[en] The objective of this retrospective study was to evaluate the clinical significance of fecal quantitative real-time polymerase chain reaction (qPCR) Salmonella results when taking the cycle threshold values (Ct) into account. The study included 120 Salmonella qPCR-positive fecal samples obtained from 88 hospitalized horses over a 2-year period. The mean Ct of the qPCR test was evaluated in regard to (1) clinical outcome and (2) systemic inflammatory response syndrome (SIRS) status (no SIRS, moderate SIRS, or severe SIRS) of the sampled horses. An ROC analysis was performed to establish the optimal cut-off Ct values associated with severe SIRS. The mean ± SD Ct value was significantly lower in samples (1) from horses with a fatal issue (27.87 ± 5.15 cycles) than in surviving horses (31.75 ± 3.60 cycles), and (2) from horses with severe SIRS (27.87 ± 2.78 cycles) than from horses with no (32.51 ± 3.59 cycles) or moderate (31.54 ± 3.02 cycles) SIRS. In the ROC analysis, the optimal cut-off value of Ct associated with a severe SIRS was 30.40 cycles, with an AUC value of 0.84 [95% confidence interval 0.76-0.91] and an OR of 0.64 [0.51-0.79]. Results suggest that including the Ct value in the interpretation of fecal qPCR results could improve the diagnostic value of this test for clinical salmonellosis in horses.
Disciplines :
Veterinary medicine & animal health
Author, co-author :
Amory, Hélène ; Université de Liège - ULiège > Fundamental and Applied Research for Animals and Health (FARAH) > FARAH: Médecine vétérinaire comparée
Cesarini Latorre, Carlota ; Université de Liège - ULiège > Fundamental and Applied Research for Animals and Health (FARAH) > FARAH: Médecine vétérinaire comparée
De Maré, Lorie ; Université de Liège - ULiège > Fundamental and Applied Research for Animals and Health (FARAH) > FARAH: Médecine vétérinaire comparée
Loublier, Clémence ; Université de Liège - ULiège > Fundamental and Applied Research for Animals and Health (FARAH) > FARAH: Médecine vétérinaire comparée
Moula, Nassim ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Méthodes expérimentales des animaux de laboratoire et éthique en expérimentation animale
Detilleux, Johann ; Université de Liège - ULiège > Département de gestion vétérinaire des Ressources Animales (DRA)
Saulmont, Marc; Regional Animal Health and Identification Association (ARSIA), 2 Allée des Artisans, ZA du Biron, 5590 Ciney, Belgium
Garigliany, Mutien-Marie ✱; Université de Liège - ULiège > Département de morphologie et pathologie (DMP) > Pathologie générale et autopsies
Lecoq, Laureline ✱; Université de Liège - ULiège > Fundamental and Applied Research for Animals and Health (FARAH)
✱ These authors have contributed equally to this work.
Language :
English
Title :
Relationship between the Cycle Threshold Value (Ct) of a Salmonella spp. qPCR Performed on Feces and Clinical Signs and Outcome in Horses.
Alternative titles :
[fr] Relation entre la valeur seuil du cycle (Ct) d'une qPCR de Salmonella spp. effectuée sur les matières fécales et les signes cliniques et l'issue chez les chevaux.
Original title :
[en] Relationship between the Cycle Threshold Value (Ct) of a Salmonella spp. qPCR Performed on Feces and Clinical Signs and Outcome in Horses.
Shaw S.D. Stämpfli H. Diagnosis and Treatment of Undifferentiated and Infectious Acute Diarrhea in the Adult Horse Vet. Clin. N. Am. Equine Pract. 2018 34 39 53 10.1016/j.cveq.2017.11.002
Teklemariam A.D. Al-Hindi R.R. Albiheyri R.S. Alharbi M.G. Alghamdi M.A. Filimban A.A.R. Al Mutiri A.S. Al-Alyani A.M. Alseghayer M.S. Almaneea A.M. et al. Human Salmonellosis: A Continuous Global Threat in the Farm-to-Fork Food Safety Continuum Foods 2023 12 1756 10.3390/foods12091756
Besser J.M. Salmonella epidemiology: A whirlwind of change Food Microbiol. 2018 71 55 59 10.1016/j.fm.2017.08.018
Hernandez J.A. Long M.T. Traub-Dargatz J.L. Besser T.E. Salmonellosis Equine Infectious Diseases 2nd ed. Sellon D. Long M.T. Saunders Elsevier St. Louis, MO, USA 2014 321 333
Kirk M.D. Pires S.M. Black R.E. Caipo M. Crump J.A. Devleesschauwer B. Doepfer D. Fazil A. Fischer-Walker C.L. Hald T. et al. World Health Organization estimates of the global and regional disease burden of 22 foodborne bacterial, protozoal, and viral diseases, 2010: A data synthesis PLoS Med. 2015 12 e1001921
European Centre for Disease Prevention and Control Salmonellosis ECDC. Annual Epidemiological Report for 2021 ECDC Stockholm, Sweden 2022 Available online: https://www.ecdc.europa.eu/sites/default/files/documents/SALM_AER_2021.pdf (accessed on 28 July 2023)
Arnold M. Piers Smith R. Tang Y. Guzinski J. Petrovska L. Bayesian Source Attribution of Salmonella Typhimurium Isolates From Human Patients and Farm Animals in England and Wales Front. Microbiol. 2021 12 579888 10.3389/fmicb.2021.579888 33584605
Espié E. De Valk H. Vaillant V. Quelquejeu N. Le Querrec F. Weill F.X. An outbreak of multidrug-resistant Salmonella enterica serotype Newport infections linked to the consumption of imported horse meat in France Epidemiol. Infect. 2005 133 373 3766 10.1017/S0950268804003449 15816165
Ward M.P. Brady T.H. Couëtil L.L. Liljebjelke K. Maurer J.J. Wu C.C. Investigation and control of an outbreak of salmonellosis caused by multidrug-resistant Salmonella typhimurium in a population of hospitalized horses Vet. Microbiol. 2005 107 233 240 10.1016/j.vetmic.2005.01.019
Steneroden K.K. Van Metre D.C. Jackson C. Morley P.S. Detection and control of a nosocomial outbreak caused by Sal-monella Newport at a large animal hospital J. Vet. Intern. Med. 2010 24 606 616 10.1111/j.1939-1676.2010.0484.x
Rankin S.C. Aceto H. Cassidy J. Holt J. Young S. Love B. Tewari D. Munro D.S. Benson C.E. Molecular character ization of cephalosporin-resistant Salmonella enterica sero type Newport isolates from animals in Pennsylvania J. Clin. Microbiol. 2002 40 4679 4684 10.1128/JCM.40.12.4679-4684.2002 12454172
Dallap Schaer B.L. Aceto H. Rankin S.C. Outbreak of salmonellosis caused by Salmonella enterica serovar Newport MDR-AmpC in a large animal veterinary teaching hospital J. Vet. Intern. Med. 2010 24 1138 1146 10.1111/j.1939-1676.2010.0546.x
Soza-Ossandón P. Rivera D. Tardone R. Riquelme-Neira R. García P. Hamilton-West C. Adell A.D. González-Rocha G. Moreno-Switt A.I. Widespread Environmental Presence of Multidrug-Resistant Salmonella in an Equine Veterinary Hospital That Received Local and International Horses Front. Vet. Sci. 2020 7 346 10.3389/fvets.2020.00346
Brenner F.W. Villar R.G. Angulo F.J. Angulo F.J. Tauxe R. Swaminathan B. Salmonella nomenclature J. Clin. Microbiol. 2000 38 2465 2467 10.1128/JCM.38.7.2465-2467.2000
Tindall B.J. Grimont P.A. Garrity G.M. Euzéby J.P. Nomenclature and taxonomy of the genus Salmonella Int. J. Syst. Evol. Microbiol. 2005 55 521 524 10.1099/ijs.0.63580-0
Chan K. Baker S. Kim C.C. Detweiler C.S. Dougan G. Falkow S. Genomic comparison of Salmonella enterica serovars and Salmonella bongori by use of an S. enterica serovar typhimurium DNA microarray J. Bacteriol. 2003 185 553 563 10.1128/JB.185.2.553-563.2003 12511502
European Food Safety Authority and European Centre for Disease Prevention and Control The European Union One Health 2018 Zoonoses Report EFSA J. 2019 17 e05926 Available online: https://www.ecdc.europa.eu/sites/default/files/documents/zoonoses-EU-one-health-2018-report.pdf (accessed on 28 July 2023) 10.2903/j.efsa.2019.5926
Martelli F. Sue K. Lawes J. Surveillance for Salmonella in horses in Great Britain Vet. Rec. 2019 184 56 58 10.1136/vr.l149
Leon I.M. Lawhon S.D. Norman K.N. Threadgill D.S. Ohta N. Vinasco J. Scott H.M. Serotype Diversity and Antimi-crobial Resistance among Salmonella enterica Isolates from Patients at an Equine Referral Hospital Appl. Environ. Microbiol. 2018 84 e02829-17 10.1128/AEM.02829-17
Uzal F.A. Arroyo L.G. Navarro M.A. Gomez D.E. Asín J. Henderson E. Bacterial and viral enterocolitis in horses: A review J. Vet. Diagn. Investig. 2022 34 354 375 10.1177/10406387211057469
van Duijkeren E. Sloet van Oldruitenborgh-Oosterbaan M.M. Houwers D.J. van Leeuwen W.J. Kalsbeek H.C. Equine salmonellosis in a Dutch veterinary teaching hospital Vet. Rec. 1994 13 248 250 10.1136/vr.135.11.248
van Duijkeren E. Flemming C. Sloet van Oldruitenborgh-Oosterbaan M.M. Kalsbeek H.C. van der Giessen J.W. Diagnosing salmonellosis in horses. Culturing of multiple versus single faecal samples Vet. Q. 1995 17 63 66 10.1080/01652176.1995.9694534
van Duijkeren E. Wannet W.J. Heck M.E. van Pelt W. Sloet van Oldruitenborgh-Oosterbaan M.M. Smit J.A. Houwers, D.J. Sero types, phage types and antibiotic susceptibilities of Salmonella strains isolated from horses in The Netherlands from 1993 to 2000 Vet. Microbiol. 2002 86 203 212 10.1016/S0378-1135(02)00007-X 11900955
Maddox T.W. Clegg P.D. Williams N.J. Pinchbeck G.L. Antimicrobial resistance in bacteria from horses: Epidemiology of antimicrobial resistance Equine Vet. J. 2015 47 756 765 10.1111/evj.12471 26084443
Walther B. Tedin K. Lübke-Becker A. Multidrug-resistant opportunistic pathogens challenging veterinary infection control Vet. Microbiol. 2017 200 71 78 10.1016/j.vetmic.2016.05.017 27291944
Martelli F. Sue K. Lawes J. Salmonella and salmonellosis in horses: An overview Vet. Rec. 2018 182 659 660 10.1136/vr.k2525
Theelen M.J. Wilson W.D. Edman J.M. Magdesian K.G. Kass P.H. Temporal trends in prevalence of bacteria isolated from foals with sepsis: 1979–2010 Equine Vet. J. 2014 46 169 173 10.1111/evj.12131
Mather A.E. Reid S.W. Maskell D.J. Parkhill J. Fookes M.C. Harris S.R. Brown D.J. Coia J.E. Mulvey M.R. Gilmour M.W. et al. Distinguishable epidemics of multidrug-resistant Salmonella Typhimurium DT104 in different hosts Science 2013 341 1514 1517 10.1126/science.1240578
Le Hello S. Bekhit A. Granier S.A. Barua H. Beutlich J. Zając M. Münch S. Sintchenko V. Bouchrif B. Fashae K. et al. The global establishment of a highly-fluoroquinolone resistant Salmonella enterica serotype Kentucky ST198 strain Front. Microbiol. 2013 4 395 10.3389/fmicb.2013.00395
Dargatz D.A. Traub-Dargatz J.L. Multidrug-resistant Salmonella and nosocomial infections Vet. Clin. N. Am. Equine Pract. 2004 20 587 600 10.1016/j.cveq.2004.07.008
Dallap Schaer B.L. Aceto H. Caruso M.A. Brace M.A. Identification of predictors of Salmonella shedding in adult horses presented for acute colic J. Vet. Intern. Med. 2012 26 1177 1185 10.1111/j.1939-1676.2012.00984.x
Burgess B.A. Bauknecht K. Slovis N.M. Morley P.S. Factors associated with equine shedding of multidrug-resistant Salmonella enterica and its impact on health outcomes Equine Vet. J. 2018 50 616 623 10.1111/evj.12823 29486062
Ekiri A.B. MacKay R.J. Gaskin J.M. Freeman D.E. House A.M. Giguère S. Troedsson M.R. Schuman C.D. von Chamier M.M. Henry K.M. et al. Epidemiologic analysis of nosocomial Salmonella infections in hospitalized horses J. Am. Vet. Med. Assoc. 2009 234 108 119 10.2460/javma.234.1.108
Burgess B.A. Morley P.S. Risk factors for shedding of Salmonella enterica among hospitalized large animals over a 10-year period in a veterinary teaching hospital J. Vet. Intern. Med. 2019 33 2239 2248 10.1111/jvim.15579
Sanchez L.C. Disorders of the gastrointestinal system Equine Internal Medicine 4th ed. Reed S.M. Warwick B.W. Sellon D. Elsevier St. Louis, MO, USA 2018 709 842
Pusterla N. Byrne B.A. Hodzic E. Mapes S. Jang S.S. Magdesian K.G. Use of quantitative real-time PCR for the detection of Salmonella spp. in fecal samples from horses at a veterinary teaching hospital Vet. J. 2010 186 252 255 10.1016/j.tvjl.2009.08.022 19766027
Ekiri A.B. Long M.T. Hernandez J.A. Diagnostic performance and application of a real-time PCR assay for the detection of Salmonella in fecal samples collected from hospitalized horses with or without signs of gastrointestinal tract disease Vet. J. 2016 208 28 32 10.1016/j.tvjl.2015.11.011
Ward M.P. Alinovi C.A. Couëtil L.L. Wu C.C. Evaluation of a PCR to detect Salmonella in fecal samples of horses admitted to a veterinary teaching hospital J. Vet. Diagn. Investig. 2005 17 118 123 10.1177/104063870501700204
Cohen N.D. Martin L.J. Simpson R.B. Wallis D.E. Neibergs H.L. Comparison of polymerase chain reaction and micro-biological culture for detection of salmonellae in equine feces and environmental samples Am. J. Vet. Res. 1996 57 780 786
Kurowski P.B. Traub-Dargatz J.L. Morley P.S. Gentry-Weeks C.R. Detection of Salmonella spp. in fecal specimens by use of real-time polymerase chain reaction assay Am. J. Vet. Res. 2002 63 1265 1268 10.2460/ajvr.2002.63.1265
Adams D.R. Stensland W.R. Wang C.H. O’Connor A.M. Trampel D.W. Harmon K.M. Strait E.L. Frana T.S. Detection of Salmonella enteritidis in pooled poultry environmental samples using a serotype-specific real-time-polymerase chain reaction assay Avian Dis. 2013 57 22 28 10.1637/10279-061312-Reg.1 23678725
Brizuela M.E. Goñi S.E. Cardama G.A. Zinni M.A. Castello A.A. Sommese L.M. Farina H.G. Correlation of SARS-CoV-2 Viral Load and Clinical Evolution of Pediatric Patients in a General Hospital From Buenos Aires, Argentina Front. Pediatr. 2022 10 883395 10.3389/fped.2022.883395 35874580
Roy M.F. Kwong J. Lambert S. Massie S. Lockhart S. Prognostic Value and Development of a Scoring System in Horses With Systemic Inflammatory Response Syndrome J. Vet. Intern. Med. 2017 31 582 10.1111/jvim.14670 28207163
Southwood L.L. Lindborg S. Myers M. Aceto H.W. Influence of Salmonella status on the long-term outcome of horses after colic surgery Vet. Surg. 2017 46 780 788 10.1111/vsu.12660 28462509
Moore M.M. Feist M.D. Real-time PCR method for Salmonella spp. targeting the stn gene J. Appl. Microbiol. 2007 102 516 530 10.1111/j.1365-2672.2006.03079.x 17241358
Piorkowski G. Baronti C. de Lamballerie X. de Fabritus L. Bichaud L. Pastorino B.A. Bessaud M. Development of generic Taqman PCR and RT-PCR assays for the detection of DNA and mRNA of β-Actin-encoding sequences in a wide range of animal species J. Virol. Methods. 2014 202 101 105 10.1016/j.jviromet.2014.02.026
Hird D.W. Casebolt D.B. Carter J.D. Pappaioanou M. Hjerpe C.A. Risk factors for salmonellosis in hospitalized horses J. Am. Vet. Med. Assoc. 1986 188 173 177
Traub-Dargatz J.L. Salman M.D. Jones R.L. Epidemiologic study of salmonellae shedding in the feces of horses and potential risk factors for development of the infection in hospitalized horses J. Am. Vet. Med. Assoc. 1990 196 1617 1622
Kim L.M. Morley P.S. Traub-Dargatz J.L. Salman M.D. Gentry-Weeks C. Factors associated with Salmonella shedding among equine colic patients at a veterinary teaching hospital J. Am. Vet. Med. Assoc. 2001 218 740 748 10.2460/javma.2001.218.740
Kilcoyne I. Magdesian K.G. Guerra M. Dechant J.E. Spier S.J. Kass P.H. Prevalence of and risk factors associated with Salmonella shedding among equids presented to a veterinary teaching hospital for colic (2013–2018) Equine Vet. J. 2022 55 446 455 10.1111/evj.13864
Alinovi C.A. Ward M.P. Couëtil L.L. Wu C.C. Risk factors for fecal shedding of Salmonella from horses in a veterinary teaching hospital Prev. Vet. Med. 2003 12 307 317 10.1016/S0167-5877(03)00143-0
Luethy D. Feldman R. Stefanovski D. Aitken M.R. Risk factors for laminitis and nonsurvival in acute colitis: Retrospective study of 85 hospitalized horses (2011–2019) J. Vet. Intern. Med. 2021 35 2019 2025 10.1111/jvim.16147
Kopper J.J. Willette J.A. Kogan C.J. Seguin A. Bolin S.R. Schott H.C. 2nd Detection of pathogens in blood or feces of adult horses with enteric disease and association with outcome of colitis J. Vet. Intern. Med. 2021 35 2465 2472 10.1111/jvim.16238
Willette J.A. Kopper J.J. Kogan C.J. Seguin M.A. Schott H.C. Effect of season and geographic location in the United States on detection of potential enteric pathogens or toxin genes in horses ≥6-mo-old J. Vet. Diagn. Investig. 2022 34 407 411 10.1177/10406387211056054 34763559
Hensel M. Meason-Smith C. Plumlee Q.D. Myers A.N. Coleman M.C. Lawhon S. Rodrigues Hoffmann A. Rech R.R. Retrospective Analysis of Aetiological Agents Associated with Pulmonary Mycosis Secondary to Enteric Salmonellosis in Six Horses by Panfungal Polymerase Chain Reaction J. Comp. Pathol. 2020 174 1 7 10.1016/j.jcpa.2019.10.002 31955794
Akinola S.A. Mwanza M. Ateba C.N. Occurrence, Genetic Diversities And Antibiotic Resistance Profiles Of Salmonella Serovars Isolated From Chickens Infect. Drug Resist. 2019 12 3327 3342 10.2147/IDR.S217421 31695452
Murray R.A. Lee C.A. Invasion genes are not required for Salmonella enterica serovar typhimurium to breach the intestinal epithelium: Evidence that salmonella pathogenicity island 1 has alternative functions during infection Infect. Immun. 2000 68 5050 5055 10.1128/IAI.68.9.5050-5055.2000 10948124
Buehler A.J. Wiedmann M. Kassaify Z. Cheng R.A. Evaluation of invA Diversity among Salmonella Species Suggests Why Some Commercially Available Rapid Detection Kits May Fail To Detect Multiple Salmonella Subspecies and Species J. Food Prot. 2019 82 710 717 10.4315/0362-028X.JFP-18-525
El Khatib K. Hadeer R.A. Saad A. Kalaydjian A. Fayad E. Mahfouz Y. Dougnon V. Daoud Z. Abdel-Massih R.M. Determination of MIC, MPC, and MSW of Ilex paraguariensis against non-typhoidal Salmonella with identification of the mechanisms of resistance and pathogenicity factors Microb. Pathog. 2023 174 105905 10.1016/j.micpath.2022.105905
Makino S. Kurazono H. Chongsanguam M. Hayashi H. Cheun H. Suzuki S. Shirahata T. Establishment of the PCR system specific to Salmonella spp. and its application for the inspection of food and fecal samples J. Vet. Med. Sci. 1999 61 1245 1247 10.1292/jvms.61.1245
Del Cerro A. Soto S.M. Landeras E. Gonzalez-Hevia M.A. Guijarro J.A. Mendoza M.C. PCR-based procedures in detection and DNA-fingerprinting of Salmonella from samples of animal origin Food Microbiol. 2002 19 567 575 10.1006/fmic.2002.0512
Malorny B. Hoorfar J. Bunge C. Helmuth R. Multicenter validation of the analytical accuracy of Salmonella PCR: Towards an international standard Appl. Environ. Microbiol. 2003 69 290 296 10.1128/AEM.69.1.290-296.2003
Murugkar H.V. Rahman H. Dutta P.K. Distribution of virulence genes in Salmonella serovars isolated from man & animals Indian J. Med. Res. 2003 117 66 70
Ziemer C.J. Steadham S.R. Evaluation of the specificity of Salmonella PCR primers using various intestinal bacterial species Lett. Appl. Microbiol. 2003 37 463 469 10.1046/j.1472-765X.2003.01430.x
Hartnack A.K. Van Metre D.C. Morley P.S. Salmonella enterica shedding in hospitalized horses and associations with diarrhea occurrence among their stablemates and gastrointestinal-related illness or death following discharge J. Am. Vet. Med. Assoc. 2012 240 726 733 10.2460/javma.240.6.726
Mainar-Jaime R.C. House J.K. Smith B.P. Kamiya D.Y. Influence of fecal shedding of Salmonella organisms on mortality in hospitalized horses J. Am. Vet. Med. Assoc. 1998 213 1162 1166 9787385
Jiang Q. Fu B. Chen Y. Wang Y. Liu H. Quantification of viable but nonculturable bacterial pathogens in anaerobic di-gested sludge Appl. Microbiol. Biotechnol. 2013 97 6043 6050 10.1007/s00253-012-4408-2 22996281
Porter W. Kelley E. Bowers J. Engelthaler D. Normalization of SARS-CoV-2 viral load via RT-qPCR provides higher-resolution data for comparison across time and between patients Virus Res. 2021 306 198604 10.1016/j.virusres.2021.198604 34662682
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