40
Fam. Didelphidae
Opossum (Didelphis marsupialis) Feral 396 84 21.2 IFAT 1:25 Yai et al. (2003)
Fam. Bovidae
Barbary sheep (Ammotragus lervia) Zoo 17 4 23.5 IFAT 1:50 Morikawa et al. (2014)
Fam. Cervidae
Brazilian dwarf brocket (Mazama nana) Captive and zoo 40 7 17.5 IFAT 1:50 Tiemann et al. (2005b)
Captive 22 1 4.5 ELISA E Zimpel et al. (2015)
Brown brocket deer (Mazama gouazoubira) Captive and zoo 66 29 43.9 IFAT 1:50 Tiemann et al. (2005b)
Marsh deer (Blastoceros dichotomus) Captive 6 1 16.7 ELISA E Zimpel et al. (2015)
Pampas deer (Ozotoceros bezoarticus) Wild National Park 23 3 13.0 IFAT 1:50 Tiemann et al. (2005a)
Pantanal 16 12 75.0 IFAT 1:50
Red brocket deer (Mazama americana) Captive
PR
4 0 0.0 ELISA E Zimpel et al. (2015)
Captive and zoo 29 18 62.0 IFAT 1:50 Tiemann et al. (2005b)
Rodon (Mazama rondoni) Captive and zoo 8 3 37.5 IFAT 1:50 Tiemann et al. (2005b)
Small red brocket (Mazama bororo) Captive and zoo 3 2 66.6 IFAT 1:50 Tiemann et al. (2005b)
Fam. Caviidae
Capybaras (Hydrochaeris hydrochaeris) Wild 213 20 9.4 IFAT 1:25 Yai et al. (2008)
Wild 63 1 1.5 IFAT 1:25 Valadas et al. (2010a)
Wild 170 0 0.0 IFAT 1:50 Abreu et al. (2016)

Among wild herbivores, Neospora has been better documented in cervids from Pantanal region (MS) (TIEMANN et al., 2005a). In that study, serum samples from 23 pampas deer (Ozotoceros bezoarticus) from the National Park of Emas, in GO, and 16 captured in bovine’s farms, from Pantanal region, in MT, were tested for the presence of N. caninum antibodies. They found 13% and 75% positivity, respectively, for the deer that live inside the park and the ones from Pantanal, which is close to farms indicating that this proximity of wild and domestic animals could increase the occurrence of N. caninum infection among deer. From the Zoo of Curitiba, PR, 17 samples from Barbary sheep (Ammotragus lervia), from the Bovidae Family, were examined and four (23.5%) presented N. caninum antibodies (MORIKAWA et al., 2014).

Yai et al. (2003) tested 396 feral opossums (Didelphis marsupialis) samples from different regions of the city of São Paulo, and 21.2% (84/396) were positive.

Sera from 14 species of wild felids from zoos were tested for the presence of N. caninum (Table 10) antibodies and 12 species had at least one positive animal (ANDRÉ et al., 2010). In addition, 11 serum samples from free range jaguars (Panthera onca) from Pantanal were examined and seven (63.6%) were positive (ONUMA et al., 2014). In both studies, IFAT with a cut-off of 1:25 and anti-cat commercial conjugate was used for IgG antibody determination.

Despite the importance of wild canids in the epidemiology of N. caninum, few studies are available in Brazil. Crab-eating fox (Cerdocyon thous) is one of most common canids of South America, (Gennari, own observations) and four of these foxes were fed with masseter muscle and brain of two N. caninum seropositive bovines (IFAT >200). The foxes received the inoculum in two consecutive days. Two animals excreted Hammondia heydorni oocysts on eight and nine dpi but not Neospora oocysts (SOARES et al., 2009b). By means of molecular techniques, Nascimento et al. (2015) identified N. caninum in brain of six from 49 (12.2%) hoary foxes (Pseudalopex vetulus syn. Lycalopex vetulus) from PB. The molecular identification of the amplified products by sequencing reaction, using Nc-5 gene, presented 99% similarity with N. caninum.

Similarly, Muradian et al. (2012) tested wild urban rodents tissues (Family Muridae), but did not detect N. caninum DNA in four mice (Mus musculus), 20 brown rats (Rattus novergicus), and 193 black rats (Rattus rattus) from São Paulo city. Regarding capybaras, the first study done (YAI et al., 2008) tested animals from 11 counties in SP by IFAT (1:25) and found a prevalence of 9.4% (20/213), suggesting that they can serve as a source of N. caninum infection for wild canids. Also in SP, 63 capybaras were examined for N. caninum by IFAT (1:25) and other diseases and found two positive animals and one of them was positive for both T. cruzi and N. caninum, but no association was observed (VALADAS et al., 2010a). Recently, 170 samples of capybaras from SP were analyzed, but none were positive, although 17 (10%) were positive for T. gondii (ABREU et al., 2016). DNA of N. caninum was found in capybaras from PR (TRUPPEL et al., 2010), in 23% (6/26) of the studied animals. Parasite DNA, aiming the Nc5 gene was found in the liver and lymph nodes and ITS-1 was found in blood, liver, heart and lymph nodes.

Horses: At present, it is uncertain if horses are infected with both N. caninum and N. hughesi (DUBEY et al., 2017). Serosurveys on horses conducted in Brazil are summarized in Table 11. N. caninum antigen was used in all studies with exception of Hoane et al. (2006), that used N. hughesi SAG1 (NhSAG1) in an in-house ELISA.

Table 11 Serological studies of N. caninum antibodies in horses from Brazil. 

State No. tested Type No. positive % positive Assay Cut-off titer or test Remarks Reference
Mato Grosso 200 Healthy 30 15.0 IFAT 1:50 Highest titer 1:400 in 1 horse. Laskoski et al. (2015)
Pará 411 Healthy horses 28 6.8 IFAT 1:50 No risk factors detected. Norlander (2014)
Paraná 72 Mares 28 38.8 IFAT 1:50 2 foals had pre-colostral antibodies Locatelli-Dittrich et al. (2006)
Paraná 14 Pregnant mares 12 85.7 IFAT 1:50 Highest titer 1:400 Hoffmann Kormann et al. (2008)
Paraná 97 Healthy horses 14 14.4 IFAT 1:50 Highest titer 1:200 in 2 horses Villalobos et al. (2012)
Paraná and Santa Catarina 112 Mares from 5 breeding farms 14 12.5 IFAT 1:50 25.7% (9/35) prevalence in mares with reproductive problem versus 6.4% (5/77) without problems. Highest titer only 1:50. Abreu et al. (2014)
Rio Grande do Sul 241 Cart horses and Crioula breed 34 15.9 IFAT 1:50 - Toscan et al. (2011)
Rio Grande do Sul 181 Pregnant mares 39 21.5 ELISA A, C 9.3% of their paired foals had pre-colostral anti-Neospora antibodies. Pivoto et al. (2014)
Rio Grande do Sul 197 Abattoir 77 39.1 IFAT 1:50 Tested for Sarcocystis spp. and T. gondii Portella et al. (2017)
Rio Grande do Sul, São Paulo, Rio de Janeiro 101 Race horses 0 0.0 NAT 1:25 - Dubey et al. (1999)
Santa Catarina 615 Healthy 25 4.1 IFAT 1:50 72 with history of neurological and reproductive problems. Moura et al. (2013)
São Paulo 325 Healthy 19 5.8 IFAT 1:50 Highest titer 1:400 Villalobos et al. (2006)
483 Diseased 73 15.1
São Paulo 26 History of ataxia. 15 57.6 IFAT 1:2 26 cerebrospinal fluids negative. Stelmann et al. (2011)
South 203 Mares 129 63.3 IFAT 1:50 Of 129, 34.8% gave birth to seropositive foals. Antonello et al. (2012)
10 states 961 Old horses from abattoirs 24 2.5 ELISA C, K - Hoane et al. (2006)

A low rate of infection (0.4%, IFAT 1:100) was found among 500 donkeys (Equus asinus) sampled in BA; positive cases were confirmed by IB (GALVÃO et al., 2015). In a previous limited survey carried out in PA, no seropositive donkeys (n=6) or mules (n=9) were found (NORLANDER, 2014). Recently, a 2% seroprevalence was reported in donkeys (n=333) from five northeastern states (AL, PB, PE, PI and RN) using IFAT (1:50). In all these studies, N. caninum NC-1 strain was used as antigen source (GENNARI et al., 2016).

In PR, antibodies to Neospora were detected in two foals (LOCATELLI-DITTRICH et al., 2006), but the information is not definitive because of the low titer (1:50) detected. In addition, Antonello et al. (2012), by IFAT (1:50, N. caninum antigen), reported a high prevalence (63.3%) of Neospora antibodies in sera of 203 thoroughbred mares and their foals before suckling in two farms from Southern Brazil. A high percentage (34.8%) of seropositive mares gave birth to seropositive foals. Additionally, 8% of seronegative mares gave birth to seropositive foals. Mare sera were titrated further to 1:200 dilution and the seropositivity decreased to 33%, but foal sera were not titrated. In another study performed in RS, Neospora antibodies were found in 21.5% of 181 mares and in 9.3% of their foals in pre-suckling sera (PIVOTO et al., 2014); in this case, antibodies were assayed using an in-house indirect ELISA, with NC-1 strain and soluble protein from tachyzoites maintained in CV-1 cells as antigen. Low levels of maternal IgG can cross the placenta in mares. Therefore, further studies are needed to confirm results of these investigations from Brazil (DUBEY et al., 2017).

Avian species:Table 12 summarizes the surveys of detection of N. caninum antibodies detection in avian species from Brazil. Seroprevalence was higher in free range chickens; 23.5% of 200 outdoors and 1.5% of 200 indoors chickens (Gallus gallus), in BA were seropositive (COSTA et al., 2008). In the same study, the authors found positive results for PCR from 6/10 (60%) seropositive chickens. 40 of 293 wild sparrows (Passer domesticus) from BA and PE were seropositive and N. caninum DNA by PCR was detected in three (7.5%) of brain and heart from 40 animals (GONDIM et al., 2010).

In a study by serological and histological methods none of the 294 wild and captive birds from nine avian orders had N. caninum antibodies. However in two psittacine birds, Apicomplexa-like tissue cysts were found and were immunostained positive with N. caninum antisera (MINEO et al., 2011).

Results of the experimental infection in birds from Brazil are summarized in Table 13. In the first Brazilian study (FURUTA et al., 2007) 50 chickens were inoculated with N. caninum tachyzoites, using different doses; chickens seroconverted but remained healthy. In 15 euthanized chickens, N. caninum tachyzoites were reported to be present in different tissues by IHC, at 15 dpi; however, no illustrations were provided. At the termination of the experiment (60 dpi), all chickens were seronegative by IFAT (<1:20) N. caninum was not found by IHC. In laying hens, no evidence of vertical transmission was found. However, 50% of embryonated chicken eggs inoculated with N. caninum died and chickens that hatched 21 dpi had neurological signs. Dogs fed chorioallantoid membranes and whole infected eggs seroconverted and excreted N. caninum oocysts in their feces, as confirmed by PCR (Nc5) (FURUTA et al., 2007).

Table 13 Detection of N. caninum in avian from experimental studies in Brazil. 

Host No. animals Dose Tests Results Reference
Chickens
(Gallus gallus domesticus) 7-days old 103, 104, 105, 106 Killed 15,30,45,60 dpi No mortality; Dpi 15:IFAT+ IHC+ Furuta et al. (2007)
Laying eggs 108 Bioassay, PCR, Histopathology Dpi 60: IFAT – IHC -
Embrionated eggs 103, 104, 105, 106 Histopathology Dogs bioassay Eggs- Mortality:18-21 days incubation Dogs shed oocyst
90-days old 3 x 106 IFAT, IHC, Histopathology, Bioassay IFAT+ Munhoz et al. (2014)
Embrionated eggs 1 x 102 2 embryos died PCR+ spleen, muscles (1bird)
Pigeons
(Columbia livia) 4 1 x 107 Blood samples each 5 days IFAT 1:20; peak 10-20dpi Mineo et al. (2009)
4 control IHC + Lungs, heart, CNS
Quails
(Coturnix coturnis japonica) 40 3.5 x 106 Histopathology + Oliveira et al. (2013)
8 5.0 x 106 IHC +
10 control PCR +

In an unconfirmed report, four littermate two-month old dogs fed with chorioallantoid membranes previously infected in ovo with 106NC-1 strain tachyzoites were euthanized 3, 4, 5 and 6 dpi (MUNHOZ et al., 2013). The authors reported immunoreactivity to N. caninum in lesions in lungs, spleen, and small and large intestine but strangely N. caninum DNA was not detected in affected tissues by conventional PCR. The gross lesions depicted resemble bacterial septicemia and the results need confirmation. The dogs did not excrete oocysts. In a follow up study, the authors, infected 90-days old chickens and embryonated eggs with 106 N. caninum tachyzoites using NC-1 strain and fed three dogs with infected organs but the dog did not excrete oocysts (MUNHOZ et al., 2014). Although there is no confirmation by IHC and microscopy, N. caninum DNA was found in the spleen and pectoral muscles of one of the birds born from the inoculated eggs (MUNHOZ et al., 2014).

An attempt to infect quails (n=58) with doses of 3.5 x 106 and 5 x 106 of N. caninum tachyzoites (NC-Bahia) was largely unsuccessful (OLIVEIRA et al., 2013). Although there was evidence of transitory infection (seroconversion and finding of parasite DNA) at 14 dpi, the quails became seronegative at 30 dpi with no demonstrable parasite DNA or antigen in their tissues; two dogs fed quail tissues did not excrete oocysts.

Experimental infection was also conducted in pigeons (Columba livia) inoculated with the 107 NC-1 tachyzoites (MINEO et al., 2009). The pigeons developed transitory N. caninum antibodies starting at 5 dpi but at the end of the experimental period of 45 days, all birds were seronegative. One infected pigeon died at 25 dpi and N. caninum and lesions were found by IHC in lungs, heart, central nervous system, liver, spleen and kidney.

Rezende-Gondim et al. (2017) cultivated N. caninum, using a chicken cell line, and temperatures between 39 °C and 41.5 °C. Multiplication of N. caninum tachyzoites in vitro was inhibited at temperatures similar to those of chickens. The authors concluded that the avian body temperatures may be one of the reasons that isolation of the parasite is difficult in avian species.

In summary, avians are a poor host for N. caninum, based on failure to isolate viable parasite from naturally infected tissues and failure to induce chronic infection in experimentally infected birds.

Clinical infections

Dogs: There are two confirmed reports of clinical neosporosis in adult dogs. A seven-year-old male Collie from Salvador, BA developed incoordination and rear limb paralysis (GONDIM et al., 2001). The dog was found to have a N. caninum IFAT titer of 1:1600. In spite of medication with Clindamycin (22 mg/kg) for 14 days the dog died. A necropsy was performed. Histologically there was encephalitis associated with tachyzoites and tissue cysts and the diagnosis was confirmed by IHC examination. Live tissue cysts were found in squash preparations from the dog brain. Tissue cysts were found in the brains of gerbils inoculated with brain homogenate of the dog. Viable N. caninum was propagated in cell cultures seeded with infected gerbil brain.

The second case was from a 10 year old dog from RS (MANN et al., 2016). Persistent dermal lesions with multifocal ulcerative nodules on the neck and pelvic limbs were observed. The dog had an IFAT N. caninum antibody titer of 1:6400. Cytological examination of the exudates from nodules showed pyogranulomatous inflammation with tachyzoites and N. caninum was identified by PCR. The dog was medicated with Clindamycin (6 mg/kg) for 28 days with resolvement of lesions. However, the dermal lesions with identifiable tachyzoites reappeared 12 days after the cessation of treatment, perhaps due to a very low dose of Clindamycin used; the usual treatment is 20-25 mg/kg.

In addition to these confirmed reports, Langoni et al. (2012) isolated N. caninum by bioassay in gerbils inoculated with brains of two of seven dogs with neurological disorders. No other details were given about these dogs or the strain of Neospora, therefore, not included in Table 1.

Cattle: Reports of confirmed neosporosis abortion from six states are summarized in Table 14. Apparently, all of these cases were sporadic abortion. Corbellini et al. (2006) investigated 161 bovine abortions from 149 farms bovine abortions during 2001 and 2003 from RS. Causes of abortion were identified in 83 (51.5%) cases. N. caninum was the most important cause, and identified in 37 fetuses; in 34 fetuses, the diagnosis was confirmed by IHC examination. Overall, 37 of 161 (23%) fetuses were infected solely with N. caninum. In six cases, there was concurrent Leptospira sp. infection. Most aborted fetuses were 4.4 months gestational age. Cows aborting a Neospora infected fetuses were 2.4 times likely to have aborted previously.

Table 14 Reports of N. caninum-associated abortion in cattle from Brazil. 

State No. aborted No. positive (%) Diagnosis Reference
Histo IHC PCR
Bahia 1 1 Yes Yes ND Gondim et al. (1999b)
Goiás 195 dead fetuses from abattoir 40 9(20.5) No No Yes Brom et al. (2014)
Paraná 34 8 (23.5) Yes Yes ND Santos et al. (2005)
Rio Grande do Sul 30 1 (3.3) Yes Yes ND Corbellini et al. (2000)
Rio Grande do Sul 46 22 (47.8) Yes Yes ND Corbellini et al.(2002)
Rio Grande do Sul 161 37 (17.4) Yes Yes ND Corbellini et al. (2006)
Rio Grande do Sul, Santa Catarina 258 55 (21.3) Yes Yes ND Pescador et al. (2007)
São Paulo 105 26 (24.7) Yes Yes Yes Cabral et al. (2009)

In a follow up publication, more detailed investigation involved 258 aborted fetuses from RS and SC. Lesions indicative of neosporosis were found in 89 (34%) of these 258 submissions based on histopathology. The diagnosis was confirmed by IHC in 55 of these 89 cases (PESCADOR et al., 2007). A striking feature was the distribution of lesions; myositis in 92%, myocarditis in 76% and pneumonitis and encephalitis in 75%. Two of these fetuses had grossly visible pale white foci in lungs, indicative of necrosis. Overall, N. caninum was the predominant (21.3% of 258) cause of abortion in this investigation. A similar conclusion was reached by Cabral et al. (2009), who combined histopathology, IHC, and PCR to diagnose N. caninum in 24.8% of 105 fetal samples from the state of SP. They detected N. caninum DNA in the brains of 22% (16 of 72), placenta of 20.0% (4 of 20), heart and liver of 16.3% (8 of 49) and pool of kidney, lungs, and spleen of 10.9% (7 of 64).

Additional provisional evidence for neosporosis was based on higher seropositivity in aborting versus non-aborting cows on a given farm (Table 15). However, most of these reports were provisional and not a case controlled study. In PR, samples from a herd collected over a nine-yr follow-up period were analyzed for Neospora infections (LOCATELLI-DITTRICH et al., 2001). They found that the proportion of abortions was 20% and 8%, respectively for the seropositive and seronegative animals.

Table 15 Seropositivity as evidence of abortion in cattle from Brazil. 

Total number of cattle/farms examined Aborting Non aborting or control Reference
Test cut-off No. tested No. seropositive (%) No. tested No. seropositive (%) Risk of abortion indicated by odd ratio (OR), significant association (SA), remarks
223 dairy cows, 5 herds IFAT, 1:200 NS NS (23.3) NS NS (8.3) OR 3.3 Corbellini et al. (2002)
2448 cattle from 205 herds, beef, dairy IFAT, 1:50 - 55/68 herds (80.9) - 84/134 herds (62.7) OR 2.5 Oshiro et al. (2007)
1256, 41 aborted IFAT, 1:200 41 24 (58.5) 1215 199 (16.4) OR 7.2 Hein et al. (2012)
1204 dairy cows from 40 farms IFAT, 1:200 NS NS (31.1) NS NS (17.7) OR 1.98 Bruhn et al. (2013)
621 cattle, 63 farms, 36 farms with abortion IFAT, 1:100 - 26/36 farms (72.2) - 12/27 farms (44.4) SA Boas et al. (2015)
3428 cattle from 174 herds IFAT, 1:100 - 99/108 herds (91.7) - 11/52 herds (21.1) SA Chiebao et al. (2015)
1273 cattle from 6 dairy herds IFAT, 1:200 305 122 (40.0) 968 40 (4.1) SA Pessoa et al. (2016)

As mentioned in Table 1, Locatelli-Dittrich et al. (2003, 2004) isolated viable N. caninum from a seven-month gestational age fetus and a three-month old blind calf. However, the etiology was not confirmed because histological examination was not performed.

Goats: Fatal neosporosis has been reported from MG and RS (Table 16). Hydrocephalus was detected in a day old goat kid, which had a high titer of antibodies on IFAT (1:400) for N. caninum and no antibodies for T. gondii (VARASCHIN et al., 2012). The cerebral hemispheres of the animal were asymmetrical the gyri were swollen, and ventricles were expanded. Histologically, there were only tissue cysts in the brain, no tachyzoites were observed and no lesions were observed in histological examination of placenta. Corbellini et al. (2001) described another case in southern Brazil, with a kid presenting neurological signs as ataxia and opistothonos, which got more severe when it was three days old, and was euthanized. Brain, heart, lungs and liver had microscopic lesions, but no grossly lesions were not observed.

Table 16 Fatal neosporosis in goats from Brazil. 

State Case no. History Diagnosis Reference
Serology Histology Immuno PCR
Minas Gerais 1- day old Born weak, unable to nurse Doe, IFAT 1:400 White matter absent, mild necrosis, perivasculitis, only tissue cysts 9.8-20.5 µm in diameter. Positive Not done Varaschin et al. (2012)
Day of birth New born kid, late term IFAT doe 1:800, presuckling kid 1:400 No lesions in placenta Negative Positive in placenta.
Abortion A chronically infected aborted 4 fetuses, 87 days after mating. IFAT doe 1:6,400 at abortion day. Positive in 1. Brain positive in 1 fetus PCR positive brain in the first and heart in the second fetus Mesquita et al. (2013)
2 stillborn Stillborn on 148 days after mating of a chronically infected doe IFAT doe 1:3,200 at parturition. Positive in 2. Positive in both. Positive in CNS of both.
Rio Grande do Sul 1- day old Born weak, unable to nurse, ataxic, euthanized day 3 No data Encephalitis, more severe in mid brain, many intact and degenerating tissue cysts of 12.4-32.2 µm in diameter. Positive Not done Corbellini et al. (2001)

Humans: Currently, there is no evidence of the zoonotic character of N. caninum, although antibodies in humans were found in immune compromised and normal patients in different parts of the world (DUBEY et al., 2017).

In Brazil, three studies were conducted. In MG, serum samples from HIV-infected patients (Group I), patients with neurological disorders (Group II), newborns (Group III) and a healthy control (Group IV) by IFAT (1:50) were assayed for N. caninum antibodies by indirect ELISA to detect immunoglobulin G (IgG), utilizing soluble antigen and IB as a confirmatory test, with lysed tachyzoites as antigen (LOBATO et al., 2006). They found IB positive patients in all groups, and HIV-infected patients and those with neurological disorders patients presented significantly higher prevalence. Combining all the tests, 37.7% (23/61) of group I, 18% (9/50) of group II, and 5% (5/91) from groups III had antibodies to N. caninum.

In the second study, antibodies to N. caninum (IFAT,1:50) were sought in Human Immunodeficiency Virus (HIV) patients; which 26.1% (81/310) patients from MS and 31.2% (10/31) patients from PR were seropositive and one patient had a titer of 1:400 (OSHIRO et al., 2015). In the third report, N. caninum antibodies (IFAT 1:100) were detected in 7 of 67 (10,5%) humans from 24 farms of MT (BENETTI et al., 2009).

Prospective and areas of future research

It is evident from this review that N. caninum infection is widely prevalent throughout Brazil. However, nothing is known of the prevalence of N. caninum oocysts in soil or in canine feces. It is also uncertain if there are additional definitive hosts, other than the domestic dog and some wild canids, as stated before. Overall, little is known of clinical neosporosis, particularly in cattle. The few reports pertain to sporadic cases of abortion with no information on epidemics or storms of abortion. There is need for a national survey in cattle using defined parameters. Future researches should focus on molecular characterization of N. caninum strains, possibility of vaccine production and relationship between wildlife and livestock epidemiology.

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Received: January 22, 2017; Accepted: June 28, 2017

*Corresponding author: Solange Maria Gennari. Departamento de Medicina Veterinária Preventiva e Saúde Animal, Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo – USP, Av. Prof. Orlando Marques de Paiva, 87, Cidade Universitária, CEP 05508-270, São Paulo, SP, Brasil. e-mail: sgennari@usp.br

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