View More View Less
  • 1 University Medical Centre, Rotterdam, The Netherlands
  • | 2 Wageningen University, The Netherlands
  • | 3 FrieslandCampina, Amersfoort, The Netherlands
Open access

Raw milk is a recognized source of Campylobacter outbreaks, but pasteurization is an effective way to eliminate the causative agent of Campylobacteriosis. Whereas breastfeeding is protective against infectious diseases, consumption of formula milk is thought to be not. However, in relation to Campylobacter, such data is currently unavailable. Although both pasteurized and formula milk are pathogen free and prepared in a quality controlled manner, the effect they have on the virulence of Campylobacter species is unknown. Here, we studied the effect of cow, goat, horse, and formula milk on Campylobacter invasion into intestinal epithelial Caco-2 cells, a pathogenic feature of this bacterial species, using a gentamicin exclusion invasion assay. We found that all milk products modulated the invasion of Campylobacter species into the Caco-2 cells in a dose-dependent manner. Control experiments showed that the milks were not toxic for the Caco-2 cells and that the effect on invasion is caused by heat labile (e.g., milk proteins) or heat stable (e.g., sugar/lipids) components depending on the Campylobacter species studied. This in vitro study shows for the first time that pasteurized and formula milk affect the invasion of Campylobacter. We recommend a prospective study to examine whether pasteurized and formula milk affect Campylobacteriosis.

  • 1.

    Drewnowski A : The contribution of milk and milk products to micronutrient density and affordability of the U.S. diet. J Am Coll Nutr 30, 422S428S (2011)

    • Search Google Scholar
    • Export Citation
  • 2.

    Turck D : Cow’s milk and goat’s milk. World Rev Nutr Diet 108, 5662 (2013)

  • 3.

    Committee on Infectious Diseases and Nutrition: Consumption of raw or unpasteurized milk and milk products by pregnant women and children. Pediatrics 133, 175179 (2014)

    • Search Google Scholar
    • Export Citation
  • 4.

    Fang G , Araujo V, Guerrant, RL: Enteric infections associated with exposure to animals or animal products. Infect Dis Clin North Am 5, 681701 (1991)

    • Search Google Scholar
    • Export Citation
  • 5.

    Oliver SP , Boor KJ, Murphy SC, Murinda SE: Food safety hazards associated with consumption of raw milk. Foodborne Pathog Dis 6, 793806 (2009)

    • Search Google Scholar
    • Export Citation
  • 6.

    Oliver SP , Jayarao BM, Almeida RA: Foodborne pathogens in milk and the dairy farm environment: food safety and public health implications. Foodborne Pathog Dis 2, 115129 (2005)

    • Search Google Scholar
    • Export Citation
  • 7.

    Skovgaard N : New trends in emerging pathogens. Int J Food Microbiol 120, 217224 (2007)

  • 8.

    de Noordhout CM , Devleesschauwer B, Angulo, FJ, Verbeke G, Haagsma J, Kirk M, Havelaar A, Speybroeck N: The global burden of listeriosis: a systematic review and meta-analysis. Lancet Infect Dis 14, 10731082 (2014)

    • Search Google Scholar
    • Export Citation
  • 9.

    Fendler C , Laitko S, Sorensen H, Gripenberg-Lerche C, Groh A, Uksila J, Granfors K, Braun J, Sieper J: Frequency of triggering bacteria in patients with reactive arthritis and undifferentiated oligoarthritis and the relative importance of the tests used for diagnosis. Ann Rheum Dis 60, 337343 (2001)

    • Search Google Scholar
    • Export Citation
  • 10.

    Hamon MA , Ribet D, Stavru F, Cossart P: Listeriolysin O: the Swiss army knife of Listeria. Trends Microbiol 20, 360368 (2012)

  • 11.

    Leung FY , Littlejohn GO, Bombardier C: Reiter’s syndrome after Campylobacter jejuni enteritis. Arthritis Rheum 23, 948950 (1980)

  • 12.

    van Doorn PA , Ruts L, Jacobs BC: Clinical features, pathogenesis, and treatment of Guillain-Barré syndrome. Lancet Neurol 7, 939950 (2008)

    • Search Google Scholar
    • Export Citation
  • 13.

    Revez J , Zhang J, Schott T, Kivisto R, Rossi M, Hanninen ML: Genomic variation between Campylobacter jejuni isolates associated with milk-borne-disease outbreaks. J Clin Microbiol 52, 27822786 (2014)

    • Search Google Scholar
    • Export Citation
  • 14.

    Sahin O , Fitzgerald C, Stroika S, Zhao S, Sippy RJ, Kwan P, Plummer PJ, Han J, Yaeger MJ, Zhang Q: Molecular evidence for zoonotic transmission of an emergent, highly pathogenic Campylobacter jejuni clone in the United States. J Clin Microbiol 50, 680687 (2012)

    • Search Google Scholar
    • Export Citation
  • 15.

    Taylor DN , Porter BW, Williams CA, Miller HG, Bopp CA, Blake PA: Campylobacter enteritis: a large outbreak traced to commercial raw milk. West J Med 137, 365369 (1982)

    • Search Google Scholar
    • Export Citation
  • 16.

    Louwen R , van Baarlen P, van Vliet AHM, van Belkum A, Hays JP, Endtz HP: Campylobacter bacteremia: a rare and under-reported event? Eur J Microbiol Immunol 2, 7687 (2012)

    • Search Google Scholar
    • Export Citation
  • 17.

    Arifeen S , Black RE, Antelman G, Baqui A, Caulfield L, Becker S: Exclusive breastfeeding reduces acute respiratory infection and diarrhea deaths among infants in Dhaka slums. Pediatrics 108, E67 (2001)

    • Search Google Scholar
    • Export Citation
  • 18.

    Bode L , McGuire M, Rodriguez JM, Geddes DT, Hassiotou F, Hartmann PE, McGuire MK: It’s alive: microbes and cells in human milk and their potential benefits to mother and infant. Adv Nutr 5, 571573 (2014)

    • Search Google Scholar
    • Export Citation
  • 19.

    Rogier EW , Frantz AL, Bruno ME, Wedlund L, Cohen DA, Stromberg AJ, Kaetzel CS: Lessons from mother: longterm impact of antibodies in breast milk on the gut microbiota and intestinal immune system of breastfed offspring. Gut Microbes 5, 663668 (2014)

    • Search Google Scholar
    • Export Citation
  • 20.

    Brown KH , Black RE, Lopez de Romana G, Creed de Kanashiro H: Infant-feeding practices and their relationship with diarrheal and other diseases in Huascar (Lima), Peru. Pediatrics 83, 3140 (1989)

    • Search Google Scholar
    • Export Citation
  • 21.

    Felisbino-Mendes MS , Villamor E, Velasquez-Melendez G: Association of maternal and child nutritional status in Brazil: a population based cross-sectional study. PLoS One 9, e87486 (2014)

    • Search Google Scholar
    • Export Citation
  • 22.

    Liu B , Newburg DS: Human milk glycoproteins protect infants against human pathogens. Breastfeed Med 8, 354362 (2013)

  • 23.

    Peterson R , Cheah WY, Grinyer J, Packer N: Glycoconjugates in human milk: protecting infants from disease. Glycobiology 23, 14251438 (2013)

    • Search Google Scholar
    • Export Citation
  • 24.

    Bode L , Jantscher-Krenn E: Structure-function relationships of human milk oligosaccharides. Adv Nutr 3, 383S391S (2012)

  • 25.

    Furst P : Dioxins, polychlorinated biphenyls and other organohalogen compounds in human milk. Levels, correlations, trends and exposure through breastfeeding. Mol Nutr Food Res 50, 922933 (2006)

    • Search Google Scholar
    • Export Citation
  • 26.

    Lawrence RM , Lawrence RA: Breast milk and infection. Clin Perinatol 31, 501528 (2004)

  • 27.

    Carvalho RS , Michail S, Ashai-Khan F, Mezoff AG: An update on pediatric gastroenterology and nutrition: a review of some recent advances. Curr Probl Pediatr Adolesc Health Care 38, 204228 (2008)

    • Search Google Scholar
    • Export Citation
  • 28.

    Bowen AB , Braden CR: Invasive Enterobacter sakazakii disease in infants. Emerg Infect Dis 12, 11851189 (2006)

  • 29.

    Cahill SM , Wachsmuth IK, Costarrica Mde L, Ben Embarek PK: Powdered infant formula as a source of Salmonella infection in infants. Clin Infect Dis 46, 268273 (2008)

    • Search Google Scholar
    • Export Citation
  • 30.

    Gilbert M , Godschalk PC, Karwaski MF, Ang CW, van Belkum A, Li J, Wakarchuk WW, Endtz HP: Evidence for acquisition of the lipooligosaccharide biosynthesis locus in Campylobacter jejuni GB11, a strain isolated from a patient with Guillain-Barré syndrome, by horizontal exchange. Infect Immun 72, 11621165 (2004)

    • Search Google Scholar
    • Export Citation
  • 31.

    Louwen R , Heikema A, van Belkum A, Ott A, Gilbert M, Ang W, Endtz HP, Bergman MP, Nieuwenhuis EE: The sialylated lipooligosaccharide outer core in Campylobacter jejuni is an important determinant for epithelial cell invasion. Infect Immun 76, 44314438 (2008)

    • Search Google Scholar
    • Export Citation
  • 32.

    Pricope-Ciolacu L , Nicolau AI, Wagner M, Rychli K: The effect of milk components and storage conditions on the virulence of Listeria monocytogenes as determined by a Caco-2 cell assay. Int J Food Microbiol 166, 5964 (2013)

    • Search Google Scholar
    • Export Citation
  • 33.

    Hall T , Dymock D, Corfield AP, Weaver G, Woodward M, Berry M: Bacterial invasion of HT29-MTX-E12 monolayers: effects of human breast milk. J Pediatr Surg 48, 353357; discussion 357358 (2013)

    • Search Google Scholar
    • Export Citation
  • 34.

    Lin AE , Autran CA, Espanola SD, Bode L, Nizet V: Human milk oligosaccharides protect bladder epithelial cells against uropathogenic Escherichia coli invasion and cytotoxicity. J Infect Dis 209, 389398 (2014)

    • Search Google Scholar
    • Export Citation
  • 35.

    Morrow AL , Ruiz-Palacios GM, Altaye M, Jiang X, Guerrero ML, Meinzen-Derr JK, Farkas T, Chaturvedi P, Pickering LK, Newburg DS: Human milk oligosaccharides are associated with protection against diarrhea in breast-fed infants. J Pediatr 145, 297303 (2004)

    • Search Google Scholar
    • Export Citation
The author instruction is available in PDF.
Please, download the file from HERE.

Senior editors

Editor(s)-in-Chief: Dunay, Ildiko Rita

Editor(s)-in-Chief: Heimesaat, Markus M.

Vice Editor(s)-in-Chief: Fuchs, Anja

Editorial Board

Chair of the Editorial Board:
Jeffrey S. Buguliskis (Thomas Jefferson University, USA)

  • Jörn Albring (University of Münster, Germany)
  • Stefan Bereswill (Charité - University Medicine Berlin, Germany)
  • Dunja Bruder (University of Megdeburg, Germany)
  • Jan Buer (University of Duisburg, Germany)
  • Jeff Buguliskis (Thomas Jefferson University, USA)
  • Edit Buzas (Semmelweis University, Hungary)
  • Charles Collyer (University of Sydney, Australia)
  • Renato Damatta (UENF, Brazil)
  • Ivelina Damjanova (Semmelweis University, Hungary)
  • Maria Deli (Biological Research Center, HAS, Hungary)
  • Olgica Djurković-Djaković (University of Belgrade, Serbia)
  • Jean-Dennis Docquier (University of Siena, Italy)
  • Anna Erdei (Eötvös Loránd University, Hungary)
  • Zsuzsanna Fabry (University of Washington, USA)
  • Beniam Ghebremedhin (Witten/Herdecke University, Germany)
  • Nancy Guillen (Institute Pasteur, France)
  • Georgina L. Hold (University of Aberdeen, United Kingdom)
  • Ralf Ignatius (Charité - University Medicine Berlin, Germany)
  • Zsuzsanna Izsvak (MDC-Berlin, Germany)
  • Achim Kaasch (University of Cologne, Germany)
  • Tamás Laskay (University of Lübeck, Germany)
  • Oliver Liesenfeld (Roche, USA)
  • Shreemanta Parida (Vaccine Grand Challenge Program, India)
  • Matyas Sandor (University of Wisconsin, USA)
  • Ulrich Steinhoff (University of Marburg, Germany)
  • Michal Toborek (University of Miami, USA)
  • Mary Jo Wick (University of Gothenburg, Sweden)
  • Susanne A. Wolf (MDC-Berlin, Germany)


Dr. Dunay, Ildiko Rita
Magdeburg, Germany

Indexing and Abstracting Services:

  • PubMed Central
  • Scopus
  • ESCI
  • CABI


CrossRef Documents 23
WoS Cites 708
Wos H-index 27
Days from submission to acceptance 219
Days from acceptance to publication 176
Acceptance Rate 70%



European Journal of Microbiology and Immunology
Publication Model Gold Open Access
Submission Fee none
Article Processing Charge 928 EUR/article
Regional discounts on country of the funding agency World Bank Lower-middle-income economies: 50%
World Bank Low-income economies: 100%
Further Discounts Editorial Board / Advisory Board members: 50%
Corresponding authors, affiliated to an EISZ member institution subscribing to the journal package of Akadémiai Kiadó: 100%
Subscription Information Gold Open Access
Purchase per Title  

European Journal of Microbiology and Immunology
Language English
Size A4
Year of
per Year
per Year
Founder Akadémiai Kiadó
H-1117 Budapest, Hungary 1516 Budapest, PO Box 245.
Publisher Akadémiai Kiadó
H-1117 Budapest, Hungary 1516 Budapest, PO Box 245.
Chief Executive Officer, Akadémiai Kiadó
ISSN 2062-509X (Print)
ISSN 2062-8633 (Online)

Monthly Content Usage

Abstract Views Full Text Views PDF Downloads
Aug 2021 0 5 2
Sep 2021 0 7 5
Oct 2021 0 7 2
Nov 2021 0 6 3
Dec 2021 0 3 0
Jan 2022 0 6 3
Feb 2022 0 0 0