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. 2020 Dec 11;17:195. doi: 10.1186/s12985-020-01462-3

A systematic literature review and meta-analysis of characterization of canine parvoviruses 2 prevalent in mainland China

Bo Dong 1,2,3,✉, Gaoqiang Zhang 1, Jiajia Zhang 4, Junyu Bai 1, Weiming Lin 1,2,3,✉
PMCID: PMC7729692  PMID: 33308261

Abstract

Background

Canine parvovirus 2 (CPV-2) is a pathogenic virus that infects dogs, causing a highly infectious disease. Monitoring CPV-2 spread is an important part of prevention; however, the prevalence and epidemiological characteristics of CPV-2 have not been systematically evaluated and analyzed in mainland China. Therefore, a systematic review and meta-analysis were performed to assess prevalence and epidemiological characteristics of CPV-2 in domestic dogs in mainland China.

Methods

In this study, Chinese and English literature on CPV-2 epidemiology published between January 2006 and December 2019 was evaluated. Regarding meta-analysis, the random-effect model was employed by forest plot with 95% of confidence interval. The number of CPV-2 infections was identified and the pooled prevalence of infection, as well as the epidemiological characteristics, was calculated using meta-analysis.

Results

A total of 39 studies (data from 137,844 dogs) met the evaluation criteria and were used in our study. The pooled prevalence of CPV-2 infection in mainland China was 36%. CPV-2 infection were associated with age, breed, sampling season and immunization status, but not with gender, publication time and diagnostic methods.

Conclusions

Our results indicated that CPV-2 is prevalent among dogs in China. It is therefore necessary to carry out continuous surveillance and epidemiological studies of CPV-2. In addition, accordingly, effective measures should be taken to prevent the transmission and spread of CPV-2 among the Chinese dog population.

Keywords: CPV-2, Systematic review, Meta-analysis

Background

Canine parvovirus 2 (CPV-2) is a linear, non-segmented, single-stranded DNA virus that belongs to the family Parvoviridae and causes a highly infectious disease [1]. The main clinical characteristics of CPV-2 infection are acute gastroenteritis symptoms, such as vomiting, fever, leucopoenia, and diarrhoea that affect dogs of different ages, especially for young puppies 6 months and younger [2]. CPV-2 infection is usually acquired through contact with infected dog faeces, vomit, saliva, and contaminated water or food. It was reported that the prevalence of CPV-2 was correlated with age, season, immune status and regional distribution [3]. In addition, the prevalence of CPV-2 also showed seasonal characteristics. Generally speaking, the infection is more serious in the spring, late autumn and early winter [4].

CPV-2 is a potentially fatal pathogen in domestic dogs and other canine species. It may also infect other animals, such as cats because it has evolved into variant types that can infect cats [5]. Studies have shown that CPV-2 is a variant of the feline parvovirus (FPV)-like virus that was found in faecal samples from dogs with diarrhoea and quickly spread around the world [6]. Subsequently, the CPV-2, which had previously been unable to infect cats, has been replaced by different but closely related antigen CPV-2 variants and is capable of infecting cats, suggesting that CPV-2 may have the ability to spread across species [7]. A transformation of animal virus into a zoonotic virus, either by mutation or by recombination, has been reported. Examples of host switching viruses include the severe acute respiratory syndrome coronavirus (SARS-CoV) [8], Middle East respiratory coronavirus (MERS-CoV) [9], and some subtypes of influenza A virus (IAV) [10–12]. Therefore, the analysis of animal virus infection rates and epidemiological characteristics is necessary to reduce the risk of cross-species transmission between animals and humans and to prevent the potential threat of animal virus pandemic among humans.

CPV-2 was first reported in the USA in 1978 and has become prevalent worldwide, especially in China and other Asian countries [13, 14]. In 1978, there was a large outbreak of mixed infection of CPV-2 and canine coronavirus (CCoV) in dogs in the USA with high morbidity and mortality, attracting extensive global attention [15]. In China, the first record of CPV-2 was in 1982, and the infections were reported in widespread regions of China because of the high morbidity and mortality [16]. Since then, a number of studies on CPV-2 infection have been performed in China. Currently, CPV-2 infection has previously been reported in 23 provinces in China, and a long-term investigation has revealed that the rates of CPV-2 infection among Chinese domestic dog populations varied from 5.9 to 85.9% [17, 18]. These data provide a basic reference for our understanding of the epidemiological characteristics of CPV-2 in China. However, regional epidemiological studies are limited by sample size, sampling location, and season because China is a large country with a diverse climate. Therefore, the prevalence and risk factors of CPV-2 in China are not fully understood. Hence, this study focussed on a systematic review and meta-analysis to summarise the prevalence of CPV-2 and examine the potential risk factors of CPV-2 infection in mainland China.

Materials and methods

Search strategy

The study search was planned and performed according to the Meta-analysis of Observational Studies in Epidemiology guidelines [19]. To identify the epidemiological studies on CPV-2 in China, the literature published either in English or Chinese was searched up to December 2019. English databases (PubMed, Google Scholar, Cochrane library, and Clinical Trials) and Chinese databases (CNKI, Cqvip, WANFANG data, and Baidu scholar) were searched using “Canine parvovirus or CPV”, “epidemiology or incidence or prevalence”, “dog or canine”, and “China or Chinese”, or variants and combinations of these words, as keywords. Studies included in this systematic review had to contain any epidemiological data related to CPV-2 among dog populations from mainland China.

Exclusion criteria

The following studies were excluded from this systematic review and meta-analysis: (1) data from countries and regions outside mainland China; (2) literature that had review studies, case reports, press releases, newsletters, forums, and questionnaire surveys; (3) non-epidemiological studies (e.g., basic research); (4) no clear sampling time, sample size, infection rate, and prevalence rate in the study; and (5) insufficient information and duplicated findings.

Data extraction

The corresponding data were extracted from studies that met inclusion criteria and extracted into a Microsoft Excel datasheet. Recorded bibliographic data contained the following information: province, study design, background information, sample size, detection method, publication year, author, detection method, and sampling season.

Quality of publications

The selected publications were independently evaluated by two reviewers based on the established inclusion criteria. These publications were selected based on the information provided in the title and/or abstract as well as their full-text availability in Chinese or English. Furthermore, these publications had to contain prevalence data related to CPV-2 in mainland China. The quality of selected publications was assessed using the Newcastle–Ottawa scale (NOS). Studies with scores of 5 or above (out of 10) were included in the meta-analysis.

Statistical analysis

This study was planned and performed according to the Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) [20]. In the eligible studies, a random effects model was utilised to calculate the pooled prevalence of CPV-2 infection among domestic dogs. Meta-analysis was performed using Review Manager 5.3 (Copenhagen: The Nordic Cochrane Centre, The Cochrane Collaboration, 2014). The pooled estimates were the outcome of the meta-analysis and visualised the heterogeneity among the included studies using Forest plots. Forest plots were used to summarise estimates with 95% confidence intervals (CIs). The heterogeneity index among the included studies was determined using the Cochrane’s Q test (chi-squared) and Higgins I2 statistics. An I2 > 50% represents substantial heterogeneity [21]. Potential publication bias was assessed using a funnel plot. It was considered significant when the P value was less than 0.05.

Results

Description of studies

Based on search strategies of databases, a total of 5008 Chinese or English articles were identified. After the preliminary screen, 76 full-text articles were selected, and papers, duplicate citations, and studies not relevant to the current meta-analysis were removed. After excluding 37 articles with incomplete data, 39 articles met the inclusion criteria and were included in the systematic review (Fig. 1). The articles were published between 2006 and 2019, and covered 20 provinces in China. A cross-sectional study of all articles was performed, and period prevalence was calculated (Table 1).

Fig. 1.

Fig. 1

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Flow chart for screening eligible studies

Table 1.

Included studies of CPV-2 infection among dogs in mainland China

Reference Publication year Province No. examined No. positive Diagnostic methods Study design
Zhao [17] 2016 Henan 19,907 1169 PCR Cross sectional
Wu [22] 2014 Beijing 352 55 PCR Cross sectional
Wang [8] 2016 Beijing 58 43 Antigen Rapid CPV Ag kit Cross sectional
Zhao [7] 2017 Heilongjiang 216 152 PCR Cross sectional
Li [23] 2010 Guangxi 45,199 3174 unknown Cross sectional
Zhang [24] 2011 Beijing 404 115 Antigen Rapid CPV Ag kit Cross sectional
Bai [25] 2011 Beijing 327 51 PCR Cross sectional
Zhang [26] 2016 Beijing 1209 232 PCR Cross sectional
Zhao [18] 2013 Beijing 269 231 Antigen Rapid CPV Ag kit Cross sectional
Chen [27] 2019 Sichuan 145 120 PCR Cross sectional
Fu [28] 2017 Jilin 339 154 Antigen Rapid CPV Ag kit Cross sectional
Zhang [29] 2019 Jilin 526 176 PCR Cross sectional
Zhuo [30] 2015 Jiangsu 4290 704 Antigen Rapid CPV Ag kit Cross sectional
Jing [31] 2018 Gansu 4052 1028 Antigen Rapid CPV Ag kit Cross sectional
Zhang [32] 2013 Henan 495 88 unknown Cross sectional
Lou [33] 2010 Jiangsu 2319 711 Antigen Rapid CPV Ag kit Cross sectional
Tai [34] 2008 Jiangsu 2824 191 Antigen Rapid CPV Ag kit Cross sectional
Huang [35] 2018 Guangxi 683 378 Antigen Rapid CPV Ag kit Cross sectional
Kang [36] 2016 Shandong 2682 296 Antigen Rapid CPV Ag kit Cross sectional
Yang [37] 2006 Sichuan 2493 1873 Antigen Rapid CPV Ag kit Cross sectional
Yang [38] 2012 Chongqing 300 60 Unknown Cross sectional
Geng [39] 2009 Beijing 189 137 Antigen Rapid CPV Ag kit Cross sectional
Fu [40] 2012 Jilin 5684 4124 Antigen Rapid CPV Ag kit Cross sectional
Yang [41] 2014 Jilin 1864 1410 Antigen Rapid CPV Ag kit Cross sectional
Zeng [42] 2013 Shanxi 6027 956 Antigen Rapid CPV Ag kit Cross sectional
Zhao [43] 2013 Ningxia 1085 360 Antigen Rapid CPV Ag kit Cross sectional
Lin [44] 2011 Liaoning 96 78 PCR Cross sectional
Sun [45] 2016 Shandong 1511 295 Antigen Rapid CPV Ag kit Cross sectional
Ju [46] 2012 Shanghai 338 86 PCR Cross sectional
Chen [47] 2012 Zhejiang 4613 644 Unknown Cross sectional
Zan [48] 2017 Tianjin 182 35 Unknown Cross sectional
Luo [49] 2014 Zhejing 578 113 Antigen Rapid CPV Ag kit Cross sectional
Ma [50] 2014 Inner Mongolia 243 134 Antigen Rapid CPV Ag kit Cross sectional
Zhao [51] 2014 Hubei 8577 1517 Antigen Rapid CPV Ag kit Cross sectional
Chen [52] 2016 Sichuan 1360 203 Antigen Rapid CPV Ag kit Cross sectional
Han [53] 2014 Xinjiang 130,40 4925 Antigen Rapid CPV Ag kit Cross sectional
Wu [54] 2011 Xinjiang 2582 863 Antigen Rapid CPV Ag kit Cross sectional
Ye [55] 2016 Hunan 362 268 Antigen Rapid CPV Ag kit Cross sectional
Wu [56] 2012 Henan 427 315 Antigen Rapid CPV Ag kit Cross sectional
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Based on search strategies of databases, a total of 39 articles met the inclusion criteria and were included in the systematic review. The included studies, published between 2006 and 2019, covered 20 provinces in China. A cross-sectional studies were carried out in all included studies. Data information such as publication year, sampling location, sample size, positive number, diagnostic method and study design were extracted from all included studies

Prevalence of CPV-2 infection in mainland China

A total of 137,844 domestic dogs and 27,464 CPV-2-positive cases were included in the meta-analysis. The total prevalence of CPV-2 in mainland China was 36% at 95% CI (0.31, 0.41), and demonstrated a strong heterogeneity (Chi2 = 29,260.2, I2 = 100%, P < 0.00001) (Fig. 2). Data from 39 studies were collected from 20 provinces, with the eastern and northern provinces being the majority. Among those provinces, the prevalence in Liaoning and Hunan provinces were higher than 70%, while that in most provinces of northern China reached above 30% (Fig. 3). The prevalence of CPV-2 in administrative districts of China (from highest to lowest) was as follows: 63% in Northeast China, 48% in Southwest China, 43% in North China, 38% in Central China, 29% in Northwest China, and 18% in East China. The prevalence of CPV-2 in Northeast China was higher than that in other administrative districts of China (Table 2).

Fig. 2.

Fig. 2

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Random-effects meta-analysis of CPV-2 infection in mainland China

Fig. 3.

Fig. 3

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Map of CPV-2 infection in mainland China. Northeast China: Heilongjiang, Jilin, Liaoning; Northern China: Inner Mongolia, Shanxi, Hebei, Beijing, Tianjin; Northwest China: Xinjiang, Qinghai, Gansu, Ningxia, Shaanxi; Eastern China: Shandong, Anhui, Jiangxi, Jiangsu, Zhejiang, Shanghai, Fujian; Southern China: Guangxi, Guangdong, Shenzhen, Hainan, Macao, Hong Kong; Central China: Henan, Hunan, Hubei; Southwest China: Tibet, Yunnan, Guizhou, Sichuan, Chongqing

Table 2.

Infection of CPV-2 in dogs in mainland China

No. studies No. positive No. test % (95% CI) Chi2 P I2 (%)
Region
 Northeast China 6 6094 8725 63% (52–74) 465.1 0 99
 North China 9 1033 3230 43% (25–61) 1027.7 0 99
 Northwest China 5 8132 26,786 29% (19–39) 1256.3 0 100
 East China 8 3040 19,155 18% (13–23) 641.6 0 99
 Central China 5 3357 29,768 38% (24–51) 2521.2 0 100
 Southwest China 4 2256 4298 48% (10–86) 2423.1 0 100
Age
 Under 6 months of age 25 14,659 30,657 68% (52–85) 33,254.4 0 100
 6 months of age or above 25 5372 28,386 20% (13–26) 6666.9 0 100
Immunization status
 Yes 24 5123 20,346 20% (15–26) 3172.5 0 99
 No 24 14,434 20,679 68% (62–75) 3152.9 0 99
Gender
 Male 13 5235 20,647 45% (30–61) 6961.5 0 100
 Female 13 4194 18,323 38% (25–50) 4175.6 0 100
Breed
 Purebred 15 9899 16,954 66% (50–82) 10,310.2 0 100
 Mutt 15 4262 14,186 24% (16–33) 2682.9 0 99
Published time
 Before 2016 25 22,915 104,615 35% (27–43) 24,380.0 0 100
 2016 or later 14 4549 32,867 40% (30–49) 3432.4 0 100
Season
 Spring 20 4684 20,887 34% (27–41) 3357.8 0 99
 Summer 18 2522 19,769 15% (11–18) 1151.1 0 98
 August 18 3382 18,894 23% (18–28) 1642.8 0 99
 Winter 18 3839 18,667 24% (18–30) 2413.3 0 99
Diagnostic methods
 Antigen Rapid CPV Ag Test kit 25 21,344 63,939 43% (34–52) 18,492.7 0 100
 PCR 9 2119 23,116 39% (21–53) 1772.5 0 100
 Unknown 5 4001 50,789 15% (10–20) 257.3 0 98
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The corresponding data related to the prevalence of CPV-2 infection in dogs were analyzed, including administrative region, age, immunization status, gender, breed, sampling season and diagnostic methods. Among these risk factors, the occurrence of CPV-2 infection was significantly associated with age, breed, sampling season and immunization status, but not with gender and diagnostic methods in dogs. Northeast China: Heilongjiang, Jilin, Liaoning; Northern China: Inner Mongolia, Shanxi, Hebei, Beijing, Tianjin; Northwest China: Xinjiang, Qinghai, Gansu, Ningxia, Shaanxi; Eastern China: Shandong, Anhui, Jiangxi, Jiangsu, Zhejiang, Shanghai, Fujian; Southern China: Guangxi, Guangdong, Shenzhen, Hainan, Macao, Hong Kong; Central China: Henan, Hunan, Hubei; Southwest China: Tibet, Yunnan, Guizhou, Sichuan, Chongqing. CI, confidence interval; Chi2, chi-square; P, P value

Correlates of CPV-2 prevalence

As shown in Table 2, we analysed the risk factors related to the prevalence of CPV-2 infection in dogs. Among these risk factors, the occurrence of CPV-2 infection was significantly associated with age, sampling season, immunisation status, and breed: (1) the prevalence of infection in young dogs under 6 months of age was 68%, while that in dogs 6 months of age or above was 20%, which is a significant difference (P < 0.05); (2) the prevalence in unimmunised dogs (68%) was higher than that in immunised dogs (20%), and shows a significant difference (P < 0.05); (3) the prevalence of CPV-2 was the highest in spring (34%) and the lowest in summer (15%), which was significantly different (P < 0.05). The infection was more frequent in spring than in other seasons; (4) the prevalence of infection in purebred dogs was 66%, while in mutts it was 24% (P < 0.05), indicating that CPV-2 was more susceptible in purebred dogs than in mutts. However, the prevalence of CPV-2 in male dogs was 45%, and in female it was 38%; The prevalence based on the antigen Rapid CPV Ag Test kit was 43%, and based on the PCR it was 39%; The prevalence relying to publication year of included studies was as follows: Before 2016 35% and 2016 or later 40%. These results all shows no significant difference (P > 0.05), indicating that CPV-2 prevalence was less affected by gender, diagnostic methods and published time.

Discussion

To the best of our knowledge, the present study is the first meta-analysis investigating the prevalence of CPV-2 infection in domestic dogs in mainland China. In recent years, a large number of studies on CPV-2 have provided a deeper understanding of CPV-2 infection in Chinese domestic dogs. Statistics of the infection rates and epidemic characteristics of CPV-2 in the region are available through epidemiological studies; however, a large sample size is required to reduce the sampling error. This is because as the number of samples increases, the sample gets closer to the population. Furthermore, the climate in the north and south of China are different, which may have an impact on the prevalence of CPV-2. To understand the prevalence and epidemiological characteristics of CPV-2 in China, it is not possible to simply integrate the epidemiological data collected at different times and locations. Therefore, this study focussed on a systematic review and meta-analysis to summarise the prevalence of CPV-2 and examine the potential risk factors of CPV-2 infection in mainland China.

The estimates provided in our studies were based on data from 20 provinces in mainland China, and it demonstrated that the total prevalence of CPV-2 in mainland China was 36%. Statistics of subgroups showed that the prevalence of CPV-2 in northeast China was 63%, which was significantly higher than that in other administrative districts. Moreover, the highest rate (81%) of prevalence is observed in Liaoning province than in other provinces. The prevalence of CPV-2 varied from 15 to 81% in 20 provinces. Therefore, our study shows that CPV-2 is prevalent in Chinese dogs.

Although dogs of all ages can be infected with CPV-2, puppies are more susceptible, and become infected by CPV-2 show illness within 3–7 days, presenting with severe gastroenteritis, lethargy, vomiting, fever, and diarrhoea [57–59]. In this study, we observed that the prevalence of CPV-2 infection was significantly higher in puppies under 6 months of age, confirming that puppies were at a greater risk of contracting CPV-2 compared to adult dogs. This difference might be due to immature development of immune organs and lymphoid tissues, resulting in weakened body resistance in puppies [60]. Moreover, the prevalence of CPV-2 in purebred dogs was lower than that in hybrids in this study. These differences may be attributed to hybrids being able to adapt better to local climates and conditions, and developing more resistance to CPV-2 [37].

According to the current subgroup meta-analysis, the prevalence of CPV-2 was 34% in spring, which was higher than in other seasons. Spring is characterized by greater temperature differences between day and night, and if the dogs' immune system do not adapt to these temperature differences, that can decrease dogs’ immunity, which could be the reason for the seasonal variations in the prevalence of CPV-2 infection. In addition, the lower critical temperature for CPV-2 survival may also explain the seasonal variation in CPV-2 infection rates. Furthermore, several studies have reported that CPV-2 infection rates were higher in spring, which could be because people spend more time walking their dogs outdoors in the spring, thus increasing the chances of dogs being exposed to viral pathogens in the environment [17]. Therefore, these results showed that CPV-2 infection occurs throughout the year and is more prevalent in the spring. It is suggested that dogs be kept warm when the temperature between day and night varies greatly in spring. In addition, outdoor activity should be reduced to decrease the risk of CPV-2 infection.

Analyzing the subgroups, the prevalence of CPV-2 in unvaccinated dogs was significantly higher than those in vaccinated dogs. The reason for this is that dogs injected with vaccine can resist infection as they produce high levels of antibodies. However, interestingly, there was also prevalence (20%) in immunised dogs in this study. This could be attributed to improper immunisation procedures, improper preservation of vaccine, and inaccurate vaccination dose leading to immune failure. It could be because some Chinese dog owners prefer to get their dogs vaccinated at a kennel or pet shop rather than at an animal hospital. In addition, some dog owners are reluctant to cooperate with the hospital to have their dogs fully examined, which results in the immune effect not being detected effectively [29]. Therefore, enhancing the scientific awareness of dog owners, standardising immunisation procedures, and strengthening supervision over the transportation and preservation of vaccines are keys to improving immunisation efficiency.

The application of in-clinic immunochromatographic assays is available for the diagnosis of CPV infection in everyday veterinary practise, as the procedure is simple, inexpensive, and timely [61]. It only requires a faecal sample to permit diagnosis in vivo, which can assist in the early diagnosis of CPV. Meanwhile, PCR technology is also used for the investigation of CPV-2, as it is rapid, efficient, and highly accurate [62]. In the current study, the prevalence found in PCR was slightly lower than that found in in-clinic immunographic assays. This could be due to the high sensitivity and specificity of PCR to identify the species level and its acceptable genetic diversity. However, the difference in prevalence detected by the two diagnostic methods was not significant (P > 0.05), indicating that there is a fair agreement between in-clinic immunographic assay and PCR findings [63].

Our study had several limitations. First, one study identified during our systematic review did not have full text, leading to loss of qualified data. Second, the factors available for analyses were limited, with only publication date, geographical location, sampling season, gender, breed, diagnostic methods, and immunisation status retained. As a result, other potential risk factors were not analysed. Furthermore, the 39 included studies were cross-sectional studies. Therefore, more high-quality epidemiological studies on CPV-2 infection in Chinese domestic dogs should be carried out in the future to gain a more comprehensive understanding of the current situation of CPV-2 in China.

Conclusions

In conclusion, based on the results of this study, we found that the CPV-2 is prevalent in mainland China and even highly prevalent in some regions in China. In addition, the results illustrated correlation between CPV-2 prevalence and seasonality, a dog’s age/gender/breed/vaccination. Furthermore, the results suggest there is a need for continuous research on CPV-2 infection in more dogs to help other researchers to delve into the risk factors for CPV-2 infection, and indicate effective measures should be taken to reduce the prevalence according to the risk factors for CPV-2 infection.

Acknowledgements

No applicable.

Abbreviations

CPV-2

Canine parvovirus 2

CCoV

Canine coronavirus

SARS-CoV

Severe acute respiratory syndrome coronavirus

MERS-CoV

Middle East respiratory coronavirus

IAV

Influenza A virus

MOOSE

Meta-analysis of observational studies in epidemiology

NOS

Newcastle–Ottawa scale

PRISMA

Preferred reporting items for systematic reviews and meta-analysis

PCR

Polymerase chain reaction

Authors’ contributions

Bo Dong and Weiming Lin collected literatures, conceived the experiments and drafted the manuscript. Gaoqiang Zhang and Jiajia Zhang evaluated the literatures. Bo Dong and Junyu Bai extract data and performed the statistical analysis. All authors read and approved the final manuscript.

Funding

This study was supported by Special Fund for Local Science and Technology Development Guided by the Chinese Government (2018L3011), Fujian natural science foundation general project (2019J01804), Major projects of Key project of Fujian provincial youth natural fund (JZ160481) and Education and scientific research projects of young and middle-aged teachers in Fujian Province (JAT160483).

Availability of data and materials

The data analyzed during the current study was available from the corresponding author on reasonable request.

Ethics approval and consent to participate

Informed consent was obtained from all individual participants included in the study.

Consent for publication

No applicable.

Competing interests

The authors declare that they have no conflict of interest.

Footnotes

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Contributor Information

Bo Dong, Email: bodong1983@qq.com.

Weiming Lin, Email: wmlin925@126.com.

References

  • 1.Decaro N, Buonavoglia C. Canine parvovirus—a review of epidemiological and diagnostic aspects, with emphasis on type 2c. Vet Microbiol. 2012;155(1):1–12. doi: 10.1016/j.vetmic.2011.09.007. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 2.Zhong Z, Liang L, Zhao J, et al. First isolation of new canine parvovirus 2a from Tibetan mastiff and global analysis of the full-length VP2 gene of canine parvoviruses 2 in China. Int J Mol Sci. 2014;15(7):12166–12187. doi: 10.3390/ijms150712166. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3.Cavalli A, Desario C, Kusi I, et al. Detection and genetic characterization of Canine parvovirus and Canine coronavirus strains circulating in district of Tirana in Albania. J Vet Diagn Invest. 2014;26(4):563–566. doi: 10.1177/1040638714538965. [DOI] [PubMed] [Google Scholar]
  • 4.Miranda C, Thompson G. Canine parvovirus: the worldwide occurrence of antigenic variants. J Gen Virol. 2016;97(9):2043–2057. doi: 10.1099/jgv.0.000540. [DOI] [PubMed] [Google Scholar]
  • 5.Bandai C, Ishiguro S, Masuya N, et al. Canine coronavirus infections in Japan: virological and epidemiological aspects. J Vet Med Sci. 1999;61(7):731–736. doi: 10.1292/jvms.61.731. [DOI] [PubMed] [Google Scholar]
  • 6.Zhao Y, Lin Y, Zeng X, et al. Genotyping and pathobiologic characterization of canine parvovirus circulating in Nanjing. Chin Virol J. 2013;10:272. doi: 10.1186/1743-422X-10-272. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 7.Zhao H, Wang J, Jiang Y, et al. Typing of canine parvovirus strains circulating in North-East China. Transbound Emerg Dis. 2017;64(2):495–503. doi: 10.1111/tbed.12390. [DOI] [PubMed] [Google Scholar]
  • 8.Wang J, Lin P, Zhao H, et al. Continuing evolution of canine parvovirus in China: isolation of novel variants with an Ala5Gly mutation in the VP2 protein. Infect Genet Evol. 2016;38:73–78. doi: 10.1016/j.meegid.2015.12.009. [DOI] [PubMed] [Google Scholar]
  • 9.Truyen U, Parrish CR. Canine and feline host ranges of canine parvovirus and feline panleukopenia virus: distinct host cell tropisms of each virus in vitro and in vivo. J Virol. 1992;66(9):5399–5408. doi: 10.1128/JVI.66.9.5399-5408.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 10.Bolles M, Donaldson E, Baric R. SARS-CoV and emergent coronaviruses: viral determinants of interspecies transmission. Curr Opin Virol. 2011;1(6):624–634. doi: 10.1016/j.coviro.2011.10.012. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 11.Azhar EI, El-Kafrawy SA, Farraj SA, et al. Evidence for camel-to-human transmission of MERS coronavirus. N Engl J Med. 2014;370(26):2499–2505. doi: 10.1056/NEJMoa1401505. [DOI] [PubMed] [Google Scholar]
  • 12.Pawestri HA, Nugraha AA, Han AX, et al. Genetic and antigenic characterization of influenza A/H5N1 viruses isolated from patients in Indonesia, 2008–2015. Virus Genes. 2020;56(4):417–429. doi: 10.1007/s11262-020-01765-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13.Appel MJG, Scott FW, Carmichael LE. Isolation and immunisation studies of a canine parvo-like virus from dogs with haemorrhagic enteritis. Vet Rec. 1979;105:156–159. doi: 10.1136/vr.105.8.156. [DOI] [PubMed] [Google Scholar]
  • 14.Zhuang QY, Qiu Y, Pan ZH, et al. Genome sequence characterization of canine parvoviruses prevalent in the Sichuan province of China. Transbound Emerg Dis. 2019;66(2):897–907. doi: 10.1111/tbed.13100. [DOI] [PubMed] [Google Scholar]
  • 15.Tanner WD, Toth DJ, Gundlapalli AV. The pandemic potential of avian influenza A (H7N9) virus: a review. Epidemiol Infect. 2015;143(16):3359–3374. doi: 10.1017/S0950268815001570. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 16.Yan HX, Xu HF, He WJ, et al. Phylogenetic analysis of HA and NA genes of influenza H1N1 viruses from 1918 to 2017. Acta Virol. 2019;63(2):195–202. doi: 10.4149/av_2019_211. [DOI] [PubMed] [Google Scholar]
  • 17.Zhao Z, Liu H, Ding K, et al. Occurrence of canine parvovirus in dogs from Henan province of China in 2009–2014. BMC Vet Res. 2016;12(1):138. doi: 10.1186/s12917-016-0753-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 18.Zhao CG, Wang TK, Gu JF, et al. Epidemic characteristics of canine parvovirus disease in Changping District, Beijing. Anim Husb Vet Med. 2013;45(11):77–79. [Google Scholar]
  • 19.Stroup DF, Berlin JA, Morton SC, et al. Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis of Observational Studies in Epidemiology (MOOSE) group. JAMA. 2000;283(15):2008–2012. doi: 10.1001/jama.283.15.2008. [DOI] [PubMed] [Google Scholar]
  • 20.Shamseer L, Moher D, Clarke M, et al. Group, preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015: elaboration and explanation. BMJ. 2015;350:g7647. doi: 10.1136/bmj.g7647. [DOI] [PubMed] [Google Scholar]
  • 21.Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med. 2002;21:1539–1558. doi: 10.1002/sim.1186. [DOI] [PubMed] [Google Scholar]
  • 22.Wu J, Gao XT, Hou SH, et al. Molecular epidemiological and phylogenetic analyses of canine parvovirus in domestic dogs and cats in Beijing, 2010–2013. J Vet Med Sci. 2015;77(10):1305–1310. doi: 10.1292/jvms.14-0665. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 23.Li GK, Chen XX, Chen AX. Analysis on the prevalence of canine parvovirus in Liuzhou from 2004 to 2009. Guangxi Anim Sci Vet Med. 2010;26(4):203–204. [Google Scholar]
  • 24.Zhang J, Xia YH, Zhou HZ, et al. Investigation on the prevalence of dog disease in Beijing, China. Chin J Prev Vet Med. 2010;3:894–898. [Google Scholar]
  • 25.Bai LH. The molecular epidemiological investigation of canine parvovirus infection in Beijing. Chin Acad Agric Sci. 2011. p. 15–6 (in Chinese).
  • 26.Zhang WW, Zhang ZX, Sun YZ, et al. Epidemiological features of Canine Parvovirus(CPV)in Beijing, China. Chin J Vet Med. 2016;52(3):82–84. [Google Scholar]
  • 27.Chen XR, Yang J, Zhang YH, et al. Molecular epidemiological investigation of canine parvovirus in Chengdu area. Chin Liv Pou Bre. 2019;09:3–5. [Google Scholar]
  • 28.Fu Y. Etiological investigation of canine parvovirus and canine distemper virus in Changchun of Jilin Province. Univ Jilin Agric. 2017 (in Chinese).
  • 29.Zhang KM. Epidemiological Survey of Canine Common Viral Diarrhea in Jilin. Agr: China. Univ. of. Jilin; 2019. [Google Scholar]
  • 30.Zhuo GR, Di HS, Lu W, et al. Investigation and treatment of canine parvovirus disease in Taizhou Jiangsu Province. Jiangsu Agric Sci. 2015;43(5):216–219. [Google Scholar]
  • 31.Jing SY, Zhao QX, Song SB, et al. Investigation and analysis of canine parvovirus disease in Lanzhou city. Anim Husb Vet Med. 2018;37(2):60–65. [Google Scholar]
  • 32.Zhang CX. Statistical analysis of clinical cases of dogs and cats in a pet hospital. Heilongjiang Anim Sci Vet Med. 2013;10:100–103. [Google Scholar]
  • 33.Lou HJ, Yan ZQ. Investigation on the prevalence of dog disease in nanjing, jiangsu province, China. Kennel Tech. 2010;2:12–14. [Google Scholar]
  • 34.Tai D, Wei P, Wu WZ, et al. Clinical investigation of canine parvovirus disease in a pet hospital in Nanjing. Chin JVet Med. 2008;44(10):57. [Google Scholar]
  • 35.Huang HX, Wang P, Liu LK, et al. Epidemiological investigation of canine parvovirus disease in Nanning. Guangxi Anim Sci Vet Med. 2018;34(2):76–79. [Google Scholar]
  • 36.Kang YL. Epidemiological investigation of canine parvovirus disease in Qingdao. Shandong Anim Sci Vet Med. 2016;37(3):40–41. [Google Scholar]
  • 37.Yang JF. Research on the clinical characteristic of canine parvovirus disease. In: The 13th national symposium on veterinary surgery the 1st symposium on small animal medicine and the 3rd symposium on cow diseases. 2006; p 430–4 (in Chinese).
  • 38.Yang CL. Epidemiological investigation of canine parvovirus disease. Vet Tribune. 2012, p 82–3 (in Chinese).
  • 39.Geng ZX, Shi YS, Zheng YP, et al. Epidemiological investigation of canine parvovirus. Chin Anim Husb Vet Med. 2009;36(11):135–137. [Google Scholar]
  • 40.Fu LJ, Pei XD, Wang XY, et al. Investigation and epidemic analysis of canine parvovirus disease. Chin Anim Husb Vet Med. 2012;39(5):225–227. [Google Scholar]
  • 41.Yang QZ, Fu L. Analysis and analysis of the situation and flow of the disease in dogs. Modern Anim husb. 2014;06:62–63. [Google Scholar]
  • 42.Zeng JH. Analysis of clinical condition and experiences of diagnose and treatement in canine parvovirus infection. Northwest A&F University. 2013 (in Chinese).
  • 43.Zhao N, Guo JN. Epidemiological investigation and treatment of canine parvovirus disease. Hubei Anim Sci Vet Med. 2013;34(3):10–13. [Google Scholar]
  • 44.Lin Y, Di QH, Fu HB, et al. Establishment and application of double PCR for canine parvovirus and canine coronavirus. Adv Anim Med. 2011;32(10):71–74. [Google Scholar]
  • 45.Sun YZ, Dai YL, Ni XX, et al. Analysis on epidemic features of canine multi-pathogen infectious diseases in Qingdao City of Shandong Province. Chin Anim Insp. 2016;33(3):14–16. [Google Scholar]
  • 46.Ju HB, Chen G, Niu GB, et al. Investigation of canine distemper and canine parvovirus infection in Shanghai. Chin J Anim Infect Dis. 2012;20(4):69–73. [Google Scholar]
  • 47.Chen HL. Investigation of common canine diseases in Shaoxing Zhejiang. Anim Sci Vet Med. 2012;04:40–41. [Google Scholar]
  • 48.Zan F, Bai HX, Cui J. Investigation and prevention control measures of common infectious diseases in canine in Tianjin area. Tianjin Agric Sci. 2017;24(4):90–93. [Google Scholar]
  • 49.Luo HQ, Song XZ, Wang QY, et al. Epidemiological investigation of canine parvovirus disease in small animal hospital in Wenzhou area. Acta Agri Zhejiangensis. 2014;26(4):887–891. [Google Scholar]
  • 50.Ma JP, Wang ZG. Epidemiological investigation and treatment of canine parvovirus disease in Ulanqab city. Heilongjiang Anim Sci Vet Med 2014; 06:137–138, 230 (in Chinese).
  • 51.Zhao WW. The prevalence and analysis of canine infectious diseases in Wuhan in recent years. Hunan Agric Univ. 2014 (in Chinese).
  • 52.Chen ZR, Chen JH, Li MJ, et al. Epidemic situation and prevention of canine parvovirus in Xichang. Guangdong Anim Husb Vet Sci Technol. 2016;41(2):39–42. [Google Scholar]
  • 53.Han GQ. Epidemiology investigation of canine distemper and canine parvovirus disease of korla of Xinjiang. Shihezi Univ. 2014 (in Chinese).
  • 54.Wu J, Liu Q, Hou Y, et al. Epidemiological investigations of canine parvoviral disease in Shihezi City of Xinjiang. Beijing Agric. 2011;05:80–82. [Google Scholar]
  • 55.Ye Y. Investigation of canine pox fever, canine parvovirus disease and coronavirus disease in Changsha and study of therapeutic effects of traditional Chinese medicine. Hunan Agri Univ. 2016 (in Chinese).
  • 56.Wu HG, Wang XM, Liu JN, et al. Epidemic characteristics of canine parvovirus disease in Zhengzhou city. Anim Husb Vet Med. 2012;44(5):111–112. [Google Scholar]
  • 57.Carman PS, Povey RC. Pathogenesis of canine parvovirus-2 in dogs: haematology, serology and virus recovery. Res Vet Sci. 1985;38:134–140. doi: 10.1016/S0034-5288(18)31816-2. [DOI] [PubMed] [Google Scholar]
  • 58.Nelson DT, Eustis SL, McAdaragh JP, et al. Lesions of spontaneous canine viral enteritis. Vet Pathol. 1979;16:680–686. doi: 10.1177/030098587901600606. [DOI] [PubMed] [Google Scholar]
  • 59.Parrish CR. Pathogenesis of feline panleukopenia virus and canine parvovirus. Baillieres Clin Haematol. 1995;8:57–71. doi: 10.1016/S0950-3536(05)80232-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 60.Xu GM, Cao SF, Che YG, et al. Analysis of the incidence and treatment of 245 ceases of canine parvovirus disease. Anim Husb Vet Med. 2017;49:117–119. [Google Scholar]
  • 61.Schmitz S, Coenen C, König M, Thiel HJ, Neiger R. Comparison of three rapid commercial Canine parvovirus antigen detection tests with electron microscopy and polymerase chain reaction. J Vet Diagn Invest. 2009;21(3):344–345. doi: 10.1177/104063870902100306. [DOI] [PubMed] [Google Scholar]
  • 62.Decaro N, Elia G, Martella V, et al. A real-time PCR assay for rapid detection and quantitation of canine parvovirus type 2 in the feces of dogs. Vet Microbiol. 2005;105(1):19–28. doi: 10.1016/j.vetmic.2004.09.018. [DOI] [PubMed] [Google Scholar]
  • 63.Kantere MC, Athanasiou LV, Spyrou V, et al. Diagnostic performance of a rapid in-clinic test for the detection of Canine Parvovirus under different storage conditions and vaccination status. J Virol Methods. 2015;215–216:52–55. doi: 10.1016/j.jviromet.2015.02.012. [DOI] [PMC free article] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

The data analyzed during the current study was available from the corresponding author on reasonable request.

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