Reliability Evaluation of MALDI-TOF MS Associated with SARAMIS Software in Rapid Identification of Thermophilic Campylobacter Isolated from Food

  • Graziella Ziino
  • Stefania Maria Marotta
  • Filippo GiarratanaEmail author
  • Alessandro Giuffrida
  • Felice Panebianco


Thermophilic Campylobacter species represent the most frequent cause of food-borne disease worldwide. Biochemical and serological tests, according to ISO 10272:2017, are routinely used in microbiology laboratories for their detection/identification. However, these procedures require a lot of time and can incur in diagnostic mistakes. Matrix-assisted laser desorption ionization time-of-flight mass spectrometry (MALDI-TOF MS) is considered a promising identification method for bacteria and fungi from clinical isolates. The aim of this study was to evaluate the reliability of MALDI-TOF MS associated with SARAMIS software, in rapid identification of food-related Campylobacter spp., considering that this method was tested only on human and animal clinical strains. A total of 276 putative thermophilic Campylobacter strains, isolated from different foodstuffs according to ISO 10272-1:2006, were identified comparing the results of MALDI-TOF MS/SARAMIS with Multiplex PCR assay. MALDI-TOF MS/SARAMIS correctly identified 96% (n = 267) of strains at the species level, while only 2.5% (n = 7) of strains were not identified. Misidentification occurred in 0.7% (n = 2) of samples. The performance of this method demonstrated an overall sensitivity (Se) of 97.45% and specificity (Sp) of 100%. Thus, this method can be used for the rapid identification of Campylobacter strains isolated from food samples according to ISO 10272:2017.


MALDI-TOF MS SARAMIS TM Campylobacter Rapid identification Food strains 


Compliance with Ethical Standards

Conflict of Interest

Graziella Ziino declares that she has no conflict of interest. Stefania Maria Marotta declares that she has no conflict of interest. Filippo Giarratana declares that he has no conflict of interest. Alessandro Giuffrida declares that he has no conflict of interest. Felice Panebianco declares that he has no conflict of interest.

Ethical Approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Informed Consent

Not applicable.


  1. Alispahic M, Hummel K, Jandreski-Cvetkovic D, Nöbauer K, Razzazi-Fazeli E, Hess M, Hess C (2010) Species-specific identification and differentiation of Arcobacter, Helicobacter and Campylobacter by full-spectral matrix-associated laser desorption/ionization time of flight mass spectrometry analysis. J Med Microbiol 59(3):295–301. CrossRefGoogle Scholar
  2. Attien P, Sina H, Moussaoui W, Zimmermann-Meisse G, Dadié T, Keller D, Riegel P, Edoh V, Kotchoni SO, Djè M, Prèvost G, Baba-Moussa L (2014) Mass spectrometry and multiplex antigen assays to assess microbial quality and toxin production of Staphylococcus aureus strains isolated from clinical and food samples. Biomed Res Int 2014:1–8. CrossRefGoogle Scholar
  3. Bessede E, Solecki O, Sifre E, Labadi L, Megraud F (2011) Identification of Campylobacter species and related organisms by matrix assisted laser desorption ionization–time of flight (MALDI-TOF) mass spectrometry. Clin Microbiol Infect 17(11):1735–1739. CrossRefGoogle Scholar
  4. Biswas S, Rolain JM (2013) Use of MALDI-TOF mass spectrometry for identification of bacteria that are difficult to culture. J Microbiol Methods 92(1):14–24. CrossRefGoogle Scholar
  5. Deckert A, Valdivieso-Garcia A, Reid-Smith R, Tamblyn S, Seliske P, Irwin R, De Wey C, Boerlin P, McEwen SA (2010) Prevalence and antimicrobial resistance in Campylobacter spp. isolated from retail chicken in two health units in Ontario. J Food Prot 73:1317–1324. CrossRefGoogle Scholar
  6. Duarte A, Santos A, Manageiro V, Martins A, Fraqueza MJ, Caniça M, Domingues FC, Oleastro M (2014) Human, food and animal Campylobacter spp. isolated in Portugal: high genetic diversity and antibiotic resistance rates. Int J Antimicrob Agents 44(4):306–313. CrossRefGoogle Scholar
  7. Dubois D, Grare M, Prere MF, Segonds C, Marty N, Oswald E (2012) Performances of the Vitek MS matrix-assisted laser desorption ionization–time of flight mass spectrometry system for rapid identification of bacteria in routine clinical microbiology. J Clin Microbiol 50(8):2568–2576. CrossRefGoogle Scholar
  8. Eaton TJ, Gasson MJ (2001) Molecular screening of Enterococcus virulence determinants and potential for genetic exchange between food and medical isolates. Appl Environ Microbiol 67(4):1628–1635CrossRefGoogle Scholar
  9. EFSA (European Food Safety Authority), ECDC (European Centre for Disease Prevention and Control) (2015) The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2014. EFSA J 13(12):4329Google Scholar
  10. EFSA (European Food Safety Authority), ECDC (European Centre for Disease Prevention and Control) (2017) The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2016. EFSA J 15(12):5077. Google Scholar
  11. EFSA Panel on Biological Hazards (BIOHAZ) (2005) Opinion of the scientific panel on biological hazards on the request from the commission related to Campylobacter in animals and foodstuffs. EFSA J 173:1–105Google Scholar
  12. EFSA Panel on Biological Hazards (BIOHAZ) (2011) Scientific opinion on Campylobacter in broiler meat production: control options and performance objectives and/or targets at different stages of the food chain. EFSA J 9:2105CrossRefGoogle Scholar
  13. Elbehiry A, Marzouk E, Hamada M, Al-Dubaib M, Alyamani E, Moussa IM, Al Rowaidhan A, Hemeg HA (2017) Application of MALDI-TOF MS fingerprinting as a quick tool for identification and clustering of foodborne pathogens isolated from food products. New Microbiol 40(3):169–178Google Scholar
  14. El-Bouri K, Johnston S, Rees E, Thomas I, Bome-Mannathoko N, Jones C, Reid M, Ben-Ismaeil B, Davies AP, Harris LG, Mack D (2012) Comparison of bacterial identification by MALDI-TOF mass spectrometry and conventional diagnostic microbiology methods: agreement, speed and cost implications. Br J Biomed Sci 69(2):47–55CrossRefGoogle Scholar
  15. Gilbert M, Karwaski MF, Bernatchez S, Young NM, Taboada E, Michniewicz J, Cunningham AM, Wakarchuk WW (2002) The genetic bases for the variation in the lipo-oligosaccharide of the mucosal pathogen, Campylobacter jejuni. Biosynthesis of sialylated ganglioside mimics in the core oligosaccharide. J Biol Chem 277(1):327–337. CrossRefGoogle Scholar
  16. Groot MN, de Boer AG, van Pelt W, van der Hulst-van Arkel MC, de Leeuw P, Widjaja HCA, Smits MA, van der Wal FJ (2014) A SpoT polymorphism correlates with chill stress survival and is prevalent in clinical isolates of Campylobacter jejuni. Poult Sci 93(11):2900–2909. CrossRefGoogle Scholar
  17. Hoelzl C, Mayerhofer U, Steininger M, Brüller W, Hofstädter D, Aldrian U (2013) Observational trial of safe food handling behavior during food preparation using the example of Campylobacter spp. J Food Prot 76(3):482–489. CrossRefGoogle Scholar
  18. Hsieh YH, Wang YF, Moura H, Miranda N, Simpson S, Gowrishankar R, Barr J, Kerdahi K, Sulaiman IM (2017) Application of MALDI-TOF MS Systems in the Rapid Identification of Campylobacter spp. of Public Health Importance. J AOAC Int 101(3):761–768. CrossRefGoogle Scholar
  19. Huber I, Pavlovic M, Maggipinto M, Konrad R, Busch U (2018) Interlaboratory proficiency test using MALDI-TOF MS for identification of food-associated bacteria. Food Anal Methods 11:1068–1075. CrossRefGoogle Scholar
  20. ISO-International Organization for Standardization 10272-1:2006 (2006) Microbiology of food and animal feeding stuffs-Horizontal method for detection and enumeration of Campylobacter spp. - Part 1: Detection method. International Organization for Standardization, GenevaGoogle Scholar
  21. ISO-International Organization for Standardization 10272-1:2017 (2017) Microbiology of food and animal feeding stuffs – horizontal method for detection and enumeration of Campylobacter spp. – Part 1: Detection method. International Organization for Standardization, GenevaGoogle Scholar
  22. Jadhav S, Sevior D, Bhave M, Palombo EA (2014) Detection of Listeria monocytogenes from selective enrichment broth using MALDI–TOF mass spectrometry. J Proteome 97:100–1066. CrossRefGoogle Scholar
  23. Janssen R, Krogfelt KA, Cawthraw SA, van Pelt W, Wagenaar JA, Owen RJ (2008) Host-pathogen interactions in campylobacter infections: the host perspective. Clin Microbiol Rev 21(3):505–518. CrossRefGoogle Scholar
  24. Karlyshev AV, Champion OL, Churcher C, Brisson JR, Jarrell HC, Gilbert M, Brochu D, St Michael F, Li J, Wakarchuk WW, Goodhead I, Sanders M, Stevens K, White B, Parkhill J, Wren BW, Szymanski CM (2005) Analysis of Campylobacter jejuni capsular loci reveals multiple mechanisms for the generation of structural diversity and the ability to form complex heptoses. Mol Microbiol 55(1):90–103CrossRefGoogle Scholar
  25. Kolinska R, Dřevínek M, Jakubů V, Žemličková H (2008) Species identification of Campylobacter jejuni ssp. jejuni and C. coli by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry and PCR. Folia Microbiol (Praha) 53(5):403–409. CrossRefGoogle Scholar
  26. Martiny D, Dediste A, Debruyne L, Vlaes L, Haddou NB, Vandamme P, Vandenberg O (2011) Accuracy of the API campy system, the Vitek 2 Neisseria–Haemophilus card and matrix-assisted laser desorption ionization time-of-flight mass spectrometry for the identification of Campylobacter and related organisms. Clin Microbiol Infect 17(7):1001–1006. CrossRefGoogle Scholar
  27. Martiny D, Visscher A, Catry B, Chatellier S, Vandenberg O (2013) Optimization of Campylobacter growth conditions for further identification by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS). J Microbiol Methods 94(3):221–223. CrossRefGoogle Scholar
  28. Mattei R, Vicario C, Nardone M, Savarino A (2012) Evaluation of the system Axima/Saramis MALDI-TOF MS bioMérieux in a clinical laboratory. Microbiol Medica 27(1):34–37CrossRefGoogle Scholar
  29. On SL (2001) Taxonomy of Campylobacter, Arcobacter, Helicobacter and related bacteria: current status, future prospects and immediate concerns. Symp Ser Soc Appl Microbiol 30:1S–15SCrossRefGoogle Scholar
  30. On SL (2013) Isolation, identification and subtyping of Campylobacter: where to from here? J Microbiol Methods 95(1):3–7. CrossRefGoogle Scholar
  31. Panda A, Ghosh AK, Mirdha BR, Xess I, Paul S, Samantaray JC, Srinivasan A, Khalil S, Rastogi N, Dabas Y (2015) MALDI-TOF mass spectrometry for rapid identification of clinical fungal isolates based on ribosomal protein biomarkers. J Microbiol Methods 9:93–105. CrossRefGoogle Scholar
  32. Stella S, Soncini G, Ziino G, Panebianco A, Pedonese F, Nuvoloni R, Di Giannatale E, Colavita G, Alberghini L, Giaccone V (2017) Prevalence and quantification of thermophilic Campylobacter spp. in Italian retail poultry meat: analysis of influencing factors. Food Microbiol 62:232–238. CrossRefGoogle Scholar
  33. Wang G, Clark CG, Taylor TM, Pucknell C, Barton C, Price L, Woodward DL, Rodgers FG (2002) Colony multiplex PCR assay for identification and differentiation of Campylobacter jejuni, C. coli, C. lari, C. upsaliensis, and C. fetus subsp. fetus. J Clin Microbiol 40(12):4744–4747CrossRefGoogle Scholar
  34. Wenning M, Breitenwieser F, Konrad R, Huber I, Busch U, Scherer S (2014) Identification and differentiation of food-related bacteria: a comparison of FTIR spectroscopy and MALDI-TOF mass spectrometry. J Microbiol Methods 103:44–52. CrossRefGoogle Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Veterinary SciencesUniversity of MessinaMessinaItaly
  2. 2.Department of Agraria“Mediterranea” University of Reggio CalabriaReggio CalabriaItaly

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