BioMed Research International

BioMed Research International / 2015 / Article

Research Article | Open Access

Volume 2015 |Article ID 460473 | https://doi.org/10.1155/2015/460473

Xiaoting Ni, Siyuan Qin, Zhilong Lou, Hongrui Ning, Xiaolin Sun, "Seroprevalence and Risk Factors of Chlamydia Infection in Domestic Rabbits (Oryctolagus cuniculus) in China", BioMed Research International, vol. 2015, Article ID 460473, 5 pages, 2015. https://doi.org/10.1155/2015/460473

Seroprevalence and Risk Factors of Chlamydia Infection in Domestic Rabbits (Oryctolagus cuniculus) in China

Academic Editor: Kent M. Reed
Received06 Feb 2015
Revised14 Mar 2015
Accepted23 Mar 2015
Published05 Apr 2015

Abstract

Chlamydia spp. are obligate intracellular bacteria distributed all over the world, known to cause various forms of diseases in animals and humans. In the present study, a serological survey was conducted to detect the seroprevalence and risk factors associated with rabbit chlamydiosis in northeast China, including Liaoning province, Jilin province, Heilongjiang province, and Inner Mongolia Autonomous Region. Antibodies to Chlamydia were determined by indirect hemagglutination assay (IHA). The overall seroprevalence was estimated at 17.88% in total of 800 blood samples. The Chlamydia seroprevalence varied in domestic rabbits from different factors, and genders of domestic rabbits were considered as major risk factors associated with Chlamydia infection. Our study revealed a widespread and high prevalence of Chlamydia infection in domestic rabbits in northeast China, with higher exposure risk in female domestic rabbits. These findings suggested the potential importance of domestic rabbits in the transmission of zoonotic Chlamydia infection, and thus Chlamydia should be taken into consideration in diagnosing rabbit diseases. To our knowledge, there is no report of Chlamydia infection in domestic rabbits in China and the results extend the host range for Chlamydia, which has important implications for public health and the local economy.

1. Introduction

Chlamydia is a genus comprising important zoonotic obligate intracellular pathogens that affect humans and a wide range of animals [1, 2]. Chlamydia infection can cause various diseases in nonhuman mammals and birds, including conjunctivitis, atypical pneumonia, enteritidis, endocarditis, and even abortion, resulting in serious economic losses [36]. Several Chlamydia species are known to infect humans and are of serious public health significance because they may result in atherosclerosis, coronary heart disease, pneumonia, and other severe diseases [7]. Chlamydia abortus and Chlamydia psittaci are of particular importance because they can cause abortion and psittacosis, respectively, in animals, birds and humans. In Egypt, a study revealed that in symptomatic gynecologically diseased women the seroprevalence of Chlamydia psittaci was 50.0%, Chlamydia abortus was 35.7%, and Chlamydia trachomatis was 15.2% [8], and in the genital tract of cattle the main Chlamydiaceae were Chlamydia psittaci and Chlamydia abortus [9]. The animal diseases caused by these microorganisms should be given more attention due to their zoonotic potential [1, 7, 10].

The breeding of domestic rabbits (Oryctolagus cuniculus) for human consumption has a long radition in China, and rabbit industry is one of green economy industries, which is emerging and promising, with broad space for development and has gone through a long glorious history and its products have brought great wealth to the rural people in China. At present, China plays an important role of breeding rabbits, and domestic rabbits yield high quality meat and hair which are transported to many parts of home and abroad. However, disease is the main challenge for rabbit industry [11, 12]. To date, there is little information about the seroprevalence of Chlamydia and the risk factors associated with Chlamydia infection in domestic rabbits in the world. Thus, the present study was aimed at determining the seroprevalence of Chlamydia infection in domestic rabbits in northeast China and identifying factors associated with the presence of Chlamydia antibodies in domestic rabbits in the study area.

2. Materials and Methods

2.1. Ethics Statement

This study was approved by the Animal Ethics Committee of Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences (Approval no. LVRIAEC2013-010). The domestic rabbits, from which the serum samples were collected, were handled in accordance with good animal practices required by the Animal Ethics Procedures and Guidelines of the People’s Republic of China.

2.2. Collection and Preparation of Serum Samples

A total of eight hundred domestic rabbits were randomly sampled from Liaoning province, Jilin province, Heilongjiang province, and Inner Mongolia Autonomous Region. From each rabbit, approximately 2 mL of blood was collected from the marginal ear vein or postmortem. After centrifugation at 3,000 rpm for 10 min, sera were collected and stored at −20°C until use. Handling of rabbits was in compliance with the Animal Ethics Procedures and Guidelines of the People’s Republic of China. Information about species, ages, geographic origin, and gender was acquired from breeders.

2.3. Serological Examination

Antibodies to Chlamydia were tested by indirect hemagglutination antibody (IHA) using a commercially marketed kit (Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, Gansu Province, China). The procedures are according to the manufacturer’s instructions and previous descriptions [13, 14]. The IHA kit was performed following the standard protocol recommended by Chinese Center for Animal Diseases Prevention and Control, and the sensitivity and specificity of the test are 100% and 95%, respectively [13]. The sensitivity and specificity values for the testing kit used in this study have been validated by The Ministry of Agriculture of the People’s Republic of China (NY/T 562–2002). In brief, 75 μL of the IHA dilution solution was transferred into 96 well V-bottomed polystyrene plates with 25 μL of serum added and diluted in a fourfold series from 1 : 4 to 1 : 64. The plates were shaken for 2 min and then incubated at 37°C for 2 h without shaking. The test was considered positive when a layer of agglutinated erythrocytes was formed in wells at dilutions of 1 : 16 or higher, and positive and negative controls were included in each test. Those sera which showed dubious results were picked out for retest.

2.4. Statistical Analyses

Regions, genders, age groups, and breeds of rabbits were analyzed in a multivariable logistic regression model, and probability () value < 0.05 was considered as statistically significant. Odds ratios (OR) with 95% confidence intervals are also calculated. All statistical analyses were performed using the PASW Statistics 18.0 (SPSS Inc., IBM Corporation, Somers, NY).

3. Results

Antibodies to Chlamydia were detected in 143 of 800 (17.88%, 95% CI 15.22–20.53) domestic rabbits. Of these, antibody titers were 1 : 16 in 22, 1 : 32 in 18, 1 : 64 in 33, 1 : 128 in 30, 1 : 256 in 27, 1 : 512 in 9, and 1 : 1024 in 4, respectively (Table 3). The Chlamydia seroprevalence varied in domestic rabbits from different regions, ranging from 15.00% (95% CI 10.05–19.95) to 20.50% (95% CI 14.91–26.10) (Table 1), but the differences were not significantly different. The juvenile rabbits had higher seroprevalence (19.83%) than that in adults (15.18%). The seroprevalence of Chlamydia was diverse in different breeds of domestic rabbits; the highest level was 20.88% in Chinese White Rabbits, followed by 17.61% in New Zealand Rabbits and 15.20% in California Rabbits (Table 1). However, the differences were not statistically significant ().


FactorCategoryNumber examinedNumber positive% (95% CI)

AgeJuvenile4649219.83 (16.20–23.46)
Adult3365115.18 (11.34–19.02)

GenderMale3194514.11 (10.29–17.93)
Female4819820.34 (16.78–23.97)

BreedChinese White Rabbit2495220.88 (15.84–25.93)
California Rabbit2503815.20 (10.75–19.65)
New Zealand Rabbit3015317.61 (13.31–21.91)

RegionLiaoning province2003919.50 (14.01–24.99)
Jilin province2004120.50 (14.91–26.10)
Heilongjiang province2003316.50 (11.36–21.64)
Inner Mongolia Autonomous Region2003015.00 (10.05–19.95)

Total80014317.88 (15.22–20.53)

In terms of gender, seroprevalence of Chlamydia in female (20.34%) was higher than that in male (14.11%), and gender was considered as major risk factors associated with Chlamydia infection in domestic rabbits (, Table 2). And the risk of Chlamydia infection in female was more than 1.56-fold increase (OR = 1.56, 95% CI = 1.06–2.29, ) compared to Chlamydia infection in male (Table 2).


GenderNumber testedNumber positivePrevalence (%)OR (95% CI)P value

Male3194514.11 (10.29–17.93)Reference
Female4819820.34 (16.78–23.97)1.56 (1.06–2.29)0.024


Biometric dataCategory Antibody titers Number positive Number testedPrevalence (%)
1 : 161 : 321 : 641 : 1281 : 2561 : 5121 : 1024

Gender Female 1716201816749831920.34
Male52131211204548114.11

Age Infancy668136214217524.00
Juvenile8612910415028917.30
Adult8613811325133615.18

RegionLiaoning province 588107103920019.50
Jilin province64899324120020.50
Heilongjiang province 641146203320016.50
Inner Mongolia Autonomous Region52675323020015.00

BreedChinese White Rabbit9614810415224920.88
California Rabbit65889113825015.20
New Zealand Rabbit7711148425330117.61

Total22183330279414380017.88

4. Discussion

Chlamydia spp. are gram-negative bacteria that cause various significant diseases in humans and animals all over the world, leading to health problems and serious economic losses. In the present study, the overall seroprevalence of Chlamydia infection in domestic rabbits was 17.88%, which was higher than that observed previously in cats (5.9%) [7], dogs (12.1%) [15], pet birds (10.80%) [16], pigeon (6.80%) [17], red deer (9.60%) [18], cattle (4.75%) [19] and dairy cattle (7.25%) [20], but lower than in sows (62.70%) [21], wild boar (63.60%) [22], and feral Canada geese (93.80%) [23] using the same serological test (IHA) in China. Differences in Chlamydia seroprevalence are likely due to differences in animal welfares, animal categories, climates, and husbandry practices. Today, there is an increasing demand for rabbit meat in China, and the safety and sanitary quality of meat pose a potential threat to local residents and other people in exported regions. Therefore, it is important to understand the extent of Chlamydia infection in domestic rabbits in China.

In the present study, Chlamydia seroprevalence in juvenile rabbits (19.83%) was higher than that in adult rabbits (15.18%), but the differences were not statistically significant (), which was consistent with the previous study [14]. And the reason why juveniles were more susceptible than adults and subadults may be that the juveniles had lower immunity compared with adults. Moreover, the Chlamydia seroprevalence between male and female rabbits was significantly different (), implying that gender is a crucial factor for Chlamydia infection in domestic rabbits.

This study revealed that gender is a significant risk factor for Chlamydia prevalence in domestic rabbits, with females having a higher seroprevalence than males. The Chlamydia seroprevalence in male and female domestic rabbit was 14.11% and 20.34%, respectively. This tendency is consistent with the studies of Tibetan pigs (females, 17.61%; males, 12.72%) [24] and also concurs with that observed in pet parrots (females, 41.22%; males, 30.06%) [14], in wild boars in Germany (females, 83.3%; males, 42.9%) [25] and Italy (females, 45.95%; males, 38.8%) [22]. Females and males were exposed to Chlamydia in the same environment, and in our study females are more sensitive to the pathogen than males for each of the breeds in each region group, which may be due to variation in immune response or antibody persistence rates between females and males.

In the present study, there was no significant difference in Chlamydia seroprevalence in rabbits in different provinces (). The statistically similar seropositivity suggests that the pathogen could be mostly transmitted by the direct contact route in domestic rabbits, which is little affected by environmental change. Thus, further studies are needed to illuminate the potential effect of Chlamydia on the geographical origin of domestic rabbits.

Chlamydia has been reported to be associated with abortion in horses, rabbits, guinea pigs, mice, and pigs [26]. More importantly, Chlamydia can cause devastating consequences of infertility, ectopic pregnancy, chronic pelvic pain, or even abortion in humans [8, 27], especially for people exposed to Chlamydia infection by working with rabbits, which increased the possibility to be infected [14, 28]. Thus, further studies are needed to illuminate the potential effect of Chlamydia on reproduction of domestic rabbits. Moreover, serological investigation of Chlamydia infection in human (particularly pregnant women) working in rabbit farms in northeast China is also warranted.

Among different breeds of domestic rabbits, Chlamydia seroprevalence in Chinese White Rabbit (20.88%) was higher than that in New Zealand Rabbit (17.61%) and California Rabbit (15.20%), but the differences were not statistically significant, which was consistent with the previous study, and the animal species factor was calculated and was found to be of no significance [29]. Further investigations should be studied about the correlation of Chlamydia infection with the animal species.

In conclusion, the results of the present study revealed that Chlamydia infection in domestic rabbits is highly prevalent in northeast China, but this severe situation has been neglected in the past. Therefore, it is important to carry out integrated control strategies and measures to prevent and control Chlamydia infection in domestic rabbits in China. This is the first report of Chlamydia seroprevalence in domestic rabbits in China.

Conflict of Interests

The authors declare that they have no competing interests.

Acknowledgments

Project support was provided by study on the distribution of animal parasitic helminths and molecular taxonomy of Tianzhu White Yak (31460659) and Quality Inspection Special Public Welfare Industry Research (201410061).

References

  1. D. Longbottom and L. J. Coulter, “Animal chlamydioses and zoonotic implications,” Journal of Comparative Pathology, vol. 128, no. 4, pp. 217–244, 2003. View at: Publisher Site | Google Scholar
  2. G. Rohde, E. Straube, A. Essig, P. Reinhold, and K. Sachse, “Chlamydial zoonoses,” Deutsches Ärzteblatt International, vol. 107, no. 10, pp. 174–180, 2010. View at: Publisher Site | Google Scholar
  3. M. Eidson, “Psittacosis/avian chlamydiosis,” Journal of the American Veterinary Medical Association, vol. 221, no. 12, pp. 1710–1712, 2002. View at: Publisher Site | Google Scholar
  4. G. Entrican and N. M. Wheelhouse, “Immunity in the female sheep reproductive tract,” Veterinary Research, vol. 37, no. 3, pp. 295–309, 2006. View at: Publisher Site | Google Scholar
  5. Y. Pannekoek, C. Visser, B. Duim, and E. R. Heddema, “Chlamydophila psittaci infections in The Netherlands,” Drugs of Today, vol. 45, pp. 151–157, 2009. View at: Google Scholar
  6. K. Verminnen and D. Vanrompay, “Chlamydophila psittaci infections in Turkeys: overview of economic and zoonotic importance and vaccine development,” Drugs of Today, vol. 45, pp. 147–150, 2009. View at: Google Scholar
  7. S.-M. Wu, S.-Y. Huang, M.-J. Xu, D.-H. Zhou, H.-Q. Song, and X.-Q. Zhu, “Chlamydia felis exposure in companion dogs and cats in Lanzhou, China: a public health concern,” BMC Veterinary Research, vol. 9, article 104, 2013. View at: Publisher Site | Google Scholar
  8. K. M. Osman, H. A. Ali, J. A. Eljakee, M. M. Gaafar, and H. M. Galal, “Antimicrobial susceptibility and molecular typing of multiple Chlamydiaceae species isolated from genital infection of women in Egypt,” Microbial Drug Resistance, vol. 18, no. 4, pp. 440–445, 2012. View at: Publisher Site | Google Scholar
  9. K. M. Osman, H. A. Ali, J. A. ElJakee, and H. M. Galal, “Chlamydiaceae in riverine buffalo (Bubalus bubalis) and cows (Bos taurus) in Egypt with and without signs of reproductive disease,” New Zealand Veterinary Journal, vol. 60, no. 4, pp. 228–233, 2012. View at: Publisher Site | Google Scholar
  10. D. S. A. Beeckman and D. C. G. Vanrompay, “Zoonotic Chlamydophila psittaci infections from a clinical perspective,” Clinical Microbiology and Infection, vol. 15, no. 1, pp. 11–17, 2009. View at: Publisher Site | Google Scholar
  11. Y. F. Chen, X. P. Xie, and S. K. Sun, “The present situation and development countermeasures of Chinese rabbit industry,” Modern Agriculture, vol. 12, pp. 6–7, 2010 (Chinese). View at: Google Scholar
  12. E. V. Boiko, A. L. Pozniak, D. S. Maltsev, A. A. Suetov, and I. V. Nuralova, “Chronic ocular Chlamydia trachomatis infection in rabbits: clinical and histopathological findings in the posterior segment,” Investigative Ophthalmology & Visual Science, vol. 55, no. 2, pp. 1176–1183, 2014. View at: Publisher Site | Google Scholar
  13. Q. Chen, X. Gong, F. Zheng, X. Cao, Z. Li, and J. Zhou, “Seroprevalence of Chlamydophila abortus infection in yaks (Bos grunniens) in Qinghai, China,” Tropical Animal Health and Production, vol. 46, no. 3, pp. 503–507, 2014. View at: Publisher Site | Google Scholar
  14. N. Z. Zhang, X. X. Zhang, D. H. Zhou et al., “Seroprevalence and genotype of Chlamydia in pet parrots in China,” Epidemiology & Infection, vol. 143, no. 1, pp. 55–61, 2015. View at: Publisher Site | Google Scholar
  15. Y. M. Tian, J. F. Cao, D. H. Zhou et al., “Seroprevalence and risk factors of Chlamydia infection in dogs in Southwestern China,” Acta Tropica, vol. 130, no. 1, pp. 67–70, 2014. View at: Publisher Site | Google Scholar
  16. W. Cong, S. Y. Huang, X. X. Zhang et al., “Chlamydia psittaci exposure in pet birds,” Journal of Medical Microbiology, vol. 63, no. 4, pp. 578–581, 2014. View at: Publisher Site | Google Scholar
  17. T. Stenzel, D. Pestka, and D. Choszcz, “The prevalence and genetic characterization of Chlamydia psittaci from domestic and feral pigeons in Poland and the correlation between infection rate and incidence of pigeon circovirus,” Poultry Science, vol. 93, no. 12, pp. 3009–3016, 2014. View at: Publisher Site | Google Scholar
  18. A. di Francesco, M. Donati, S. Nicoloso et al., “Chlamydiosis: Seroepidemiologic survey in a red deer (Cervus elaphus) population in Italy,” Journal of Wildlife Diseases, vol. 48, no. 2, pp. 488–491, 2012. View at: Publisher Site | Google Scholar
  19. K. Wilson, D. Sammin, S. Harmeyer, M. Nath, M. Livingstone, and D. Longbottom, “Seroprevalence of chlamydial infection in cattle in Ireland,” The Veterinary Journal, vol. 193, no. 2, pp. 583–585, 2012. View at: Publisher Site | Google Scholar
  20. D. H. Zhou, F. R. Zhao, H. Y. Xia et al., “Seroprevalence of chlamydial infection in dairy cattle in Guangzhou, Southern China,” Irish Veterinary Journal, vol. 66, no. 1, article 2, 2013. View at: Publisher Site | Google Scholar
  21. X. X. Zhang, R. C. Li, G. H. Liu et al., “High seroprevalence of Chlamydia infection in sows in Hunan province, subtropical China,” Tropical Animal Health and Production, vol. 46, no. 4, pp. 701–704, 2014. View at: Publisher Site | Google Scholar
  22. A. di Francesco, M. Donati, F. Morandi et al., “Seroepidemiologic survey for Chlamydia suis in wild boar (Sus scrofa) populations in Italy,” Journal of Wildlife Diseases, vol. 47, no. 3, pp. 709–712, 2011. View at: Publisher Site | Google Scholar
  23. V. Dickx, I. D. Kalmar, P. Tavernier, and D. Vanrompay, “Prevalence and genotype distribution of Chlamydia psittaci in feral Canada geese (Branta canadensis) in Belgium,” Vector-Borne and Zoonotic Diseases, vol. 13, no. 6, pp. 382–384, 2013. View at: Publisher Site | Google Scholar
  24. N.-Z. Zhang, D.-H. Zhou, X.-C. Shi et al., “First report of chlamydiaceae seroprevalence in Tibetan pigs in Tibet, China,” Vector-Borne and Zoonotic Diseases, vol. 13, no. 3, pp. 196–199, 2013. View at: Publisher Site | Google Scholar
  25. H. Hotzel, A. Berndt, F. Melzer, and K. Sachse, “Occurrence of Chlamydiaceae spp. in a wild boar (Sus scrofa L.) population in Thuringia (Germany),” Veterinary Microbiology, vol. 103, no. 1-2, pp. 121–126, 2004. View at: Publisher Site | Google Scholar
  26. K. Schautteet and D. Vanrompay, “Chlamydiaceae infections in pig,” Veterinary Research, vol. 42, article 29, 2011. View at: Publisher Site | Google Scholar
  27. A. C. Ikeme, H. U. Ezegwui, L. C. Ikeako, I. Agbata, and E. Agbata, “Seroprevalence of Chlamydia trachomatis in Enugu, Nigeria,” Nigerian Journal of Clinical Practice, vol. 14, no. 2, pp. 176–180, 2011. View at: Publisher Site | Google Scholar
  28. D. Baud, L. Regan, and G. Greub, “Emerging role of Chlamydia and Chlamydia-like organisms in adverse pregnancy outcomes,” Current Opinion in Infectious Diseases, vol. 21, no. 1, pp. 70–76, 2008. View at: Publisher Site | Google Scholar
  29. K. M. Osman, H. A. Ali, J. A. Eljakee, and H. M. Galal, “Prevalence of Chlamydophila psittaci infections in the eyes of cattle, buffaloes, sheep and goats in contact with a human population,” Transboundary and Emerging Diseases, vol. 60, no. 3, pp. 245–251, 2013. View at: Publisher Site | Google Scholar

Copyright © 2015 Xiaoting Ni et al. 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.


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