Chief EditorK.M.L. Pathak
Print ISSN 0367-6722
Online ISSN 0976-0555
NAAS Rating 6.43
Impact Factor 0.5 (2023)
Canine Parvoviral Enteritis and Its Determinants-An Epidemiological Analysis
- Email email@example.com
First Online 26-05-2021|
Methods: Retrospective data on the incidence of CPVE in Namakkal region, Tamil Nadu was collected (2017-2019) from Veterinary Clinical Complex (VCC), Veterinary College and Research Institute (VC and RI), Namakkal, Tamil Nadu and had been subjected to temporal and spatial clustering and regression analysis. One hundred and twenty three faecal samples were collected from dogs with clinical signs of CPVE and subjected to PCR using H primer of CPV. Cross-sectional study was used to investigate the relationship between the disease and hypothesized causal factors. Relative risk, odds ratio were used to determine the causal association. Weather data was collected for the period from 2017-2019 from Animal Feed Analytical and Quality Control Laboratory (AFAQAL), VC and RI, Namakkal to assess the relationship of disease occurrence with the environmental determinants. Multiple linear regression model was developed for prediction of CPVE by correlation of environmental determinants with the occurrence of CPVE.
Result: Temporal analysis revealed endemic pattern of CPVE started last week of April, peaks in June and ends in August and second peak was noticed at November month. Higher incidences (>70%) were noticed in males and less than 6 months age group dogs. Polymerase chain reaction for confirmation of CPV infection in dogs revealed the positivity of 70.73%. Analysis of risk factors associated with CPVE revealed that vaccination, roaming of dogs, maternal vaccination and early weaning having positive statistical association with the incidence of CPVE. Multiple linear regression model revealed that relative humidity is positively associated with the occurrence of CPVE in dogs. Vaccination of dogs against CPV and administration of boosters at regular intervals, weaning of dogs after 45 days of age are used as primary strategies for prevention of CPVE.
MATERIALS AND METHODS
Total of one hundred twenty three faecal samples were collected aseptically from the dogs suspected for CPV infection, brought for treatment to Infectious disease unit, VCC Complex, VC&RI, Namakkal from May, 2019 to April, 2020 in phosphate buffered saline (pH-7.0) and stored at 4oC till further processing. Epidemiological data on the age, sex, breed, vaccination status, dam vaccination details, roaming status, colostrum feeding, etc. of CPVE suspected dogs were collected using structured proforma. The faecal samples of 123 dogs were subjected to template DNA extraction through hot and cold method as described by Schunck et al., (1995). Extracted template DNAs were subjected to polymerase chain reaction (PCR) as per the method described by Buonavoglia et al., (2001) using specific primer for large fragment of the capsid protein-encoding gene of CPV encompassing at least six or seven informative amino acids responsible for important biological properties of the virulence. The sequence of H primer used for PCR is given below.
Hrev - CAT TTG GAT AAA CTG GTG GT
The PCR cyclical conditions consists of initial denaturation of 95oC for 5 minutes, 30 cycles of denaturation at 95oC, one minute annealing at 55oC for 2 minutes, extension at 72oC for 30 seconds and final extension at 72oC for 10 minutes. Positivity to CPV infection was identified by detection of 630 bp PCR product upon gel electrophoresis of amplified PCR product.
Cross-sectional study was used to investigate the relationship between the disease and hypothesized causal factors. Relative risk and odds ratio were used to determine the causal association as per the formula described by Martin et al., (1994).
Multiple linear regression analysis
It was applied to develop the prediction model as per the protocol followed by Selvaraju (2010) using Vassarstats® open software tool and validated with existing data. Multiple linear regression generalizes this methodology to allow for multiple predictor variables, such as monthly mean maximum temperature, monthly mean minimum temperature, relative humidity (@ 8.00 h IST), relative humidity (@ 14.00 h IST), monthly total rain fall and wind speed.
Commonly used multiple linear regression model as follows:
RESULTS AND DISCUSSION
Retrospective analysis of canine parvoviral enteritis
Retrospective data on CPVE was collected from the VCC, VC&RI, Namakkal for the period from August, 2017 to July, 2019. Collected data had been analysed and graphical representation of gender, age and breed wise prevalence of CPVE was done.
1) Age-wise representation of canine parvoviral enteritis
Age-wise representation of CPVE revealed that higher incidence (72.66%) was recorded in less than six months age group (Fig 1). This finding is in corresponding with Hoskins, (1997), who reported that puppies between 6 weeks and 6 months of age appear to be more susceptible. For the first few weeks of life, puppies are protected against infection by maternally derived antibody (assuming the bitch has antibodies). However, maternal antibody to parvovirus has a half-life of approximately 10 days and as their maternal antibody titers decline, puppies become susceptible to infection (O’Brien, 1994). Declining of maternal antibody level after 3 months age in dogs might be one of the predisposing factors, which make them more prone to CPV infection (Parrish et al., 1988). The higher incidence of CPVE below 6 months might be due to the affinity of the virus for rapidly multiplying intestinal crypt cells in weaning pups with higher mitotic index due to changes in bacterial flora as well as in the diet due to weaning (Prittie, 2004).
2) Sex-wise representation of canine parvoviral enteritis
In this study, majority of the dogs represented with clinical signs of CPVE were of males (73.20%) rather than females (26.80%) which is in concurrence with the findings of Gombac et al., (2008) and Thomas et al., (2014). They reported a higher incidence of CPV in male dogs (78.26%) (Fig 2). The reason for high representation of males might be due to more chance of exposure of them to virus load due to behavioral characteristics mainly roaming and territorial behavior which also well explained by Deka et al., (2013). Preference of rearing males than females might be another probable reason for high representation of CPVE.
3) Breed-wise representation of canine parvoviral enteritis
Highest representation (55.29%) of CPVE was noticed in non-descript dogs than the pure breed dogs including Germen Shepherds, Doberman, Spitz, etc (Fig 3). Shukla et al., (2009) and Joshi et al., (2000) reported higher CPVE incidence of 56.9% and 27.23% in non-descript dogs than pure breeds, respectively. Higher prevalence of CPVE in non-descriptors might be due to population density making their close proximity to spread the infection or following poor vaccination schedule due to lack of awareness in public (Behera et al., 2015).
Incidence of CPVE in Spitz, Germen Shepherd, Labrador, Dobermann were of 9.3%, 7.3%, 6.8% and 4.4% respectively. Spitz is the most common toy breed reared in the reported geographical area next to non-descripts due to its availability and easy maintenance as pet or companion animal compared to other breeds. This might be the reason for high representation of CPVE in Spitz following non-descripts. Behera et al., (2015) reported that German Shepherd and Labrador Retriever were found to be more susceptible with the incidences of 17.24% and 10.34%, respectively and same pattern of incidence was also noticed in this study. Houston et al., (1996) reported that certain breeds have been shown to be at increased risk for severe CPV enteritis, including the Rottweilers, Doberman Pinscher, Labrador Retriever and German Shepherd and the reasons for breed susceptibility are unclear. There were significant alterations in the haemato-biochemical parameters in diseased vaccinated dogs (Hafid, 2019). Lower incidence of CPVE in pure bred in this region might be due to 1) only few pet owners are fascinated towards the rearing of pure bred dogs, 2) more maintenance cost and 3) less adoptability of pure bred dogs to the stressful tropical climatic conditions and high susceptibility to diseases.
Prevalence of CPVE in vaccinated and unvaccinated dogs
Vaccination of colostrum recipient puppies in early part of life preferably at 42 days of age and colostrum deprived puppies at 28 days of age with first dose of live attenuated canine parvoviral vaccine, boosters at 21 days interval up to 16 weeks of age, regular annual booster up to three years followed by boosters once in three years will protect them against CPVE (Greene and Decaro, 2012). Commercially available vaccines contain live attenuated canine parvovirus, canine distemper, parainfluenza virus and inactivated Leptospira antigens and canine adenovirus. Immunization of puppies usually started at 42 days of age. In this study, more than 95% of dogs did not receive complete recommended vaccination protocol (Fig 4). Probable reasons for the occurrence of CPVE in vaccinated dogs are, 1) administration of primary dose alone, 2) delayed booster vaccination, 3) lack of awareness on vaccination and 4) affordability of the pet owners.
Temporal distribution pattern of CPVE
Temporal analysis of CPVE (2017-19) in Namakkal, Tamil Nadu revealed the epidemic started at the last week of April, peaks in June and ends in August and second peak was noticed at November month (Fig 5). Kokilapriya et al., (2017) also reported higher prevalence during South-West monsoon (July, 16.3% and August, 12.3%) and North-East monsoon (November, 12.7% and December, 16.3%) and lower during summer season (March, 4.1%, April, 4.7% and May, 4.8%). Dogs were three times more likely to be admitted with CPV enteritis in July, August and September months compared with the rest of the year (Houston et al., 1996).
Confirmation of CPV infection
Collected faecal samples (123 numbers) were subjected to PCR for the confirmation using H primer as per the method described by Buonavoglia et al., (2001). The “H” primer was selected to amplify a large fragment of the capsid protein encoding gene of CPV, encompassing at least six or seven informative amino acids responsible for important biological properties of the virus (Parker and Parrish, 1997). Hence, the same primer was used to identify the presence of CPV infection in the selected cases of CPVE. Out of 123, 87 animals (70.73%) were confirmed for CPVE by the detection PCR product at 630 bp on gel electrophoresis of amplified product (Plate 1).
Identification of risk factors associated with CPVE
Cross-sectional study was used to investigate the relationship between disease and hypothesized causal factors. Relative Risk (RR) and Odds Ratio (OR) were used to determine the causal association as per the formula described by Martin et al., (1994). Vaccination of puppies, maternal vaccination, roaming of dogs and time of weaning are considered as important risk factors and association in the occurrence of disease are calculated follows:
In this study, vaccination (RR - 2.42, OR - 11.85), roaming of dogs (RR - 2.28, OR -7.02), maternal vaccination (RR - 2.22, OR - 6.27) and early weaning (RR - 3.05, OR - 13.83) having positive statistical association with the occurrence of CPVE in dogs. Houston et al., (1996) also reported that lack of vaccination in dogs is considered as an important risk factors associated with CPVE. Lack of maternal vaccination leads to increased susceptibility of puppies born to unimmunized bitches. This fact was also well explained by Carr et al., (1997), who reported that the failure of passive transfer of antibodies via colostrum, incomplete or ineffective primary vaccination course, or failure of vaccination to induce immunity are the risk factors associated with CPV infection in puppies.
Weather based forecast model for prediction of association of environmental determinants with CPVE
Multiple linear regression developed for detection of association of weather parameters with CPVE:
In this model, preceding thirty days average of predictor variables on daily basis is used to give early warning. If the value of the dependant variable is less than one (Y<1), there is a remote chance for the occurrence of disease and if greater than one there is more chance of the disease. The model is qualitatively valid only for the Namakkal area within the range of predictor variables. In this model, relative humidity both at 7.30 h IST and 14.30 h IST have strong correlation in the occurrence of CPVE. Kokilapriya et al., (2017) also reported that the humidity and rainfall were associated with the increased incidence of CPVE in dogs in Chennai, Tamil Nadu usually occurs in the South - West monsoon season. Kelman et al., (2020) reported that climate variables, temperature during hottest month and lower annual rainfall were strongly correlated with CPVE incidence in Australia. Hence, the occurrence of CPVE is depending upon the climatic variables prevailing in the respective geographical area.
- Behera, M., Panda, S.K., Sahoo, P.K., Acharya, A.P., Patra, S. Das and Pati, S. (2015). Epidemiological study of canine parvovirus infection in and around Bhubaneswar, Odisha, India, Veterinary World. 8 (1): 33-37.
- Binn, L.N., Lazar, B.C., Eddy, G.A. and Kajima, M. (1970). Recovery and characterization of a minute virus of canines, Infect. Immun. 1: 503-508.
- Carr, S., Macintire, D.K. and Swango, L.J. (1997). Canine parvovirus. Part I. Pathogenesis and vaccination, Compend Contin Educ Pract., 19: 125-133.
- Chethan, G.E., Singh, M., Chander, V., Singh, A.D., Rajesh, J.B., Prasad, H. and De, U.K. (2021). Occurrence of Canine parvovirus-2 and Canine adenovirus-1 Infections in Dogs: A Hospital Based Study. Indian J. Anim. Res., (55): 217-221.
- Deka, D., Phukan, A. and Sarma, D.K. (2013). Epidemiology of parvovirus and coronavirus infections in dogs in Assam. Indian Vet. J. 90(9): 49-51.
- Greene, C. and Decaro, N. (2012). Canine Viral Enteritis. In: Infectious Diseases of the Dog and Cat. Fourth edition, [Greene, G., (Eds.)]. Elsevier Saunders, Missouri, USA. pp. 25-42.
- Gombac, M., Svara, T., Tadic, M. and Pogacnic, M. (2008). Retrospective study of canine parvovirosis in Slovenia. Case Report. Slovenia Vet. Res. 45(2): 73-78.
- Hafid, N. (2019). Algerian indigenous dog: Hemato-biochemical profile in healthy and gastroenteritis diseased case. Agricultural Science Digest. 39: 244-249.
- Hoskins, J.D. (1997). Update on canine parvoviral enteritis. Vet. Med. 92: 694-709.
- Houston, D.M., Ribble, C.S. and Head, L.L. (1996). Risk factors associated with parvovirus enteritis in dogs: 283 cases (1982-1991). J. Am. Vet. Med. Assoc. 208: 542-546.
- Joshi, D.V., Singh, S.P., Rao, V.D.P. and Patel, B.J. (2000). Diagnosis of canine parvovirus infection by counter immunoelectrophoresis. Indian Vet. J. 77: 899-900.
- Kapil, S. (1995). Laboratory diagnosis of canine viral enteritis. Curr. Vet. Ther. 12: 697-701.
- Kelman, M., Barrs, V.R., Norris, J.M. and Ward, M.P. (2020). Socioeconomic, geographic and climatic risk factors for canine parvovirus infection and euthanasia in Australia, Prev. Vet. Med. 174: 104816.
- Kokilapriya, A., Balagangatharathilagar, M., Chandrasekaran, D., Parthiban, M. and Thennarasu, A. (2017). Seasonal variations of infectious haemorrhagic gastroenteritis in puppies in Tamil Nadu. Ind. Vet. J. 94(9): 9-10.
- Luo, H., Li, H. and Zhang, H. (2017). Epidemiology of Canine distemper and Canine parvovirus in pet dogs in Wenzhou, China. Indian J. Anim. Res. 51(1): 159-161
- Martin, S.W., A.H. Meek and P. Willeberg, (1994). Veterinary Epidemiology: Principles and Methods. 1st edn., Iowa State University Press, Ames, Iowa, U.S.A. pp. 22-148.
- O’Brien, S.E. (1994). Serologic response of pups to the low-passage, modified-live canine parvovirus-2 component in a combination vaccine, J Am Vet Med Assoc. 204: 1207-1209.
- Parker, J.S.L. and Parrish, C.R. (1997). Canine parvovirus host range is determined by the specific conformation of an additional region of the capsid. Journal of Virology, 71: 9214-9222.
- Parrish, C.R., O’Connell, P.H., Evermann, J.F. and Carmichael, L.E. (1985). Natural variation of canine parvovirus. Science. 230: 1046-1048.
- Parrish, C.R., Have, P. Foreyt, W.J., Evermann, J.F., Senda, M. and Carmichael, L.E. (1988). The global spread and replacement of canine parvovirus strains. J. Gen. Virol. 69: 1111-1116.
- Parrish, C.R., Aquadro, C.F., Strassheim, M.L., Evermann, J.F., Sgro, J.Y. and Mohammed, H.O. (1991). Rapid antigenic-type replacement and DNA sequence evolution of canine parvovirus. J. Virol. 65(12): 6544-6552.
- Prittie, J. (2004). Canine parvoviral enteritis: a review of diagnosis, management and prevention, J. Vet. Emerg. Crit. Care. 14: 167-176.
- Schunck, B., Kraft, W. and Truyen, U. (1995). A simple touch-down polymerase chain reaction for the detection of canine parvovirus and feline panleukopenia virus in feces. Journal of Virological Methods. 55: 427-433.
- Selvaraju, G. (2010). Development of disease forecasting system against diseases of small ruminants. Ph.D., thesis submitted to Tamil Nadu Veterinary and Animal Sciences University, Chennai. 51
- Shukla, A., Gupta, P.C. and D.K. Kumar, B. (2009). Epidemiology on canine parvovirus infection. Indian J. Vet. Res. 18(2): 42-44.
- Thomas, J, Singh, M., Goswami, T.K., Verma, S. and Badasara, S.K. (2014). Polymerase chain reaction based epidemiological investigation of canine parvoviral disease in dogs at Bareilly region. Veterinary World. 7(11): 929-932.
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.
This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.