Startseite Molecular detection of Coxiella burnetii infection (Q fever) in livestock in Makkah Province, Saudi Arabia
Artikel
Lizenziert
Nicht lizenziert Erfordert eine Authentifizierung

Molecular detection of Coxiella burnetii infection (Q fever) in livestock in Makkah Province, Saudi Arabia

  • Hassan M. Baroom EMAIL logo , Naser A. Alkenani EMAIL logo , Bassam O. Al-Johny , Adi A. Almohimeed , Mohammed S. Mohammed , Layla A. Alshehri , Shaker S. Althobaiti , Raga I. Omar , Majed A. Alshaeri und Saleh M. Al-mmaqar ORCID logo EMAIL logo
Veröffentlicht/Copyright: 24. Oktober 2024
Veröffentlichen auch Sie bei De Gruyter Brill

Abstract

The study aims to investigate the prevalence of Q fever in livestock and ticks in Makkah Province, Saudi Arabia, by molecular methods. Using DNA obtained from (40) blood samples, (60) vaginal swabs and ticks (120) samples. Real-time PCR was used to detect the IS1111 insertion sequence of Coxiella burnetii in aborted animals. Among 40 blood samples only one sample of the camel was found to be infected with an overall prevalence of 2.5 %. The highest prevalence (10 %) was recorded in AL-Laith in one camel blood sample out of 10 samples examined. Of 60 vaginal swabs examined for C. burnetii DNA, four samples were found to be infected with an overall prevalence of 6.6 %. The highest prevalence (10 %) was recorded in Makkah in two camel vaginal swabs out of 20 samples, followed by Jeddah and AL-Laith with a prevalence of (5.6 %) by detection of one sample positive out of 18 samples on each of them, while vaginal swabs from AL-Kamil were negative. Three types of ticks were identified Hyalomma dromedarii, Hyalomma anatolicum, and Hyalomma excavatum. H. dromedarii tick is the most common in aborted camels with a prevalence (6.7 %) in Makkah followed by Jeddah (5 %). The findings of this study revealed that C. burnetii infection is prevalent in agricultural animals especially camels and ticks maintained at livestock farms in Makkah Province. However, these animals and ticks may pass on C. burnetii infections to nearby people and other animals in the study area.


Corresponding authors: Hassan M. Baroom, Department of Biological Sciences, Faculty of Science, King Abdulaziz University, P.O. Box: 80203, Jeddah, 21589, Saudi Arabia; and Department of Microbiology, Faculty of Science Um Alqura University, Makkah, Saudi Arabia, E-mail: ; Naser A. Alkenani, Department of Biological Sciences, Faculty of Science, King Abdulaziz University, P.O. Box: 80203, Jeddah, 21589, Saudi Arabia; and Faculty of Sciences, Environmental Protection and Sustainability Research Group, King Abdulaziz University, Jeddah, Saudi Arabia, E-mail: ; and Saleh M. Al-mmaqar, Department of Biological Sciences, Faculty of Science, King Abdulaziz University, P.O. Box: 80203, Jeddah, 21589, Saudi Arabia; and Department of Biology, Faculty of Education, Albaydha University, Al-Baydha, Yemen, E-mail:

Funding source: King Abdulaziz University-DSR

Award Identifier / Grant number: IFPIP:988-130-1443

Acknowledgements

The authors gratefully acknowledge the technical and financial support provided by the Ministry of Education and King Abdulaziz University DSR, Jeddah, Saudi Arabia. Additionally, the authors acknowledge assistance from the Science and Technology Unit, Deanship of Graduate Studies and assistance from the Dept. of Biological Sciences, Faculty of Science, King Abdul Aziz University (KAU), Jeddah, KSA. The authors also acknowledge the Director of Animal Wealth Department, Makkah Region Branch for cooperative in collecting samples. Thanks, extend to the management of Jeddah Islamic Veterinary Diagnostic Laboratory.

  1. Research ethics: This study was approved by the research commenced from the King Abdulaziz University, Faculty of Science Biosafety, Animal Care, and Use Committee (Approval no. RHKB7796- 8002472220). Permission was requested and granted by the Animal Resources Sector of the Ministry of Environment, Water and Agriculture (MEWA), Jeddah, Saudi Arabia to undertake the research. The investigation was carried out in compliance with the Animal Welfare Act (system) for the States of Cooperation Council for Arab States of the Gulf [MEWA-AWA-2016-7 (13)].

  2. Informed consent: Not applicable.

  3. Author contributions: HMB, MSM and NAA: Conceptualization, methodology, writing original draft, writing review and editing. HMB, MSM and MAA: Data collec­tion and curation. HMB, AAA, SSA and LAA: Conceptualisation, methodology, and carried out the DNA extraction and qPCR assays. RIO, BOA and SMA: Carried out data analysis, writing-original draft. All the authors have accepted responsibility for the entire content of this submitted manuscript and approved the submission.

  4. Use of Large Language Models, AI and Machine Learning Tools: None declared.

  5. Competing interests: No potential conflict of interest was reported by the authors.

  6. Research funding: This research work was funded by an institutional Fund Project under grant number (IFPIP:988-130-1443).

  7. Data availability: Not applicable.

References

1. Maurin, M, Raoult, D. Q fever. Clin Microbiol Rev 1999;12:518–53. https://doi.org/10.1128/cmr.12.4.518.Suche in Google Scholar

2. Van Den Brom, R, Schimmer, B, Schneeberger, PM, Swart, WA, van der Hoek, W, Vellema, P. Sero-epidemiological survey for Coxiella burnetii antibodies and associated risk factors in Dutch livestock veterinarians. PLoS One 2013;8:e54021. https://doi.org/10.1371/journal.pone.0054021.Suche in Google Scholar PubMed PubMed Central

3. Tissot-Dupont, H, Amadei, A, Nezri, M, Raoult, D. Wind in November, Q fever in December. Emerg Infect Dis 2004;10:1264–9. https://doi.org/10.3201/eid1007.030724.Suche in Google Scholar PubMed PubMed Central

4. Wallenstein, A, Moore, P, Webster, H, Johnson, C, van der Burgt, G, Pritchard, G, et al.. Q-fever outbreak in Cheltenham, United Kingdom, in 2007 and the use of dispersion modeling to investigate the possibility of airborne spread. Euro Surveill 2010;15:19521.10.2807/ese.15.12.19521-enSuche in Google Scholar

5. Gilsdorf, AKC, Grimm, SJE, Wagner, WC, Alpers, KL. Q-fever outbreak due to sheep farming near residential areas. Germany Epidemiol Infect 2005;136:1084–7.10.1017/S0950268807009533Suche in Google Scholar PubMed PubMed Central

6. Rodolakis, A. Q fever in dairy animals. Ann N Y Acad Sci 2009;1166:90–3. https://doi.org/10.1111/j.1749-6632.2009.04511.x.Suche in Google Scholar PubMed

7. Norlander, L. Q fever epidemiology and pathogenesis. Microb Infect 2000;2:417–24. https://doi.org/10.1016/s1286-4579(00)00325-7.Suche in Google Scholar PubMed

8. Schulze, LSC, Borchardt, S, Ouellet, V, Heuwieser, W. Effect of a phase I Coxiella burnetii inactivated vaccine on body temperature and milk yield in dairy Cows. J Dairy Sci 2016;99:541–50. https://doi.org/10.3168/jds.2015-9628.Suche in Google Scholar PubMed

9. Duron, O, Sidi-Boumedine, K, Rousset, E, Moutailler, S, Jourdain, E. The importance of ticks in Q. fever transmission: what has (and has not) been demonstrated? Trends Parasitol 2015;31:536–52. https://doi.org/10.1016/j.pt.2015.06.014.Suche in Google Scholar PubMed

10. Duron, O, Noël, V, Mccoy, KD, Sidi-Boumedine, K, Morel, O, Arnathau, C, et al.. The recent evolution of a maternally-inherited endosymbiont of ticks led to the emergence of the Q fever pathogen, Coxiella burnetii. PLoS Pathog 2015;11:1–23. https://doi.org/10.1371/journal.ppat.1004892.Suche in Google Scholar PubMed PubMed Central

11. Fard, SN, Khalili, M. PCR-detection of Coxiella burnetii in ticks collected from sheep and goats in Southeast Iran. J Arthropod-Borne Dis 2011;5:1.Suche in Google Scholar

12. Klee, SR, Tyczka, J, Ellerbrok, H, Franz, T, Linke, S, Baljer, G, et al.. Highly sensitive real-time PCR for specific detection and quantification of Coxiella burnetii. BMC Microbiol 2006;6:2. https://doi.org/10.1186/1471-2180-6-2.Suche in Google Scholar PubMed PubMed Central

13. Seshadri, RIT, Paulsen, JA, Eisen, TD, Read, KE, Nelson, WC, Nelson, NL, et al.. Complete genome sequence of the Q-fever pathogen Coxiella burnetii. Proc Natl Acad Sci U S A 2003;100:5455–60. https://doi.org/10.1073/pnas.0931379100.Suche in Google Scholar PubMed PubMed Central

14. Jourdain, E, Duron, O, Severine, B, Gonzalez-Acuna, D, Sidi-Boumedine, K. Molecular methods routinely used to detect Coxiella burnetii in ticks cross-react with Coxiella-like bacteria. Infect Ecol Epidemiol 2015;5:29230. https://doi.org/10.3402/iee.v5.29230.Suche in Google Scholar PubMed PubMed Central

15. Rehacek, J, Kovacova, E, Lisak, V, Rumin, W. Occurrence of Coxiella burnetii, Rickettsia slovaca, and organisms resembling bacillary rickettsiae in their natural foci in Slovakia 20 years after their first detection. Folia Parasitol (Praha) 1990;37:285–6.Suche in Google Scholar

16. Duron, O, Jourdain, E, McCoy, KD. Diversity and global distribution of the Coxiella intracellular bacterium in seabird ticks. Ticks Tick Borne Dis 2014;5:557–63. https://doi.org/10.1016/j.ttbdis.2014.04.003.Suche in Google Scholar PubMed

17. Abdel Rahman, ARJN. Studies on Q fever in farm animals in Kingdom of Saudi Arabia [Doctoral dissertation]. Sudan University of Science and Technology; 2014.Suche in Google Scholar

18. Akbarian, Z, Ziay, G, Schauwers, W, Noormal, B, Saeed, I, Qanee, AH, et al.. Brucellosis and Coxiella burnetii infection in householders and their animals in secure villages in Herat province, Afghanistan: a cross-sectional study. PLoS Neglected Trop Dis 2015;9:2–17. https://doi.org/10.1371/journal.pntd.0004112.Suche in Google Scholar PubMed PubMed Central

19. Jaff, D, Wilson, P. Q fever: a neglected disease in the Middle East. J Health Syst 2016;16.Suche in Google Scholar

20. Almogren, A, Shakoor, Z, Hasanato, R, Adam, MH. Q fever: a neglected zoonosis in Saudi Arabia. Ann Saudi Med 2013;33:464–8. https://doi.org/10.5144/0256-4947.2013.464.Suche in Google Scholar PubMed PubMed Central

21. Aljafar, A, Salem, M, Housawi, F, Zaghawa, A, Hegazy, Y. Seroprevalence and risk factors of Q fever (C. burnetii infection) among ruminants reared in the eastern region of the Kingdom of Saudi Arabia. Trop Anim Health Prod 2020;52:2631–8. https://doi.org/10.1007/s11250-020-02295-6.Suche in Google Scholar PubMed

22. Elsohaby, I, Elmoslemany, A, El-Sharnouby, M, Alkafafy, M, Alorabi, M, El-Deeb, WM, et al.. Flock management risk factors associated with Q. fever infection in sheep in Saudi Arabia. Animals Basel 2021;11:1948. https://doi.org/10.3390/ani11071948.Suche in Google Scholar PubMed PubMed Central

23. Mohammed, OB, Jarelnabi, AA, Aljumaah, RS, Alshaikh, MA, Bakhiet, AO, Omer, SA, et al.. Coxiella burnetii, the causative agent of Q fever in Saudi Arabia: molecular detection from camel and other domestic livestock. Asian Pac J Tropical Med 2014;15:719.10.1016/S1995-7645(14)60122-XSuche in Google Scholar

24. ‏, PG, Ana, H, Raphaël, G. Efficacy and safety of an inactivated phase I Coxiella burnetii vaccine to control Q fever in ruminants: a Systematic Review. Animals 2024;14:1484. https://doi.org/10.3390/ani14101484.Suche in Google Scholar PubMed PubMed Central

25. Long, CM. Q fever vaccine development: current strategies and future considerations. Pathogens 2021;10:1223. https://doi.org/10.3390/pathogens10101223.Suche in Google Scholar PubMed PubMed Central

26. Abeykoon, AH, Clark, NJ, Soares, MRJ, Vincent, GA, Stevenso, MA, Firestone, SM, et al.. Coxiella burnetii in the environment: a systematic review and critical appraisal of sampling methods. Zoonoses Public Health 2021;68:165–81. https://doi.org/10.1111/zph.12791.Suche in Google Scholar PubMed

27. Ahmadinezhad, M, Mounesan, L, Doosti-Irani, A, Behzadi, MY. The prevalence of Q fever in the Eastern Mediterranean region: a systematic review and meta-analysis. Epidemiol Health 2022;44:e2022097. https://doi.org/10.4178/epih.e2022097.Suche in Google Scholar PubMed PubMed Central

28. GAS. General Authority for Statistics. Saudi Arabia statistical yearbook chapter 1. Poulation and Demography: Population in Makkah region; 2019, 55:1–3 pp.Suche in Google Scholar

29. James, GF, Lynn, A, Glen, O, Kathleen, PC, Mark, W, Taylor, BB. Laboratory animal medicine, American College of Labrotary, 3rd edn Cambridge, MA: Academic Press; 2015.Suche in Google Scholar

30. Walker, AR, Bouattar, A, Camicas, JL, Estrada-Pena, A, Horak, IG, Latif, AA, et al.. Ticks of domestic animals in Africa: a guide to identification of species. Edinburgh; 2003. Bioscience Reports.Suche in Google Scholar

31. Gomez, KA, Gomez, AA. Statistical procedures for agricultural research, 2 ed. NewYork: John wiley and sons; 1984:680 p.Suche in Google Scholar

32. Hadush, A, Kandi, V, Pal, M. Epidemiology and public health implications of Q fever. Perspect Med Res 2016;4:42–6.Suche in Google Scholar

33. Ullah, Q, El-Adawy, H, Jamil, T, Jamil, H, Qureshi, ZI, Saqib, M, et al.. Serological and molecular investigation of Coxiella burnetii in small ruminants and ticks in Punjab, Pakistan. Int J Environ Res Publ Health 2019;16:4271. https://doi.org/10.3390/ijerph16214271.Suche in Google Scholar PubMed PubMed Central

34. Ezatkhah, M, Alimolaei, M, Khalili, M, Sharifi, H. Seroepidemiological study of Q fever in small ruminants from Southeast Iran. J Infect Public Health 2015;8:170–6. https://doi.org/10.1016/j.jiph.2014.08.009.Suche in Google Scholar PubMed

35. Doosti, A, Arshi, A, Sadeghi, M. Investigation of Coxiella burnetii in Iranian camels. Comp Clin Pathol 2014;23:43–6. https://doi.org/10.1007/s00580-012-1567-6.Suche in Google Scholar

36. Kirkan, F, Kaya, O, Tekbiyik, S, Parin, U. Detection of Coxiella burnetii in cattle by PCR Turk. J Vet Anim Sci 2008;32:215–20.Suche in Google Scholar

37. Cabrera, OR, Rı´os-Osorio, LA, Keynan, Y, Rueda, ZV, Gutiérrez, LA. Molecular detection of Coxiella burnetii in livestock farmers and cattle from Magdalena Medio in Antioquia, Colombia. PLoS One 2020;15:e0234360. https://doi.org/10.1371/journal.pone.0234360.Suche in Google Scholar PubMed PubMed Central

38. Seo, M-G, Ouh, I-O, Lee, S-H, Kim, JW, Rhee, MH, Kwon, O-D, et al.. Prevalence of Coxiella burnetii in cattle at South Korean national breeding stock farms. PLoS One 2017;12:e0177478. https://doi.org/10.1371/journal.pone.0177478.Suche in Google Scholar PubMed PubMed Central

39. Bildfell, RJ, Thomson, GW, Haines, DM, McEwen, BJ, Smart, N. Coxiella burnetii infection is associated with placentitis in cases of bovine abortion. J Vet Diagn Invest 2000;12:419–25. https://doi.org/10.1177/104063870001200505.Suche in Google Scholar PubMed

40. Khalafalla, AI, Al Eknah, MM, Abdelaziz, M, Ghoneim, IM. A study on some reproductive disorders in dromedary camel herds in Saudi Arabia with special references to uterine infections and abortion. Trop Anim Health Prod 2017;49:967–74. https://doi.org/10.1007/s11250-017-1284-x.Suche in Google Scholar PubMed

41. El Tigani-Asil, ETA, Blanda, V, Abdelwahab, GE, Hammadi, ZMA, Habeeba, S, Khalafalla, AI, et al.. Molecular investigation on tick-borne hemoparasites and Coxiella burnetii in dromedary camels (Camelus dromedarius) in Al Dhafra region of Abu Dhabi, UAE. Animals 2021;11:666. https://doi.org/10.3390/ani11030666.Suche in Google Scholar PubMed PubMed Central

42. El-Deeb, W, Ghoneim, I, Fayez, M, Elsohaby, I, Alhaider, A, ElGioushy, M. Acute phase proteins, proinflammatory cytokines and oxidative stress biomarkers in sheep, goats, and she-camels with Coxiella burnetii infection-induced abortion. Comp Immunol Microbiol Infect Dis 2019;67:101352. https://doi.org/10.1016/j.cimid.2019.101352.Suche in Google Scholar PubMed

43. Berri, M, Laroucau, K, Rodolakis, A. The detection of Coxiella burnetii from ovine genital swabs, milk, and fecal samples by the use of a single touchdown polymerase chain reaction. Vet Microbi 2000;72:285–93. https://doi.org/10.1016/s0378-1135(99)00178-9.Suche in Google Scholar PubMed

44. Elbir, H, Almathen, F, Alhumam, NA. A glimpse of the bacteriome of Hyalomma dromedarii ticks infesting camels reveals human Helicobacter pylori pathogen. J Infect Dev Countries 2019;13:1001–12. https://doi.org/10.3855/jidc.11604.Suche in Google Scholar PubMed

45. Onyiche, TE, Răileanu, C, Tauchmann, O, Fischer, S, Vasić, A, Schäfer, M, et al.. Prevalence and molecular characterization of ticks and tick-borne pathogens of one-humped camels (Camelus dromedarius) in Nigeria. Parasites Vectors 2020;13:1–16. https://doi.org/10.1186/s13071-020-04272-2.Suche in Google Scholar PubMed PubMed Central

46. Al-Deeb, MA, Muzaffar, S. Prevalence, distribution on host’s body, and chemical control of camel ticks Hyalomma dromedarii in the United Arab Emirates. Vet World 2020;13:114–20. https://doi.org/10.14202/vetworld.2020.114-120.Suche in Google Scholar PubMed PubMed Central

47. Perveen, N, Muzaffar, SB, Al-Deeb, MA. Ticks and tick-borne diseases of livestock in the Middle East and North Africa: a review. Insects 2021;12:83. https://doi.org/10.3390/insects12010083.Suche in Google Scholar PubMed PubMed Central

48. Van Straten, M, Jongejan, F. Ticks (Acari: Ixodidae) infesting the Arabian camel (Camelus dromedarius) in the Sinai, Egypt with a note on the acaricidal efficacy of ivermectin. Exp Appl Acarol 1993;17:605–16. https://doi.org/10.1007/bf00053490.Suche in Google Scholar

49. Abdullah, HHA, El-Molla, A, Salib, FA, Allam, NAT, Ghazy, AA, Abdel-Shafy, S. Morphological and molecular identification of the brown dog tick Rhipicephalus sanguineus and the camel tick Hyalomma dromedarii (Acari: Ixodidae) vectors of rickettsioses in Egypt. Vet World 2016;9:1087–101. https://doi.org/10.14202/vetworld.2016.1087-1101.Suche in Google Scholar PubMed PubMed Central

50. Razmi, GR, Ebrahimzadeh, E, Aslani, MR. A study about tick vectors of bovine theileriosis in an endemic region of Iran. J Vet Med Ser B: Infec Dise Vete Pub Heal 2003;50:309–10. https://doi.org/10.1046/j.1439-0450.2003.00677.x.Suche in Google Scholar PubMed

51. Körner, S, Makert, GR, Ulbert, S, Pfeffer, M, Mertens-Scholz, K. The prevalence of Coxiella burnetii in hard ticks in Europe and their role in Q fever transmission revisited – a systematic review. Front Vet Sci 2021;8:655715. https://doi.org/10.3389/fvets.2021.655715.Suche in Google Scholar PubMed PubMed Central

52. Davoust, B, Marié, JL, Pommier de Santi, V, Berenger, JM, Edouard, S, Raoult, D. Three-toed sloth as putative reservoir of Coxiella burnetii, Cayenne, French Guiana. Emerg Infect Dis 2014;20:1760–1. https://doi.org/10.3201/eid2010.140694.Suche in Google Scholar PubMed PubMed Central

53. Noda, AA, Rodríguez, I, Miranda, J, Contreras, V, Mattar, S. First molecular evidence of Coxiella burnetii infecting ticks in Cuba. Ticks Tick Borne Dis 2016;7:68–70. https://doi.org/10.1016/j.ttbdis.2015.08.008.Suche in Google Scholar PubMed

54. Ni, J, Lin, H, Xu, X, Ren, Q, Aizezi, M, Luo, J, et al.. Coxiella burnetii is widespread in ticks (Ixodidae) in the Xinjiang areas of China. BMC Vet Res 2020;16:317. https://doi.org/10.1186/s12917-020-02538-6.Suche in Google Scholar PubMed PubMed Central

55. Loftis, AD, Reeves, WK, Szumlas, DE, Abbassy, MM, Helmy, IM, Moriarity, JR, et al.. Rickettsial agents in Egyptian ticks collected from domestic animals. Exp Appl Acarol 2006;40:67. https://doi.org/10.1007/s10493-006-9025-2.Suche in Google Scholar PubMed

56. Hornok, S, Abichu, G, Meli, ML, Tánczos, B, Sulyok, KM, Gyuranecz, M, et al.. Influence of the biotope on the tick infestation of cattle and on the tick-borne pathogen repertoire of cattle ticks in Ethiopia. PLoS One 2014;9:e106452. https://doi.org/10.1371/journal.pone.0106452.Suche in Google Scholar PubMed PubMed Central

57. Pacheco, RC, Echaide, IE, Alves, RN, Beletti, ME, Nava, S, Labruna, MB. Coxiella burnetii in ticks, Argentina. Emerg Infect Dis 2013;19:344–6. https://doi.org/10.3201/eid1902.120362.Suche in Google Scholar PubMed PubMed Central

58. Reye, AL, Arinola, OG, Hübschen, JM, Muller, CP. Pathogen prevalence in ticks collected from the vegetation and livestock in Nigeria. Appl Environ Microbiol 2012;78:2562–8. https://doi.org/10.1128/aem.06686-11.Suche in Google Scholar PubMed PubMed Central

59. Andoh, M, Andoh, R, Teramoto, K, Komiya, T, Kaneshima, T, Takano, A, et al.. Survey of Coxiella burnetii in ticks collected from dogs in Japan. J Vet Med Sci 2013;75:1115–7. https://doi.org/10.1292/jvms.12-0570.Suche in Google Scholar PubMed

60. Cardinale, E, Esnault, O, Beral, M, Naze, F, Michault, A. Emergence of Coxiella burnetii in ruminants on Reunion Island? Prevalence and risk factors. PLoS Negl Trop Dis 2014;8:e3055. https://doi.org/10.1371/journal.pntd.0003055.Suche in Google Scholar PubMed PubMed Central

61. Nelder, MP, Reeves, WK, Adler, PH, Wozniak, A, Wills, W. Ectoparasites and associated pathogens of free-roaming and captive animals in zoos of South Carolina. Vector Borne Zoon Dis 2009;9:469–77. https://doi.org/10.1089/vbz.2008.0008.Suche in Google Scholar PubMed

Received: 2024-05-28
Accepted: 2024-10-05
Published Online: 2024-10-24
Published in Print: 2025-05-26

© 2024 Walter de Gruyter GmbH, Berlin/Boston

Heruntergeladen am 6.11.2025 von https://www.degruyterbrill.com/document/doi/10.1515/znc-2024-0126/html
Button zum nach oben scrollen