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Effects of Age and Breed on the Prevalence of Neospora caninum in Commercial Dairy Cattle from Pakistan

TL;DR: Results indicate that N. caninum infection is widespread among dairy cattle in Pakistan, and animals over 2 yr of age and crossbreds were more likely to be seropositive than the other cattle examined.
Abstract: Neospora caninum is a major cause of bovine abortion worldwide. A serological survey was carried out to determine the seroprevalence of exposure to N. caninum in dairy cattle based on age and breed from Punjab and Sindh provinces, Pakistan. Serum samples from 641 animals from 12 herds from Punjab (n = 7) and Sindh (n = 5) provinces were tested for antibodies against N. caninum using a commercially available competitive enzyme-linked immunosorbent assay. Positive reactions to N. caninum were seen in 277 (43%) of the 641 of the samples. Seropositive animals were present in all 12 herds. Animals over 2 yr of age (47%) and crossbreds (55%) were more likely to be seropositive than the other cattle examined. These results indicate that N. caninum infection is widespread among dairy cattle in Pakistan.

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Summary

  • A serological survey was carried out to determine the seroprevalence of exposure to N. caninum in dairy cattle based on age and breed from Punjab and Sindh provinces, Pakistan.
  • Serum samples from 641 animals from 12 herds from Punjab (n 1⁄4 7) and Sindh (n 1⁄4 5) provinces were tested for antibodies against N. caninum using a commercially available competitive enzyme-linked immunosorbent assay.
  • Seropositive animals were present in all 12 herds.
  • The majority of congenital infections result in the birth of apparently healthy calves.
  • It has been demonstrated that they can become infected by consuming N. caninum– infected tissues (Gondim et al., 2002) or bovine placenta (Dijkstra et al., 2001).
  • The present study was done in healthy dairy cows from farms in Punjab and Sindh provinces, Pakistan.
  • Information regarding abortion history was available for only 2 farms (10 and 11).
  • Age-wise prevalence, though not statistically significant (P . 0.05), was greatest in animals older than 2 yr of age (Table II).

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Effects of Age and Breed on the Prevalence of
Neospora caninum
in Commercial
Dairy Cattle from Pakistan
Author(s): Muhammad Mudasser Nazir , Azhar Maqbool , Muhammad Sarwar Khan , Afzal Sajjid , and
David S. Lindsay
Source: Journal of Parasitology, 99(2):368-370. 2013.
Published By: American Society of Parasitologists
DOI: http://dx.doi.org/10.1645/GE-3173.1
URL: http://www.bioone.org/doi/full/10.1645/GE-3173.1
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J. Parasitol., 99(2), 2013, pp. 368–370
Ó American Society of Parasitologists 2013
Effects of Age and Breed on the Prevalence of Neospor a caninum in Commercial Dairy
Cattle from Pakistan
Muhammad Mudasser Nazir, Azhar Maqbool, Muhammad Sarwar Khan*, Afzal Sajjid, and David S. Lindsay, Department of Parasitology,
University of Veterinary and Animal Sciences, Lahore 54600, Pakistan; *Department of Clinical Medicine and Surgery, University of Veterinary and Animal
Sciences, Lahore 54600, Pakistan; †Veterinary Research Institute, Lahore 54810, Pakistan; ‡Department of Biomedical Sciences and Pathobiology, Virginia-
Maryland Regional College of Veterinary Medicine, Virginia Tech, Blacksburg, Virginia 24061. Correspondence should be sent to: lindsayd@vt.edu
ABSTRACT: Neospora caninum is a major cause of bovine abortion
worldwide. A serological survey was carried out to determine the
seroprevalence of exposure to N. caninum in dairy cattle based on age
and breed from Punjab and Sindh provinces, Pakistan. Serum samples
from 641 animals from 12 herds from Punjab (n ¼ 7) and Sindh (n ¼ 5)
provinces were tested for antibodies against N. cani num using a
commercially available competitive enzyme-linked immunosorbent
assay. Positive reactions to N. caninum were seen in 277 (43%) of the
641 of the samples. Seropositive animals were present in all 12 herds.
Animals over 2 yr of age (47%) and crossbreds (55%) were more likely to
be seropositive than the other cattle examined. These results indicate that
N. caninum infection is widespread among dairy cattle in Pakistan.
Neospora caninum is an important cause of abortion in dairy cattle,
causing significant economic losses to the industry worldwide (Dubey and
Lindsay, 1996). The parasite was recognized in dogs in Norway in 1984 as
a cause of neuromuscular degeneration, leading to hind limb paralysis
(Bjerkas et al., 1984). Because of structural and antigenic differences from
Toxoplasma gondii, it was described as a new species in 1988 (Dubey,
Carpenter, et al., 1988) and isolated from naturally infected dogs that
same year (Dubey, Hattel, et al., 1988). In 1989 N. caninum was first
reported as a cause of bovine abortion (Thilsted and Dubey, 1989).
Domestic dogs are definitive hosts for N. caninum (McAllister et al., 1998;
Lindsay, Dubey, et al., 1999; Lindsay, Upton, et al., 1999). Horizontal
transmission of N. caninum can result in abortion storms (Thilsted and
Dubey, 1989), but vertical (transplacental) transmission of the N. caninum
is the most economically important outcome of infection (Bj
¨
orkman et al.,
1996; Par
´
e et al., 1996; Schares et al., 1998). The majority of congenital
infections result in the birth of apparently healthy calves. Cows may abort
repeatedly due to N. caninum or give birth to apparently healthy calves,
calves with subclinical N. caninum infection, or uninfected calves. Most
congenitally infected calves remain clinically asymptomatic. Most N.
caninum–induced abortions occur at 5–6 mo of gestation (Dubey, 1999).
Horizontal transmission occurs when cows ingest sporulated N.
caninum oocysts shed by dogs (McAllister et al., 1998). Domestic dogs
are natural definitive hosts for the parasite (McAllister et al., 1998;
Lindsay, Dubey, et al., 1999; Lindsay, Upton, et al., 1999). It has been
demonstrated that they can become infected by consuming N. caninum
infected tissues (Gondim et al., 2002) or bovine placenta (Dijkstra et al.,
2001). Experimentally infected dogs excrete few oocysts (Lindsay et al.,
2001), and the role of dogs and N. caninum oocyst excretion is an area of
active research in the epizootiology of the disease (Bandini et al., 2011;
Cavalcante et al., 2011; King et al., 2012).
Dairy herd health is extremely important to the economy of Pakistan
because it is the third largest milk-producing country in the world (FAO,
2009). We have recently reported the seropositivity rate of N. caninum in
dairy herds with a history of high rates of abortion (Shabbir et al., 2011).
Brucella abortus was the most common agent found in aborting cattle
(77%), while N. caninum was present in 47% of aborting animals, and
dual infections with these agents were present in 28%of the animals.
However, N. caninum was found in 39% of nonaborting cattle, while B.
abortus was found in 27% of nonaborting cattle (Shabbir et al., 2011).
We became interested in determining if horizontal or vertical
transmission is more important in maintaining the parasite in the cattle
population in Pakistan. In the present study, we examined animals from 3
age groups to consider this question. Additionally, we examined the effects
of breed on prevalence to determine if genetic factors may play a role in
susceptibility to N. caninum. The present study was done in healthy dairy
cows from farms in Punjab and Sindh provinces, Pakistan.
Pakistan is an agricultural country, located in southern Asia with hot
dry summers, during which temperatures reach over 40 C, and mild
winters with average temperatures between 15 and 20 C. Pakistan is
located at latitude between 248 and 378 north and longitude between 618
and 768 east, and has 803,940 km
2
of land, a human population of 1.8
million, and a cattle population of 24.2 million. Between January 2009 and
August 2010, serum samples were taken from 641 clinically normal cattle
on 12 dairy farms, 7 from Punjab and 5 from Sindh provinces (Tables I–
III). Information regarding abortion history was available for only 2
farms (10 and 11). Farm 10 reported abortions in the last year, while farm
11 reported abortions over the last 4 yr. Only 6 cows aborted in herd 10 in
the previous year; in herd 11, 21 of the 37 cows had no history of abortion,
and the remaining 16 had aborted previously. Some of the cows may have
had repeated abortions, but no supporting data were available. Samples
were selected from clinically healthy cows of different breeds and different
age groups using animal numbers provided by the producers by an
individual who had no knowledge of animals status. We sampled 3 age
groups of cows, including calves (8 mo of age), heifers (.8moto2yr
old), and adult lactating cows (.2 yr old) to determine the variations of
serological prevalence against N. caninum between different age groups
(Table II). Cattle included crossbred (local 3 exotic), non-descript (no
cross-discernable based on animal appearance), and purebred (Table III).
Water and feed were available ad libitum.
Blood was collected from the jugular vein; serum was separated at the
Department of Parasitology, University of Veterinary and Animal
Sciences, Lahore, Pakistan, and stored at 20 C until assayed. Serum
reactivity to N. caninum was evaluated using a commercially available
competitive enzyme-linked immunosorbent assay kit (cELISA, VMRD,
Pullman, Washington). The procedures were performed according to the
manufacturer’s instructions, and results were expressed as percent
inhibition.
Pearson’s v
2
test was used to compare seropositive status with age and
breed using (SPSS for Windows, version 13.0; SPSS, Chicago, Illinois),
and P , 0.05 was considered significant.
The cELISA indicated that 277 (43%) of the 641 cows were seropositive
to N. caninum. A significant difference (P , 0.05) of seropositivity was
observed between different herds (Table I). The age of the cows were
categorized into 3 groups, below 8 mo of age, 8 mo to 2 yr of age, and
above 2 yr old. Neospora caninum seroprevalences were 39% (37/94), 36%
(59/162) and 47% (181/385), respectively. Age-wise prevalence, though
not statistically significant (P . 0.05), was greatest in animals older than 2
yr of age (Table II). The prevalence was significantly different (P , 0.05)
between purebred, crossbred, and non-descript animals. However, no
DOI: 10.1645/GE-3173.1
368
American Society of Parasitology. Muhammad Mudasser Nazir, Azhar Maqbool, Muhammad Sarwar Khan, Afzal Sajjid, and David S.
Lindsay (2013). "Effects of Age and Breed on the Prevalence of Neospora caninum in Commercial Dairy Cattle from Pakistan," Journal of
Parasitology, Vol. 99, No. 2, pp. 368-370. doi: http://dx.doi.org/10.1645/GE-3173.1

significant difference (P . 0.05) was found between sub-breeds, i.e., exotic
and local breeds.
The prevalence was not significantly different (P . 0.05) within the
exotic breeds, i.e., Jersey and Freisian, and local breeds, i.e., Sahiwal,
Rojan, Dajal, and Dhanni (Table III). Seroprevalence was highest in
crossbred animals (Table III).
The high prevalence of ex posure to N. caninum (43%) even in
apparently healthy animals indicates that N. caninum may be an important
risk factor of abortions in these provinces of Pakistan. The seroprevalence
of N. caninum varies within countries, between regions in countries, and
between beef and dairy cattle in areas examined (Dubey et al., 2007).
Seropr evalence depends largely on management and environmental
conditions of the country being studied (Dubey et al., 2007). The overall
high prevalence of N. caninum among dairy cattle herds corresponds to
previous observations made by Shabbir et al. (2011) who reported high
prevalence in aborting animals and in those that were at risk. The
prevalence of N. caninum in all the age groups strongly suggests
transplacental and horizontal transmission (Dubey et al., 2007), but the
rate of transmission may be different in different scenarios (Bartels et al.,
2007; Dijkstra et al., 2008; Williams et al., 2009).
Sadrebazzaza et al. (2004) concluded that there is no significant
relationship between N. caninum seropositivity and age. Howe ver,
Guimaraes et al. (2004) reported that N. caninum seropositivity was
higher in cattle above 2 yr of age and that horizontal transmission could
be responsible for this situation. In the present study, the highest
prevalence in age groups over 2 yr agrees with this study and observations
made by others that seroprevalence increases with animal age (Dubey et
al., 2007; Eiras et al., 2011).
The results of our study showed a significant difference in prevalence of
N. caninum among different breeds of cattle in our cattle populations and
that it was significantly (P , 0.05) higher in crossbreds. There are many
reports worldwide demonstrating differences in seropositivity of different
cattle breeds in N. caninum prevalence studies (Armengol et al., 2007;
Dubey et al., 2007; Duong et al., 2008; Munhoz et al., 2009). However,
these reports should be interpreted carefully because production systems
may be a possible explanation rather than breed-related susceptibility. The
extent of abortion and immune responses after N. caninum infection is
likely affected by the breed of cattle (Armengol et al., 2007; Almeria et al.,
2009; Romero-Salas et al., 2010; Santolaria et al., 2011). Experimental
studies need to be conducted with different bovine breeds before the
influence of breed can be accurately evaluated and its importance in the
epizootiology of bovine N. caninum infections can be determined.
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  • ...In contrast, other studies in different countries, such as Brazil (Corbellini et al., 2006; Teixeira et al., 2010), Croatia (Beck, Marinculić, Mihaljević, Benić, & Martinković, 2010), Jordan (Talafha and Al-Majali, 2013), Pakistan (Nazir et al., 2013), Romania (Imre et al., 2012), Senegal (Kamga-Waladjo et al., 2010) and Venezuela (Escalona et al., 2010), found no association between age and infection by N. caninum, which suggests that for these herds, transplacental transmission is probably more important....

    [...]

  • ..., 2010), Croatia (Beck, Marinculić, Mihaljević, Benić, & Martinković, 2010), Jordan (Talafha and Al-Majali, 2013), Pakistan (Nazir et al., 2013), Romania (Imre et al....

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Journal ArticleDOI
TL;DR: The finding discloses the strong association of N. caninum with reproductive disorders compared to Brucella spp.
Abstract: This case-control study aimed at assessing the relative association of Neospora caninum and Brucella species exposure with reproductive disorders. The study was carried out between October 2011 and June 2012 on 731 dairy cows sampled from 150 dairy farms in selected 17 conurbations of Ethiopia. Two hundred sixty-six of the cows were categorized as cases based on their history of abortion or stillbirth while the remaining 465 were controls. The presence of antibody to N. caninum was screened using indirect ELISA, while Brucella spp. exposure was assayed serially using Rose Bengal Plate Test and Complement Fixation Test. Exposure to N. caninum was more frequently observed among cases (23.8 %) than controls (12.7 %), while no significant difference (p > 0.05) was noted for Brucella exposure between the two groups. Moreover, the proportion of cows with disorders like retention of fetal membrane, endometritis and increased inter-calving period were significantly higher (p < 0.05) among Neospora seropositive cows. In conclusion, the finding discloses the strong association of N. caninum with reproductive disorders compared to Brucella spp. exposure. However, neither N. caninum nor Brucella spp. could explain the majority (73.2 %) of the reported abortions and stillbirths in cattle. Hence, this observation underscores the need for more intensive investigation on the identification of causes of the aforementioned disorders in dairy cattle of Ethiopia.

18 citations


Cites background from "Effects of Age and Breed on the Pre..."

  • ...caninum prevalence rather than the breed itself (Dubey et al. 2007; Nazir et al. 2013)....

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  • ...Due to lack of consistency and conclusive evidence on breed effect, management-related factors have been attributed to variation in N. caninum prevalence rather than the breed itself (Dubey et al. 2007; Nazir et al. 2013)....

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Journal ArticleDOI
TL;DR: This study is the first to report the risk factors for N. caninum , BHV-1, and BVDV infection in the central part of Iran and allows us to conclude that these agents are widely distributed in this region.
Abstract: This study aimed to determine the seroprevalence and identify the risk factors associated with Neospora caninum, Bovine herpesvirus type 1 (BHV-1), and Bovine viral diarrhea virus (BVDV) infection on industrial Holstein dairy cattle farms in Isfahan province, Central Iran. Blood samples were taken from 216 apparently healthy cattle from 16 randomly selected Holstein dairy farms in the North, South, East, and West of Isfahan in the summer of 2017. The antibodies to N. caninum, BHV-1, and BVDV were detected using a commercially available ELISA kit. The overall seroprevalence for N. caninum, BHV-1, and BVDV was 19%, 72.2%, and 52.8%, respectively. The significant major risk factors of BHV-1 in cattle were identified as farm direction, age groups, parity, and milk yield by the univariate analysis (p < 0.05). The significant major risk factors of BVDV in cattle were identified as age groups, parity, milk yield, and stage of pregnancy (p < 0.05). The only significant major risk factor of N. caninum was farm direction (p < 0.05). A significant association of concurrent infection with BVDV and BHV-1 has shown in the current study (p < 0.05). This study is the first to report the risk factors for N. caninum, BHV-1, and BVDV infection in the central part of Iran and allows us to conclude that these agents are widely distributed in this region.

18 citations

Journal ArticleDOI
TL;DR: The findings suggest N. caninum is likely to be an important cause of abortion in cattle in Tanzania and management practices, such as restricted grazing, are likely to reduce the risk of infection and suggest contamination of communal grazing areas may be important for transmission.
Abstract: Neospora caninum is a protozoan intracellular parasite of animals with a global distribution. Dogs act as definitive hosts, with infection in cattle leading to reproductive losses. Neosporosis can be a major source of income loss for livestock keepers, but its impacts in sub-Saharan Africa are mostly unknown. This study aimed to estimate the seroprevalence and identify risk factors for N. caninum infection in cattle in northern Tanzania, and to link herd-level exposure to reproductive losses. Serum samples from 3,015 cattle were collected from 380 households in 20 villages between February and December 2016. Questionnaire data were collected from 360 of these households. Household coordinates were used to extract satellite derived environmental data from open-access sources. Sera were tested for the presence of N. caninum antibodies using an indirect ELISA. Risk factors for individual-level seropositivity were identified with logistic regression using Bayesian model averaging (BMA). The relationship between herd-level seroprevalence and abortion rates was assessed using negative binomial regression. The seroprevalence of N. caninum exposure after adjustment for diagnostic test performance was 21.5% [95% Credibility Interval (CrI) 17.9–25.4]. The most important predictors of seropositivity selected by BMA were age greater than 18 months [Odds ratio (OR) = 2.17, 95% CrI 1.45–3.26], the local cattle population density (OR = 0.69, 95% CrI 0.41–1.00), household use of restricted grazing (OR = 0.72, 95% CrI 0.25–1.16), and an increasing percentage cover of shrub or forest land in the environment surrounding a household (OR = 1.37, 1.00–2.14). There was a positive relationship between herd-level N. caninum seroprevalence and the reported within-herd abortion rate (Incidence Rate Ratio = 1.03, 95% CrI 1.00–1.06). Our findings suggest N. caninum is likely to be an important cause of abortion in cattle in Tanzania. Management practices, such as restricted grazing, are likely to reduce the risk of infection and suggest contamination of communal grazing areas may be important for transmission. Evidence for a relationship between livestock seropositivity and shrub and forest habitats raises questions about a potential role for wildlife in the epidemiology of N. caninum in Tanzania.

17 citations

References
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Journal ArticleDOI
TL;DR: This review considers firstly the frequency with which exogenous and endogenous transmission occur, secondly the role of the immune response in controlling N. caninum infection and thirdly how the parasite persists in an immune-competent host and is re-activated during pregnancy.
Abstract: Vertical transmission of the protozoan parasite, Neospora caninum is highly efficient and can take two forms - endogenous transplacental transmission resulting from activation of the quiescent bradyzoite stage during pregnancy or exogenous transplacental transmission resulting from ingestion of oocysts during pregnancy. Calves born carrying infection derived from either endogenous or exogenous transplacental transmission are capable of infecting their offspring when they start to breed. This review considers firstly the frequency with which exogenous and endogenous transmission occur, secondly the role of the immune response in controlling N. caninum infection and thirdly how the parasite persists in an immune-competent host and is re-activated during pregnancy.

111 citations


"Effects of Age and Breed on the Pre..." refers background in this paper

  • ...The prevalence of N. caninum in all the age groups strongly suggests transplacental and horizontal transmission (Dubey et al., 2007), but the rate of transmission may be different in different scenarios (Bartels et al., 2007; Dijkstra et al., 2008; Williams et al., 2009)....

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Journal ArticleDOI
TL;DR: A total of 810 dairy cattle were blood sampled and used to evaluate serological screening for Neospora caninum infection in dairy cattle herds in Mashhad (Khorasan province, Iran) and showed no significant difference in seroprevalence.

90 citations

Journal ArticleDOI
TL;DR: The features of the oocyst of N. caninum are similar to those of Hammondia heydorni oocysts from dog faeces and Toxoplasma gondii and Hammondia hammondi oocytests from cat faece, and the nucleus was centrally or slightly posteriorly located.

86 citations

Journal ArticleDOI
TL;DR: To determine the prevalence of Neospora caninum antibodies and associated factors, blood sera from 623 female dairy cattle from 23 farms in the north of the state of Paraná, Brazil, were analyzed by means of the indirect immunofluorescent-antibody test and antibodies were found in 21.6% of dogs.

85 citations

Journal ArticleDOI
TL;DR: The results demonstrated that N. caninum in dogs is widespread, including the semi-arid to arid regions of north-western New South Wales and the Northern Territory and the populations of free-ranging dogs are likely to be important contributors to the sylvatic life cycle of N.caninum.

51 citations


"Effects of Age and Breed on the Pre..." refers background in this paper

  • ...Experimentally infected dogs excrete few oocysts (Lindsay et al., 2001), and the role of dogs and N. caninum oocyst excretion is an area of active research in the epizootiology of the disease (Bandini et al., 2011; Cavalcante et al., 2011; King et al., 2012)....

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Frequently Asked Questions (1)
Q1. What have the authors contributed in "Effects of age and breed on the prevalence of neospora caninum in commercial dairy cattle from pakistan" ?

Animals over 2 yr of age ( 47 % ) and crossbreds ( 55 % ) were more likely to be seropositive than the other cattle examined. The authors have recently reported the seropositivity rate of N. caninum in dairy herds with a history of high rates of abortion ( Shabbir et al., 2011 ). In the present study, the authors examined animals from 3 age groups to consider this question. Additionally, the authors examined the effects of breed on prevalence to determine if genetic factors may play a role in susceptibility to N. caninum. The present study was done in healthy dairy cows from farms in Punjab and Sindh provinces, Pakistan. Farm 10 reported abortions in the last year, while farm 11 reported abortions over the last 4 yr. The authors sampled 3 age groups of cows, including calves ( 8 mo of age ), heifers (. 8 mo to 2 yr old ), and adult lactating cows (. 2 yr old ) to determine the variations of serological prevalence against N. caninum between different age groups ( Table II ).