Home First report of Chlamydia psittaci seroprevalence in black-headed gulls (Larus ridibundus) at Dianchi Lake, China
Article Open Access

First report of Chlamydia psittaci seroprevalence in black-headed gulls (Larus ridibundus) at Dianchi Lake, China

  • Hua Chang , Jiangqiang Han , Yan Yang , Gang Duan , Fengcai Zou , Xun Xiang EMAIL logo and Feiyan Dai EMAIL logo
Published/Copyright: August 9, 2018

Abstract

Chlamydiosis is an important zoonosis which can transmit from birds to humans, and investigation first reported the seroprevalence of Chlamydia psittaci in black-headed gulls (Larus ridibundus) at the Dianchi Lake, China. A total of 1029 serum samples collected from black-headed gulls between 2012-2015 were analyzed. The gulls were randomly caught and blood collected at Dianchi Lake, China. All the samples were analyzed for the presence of antibodies to C. psittaci by indirect hemagglutination assay (IHA). In this survey, the total infection rate was 11.86% (122/1029). The results of the present survey documented the existence of relatively high C. psittaci seroprevalence in black-headed gulls, which have a potential risk to the wild bird health and human health. Comprehensive practical control approaches and measures should be executed.

1 Introduction

Chlamydiosis is a naturally occurring zoonotic disease that causes serious psittacosis, myocarditis, and pneumonia in humans [1]. Chlamydia psittaci is an obligate intracellular bacterium that is evident to be responsible for the infection of different species (such as parrots, pigeons, doves, waterfowl, songbirds and the like) of wild birds and humans [2]. The oldest report of chlamydiosis can be dated as far back to 1880, when humans were infected by C. psittaci in a case report within Switzerland [3]. Upon further studies, researchers isolated the same pathogen in certain patients and amazon parrots, which led to the awareness of posing public health concerns of Chlamydia in humans and animals (such as infected avian and birds) [4, 5, 6, 7]. C. psittaci can be detected in the droppings of infected birds, and the bacterium can remain infectious in the environment over months [8]. In addition, wild birds usually act as carrier during long-distance migration; therefore, a portion of birds could contribute to the potential interspecies and intraspecies transmission of Chlamydiosis [9]. Human infection usually occurs when a person inhales the bacterium shed in faeces and secretions of infected birds [10]. One important avian carrier is the black-headed gulls, a species of migratory birds distributed in Eurasia and along the east coast of North America. During the winter season, they migrate to North Africa, the Philippines, Japan, or China from Siberia. Black-headed gulls could potentially be hosts of C. psittaci and act as notable carriers in spreading Chlamydiosis via seagulls to humans. However, no information is available regarding the seroprevalence of Chlamydia infection in the migratory Black-headed gulls located at the Dianchi Lake of China [11]. Black-headed gulls migrate from Siberia to the Dianchi Lake between December and March every year. During these periods, favorable temperatures allow the spread of C. psittaci from black-headed gulls to humans through manual feeding, petting or other direct physical contact [12]. However, the symptoms of Chlamydia in human and animals are mild and difficult to diagnose, thus the C. psittaci infections within the wild birds and general public may be underestimated [13]. C. psittaci is a major concern for public health. If black-headed gulls carry these pathogens, infectious diseases maybe transmitted through water, resulting in infection in humans during the migration process. Thus, the objective of the present study is to determine the seroprevalence of Chlamydial infection in black-headed gulls at the Dianchi Lake, near Kunming of Yunnan Province, southwest of China.

2 Materials and Methods

2.1 Sample Collection

1029 black-headed gulls were caught at Wildlife Bird Observatory near Dianchi Lake between the months of December and February, from 2012 to 2015. The black-headed gulls were taken randomly and blood samples of black-headed gulls were collected from the wing veins of each bird. Blood samples were centrifuged (3,000×g) for 5 min at room temperature (15°C), and serum samples were stored at -20°C for the detection of Chlamydia psittaci antibodies.

Ethical approval

The research related to animals use has been complied with all the relevant national regulations and institutional policies for the care and use of animals. The sampling protocols were approved by an independent Wildlife Animal Care and Ethics Committee of Yunnan Agricultural University (YNPAA2015001).

2.2 Determination of antibodies against C. psittaci

Antibodies to Chlamydia psittaci were determined by indirect hemagglutination assay (IHA) using commercial kit as reported previously [14, 15, 16, 17, 18, 19]. The kit was purchased by Lanzhou Veterinary Research Institute, Chinese Academy of Agriculture Sciences. The detection procedures were carried out as previously reported [17, 18]. In summary, 75 μL of dilution IHA solution was transferred into 96-well V-bottomed polystyrene plates supplemented with 25 μL of serum and diluted in a four-fold series from 1:4 to 1:64 with physiological saline. The plates were shaken for 2 min and incubated at 37oC for 2 h without shaking. The result was considered positive when a layer of agglutinated erythrocytes was formed at dilutions of 1:16 or higher, and both positive and negative controls (blank controls) were included in each test.

3 Results

We tested for anti-C. psittaci antibodies from 1029 serum samples of black-headed gulls using IHA. Out results demonstrated that 112 of 1029 (11.9%) serum samples were positive for chlamydial infection by IHA (Table 1). Furthermore, the prevalence was 6.3% (17/270) in 2012, 10.1% (57/565) in 2013, 20.4% (23/113) in 2014, and 30.9% (25/81) in 2015, respectively, suggesting that the annual prevalence of chlamydial infection among black-headed gulls had increased progressively throughout the years at the Dianchi lake.

Table 1

Prevalence of chlamydial infection among black-headed gulls in the Dianchi Lake, China, examined by indirect hemagglutination test (IHA).

LocationNo. TestedNo. positive(%)Prevalence
Dianchi Lake, China270176.3
5655710.1
1132320.4
812530.9
Total102912211.9

4 Discussion

This data indicates that chlamydial infection was present in migratory black-headed gulls at the Dianchi Lake from Siberia. In this study, the overall Chlamydia seroprevalence in black-headed gulls was 11.9%, comparatively higher to then previous reports of wild birds (5.7% of feral pigeons (Streptopelia chinensis)) in Slovakia [13], 6.0% of wild birds in Poland [14], yet the chlamydia seroprevalence in black-headed gulls is a lower value than that of North Atlantic Seabirds (Morus bassanus, Larus argentatus, Uria aalge), at 18.5% [20]. The difference is likely due to variations in ecologic factors, geography, and hygienic conditions. More importantly, the new findings of our study further indicate that the seroprevalence of C. psittaci in the black-headed gulls of China is increasing. This result urges the implementation of comprehensive control measures to reduce Chlamydiosis prevalence in migratory black-headed gulls.


§These authors equally contributed to this work.


Acknowledgements

This study was supported by the National Natural Science Foundation of China (No. 31760730) and the Open Funds of Key Laboratory of Fujian Province Livestock Epidemic Prevention and Control and Biological technology (No.2016KL01) and Natural Science Foundation of Yunnan Agricultural University (2015ZR04).

  1. Conflict of interest: Authors state no conflict of interest

References

[1] Voigt A, Schöfl G, Saluz HP. The Chlamydia psittaci genome: a comparative analysis of intracellular pathogens. Plos One. 2012;7:e35097.10.1371/journal.pone.0035097Search in Google Scholar

[2] Kaleta EF, Taday EM. Avian host range of Chlamydophila spp. based on isolation, antigen detection and serology. Avian Pathol. 2003; 32(5):435-461.10.1080/03079450310001593613Search in Google Scholar

[3] Harris RL, Williams TW Jr. “Contribution to the Question of Pneumotyphus”: a discussion of the original article by J.Ritter in 1880. Reviews of Infectious Diseases. 1985;7:119-122.10.1093/clinids/7.1.116Search in Google Scholar

[4] Huminer D, Samra Z, Weisman Y, Pitlik S. Family outbreaks of psittacosis in Israel. Lancet. 1988; 2: 615-618.10.1016/S0140-6736(88)90650-2Search in Google Scholar

[5] Rehn M, Ringberg H, Runehagen A, Herrmann B, Olsen B, Petersson AC, et al.. Unusual increase of psittacosis in southern Sweden linked to wild bird exposure, January to April 2013. Euro Surveill. 2013; 18(19):20478.10.2807/ese.18.19.20478-enSearch in Google Scholar

[6] Pannekoek Y, Dickx V, Beeckman DS, Jolley KA, Keijzers WC, Vretou E, et al.. Multi locus sequence typing of Chlamydia reveals an association between Chlamydia psittacigenotypes and host species. PLoS One. 2010; 5(12):e14179.10.1371/journal.pone.0014179Search in Google Scholar PubMed PubMed Central

[7] Branley J, Bachmann NL, Jelocnik M, Myers GS, Polkinghorne A. Australian human and parrot Chlamydia psittaci strains cluster within the highly virulent 6BC clade of this important zoonotic pathogen. Sci Rep. 2016; 6:30019.10.1038/srep30019Search in Google Scholar PubMed PubMed Central

[8] Belchior E, Barataud D, Ollivier R, Capek I, Laroucau K, de Barbeyrac B, et al.. Psittacosis outbreak after participation in a bird fair, Western France, December 2008. Epidemiol Infect. 2011; 139(10):1637-1641.10.1017/S0950268811000409Search in Google Scholar PubMed

[9] Centers for Disease Control and Prevention. Compendium of measures to control Chlamydia psittaci infection among humans (psittacosis) and pet birds (avian chlamydiosis), 2000. MMWR Recomm Rep. 2000; 49(RR-8): 3-17.Search in Google Scholar

[10] Telfer BL, Moberley SA, Hort KP, Branley JM, Dwyer DE, Muscatello DJ, et al.. Probable psittacosis outbreak linked to wild birds. Emerging Infectious Diseases. 2005;11: 391-397.10.3201/eid1103.040601Search in Google Scholar PubMed PubMed Central

[11] Miao Q, Han JQ, Xiang X, Yuan F, Liu Y, Duan G, et al.. Prevalence of antibody to Toxoplasma gondii in black-headed gulls (Chroicocephalus ridibundus), Dianchi Lake, China. J Wildl Dis. 2014; 50(3):717-719.10.7589/2014-01-016Search in Google Scholar PubMed

[12] Tian YM, Cao JF, Zhou DH, Zou FC, Miao Q, Liu ZL, et al.. Seroprevalence and risk factors of Chlamydia infection in dogs in Southwestern China. Acta Tropica. 2014;130:67-70.10.1016/j.actatropica.2013.09.027Search in Google Scholar PubMed

[13] Čechová L, Halánová M, Kalinová Z, Čisláková L, Halán M, Valenčáková A. Detection of Chlamydia psittaci in feral pigeons (Columba livia domestica) in Slovakia and their characterisation. Annals of Agricultural and Environmental Medicine. 2016; 23:75-78.10.5604/12321966.1196856Search in Google Scholar PubMed

[14] Krawiec M, Piasecki T, Wieliczko A. Prevalence of Chlamydia psittaci and Other Chlamydia Species in Wild Birds in Poland. Vector-Borne and Zoonotic Diseases. 2015;15: 652-655.10.1089/vbz.2015.1814Search in Google Scholar PubMed PubMed Central

[15] Cong W, Huang SY, Zhang XY, Zhou DH, Xu MJ, Zhao Q, et al.. Seroprevalence of Chlamydia psittaci infection in market-soldadult chickens, ducks and pigeons in north-western China. Journal of Medical Microbiology. 2013;62:1211-1114.10.1099/jmm.0.059287-0Search in Google Scholar PubMed

[16] Zhang NZ, Zhou DH, Shi XC, Nisbet AJ, Huang SY, Ciren D, et al.. First report of Chlamydiaceae seroprevalence in Tibetan Pigs in Tibet, China. Vector-Borne and Zoonotic Diseases. 2013;13:196-199.10.1089/vbz.2012.1208Search in Google Scholar PubMed PubMed Central

[17] Huang SY, Wu SM, Xu MJ, Zhou DH, Danba C, Gong G, et al.. Firstrecord of Chlamydia abortus seroprevalence in Tibetan sheep in Tibet, China. Small Ruminant Research. 2013; 112: 243-245.10.1016/j.smallrumres.2012.12.012Search in Google Scholar

[18] Zhou DH, Zhao FR, Xia HY, Zu MJ, Huang SY, Song HQ, et al.. Seroprevalence of chlamydial infection in dairy cattle in Guangzhou, southern China. Irish Veterinary Journal. 2013; 66: 1-4.10.1186/2046-0481-66-2Search in Google Scholar PubMed PubMed Central

[19] Wu SM, Huang SY, Xu MJ, Zhou DH, Song HQ, Zhu XQ. Chlamydia felis exposure in companion dogs and cats in Lanzhou, China: a public healthconcern. BMC Veterinary Research. 2013; 9: 104.10.1186/1746-6148-9-104Search in Google Scholar PubMed PubMed Central

[20] Aaziz R, Gourlay P, Vorimore F, Sachse K, Siarkou VI, Laroucau K.. Chlamydiaceae in North Atlantic Seabirds Admitted to a Wildlife Rescue Center in Western France. Applied and Environmental Microbiology. 2015;81: 4581-4590.10.1128/AEM.00778-15Search in Google Scholar PubMed PubMed Central

Received: 2018-01-09
Accepted: 2018-04-09
Published Online: 2018-08-09

© 2018 Hua Chang et al., published by De Gruyter

This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 License.

Articles in the same Issue

  1. Research Article
  2. Purification of Tea saponins and Evaluation of its Effect on Alcohol Dehydrogenase Activity
  3. Runt-related transcription factor 3 promoter hypermethylation and gastric cancer risk: A meta-analysis
  4. Risk Factors for Venous Thromboembolism in Hospitalized Patients in the Chinese Population
  5. Value of Dual-energy Lung Perfusion Imaging Using a Dual-source CT System for the Pulmonary Embolism
  6. A new combination of substrates: biogas production and diversity of the methanogenic microorganisms
  7. mTOR modulates CD8+ T cell differentiation in mice with invasive pulmonary aspergillosis
  8. Direct Effects on Seed Germination of 17 Tree Species under Elevated Temperature and CO2 Conditions
  9. Role of water soluble vitamins in the reduction diet of an amateur sportsman
  10. Aberrant DNA methylation involved in obese women with systemic insulin resistance
  11. 16S ribosomal RNA-based gut microbiome composition analysis in infants with breast milk jaundice
  12. Characterization of Haemophilus parasuis Serovar 2 CL120103, a Moderately Virulent Strain in China
  13. MiRNA-145 induces apoptosis in a gallbladder carcinoma cell line by targeting DFF45
  14. Telmisartan induces osteosarcoma cells growth inhibition and apoptosis via suppressing mTOR pathway
  15. Optimizing the Formulation for Ginkgolide B Solid Dispersion
  16. Determination of the In Vitro Gas Production and Potential Feed Value of Olive, Mulberry and Sour Orange Tree Leaves
  17. Factors Influencing the Successful Isolation and Expansion of Aging Human Mesenchymal Stem Cells
  18. The Value of Diffusion-Weighted Magnetic Resonance Imaging in Predicting the Efficacy of Radiation and Chemotherapy in Cervical Cancer
  19. Chemical profile and antioxidant activity of Trollius europaeus under the influence of feeding aphids
  20. SSR Markers Suitable for Marker Assisted Selection in Sunflower for Downy Mildew Resistance
  21. A Fibroblast Growth Factor Antagonist Peptide Inhibits Breast Cancer in BALB/c Mice
  22. Antihyperglycemic and antihyperlipidemic effects of low-molecular-weight carrageenan in rats
  23. Microbial indicators and environmental relationships in the Umhlangane River, Durban, South Africa
  24. TUFT1 promotes osteosarcoma cell proliferation and predicts poor prognosis in osteosarcoma patients
  25. Long non-coding RNA-2271 promotes osteogenic differentiation in human bone marrow stem cells
  26. The prediction of cardiac events in patients with acute ST segment elevation myocardial infarction: A meta–analysis of serum uric acid
  27. Risk expansion of Cr through amphibious clonal plant from polluted aquatic to terrestrial habitats
  28. Overexpression of Zinc Finger Transcription Factor ZAT6 Enhances Salt Tolerance
  29. Sini decoction intervention on atherosclerosis via PPARγ-LXRα-ABCA1 pathway in rabbits
  30. Soluble myeloid triggering receptor expressed on myeloid cell 1 might have more diagnostic value for bacterial ascites than C-reactive protein
  31. A Preliminary Study on the Newly Isolated High Laccase-producing Fungi: Screening, Strain Characteristics and Induction of Laccase Production
  32. Hydrolytic Enzyme Production by Thermophilic Bacteria Isolated from Saudi Hot Springs
  33. Analysis of physiological parameters of Desulfovibrio strains from individuals with colitis
  34. Emodin promotes apoptosis of human endometrial cancer through regulating the MAPK and PI3K/ AKT pathways
  35. Down-regulation of miR-539 indicates poor prognosis in patients with pancreatic cancer
  36. Inhibitory activities of ethanolic extracts of two macrofungi against eggs and miracidia of Fasciola spp.
  37. PAQR6 expression enhancement suggests a worse prognosis in prostate cancer patients
  38. Characterization of a potential ripening regulator, SlNAC3, from Solanum lycopersicum
  39. Expression of Angiopoietin and VEGF in cervical cancer and its clinical significance
  40. Umbilical Cord Tissue Derived Mesenchymal Stem Cells Can Differentiate into Skin Cells
  41. Isolation and Characterization of a Phage to Control Vancomycin Resistant Enterococcus faecium
  42. Glycogen Phosphorylase Isoenzyme Bb, Myoglobin and BNP in ANT-Induced Cardiotoxicity
  43. BAG2 overexpression correlates with growth and poor prognosis of esophageal squamous cell carcinoma
  44. Relationship between climate trends and grassland yield across contrasting European locations
  45. Review Articles
  46. Mechanisms of salt tolerance in halophytes: current understanding and recent advances
  47. Salivary protein roles in oral health and as predictors of caries risk
  48. Nanoparticles as carriers of proteins, peptides and other therapeutic molecules
  49. Survival mechanisms to selective pressures and implications
  50. Up-regulation of key glycolysis proteins in cancer development
  51. Communications
  52. In vitro plant regeneration of Zenia insignis Chun
  53. DNA barcoding of online herbal supplements: crowd-sourcing pharmacovigilance in high school
  54. Case Reports
  55. Management of myasthenia gravis during pregnancy: A report of eight cases
  56. Three Cases of Extranodal Rosai-Dorfman Disease and Literature Review
  57. Letters to the Editor
  58. First report of Chlamydia psittaci seroprevalence in black-headed gulls (Larus ridibundus) at Dianchi Lake, China
  59. Special Issue on Agricultural and Biological Sciences - Part II
  60. Chemical composition of essential oil in Mosla chinensis Maxim cv. Jiangxiangru and its inhibitory effect on Staphylococcus aureus biofilm formation
  61. Secondary metabolites of Antarctic fungi antagonistic to aquatic pathogenic bacteria
  62. Study of Seizure-Manifested Hartnup Disorder Case Induced by Novel Mutations in SLC6A19
  63. Transcriptome analysis of Pinus massoniana Lamb. microstrobili during sexual reversal
  64. Mechanism of oxymatrine-induced human esophageal cancer cell apoptosis by the endoplasmic reticulum stress pathway
  65. Methylation pattern polymorphism of cyp19a in Nile tilapia and hybrids
  66. A Method of Biomedical Information Classification based on Particle Swarm Optimization with Inertia Weight and Mutation
  67. A novel TNNI3 gene mutation (c.235C>T/ p.Arg79Cys) found in a thirty-eight-year-old women with hypertrophic cardiomyopathy
  68. Remote Sensing-Based Extraction and Analysis of Temporal and Spatial Variations of Winter Wheat Planting Areas in the Henan Province of China
  69. Topical Issue on Precision Medicine
  70. Serum sTREM-1, PCT, CRP, Lac as biomarkers for death risk within 28 days in patients with severe sepsis
  71. IL-17 gene rs3748067 C>T polymorphism and gastric cancer risk: A meta-analysis
  72. Efficacy of Danhong injection on serum concentration of TNF-α, IL-6 and NF-κB in rats with intracerebral hemorrhage
  73. An ensemble method to predict target genes and pathways in uveal melanoma
  74. Evaluation of the quality of CT images acquired with smart metal artifact reduction software
  75. NPM1A in plasma is a potential prognostic biomarker in acute myeloid leukemia
  76. Arterial infusion of rapamycin in the treatment of rabbit hepatocellular carcinoma to improve the effect of TACE
  77. New progress in understanding the cellular mechanisms of anti-arrhythmic drugs
Downloaded on 2.10.2025 from https://www.degruyterbrill.com/document/doi/10.1515/biol-2018-0030/html
Scroll to top button