performance. Over 60% of the farms tested positive. According to the authors, the overall conception rate was lower on seropositive farms than on seronegative farms (37.1% ± 10.3 vs. 39.8% ± 11.7; *p* < 0.05). The authors found similar data for the first service conception rate (32.9% ± 11.8 vs. 36.1% ± 13.2; *p* < 0.05). However, no significant differences were observed for calving to the first AI interval and number of days open.

Overall, the evidence seems to indicate a relationship between *C. burnetii* infection and adverse reproductive performance. However, to determine the extent of the effect *C. burnetii* has on fertility/sub-fertility, more controlled studies with larger numbers of animals need to be performed, and determining what merits a "*C. burnetii* infection" definition needs to be examined more closely.

**4. Conclusions**

This literature review offers a comprehensive evaluation of existing data on the impact of Q fever on cattle reproduction. Most studies, especially those with evidence scores of three and four, suggest the involvement of *C. burnetii* infection in various reproductive parameters, including the ASPW complex, RFMs and infertility/sub-fertility. Particularly compelling evidence emerges regarding the ASPW complex, with 43 studies addressing this aspect. However, substantial gaps persist in research, notably concerning RFMs, infertility/sub-fertility and metritis/endometritis (considering metritis and endometritis separately), warranting larger animal cohorts in more controlled settings to provide clarity. As we endeavour to deepen our understanding of how *C. burnetii* infection in cows affects reproduction, the intricate interplay of direct and indirect effects, compounded by co-infections with other pathogens, management practices and environmental factors, underscores the complexity of this research domain.

One key recommendation arising from this review is to encourage authors to adopt more precise definitions and robust methodologies for detecting the presence of *C. burnetii*, as well as to strive for consistency in defining various reproductive parameters. Such improvements would likely increase the capacity of future reviews to offer stronger evidence regarding *C. burnetii* involvement and impact on studied parameters. Furthermore, adherence to the World Organization for Animal Health guidelines regarding the use of robust diagnostic tools is paramount for confirming *C. burnetii* involvement in reproductive parameters. For instance, in cases of abortions and stillbirths, samples from the placenta, vaginal discharges and aborted foetus tissues (spleen, liver, lung or stomach content) should ideally undergo diagnosis via IHC, in situ hybridization or PCR. While serological tests detecting specific IgG antibodies provide evidence of recent *C. burnetii* infection or past exposure and are sometimes preferred for practical reasons, they are not as definitive as PCR for case confirmation.

The observed reproductive effects not only impact farm management and economics but also contribute to environmental contamination. Given the zoonotic nature of Q fever, increased shedding of *C. burnetii* elevates the risk of human exposure and subsequent contraction of the disease. Therefore, proactive measures are essential to safeguard both animal and human health.

**Author Contributions:** Conceptualization, P.G.; methodology, P.G.; validation, P.G., I.G.-I., L.A.Q. and R.G.; writing—original draft preparation, P.G.; writing—review and editing, P.G., I.G.-I., L.A.Q. and R.G.; visualization, P.G. and R.G.; project administration, P.G. All authors have read and agreed to the published version of the manuscript.

**Funding:** This research received no external funding.

**Institutional Review Board Statement:** In this study a systematic review using bibliographic research was carried out and no experiments were performed on animals.

**Informed Consent Statement:** Not applicable.

**Data Availability Statement:** Data is contained within the article.
performance. Over 60% of the farms tested positive. According to the authors, the overall conception rate was lower on seropositive farms than on seronegative farms (37.1% ± 10.3 vs. 39.8% ± 11.7; *p* < 0.05). The authors found similar data for the first service conception rate (32.9% ± 11.8 vs. 36.1% ± 13.2; *p* < 0.05). However, no significant differences were observed for calving to the first AI interval and number of days open.

Overall, the evidence seems to indicate a relationship between *C. burnetii* infection and adverse reproductive performance. However, to determine the extent of the effect *C. burnetii* has on fertility/sub-fertility, more controlled studies with larger numbers of animals need to be performed, and determining what merits a "*C. burnetii* infection" definition needs to be examined more closely.

**4. Conclusions**

This literature review offers a comprehensive evaluation of existing data on the impact of Q fever on cattle reproduction. Most studies, especially those with evidence scores of three and four, suggest the involvement of *C. burnetii* infection in various reproductive parameters, including the ASPW complex, RFMs and infertility/sub-fertility. Particularly compelling evidence emerges regarding the ASPW complex, with 43 studies addressing this aspect. However, substantial gaps persist in research, notably concerning RFMs, infertility/sub-fertility and metritis/endometritis (considering metritis and endometritis separately), warranting larger animal cohorts in more controlled settings to provide clarity. As we endeavour to deepen our understanding of how *C. burnetii* infection in cows affects reproduction, the intricate interplay of direct and indirect effects, compounded by co-infections with other pathogens, management practices and environmental factors, underscores the complexity of this research domain.

One key recommendation arising from this review is to encourage authors to adopt more precise definitions and robust methodologies for detecting the presence of *C. burnetii*, as well as to strive for consistency in defining various reproductive parameters. Such improvements would likely increase the capacity of future reviews to offer stronger evidence regarding *C. burnetii* involvement and impact on studied parameters. Furthermore, adherence to the World Organization for Animal Health guidelines regarding the use of robust diagnostic tools is paramount for confirming *C. burnetii* involvement in reproductive parameters. For instance, in cases of abortions and stillbirths, samples from the placenta, vaginal discharges and aborted foetus tissues (spleen, liver, lung or stomach content) should ideally undergo diagnosis via IHC, in situ hybridization or PCR. While serological tests detecting specific IgG antibodies provide evidence of recent *C. burnetii* infection or past exposure and are sometimes preferred for practical reasons, they are not as definitive as PCR for case confirmation.

The observed reproductive effects not only impact farm management and economics but also contribute to environmental contamination. Given the zoonotic nature of Q fever, increased shedding of *C. burnetii* elevates the risk of human exposure and subsequent contraction of the disease. Therefore, proactive measures are essential to safeguard both animal and human health.

**Author Contributions:** Conceptualization, P.G.; methodology, P.G.; validation, P.G., I.G.-I., L.A.Q. and R.G.; writing—original draft preparation, P.G.; writing—review and editing, P.G., I.G.-I., L.A.Q. and R.G.; visualization, P.G. and R.G.; project administration, P.G. All authors have read and agreed to the published version of the manuscript.

**Funding:** This research received no external funding.

**Institutional Review Board Statement:** In this study a systematic review using bibliographic research was carried out and no experiments were performed on animals.

**Informed Consent Statement:** Not applicable.

**Data Availability Statement:** Data is contained within the article.
**Acknowledgments:** The authors wish to thank Jo Halliday, University of Glasgow, for her contribu-
tions in preparing this review.

**Conflicts of Interest:** The author P.G. works for the company Ceva Santé Animale, which produces and commercialises a Q fever vaccine for ruminants. The other authors declare no conflicts of interest.

References

1. Arricau-Bouvery, N.; Rodolakis, A. Is Q Fever an emerging or re-emerging zoonosis? *Vet. Res.* **2005**, *36*, 327–349. [CrossRef]

2. Eldin, C.; Mélenotte, C.; Mediannikov, O.; Ghigo, E.; Million, M.; Edouard, S.; Mege, J.-L.; Maurin, M.; Raoult, D. From Q fever to *Coxiella burnetii* infection: A paradigm change. *Clin. Microbiol. Rev.* **2016**, *30*, 115–190. [CrossRef] [PubMed]

3. Sidi-Boumedine, K.; Rousset, E.; Henning, K.; Ziller, M.; Niemczuck, K.; Roest, H.; Thiéry, R. Development of harmonised schemes for the monitoring and reporting of Q-fever in animals in the European Union. *EFSA Support. Publ.* **2010**, *7*, 48E. [CrossRef]

4. Lurier, T.; Rousset, E.; Gasqui, P.; Sala, C.; Claustre, C.; Abrial, D.; Dufour, P.; De Crémoux, R.; Gache, K.; Delignette-Muller, M.L.; et al. Evaluation using latent class models of the diagnostic performances of three ELISA tests commercialized for the serological diagnosis of *Coxiella burnetii* infection in domestic ruminants. *Vet. Res.* **2021**, *52*, 56. [CrossRef]

5. Garcia-Ispierto, I.; Tutusaus, J.; López-Gatius, F. Does *Coxiella burnetii* affect reproduction in cattle? A Clinical Update. *Reprod. Domest. Anim. Zuchthyg.* **2014**, *49*, 529–535. [CrossRef]

6. World Organisation for Animal Health. Chapter 3.1.17 Q fever. In *Manual of Diagnostic Tests and Vaccines for Terrestrial Animals*, 12th ed.; World Organisation for Animal Health (WOAH): Paris, France, 2023; Volume 2018.

7. den Brom, R.V.; van Engelen, E.; Roest, H.I.J.; van der Hoek, W.; Vellema, P. *Coxiella burnetii* infections in sheep or goats: An opinionated review. *Vet. Microbiol.* **2015**, *181*, 119–129. [CrossRef] [PubMed]

8. Ali, S.; Zhao, Z.; Zhen, G.; Kang, J.Z.; Yi, P.Z. Reproductive problems in small ruminants (sheep and goats): A substantial economic loss in the world. *Large Anim. Rev.* **2019**, *25*, 215–223.

9. Agerholm, J.S. *Coxiella burnetii* associated reproductive disorders in domestic animals-a critical review. *Acta Vet. Scand.* **2013**, *55*, 13. [CrossRef]

10. Peter, A.T. Abortions in dairy cows: New insights and economic impact. Proceedings of Western Canadian Dairy Seminar, Red Deer, Alberta, Canada. *Adv. Dairy Technol.* **2000**, *12*, 233–244.

11. Robi, D.T.; Gelalch, B.D.; Deresa, F.B. Case-control study on risk factors associated with brucellosis in aborted cattle of Jimma zone, Ethiopia. *Iran. J. Vet. Sci. Technol.* **2019**, *11*, 27–36. [CrossRef]

12. Hovingh, E. *Aborptions in Dairy Cattle I: Common Causes of Abortions*; Virginia Cooperative Extension (VCE): Blacksburg, VA, USA, 2009.

13. Mee, J.F.; Jawor, P.; Stefaniak, T. Role of infection and immunity in bovine perinatal mortality: Part 1. Causes and current diagnostic approaches. *Animals* **2021**, *11*, 1033. [CrossRef] [PubMed]

14. Wolf-Jäckel, G.A.; Hansen, M.S.; Larsen, G.; Holm, E.; Agerholm, J.S.; Jensen, T.K. Diagnostic studies of abortion in Danish cattle 2015–2017. *Acta Vet. Scand.* **2020**, *62*, 1. [CrossRef]

15. Cuttance, E.; Laven, R. Estimation of perinatal mortality in dairy calves: A review. *Vet. J.* **2019**, *252*, 105356. [CrossRef] [PubMed]

16. Fourichon, C.; Seegers, H.; Malher, X. Effect of disease on reproduction in the dairy cow: A meta-analysis. *Theriogenology* **2000**, *53*, 1729–1759. [CrossRef] [PubMed]

17. Beagley, J.C.; Whitman, K.J.; Baptiste, K.E.; Scherzer, J. Physiology and treatment of retained fetal membranes in cattle. *J. Vet. Intern. Med.* **2010**, *24*, 261–268. [CrossRef]

18. Sheldon, I.M.; Lewis, G.S.; LeBlanc, S.; Gilbert, R.O. Defining postpartum uterine disease in cattle. *Theriogenology* **2006**, *65*, 1516–1530. [CrossRef] [PubMed]

19. Fricke, P.M.; Wiltbank, M.C. Symposium Review: The implications of spontaneous versus synchronized ovulations on the reproductive performance of lactating dairy cows. *J. Dairy Sci.* **2022**, *105*, 4679–4689. [CrossRef]

20. González-Recio, O.; Alenda, R. Genetic parameters for female fertility traits and a fertility index in Spanish dairy cattle. *J. Dairy Sci.* **2005**, *88*, 3282–3289. [CrossRef] [PubMed]

21. Esslemont, R.J.; Kossaibati, M.A. The use of databases to manage fertility. *Anim. Reprod. Sci.* **2000**, *60*, 725–741. [CrossRef]

22. Page, M.J.; McKenzie, J.E.; Bossuyt, P.M.; Boutron, I.; Hoffmann, T.C.; Mulrow, C.D.; Shamseer, L.; Tetzlaff, J.M.; Akl, E.A.; Brennan, S.E.; et al. The PRISMA 2020 statement: An updated guideline for reporting systematic reviews. *Int. J. Surg.* **2021**, *88*, 105906. [CrossRef]

23. To, H.; Htwe, K.K.; Kako, N.; Kim, H.J.; Yamagufhi, T.; Fukushi, H.; Hirai, K. Prevalence of *Coxiella burnetii* infection in dairy cattle with reproductive disorders. *J. Vet. Med. Sci.* **1998**, *60*, 859–861. [CrossRef] [PubMed]

24. Plommet, M.; Capponi, M.; Gestin, J.; Renoux, G.; Marly, J.; Sahuc, D.; Petit, A. Fièvre Q expérimentale des bovins. *Ann. Rech. Vét.* **1973**, *4*, 325–346.

25. Methley, A.M.; Campbell, S.; Chew-Graham, C.; McNally, R.; Cheraghi-Sohi, S. PICO, PICOS and SPIDER: A comparison study of specificity and sensitivity in three search tools for qualitative systematic reviews. *BMC Health Serv. Res.* **2014**, *14*, 579. [CrossRef] [PubMed]
**Acknowledgments:** The authors wish to thank Jo Halliday, University of Glasgow, for her contribu-
tions in preparing this review.

**Conflicts of Interest:** The author P.G. works for the company Ceva Santé Animale, which produces and commercialises a Q fever vaccine for ruminants. The other authors declare no conflicts of interest.

References

1. Arricau-Bouvery, N.; Rodolakis, A. Is Q Fever an emerging or re-emerging zoonosis? *Vet. Res.* **2005**, *36*, 327–349. [CrossRef]

2. Eldin, C.; Mélenotte, C.; Mediannikov, O.; Ghigo, E.; Million, M.; Edouard, S.; Mege, J.-L.; Maurin, M.; Raoult, D. From Q fever to *Coxiella burnetii* infection: A paradigm change. *Clin. Microbiol. Rev.* **2016**, *30*, 115–190. [CrossRef] [PubMed]

3. Sidi-Boumedine, K.; Rousset, E.; Henning, K.; Ziller, M.; Niemczuck, K.; Roest, H.; Thiéry, R. Development of harmonised schemes for the monitoring and reporting of Q-fever in animals in the European Union. *EFSA Support. Publ.* **2010**, *7*, 48E. [CrossRef]

4. Lurier, T.; Rousset, E.; Gasqui, P.; Sala, C.; Claustre, C.; Abrial, D.; Dufour, P.; De Crémoux, R.; Gache, K.; Delignette-Muller, M.L.; et al. Evaluation using latent class models of the diagnostic performances of three ELISA tests commercialized for the serological diagnosis of *Coxiella burnetii* infection in domestic ruminants. *Vet. Res.* **2021**, *52*, 56. [CrossRef]

5. Garcia-Ispierto, I.; Tutusaus, J.; López-Gatius, F. Does *Coxiella burnetii* affect reproduction in cattle? A Clinical Update. *Reprod. Domest. Anim. Zuchthyg.* **2014**, *49*, 529–535. [CrossRef]

6. World Organisation for Animal Health. Chapter 3.1.17 Q fever. In *Manual of Diagnostic Tests and Vaccines for Terrestrial Animals*, 12th ed.; World Organisation for Animal Health (WOAH): Paris, France, 2023; Volume 2018.

7. den Brom, R.V.; van Engelen, E.; Roest, H.I.J.; van der Hoek, W.; Vellema, P. *Coxiella burnetii* infections in sheep or goats: An opinionated review. *Vet. Microbiol.* **2015**, *181*, 119–129. [CrossRef] [PubMed]

8. Ali, S.; Zhao, Z.; Zhen, G.; Kang, J.Z.; Yi, P.Z. Reproductive problems in small ruminants (sheep and goats): A substantial economic loss in the world. *Large Anim. Rev.* **2019**, *25*, 215–223.

9. Agerholm, J.S. *Coxiella burnetii* associated reproductive disorders in domestic animals-a critical review. *Acta Vet. Scand.* **2013**, *55*, 13. [CrossRef]

10. Peter, A.T. Abortions in dairy cows: New insights and economic impact. Proceedings of Western Canadian Dairy Seminar, Red Deer, Alberta, Canada. *Adv. Dairy Technol.* **2000**, *12*, 233–244.

11. Robi, D.T.; Gelalch, B.D.; Deresa, F.B. Case-control study on risk factors associated with brucellosis in aborted cattle of Jimma zone, Ethiopia. *Iran. J. Vet. Sci. Technol.* **2019**, *11*, 27–36. [CrossRef]

12. Hovingh, E. *Abortions in Dairy Cattle I: Common Causes of Abortions*; Virginia Cooperative Extension (VCE): Blacksburg, VA, USA, 2009.

13. Mee, J.F.; Jawor, P.; Stefaniak, T. Role of infection and immunity in bovine perinatal mortality: Part 1. Causes and current diagnostic approaches. *Animals* **2021**, *11*, 1033. [CrossRef] [PubMed]

14. Wolf-Jäckel, G.A.; Hansen, M.S.; Larsen, G.; Holm, E.; Agerholm, J.S.; Jensen, T.K. Diagnostic studies of abortion in Danish cattle 2015–2017. *Acta Vet. Scand.* **2020**, *62*, 1. [CrossRef]

15. Cuttance, E.; Laven, R. Estimation of perinatal mortality in dairy calves: A review. *Vet. J.* **2019**, *252*, 105356. [CrossRef] [PubMed]

16. Fourichon, C.; Seegers, H.; Malher, X. Effect of disease on reproduction in the dairy cow: A meta-analysis. *Theriogenology* **2000**, *53*, 1729–1759. [CrossRef] [PubMed]

17. Beagley, J.C.; Whitman, K.J.; Baptiste, K.E.; Scherzer, J. Physiology and treatment of retained fetal membranes in cattle. *J. Vet. Intern. Med.* **2010**, *24*, 261–268. [CrossRef]

18. Sheldon, I.M.; Lewis, G.S.; LeBlanc, S.; Gilbert, R.O. Defining postpartum uterine disease in cattle. *Theriogenology* **2006**, *65*, 1516–1530. [CrossRef] [PubMed]

19. Fricke, P.M.; Wiltbank, M.C. Symposium Review: The implications of spontaneous versus synchronized ovulations on the reproductive performance of lactating dairy cows. *J. Dairy Sci.* **2022**, *105*, 4679–4689. [CrossRef]

20. González-Recio, O.; Alenda, R. Genetic parameters for female fertility traits and a fertility index in Spanish dairy cattle. *J. Dairy Sci.* **2005**, *88*, 3282–3289. [CrossRef] [PubMed]

21. Esslemont, R.J.; Kossaibati, M.A. The use of databases to manage fertility. *Anim. Reprod. Sci.* **2000**, *60*, 725–741. [CrossRef]

22. Page, M.J.; McKenzie, J.E.; Bossuyt, P.M.; Boutron, I.; Hoffmann, T.C.; Mulrow, C.D.; Shamseer, L.; Tetzlaff, J.M.; Akl, E.A.; Brennan, S.E.; et al. The PRISMA 2020 statement: An updated guideline for reporting systematic reviews. *Int. J. Surg.* **2021**, *88*, 105906. [CrossRef]

23. To, H.; Htwe, K.K.; Kako, N.; Kim, H.J.; Yamagufhi, T.; Fukushi, H.; Hirai, K. Prevalence of *Coxiella burnetii* infection in dairy cattle with reproductive disorders. *J. Vet. Med. Sci.* **1998**, *60*, 859–861. [CrossRef] [PubMed]

24. Plommet, M.; Capponi, M.; Gestin, J.; Renoux, G.; Marly, J.; Sahuc, D.; Petit, A. Fièvre Q expérimentale des bovins. *Ann. Rech. Vét.* **1973**, *4*, 325–346.

25. Methley, A.M.; Campbell, S.; Chew-Graham, C.; McNally, R.; Cheraghi-Sohi, S. PICO, PICOS and SPIDER: A comparison study of specificity and sensitivity in three search tools for qualitative systematic reviews. *BMC Health Serv. Res.* **2014**, *14*, 579. [CrossRef] [PubMed]
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28. Sodoma, E.; Mitterhuemer, S.; Krassnig, G.; Stellnberger, K.; Reisp, K.; Schmoll, F.; Dünser, M. Infectious causes of abortions in cattle-own experiences and investigations from 2018 (January–September). *Tierarztl. Prax. Ausg. G Grosstiere Nutztiere* **2019**, *47*, 143–150. [PubMed]

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27. Derdour, S.-Y.; Hafsi, F.; Azzag, N.; Tennah, S.; Laamari, A.; China, B.; Ghalmi, F. Prevalence of the main infectious causes of abortion in dairy cattle in Algeria. *J. Vet. Res.* **2017**, *61*, 337–343. [CrossRef]

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**Disclaimer/Publisher's Note:** The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.