Skip to main content

Salmonella Abortusovis: An Epidemiologically Relevant Pathogen

Current Microbiology volume 79, Article number: 3 (2022) Cite this article

Abstract

The ovine pathogen Salmonella enterica serovar Abortusovis (SAO), a pathogen strictly adapted to ovine hosts, is endemic in several European and Asian countries, where it causes significant economic losses due to the high rates of abortion in infected flocks. In some countries (i.e. Switzerland and Croatia), re-emergence of infection by SAO occurred after decades during which the disease has not been reported. The introduction of (SAO) epidemic strains in new areas is difficult to control due to the asymptomatic behaviors in infected adult lambs, rams, and nonpregnant ewes. Culture-based diagnosis may provide false-negative results. Moreover, the retrospective identification of Salmonella infection in ewes is challenging as excretion of the causative agent is transient and the serum antibodies fall to low titres soon after the abortion. Therefore, regular monitoring of pathogen exposure, mainly through seroconversion assessment, is advisable to prevent disease introduction and spread in SAO-free areas, especially in case of animal export, and to reduce abortion risk.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price includes VAT (USA)
Tax calculation will be finalised during checkout.

Fig. 1

Data Availability

Data used for the manuscript have been retrieved from published studies and other publications available online. Data sources are listed in the References section.

Code Availability

Not applicable.

References

  1. Spickler AR (2017) Salmonella Abortusovis. https://www.cfsph.iastate.edu/Factsheets/pdfs/salmonella_abortusovis.pdf. Accessed 6 Dec 2021

  2. Belloy L, Decrausaz L, Boujon P, Hächler H, Waldvogel AS (2009) Diagnosis by culture and PCR of Salmonella Abortusovis infection under clinical conditions in aborting sheep in Switzerland. Vet Microbiol 138:373–377

    CAS  Article  Google Scholar 

  3. Uzzau S (2013) Salmonella infections in sheep. In: Barrow PA, Methner U (eds) Salmonella in domestic animals, 2nd edn. CAB International, Wallingford

    Google Scholar 

  4. Wirz-Dittus S, Belloy L, Hüssy D, Waldvogel AS, Doherr MG (2010) Seroprevalence survey for Salmonella Abortusovis infection in Swiss sheep flocks. Prev Vet Med 97:126–130

    Article  Google Scholar 

  5. Cagiola M, Severi G, Forti K, Menichelli M, Papa P, De Giuseppe A, Pasquali P (2007) Abortion due to Salmonella enterica serovar Abortusovis (S. Abortusovis) in ewes is associated to a lack of production of IFN-γ and can be prevented by immunization with inactivated S. Abortusovis vaccine. Vet Microbiol 121:330–337

    CAS  Article  Google Scholar 

  6. Grimont PAD, Weill F-X (2007) Antigenic formulae of the Salmonella serovars, 9 edition, World Health Organization Collaborating Centre for reference and research on Salmonella. Institut Pasteur, Paris

    Google Scholar 

  7. Issenhut-Jeanjean S, Roggentin P, Mikoleit M, Guibourdenche M, De Pinna E, Nair S, Fields PI, Weill FX (2014) Supplement 2008–2010 (no. 48) to the White–Kauffmann–Le Minor scheme. Res Microbiol 165:526–530

    Article  Google Scholar 

  8. Uzzau S, Leori GS, Petruzzi V, Watson PR, Schianchi G, Bacciu D, Mazzarello V, Wallis TS, Rubino S (2001) Salmonella enterica serovar-host specificity does not correlate with the magnitude of intestinal invasion in sheep. Infect Immun 69:3092–3099

    CAS  Article  Google Scholar 

  9. Singh V (2013) Salmonella serovars and their host specificity. J Vet Sci Anim Husb 1:1–4

    Google Scholar 

  10. Borel N, Frey CF, Gottstein B, Hilbe M, Pospischil A, Franzoso FD, Waldvogel A (2014) Laboratory diagnosis of ruminant abortion in Europe. Vet J 200:218–229

    Article  Google Scholar 

  11. Wirz-Dittus S, Belloy L, Doherr MG, Hüssy D, Sting R, Gabioud P, Waldvogel AS (2010) Use of an indirect enzyme-linked immunosorbent assay for detection of antibodies in sheep naturally infected with Salmonella Abortusovis. J Vet Diagn Investig 22:531–536

    Article  Google Scholar 

  12. Mahdavi Roshan H, Saadati D, Najimi M (2018) Molecular detection of Brucella melitensis, Coxiella burnetii and Salmonella abortusovis in aborted fetuses of Baluchi sheep in Sistan region, south-eastern Iran. Iran J Vet Res 19:128–132

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Jack KJ (1968) Salmonella Abortusovis: an atypical Salmonella. Vet Res 82:1168–1174

    Google Scholar 

  14. Echeita MA, Aladueña AM, Díez R, Arroyo M, Cerdán F, Gutiérrez R, de la Fuente M, González-Sanz R, Herrera-León S, Usera MA (2005) Distribución de los serotipos y fagotipos de Salmonella de origen humano aislados en España en 1997–2001. Enferm Infect Microbiol Clin 23:127–134

    Article  Google Scholar 

  15. Valdezate S, Astorga R, Herrera-Leon S, Perea A, Usera MA, Huerta B, Echeita A (2007) Epidemiological tracing of Salmonella enterica serotype Abortusovis from Spanish ovine flocks by PFGE fingerprinting. Epidemiol Infect 135:695–702

    CAS  Article  Google Scholar 

  16. González L (2000) Salmonella abortus ovis infection. In: Martin WB, Aitken ID (eds) Diseases of sheep, 3rd edn. Blackwell Science, Oxford, pp 102–107

    Google Scholar 

  17. Schiaffino A, Beuzòn CR, Uzzau S, Leori G, Cappuccinelli P, Casadesus J, Rubino S (1996) Strain typing with IS200 fingerprints in Salmonella Abortusovis. Appl Environ Microbiol 62:2375–2380

    CAS  Article  Google Scholar 

  18. Boss PH, Nicolet J, Margadant A (1977) The course of a Salmonella abortusovis infection in a herd of sheep. Schweiz Arch Tierh 119:395–404

    CAS  PubMed  Google Scholar 

  19. Fras A (1948) Salmonella Abortusovis as a cause of ovine abortion in Yugoslavia. Doctoral dissertation, School of Veterinary Medicine, University of Zagreb, Zagreb, Croatia

  20. Habrun B, Listes E, Spicic S, Cvetnic Z, Lukacevic D, Jemersic L, Lojkic M, Kompes G (2006) An outbreak of Salmonella Abortusovis abortions in sheep in South Croatia. J Vet Med B 53:286–290

    CAS  Article  Google Scholar 

  21. Colombo MM, Leori G, Rubino S, Barbato A, Cappuccinelli P (1992) Phenotypic features and molecular characterization of plasmids in Salmonella Abortusovis. J Gen Microbiol 138:725–731

    CAS  Article  Google Scholar 

  22. Nikbakht GH, Raffatellu M, Uzzau S, Tadjbakhsh H, Rubino S (2002) IS200 fingerprinting of Salmonella enterica serotype Abortusovis strains isolated in Iran. Epidemiol Infect 128:333–336

    CAS  Article  Google Scholar 

  23. Dionisi AM, Carattoli A, Luzzi I, Magistrali C, Pezzotti G (2006) Molecular genotyping of Salmonella enterica Abortusovis by pulsed field gel electrophoresis. Vet Microbiol 116:217–223

    CAS  Article  Google Scholar 

  24. Bacciu D, Falchi G, Spazziani A, Bossi L, Marogna G, Leori GS, Rubino S, Uzzau S (2004) Transposition of the heat-stable toxin astA gene into a gifsy-2-related prophage of Salmonella enterica serovar Abortusovis. J Bacteriol 186:4568–4574

    CAS  Article  Google Scholar 

  25. Uzzau S, Marogna G, Leori GS, Curtiss R 3rd, Schianchi G, Stocker BA, Rubino S (2005) Virulence attenuation and live vaccine potential of aroA, crp cdt cya, and plasmid-cured mutants of Salmonella enterica serovar Abortusovis in mice and sheep. Infect Immun 73:4302–4308

    CAS  Article  Google Scholar 

  26. World Organization for Animal Health [OIE] (2019). Manual of diagnostic tests and vaccines for terrestrial animals 2019. Chapter 3.9.8 Salmonellosis. https://www.oie.int/fileadmin/Home/eng/Health_standards/tahm/3.09.08_SALMONELLOSIS.pdf. Accessed Feb 2020

  27. ISO 6579–1:2017 Microbiology of the food chain—horizontal method for the detection, enumeration and serotyping of Salmonella—part 1: detection of Salmonella spp.

  28. Sting R, Nagel C, Steng G (1997) Detection methods for Salmonella Abortusovis and examination in sheep flocks in northern Baden-Würtenberg. Zbl Vet Med B 44:87–98

    CAS  Article  Google Scholar 

  29. Deligios M, Bacciu D, Deriu E, Corti G, Bordoni R, De Bellis G, Leori GS, Rubino S, Uzzau S (2014) Draft genome sequence of the host-restricted Salmonella enterica Serovar Abortusovis Strain SS44. Genome Announc 2(2):e00261–e00314. https://doi.org/10.1128/genomeA.00261-14

    Article  PubMed  PubMed Central  Google Scholar 

  30. Beuzón CR, Schiaffino A, Leori G, Cappuccinelli P, Rubino S, Casadesús J (1997) Identification of Salmonella Abortusovis by PCR amplification of a serovar-specific IS200 element. Appl Environ Microb 63:2082–2085

    Article  Google Scholar 

  31. Masala G, Porcu R, Daga C, Denti S, Canu G, Patta C, Tola S (2007) Detection of pathogens in ovine and caprine abortion samples from Sardinia, Italy, by PCR. J Vet Diagn Investig 19:96–98

    Article  Google Scholar 

  32. Navarro JA, Ortega N, Buendia AJ, Gallego MC, Martínez CM, Caro MR, Sánchez J, Salinas J (2009) Diagnosis of placental pathogens in small ruminants by immunohistochemistry and PCR on paraffin-embedded samples. Vet Rec 165:175–178

    CAS  Article  Google Scholar 

  33. Jensen AN, Nielsen LR, Baggesen DL (2013) Use of real-time PCR on fecal samples for detection of sub-clinical Salmonella infection in cattle did not improve the detection sensitivity compared to conventional bacteriology. Vet Microbiol 163:373–377

    CAS  Article  Google Scholar 

  34. Amagliani G, Petruzzelli A, Carloni E, Tonucci F, Foglini M, Micci E, Ricci M, Di Lullo S, Rotundo L, Brandi G (2016) Presence of Escherichia coli O157, Salmonella spp., and Listeria monocytogenes in raw ovine milk destined for cheese production and evaluation of the equivalence between the analytical methods applied. Foodborne Pathog Dis 13:626–632

    CAS  Article  Google Scholar 

  35. McClelland M, Sanderson KE, Clifton SW, Latreille P, Porwollik S, Sabo A, Meyer R, Bieri T, Ozersky P, McLellan M, Harkins CR, Wang C, Nguyen C, Berghoff A, Elliott G, Kohlberg S, Strong C, Du F, Carter J, Kremizki C, Layman D, Leonard S, Sun H, Fulton L, Nash W, Miner T, Minx P, Delehaunty K, Fronick C, Magrini V, Nhan M, Warren W, Florea L, Spieth J, Wilson RK (2004) Comparison of genome degradation in Paratyphi A and Typhi, human-restricted serovars of Salmonella enterica that cause typhoid. Nat Genet 36:1268–1274

    CAS  Article  Google Scholar 

  36. Porwollik S, Boyd EF, Choy C, Cheng P, Florea L, Proctor E, McClelland M (2004) Characterization of Salmonella enterica subspecies I genovars by use of microarrays. J Bacteriol 186:5883–5898

    CAS  Article  Google Scholar 

  37. Martín-Atance P, León L, Candela MG (2012) Serology as an epidemiological tool for Salmonella Abortusovis surveillance in the wild-domestic ruminant interface. In: Kumar Y (ed) Salmonella. A diversified superbug. InTech Open, London

    Google Scholar 

  38. Pardon P, Sanchis R, Marly J, Lantier F, Pépin M, Popoff M (1988) Ovine salmonellosis by Salmonella abortusovis. Ann Rech Vet 19:221–235

    CAS  PubMed  Google Scholar 

  39. Davies RH, Dalziel R, Gibbens JC, Wilesmith JW, Ryan JMB, Evans SJ, Byrne C, Paiba GA, Pascoe SJS, Teale CJ (2004) National survey for Salmonella in pigs, cattle and sheep at slaughter in Great Britain (1999–2000). J Appl Microbiol 96:750–760

    CAS  Article  Google Scholar 

  40. Brennan FR, Oliver JJ, Baird GD (1994) Differences in the immune response of mice and sheep to an aromatic-dependent mutant of Salmonella typhimurium. J Med Microbiol 41:20–28

    CAS  Article  Google Scholar 

  41. Berthon P, Gohin I, Lantier I, Olivier M (1994) Humoral immune response to Salmonella abortusovis in sheep: in vitro induction of an antibody synthesis from either sensitized or unprimed lymph node cells. Vet Immunol Immunopathol 41:275–294

    CAS  Article  Google Scholar 

  42. Veling J, van Zijderveld FG, van Zijderveld-van Bemmel AM, Barkema HW, Schukken YH (2000) Evaluation of three newly developed enzyme-linked immunosorbent assays and two agglutination tests for detecting Salmonella enterica subsp. enterica serovar dublin infections in dairy cattle. J Clin Microbiol 38:4402–4407

    CAS  Article  Google Scholar 

  43. Terrestrial Animal Health Standard Commission (2017) Report of the meeting of the OIE Terrestrial Animal Health Standards Commission. Chapter 1.4. Animal health surveillance. Paris, 18–29 September 2017. https://www.oie.int/fileadmin/Home/eng/Internationa_Standard_Setting/docs/pdf/A_TAHSC_Sept__2017_Report.pdf. Accessed 6 Dec 2021

  44. Silva D, Sanz MA (2019) A atualidade dos abortos em ovinos. Apormor News n. 4 Sept. 2019. http://www.apormor.pt/index.php/noticias/newsletter

  45. Pérez Béjar Linarejos R (2007) Aspectos epidemiológicos de las enfermedades contagiosas de la reproducción en las poblaciones de rumiantes silvestres y domésticos del Parque Natural de las Sierras de Cazorla, Segura y Las Villas (Jaén). Tesis Doctoral. Universidad de Murcia, Spain

  46. León Vizcaíno L, Alonso De Vega F, Garrido Abellán F, González Candela M, Martínez Carrasco-Pleite C, Pérez Béjar L, Cubero Pablo MJ, Ruiz De Ybáñez Carnero R, Arenas Casas A (2002) Estudio en masa sobre infecciones que causan mortalidad perinatal congénita entre rumiantes domésticos y silvestres en las sierras béticas. In: XXXIII Jornadas Científicas y XII Internacionales de la Sociedad Española de Ovinotecnia y Caprinotecnia. Consejería de Agricultura y Pesca, Junta de Andalucía, pp 325–330

  47. Pardon P, Sanchis R, Marly J, Lantier F, Guilloteau L, Buzoni-Gatel D, Oswald IP, Pepin M, Kaeffer B, Berthon P, Popoff MY (1990) Experimental ovine salmonellosis (Salmonella Abortusovis): pathogenesis and vaccination. Res Microbiol 141:945–953

    CAS  Article  Google Scholar 

  48. García-Seco T, Montbrau C, Fontseca M, March R, Sitja M, Domínguez BJ (2021) Efficacy of a Salmonella enterica serovar Abortusovis (S. Abortusovis) inactivated vaccine in experimentally infected gestating ewes. Res Vet Sci 135:486–494

    Article  Google Scholar 

Download references

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or nonprofit sectors.

Author information

Authors and Affiliations

  1. Dipartimento di Scienze Biomolecolari, Università degli Studi di Urbino Carlo Bo, via S. Chiara, 27, 61029, Urbino, PU, Italy

    Giulia Amagliani & Giorgio Brandi

  2. Diatheva Srl, via. Sant’Anna, 131/135, 61030, Fano, PU, Italy

    Maria E. La Guardia, Sabrina Dominici & Enrica Omiccioli

Authors
  1. Giulia Amagliani
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Maria E. La Guardia
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sabrina Dominici
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Giorgio Brandi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Enrica Omiccioli
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

EO had the idea for the article and performed the literature search. GA wrote the first version of the manuscript; MELG, SD, and GB reviewed and finalised the manuscript; GA and EO finalised the reviewed manuscript, approved and prepare it for submission. All authors have read and agreed to the published version of the manuscript.

Corresponding author

Correspondence to Giulia Amagliani.

Ethics declarations

Conflict of interest

There are no conflicts of interests/competing interests to be declared by the authors.

Ethical Approval

Not applicable.

Consent to Participate

Not applicable.

Consent for Publication

Not applicable.

Additional information

Publisher's Note

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

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Amagliani, G., La Guardia, M.E., Dominici, S. et al. Salmonella Abortusovis: An Epidemiologically Relevant Pathogen. Curr Microbiol 79, 3 (2022). https://doi.org/10.1007/s00284-021-02689-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00284-021-02689-1