Hostname: page-component-78c5997874-lj6df Total loading time: 0 Render date: 2024-11-10T12:49:50.245Z Has data issue: false hasContentIssue false
  • English
  • Français

Effects of antibiotic resistance (AR) and microbiota shifts on Campylobacter jejuni-mediated diseases

Published online by Cambridge University Press:  18 April 2018

Phillip T. Brooks  and
Linda S. Mansfield
Phillip T. Brooks
Affiliation:
Comparative Enteric Diseases Laboratory, College of Veterinary Medicine, Michigan State University, East Lansing, Michigan, USA Comparative Medicine and Integrative Biology, College of Veterinary Medicine, Michigan State University, East Lansing, Michigan, USA Institute for Integrative Toxicology, Michigan State University, East Lansing, Michigan, USA
Linda S. Mansfield*
Affiliation:
Comparative Enteric Diseases Laboratory, College of Veterinary Medicine, Michigan State University, East Lansing, Michigan, USA Comparative Medicine and Integrative Biology, College of Veterinary Medicine, Michigan State University, East Lansing, Michigan, USA
*
*Corresponding author. E-mail: mansfie4@cvm.msu.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

Campylobacter jejuni is an important zoonotic pathogen recently designated a serious antimicrobial resistant (AR) threat. While most patients with C. jejuni experience hemorrhagic colitis, serious autoimmune conditions can follow including inflammatory bowel disease (IBD) and the acute neuropathy Guillain Barré Syndrome (GBS). This review examines inter-relationships among factors mediating C. jejuni diarrheal versus autoimmune disease especially AR C. jejuni and microbiome shifts. Because both susceptible and AR C. jejuni are acquired from animals or their products, we consider their role in harboring strains. Inter-relationships among factors mediating C. jejuni colonization, diarrheal and autoimmune disease include C. jejuni virulence factors and AR, the enteric microbiome, and host responses. Because AR C. jejuni have been suggested to affect the severity of disease, length of infections and propensity to develop GBS, it is important to understand how these interactions occur when strains are under selection by antimicrobials. More work is needed to elucidate host–pathogen interactions of AR C. jejuni compared with susceptible strains and how AR C. jejuni are maintained and evolve in animal reservoirs and the extent of transmission to humans. These knowledge gaps impair the development of effective strategies to prevent the emergence of AR C. jejuni in reservoir species and human populations.

Keywords

Campylobacter jejuniGuillain-Barré Syndromemicrobiomemouse modelsautoimmunityinflammationantibioticsantimicrobial resistance
Type
Review Article
Information
Animal Health Research Reviews , Volume 18 , Special Issue 2: Antimicrobial resistance: from basic science to translational innovation , December 2017 , pp. 99 - 111
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Allos, BM (2001). Campylobacter jejuni infections: update on emerging issues and trends. Clinical Infectious Diseases 32: 1201–1206.Google Scholar
Almofti, YA, Dai, M, Sun, Y, Hao, H, Liu, Z, Cheng, G and Yuan, Z (2011). The physiologic and phenotypic alterations due to macrolide exposure in Campylobacter jejuni. International Journal of Food Microbiology 151: 52–61.Google Scholar
Altekruse, SF, Stern, NJ, Fields, PI and Swerdlow, DL (1999). Campylobacter jejuni--an emerging foodborne pathogen. Emerging Infectious Diseases 5: 28–35.Google Scholar
Amar, C, Kittl, S, Spreng, D, Thomann, A, Korczak, BM, Burnens, AP and Kuhnert, P (2014). Genotypes and antibiotic resistance of canine Campylobacter jejuni isolates. Veterinary Microbiology 168: 124–130.Google Scholar
Archelos, JJ, Fortwangler, T and Hartung, HP (1997). Attenuation of experimental autoimmune neuritis in the Lewis rat by treatment with an antibody to L-selectin. Neuroscience Letters 235: 9–12.Google Scholar
Bell, JA, St Charles, JL, Murphy, AJ, Rathinam, VA, Plovanich-Jones, AE, Stanley, EL, Wolf, JE, Gettings, JR, Whittam, TS and Mansfield, LS (2009). Multiple factors interact to produce responses resembling spectrum of human disease in Campylobacter jejuni infected C57BL/6 IL-10-/- mice. BMC Microbiology 9: 57.Google Scholar
Bell, JA, Jerome, JP, Plovanich-Jones, AE, Smith, EJ, Gettings, JR, Kim, HY, Landgraf, JR, Lefébure, T, Kopper, JJ, Rathinam, VA, Charles, JLS, Buffa, BA, Brooks, AP, Poe, SA, Eaton, KA, Stanhope, MJ and Mansfield, LS (2013a). Outcome of infection of C57BL/6 IL-10−/− mice with Campylobacter jejuni strains is correlated with genome content of open reading frames up- and down-regulated in vivo. Microbial Pathogenesis 54: 119.Google Scholar
Bell, JA, Jerome, JP, Plovanich-Jones, AE, Smith, EJ, Gettings, JR, Kim, HY, Landgraf, JR, Lefebure, T, Kopper, JJ, Rathinam, VA, St Charles, JL, Buffa, BA, Brooks, AP, Poe, SA, Eaton, KA, Stanhope, MJ and Mansfield, LS (2013b). Outcome of infection of C57BL/6 IL-10(−/−) mice with Campylobacter jejuni strains is correlated with genome content of open reading frames up- and down-regulated in vivo. Microbial Pathogenesis 54: 1–19.Google Scholar
Bereswill, S, Fischer, A, Plickert, R, Haag, LM, Otto, B, Kühl, AA, Dasti, JI, Zautner, AE, Muñoz, M, Loddenkemper, C, Gross, U, Göbel, UB and Heimesaat, MM (2011). Novel murine infection models provide deep insights into the “ménage à trois” of Campylobacter jejuni, microbiota and host innate immunity. PLoS ONE 6: e20953.Google Scholar
Blaser, MJ, Glass, RI, Hug, MI, Stoll, B, Kibrya, GM and Alim, ARMA (1980). Isolation of Campylobacter fetus subsp. jejuni from Bangladeshi children. Journal of Clinical Microbiology 12: 744–747.Google Scholar
Bopp, DJ, Sauders, BD, Waring, AL, Ackelsberg, J, Dumas, N, Braun-Howland, E, Dziewulski, D, Wallace, BJ, Kelly, M, Halse, T, Musser, KA, Smith, PF, Morse, DL and Limberger, RJ (2003). Detection, isolation, and molecular subtyping of Escherichia coli O157:H7 and Campylobacter jejuni associated with a large waterborne outbreak. Journal of Clinical Microbiology 41: 174–180.Google Scholar
Brooks, PT, Brakel, KA, Bell, JA, Bejcek, CE, Gilpin, T, Brudvig, JM and Mansfield, LS (2017). Transplanted human fecal microbiota enhanced Guillain Barre syndrome autoantibody responses after Campylobacter jejuni infection in C57BL/6 mice. Microbiome 5: 92.Google Scholar
Bruce, D, Zochowski, W and Fleming, GA (1980). Campylobacter infections in cats and dogs. The Veterinary Record 107: 200–201.Google Scholar
Buffie, CG and Pamer, EG (2013). Microbiota-mediated colonization resistance against intestinal pathogens. Nature Reviews Immunology 13: 790–801.Google Scholar
Cagliero, C, Cloix, L, Cloeckaert, A and Payot, S (2006). High genetic variation in the multidrug transporter cmeB gene in Campylobacter jejuni and Campylobacter coli. Journal of Antimicrobial Chemotherapy 58: 168–172.Google Scholar
Caldwell, MB, Guerry, P, Lee, EC, Burans, JP and Walker, RI (1985). Reversible expression of flagella in Campylobacter jejuni. Infection and Immunity 50: 941–943.Google Scholar
Cawthraw, SA, Wassenaar, TM, Ayling, R and Newell, DG (1996). Increased colonization potential of Campylobacter jejuni strain 81116 after passage through chickens and its implication on the rate of transmission within flocks. Epidemiology and Infection 117: 213–215.Google Scholar
Cawthraw, SA, Feldman, RA, Sayers, AR and Newell, DG (2002). Long-term antibody responses following human infection with Campylobacter jejuni. Clinical and Experimental Immunology 130: 101–106.Google Scholar
CDC (2011). Vital signs: incidence and trends of infection with pathogens transmitted commonly through food--foodborne diseases active surveillance network, 10 U.S. Sites, 1996–2010. MMWR. Morbidity and Mortality Weekly Report 60: 749–755.Google Scholar
CDC (2013). Antibiotic Resistance Threats in the United States, 2013. Diseases, National Center for Emerging and Zoonotic Infectious Diseases (ed.). Atlanta, GA: U.S. Department of Health and Human Services, pp. 1–114.Google Scholar
CDC (2017). National Antimicrobial Resistance Monitoring System (NARMS) Now: Human Data. Atlanta, Georgia: U.S. Department of Health and Human Services, C.Google Scholar
Cha, W, Mosci, RE, Wengert, SL, Venegas Vargas, C, Rust, SR, Bartlett, PC, Grooms, DL and Manning, SD (2017). Comparing the genetic diversity and antimicrobial resistance profiles of Campylobacter jejuni recovered from cattle and humans. Frontiers in Microbiology 8: 818.Google Scholar
Chaban, B, Ngeleka, M and Hill, JE (2010). Detection and quantification of 14 Campylobacter species in pet dogs reveals an increase in species richness in feces of diarrheic animals. BMC Microbiology 10: 73.Google Scholar
Chang, C and Miller, JF (2006). Campylobacter jejuni colonization of mice with limited enteric flora. Infection and Immunity 74: 52615271.Google Scholar
Chervonsky, AV (2013). Microbiota and autoimmunity. Cold Spring Harbor Perspectives in Biology 5: a007294.Google Scholar
de Boer, P, Wagenaar, JA, Achterberg, RP, van Putten, JP, Schouls, LM and Duim, B (2002). Generation of Campylobacter jejuni genetic diversity in vivo. Molecular Microbiology 44: 351–359.Google Scholar
Ercolini, AM and Miller, SD (2009). The role of infections in autoimmune disease. Clinical and Experimental Immunology 155: 1–15.Google Scholar
Farmer, RG (1990). Infectious causes of diarrhea in the differential diagnosis of inflammatory bowel disease. The Medical Clinics of North America 74: 29–38.Google Scholar
FDA (2014). FDA Releases 2014 NARMS Integrated Report; Finds Measurable Improvements in Antimicrobial Resistance Levels. Medicine, C.f.V. (ed.). Rockville, MD.Google Scholar
Fearnhead, P, Smith, NG, Barrigas, M, Fox, A and French, N (2005). Analysis of recombination in Campylobacter jejuni from MLST population data. Journal of Molecular Evolution 61: 333–340.Google Scholar
Fernandez-Cruz, A, Munoz, P, Mohedano, R, Valerio, M, Marin, M, Alcala, L, Rodriguez-Creixems, M, Cercenado, E and Bouza, E (2010). Campylobacter bacteremia: clinical characteristics, incidence, and outcome over 23 years. Medicine 89: 319–330.Google Scholar
Fitzgeorge, RB, Baskerville, A and Lander, KP (1981). Experimental infection of rhesus monkeys with a human strain of Campylobacter jejuni. The Journal of Hygiene 86: 343–351.Google Scholar
Fox, JG (1992). In vivo models of enteric campylobacteriosis: natural and experimental infections. In: Nachamkin, I, Blaser, MJ, Tompkins, LS (eds) Campylobacter Jejuni: Current Status and Future Trends. Washington, DC: ASM Press, pp. 131–138.Google Scholar
Fox, JG, Moore, R and Ackerman, JI (1983). Campylobacter-Jejuni-Associated diarrhea in dogs. Journal of the American Veterinary Medical Association 183: 1430–1433.Google Scholar
Fox, JG, Rogers, AB, Whary, MT, Ge, Z, Taylor, NS, Xu, S, Horwitz, BH and Erdman, SE (2004). Gastroenteritis in NF-kappaB-deficient mice is produced with wild-type Camplyobacter jejuni but not with C. jejuni lacking cytolethal distending toxin despite persistent colonization with both strains. Infection and Immunity 72: 1116–1125.Google Scholar
Garcia Rodriguez, LA, Ruigomez, A and Panes, J (2006). Acute gastroenteritis is followed by an increased risk of inflammatory bowel disease. Gastroenterology 130: 1588–1594.Google Scholar
Gilbert, M, Karwaski, MF, Bernatchez, S, Young, NM, Taboada, E, Michniewicz, J, Cunningham, AM and 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. Journal of Biological Chemistry 277: 327–337.Google Scholar
Gilbert, M, Godschalk, PC, Karwaski, MF, Ang, CW, van Belkum, A, Li, J, Wakarchuk, WW and Endtz, HP (2004). 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. Infection and Immunity 72: 1162–1165.Google Scholar
Godschalk, PC, Heikema, AP, Gilbert, M, Komagamine, T, Ang, CW, Glerum, J, Brochu, D, Li, J, Yuki, N, Jacobs, BC, van Belkum, A and Endtz, HP (2004). The crucial role of Campylobacter jejuni genes in anti-ganglioside antibody induction in Guillain-Barre syndrome. The Journal of Clinical Investigation 114: 1659–1665.Google Scholar
Godschalk, PC, Bergman, MP, Gorkink, RF, Simons, G, van den Braak, N, Lastovica, AJ, Endtz, HP, Verbrugh, HA and van Belkum, A (2006). Identification of DNA sequence variation in Campylobacter jejuni strains associated with the Guillain-Barre syndrome by high-throughput AFLP analysis. BMC Microbiology 6: 32.Google Scholar
Godschalk, PC, Kuijf, ML, Li, J, St Michael, F, Ang, CW, Jacobs, BC, Karwaski, MF, Brochu, D, Moterassed, A, Endtz, HP, van Belkum, A and Gilbert, M (2007). Structural characterization of Campylobacter jejuni lipooligosaccharide outer cores associated with Guillain-Barre and miller fisher syndromes. Infection and Immunity 75: 1245–1254.Google Scholar
Guerry, P, Szymanski, CM, Prendergast, MM, Hickey, TE, Ewing, CP, Pattarini, DL and Moran, AP (2002). Phase variation of Campylobacter jejuni 81–176 lipooligosaccharide affects ganglioside mimicry and invasiveness in vitro. Infection and Immunity 70: 787–793.Google Scholar
Halbert, LW, Kaneene, JB, Linz, J, Mansfield, LS, Wilson, D, Ruegg, PL, Warnick, LD, Wells, SJ, Fossler, CP, Campbell, AM and Geiger-Zwald, AM (2006). Genetic mechanisms contributing to reduced tetracycline susceptibility of campylobacter isolated from organic and conventional dairy farms in the midwestern and northeastern United States. Journal of Food Protection 69: 482–488.Google Scholar
Hermans, D, Pasmans, F, Heyndrickx, M, Van Immerseel, F, Martel, A, Van Deun, K and Haesebrouck, F (2012). A tolerogenic mucosal immune response leads to persistent Campylobacter jejuni colonization in the chicken gut. Critical Reviews in Microbiology 38: 17–29.Google Scholar
Hill, GA and Grimes, DJ (1984). Seasonal study of a freshwater lake and migratory waterfowl for Campylobacter jejuni. Canadian journal of Microbiology 30: 845–849.Google Scholar
Hold, GL, Smith, M, Grange, C, Watt, ER, El-Omar, EM and Mukhopadhya, I (2014). Role of the gut microbiota in inflammatory bowel disease pathogenesis: what have we learnt in the past 10 years? World Journal of Gastroenterology 20: 1192–1210.Google Scholar
Holmes, AH, Moore, LS, Sundsfjord, A, Steinbakk, M, Regmi, S, Karkey, A, Guerin, PJ and Piddock, LJ (2016). Understanding the mechanisms and drivers of antimicrobial resistance. Lancet 387: 176–187.Google Scholar
Honda, K and Littman, DR (2012). The microbiome in infectious disease and inflammation. Annual Review of Immunology 30: 759–795.Google Scholar
Horwitz, MA and Silverstein, SC (1980). Influence of the Escherichia coli capsule on complement fixation and on phagocytosis and killing by human phagocytes. The Journal of Clinical Investigation 65: 82–94.Google Scholar
Humphrey, S, Chaloner, G, Kemmett, K, Davidson, N, Williams, N, Kipar, A, Humphrey, T and Wigley, P (2014). Campylobacter jejuni is not merely a commensal in commercial broiler chickens and affects bird welfare. MBio 5: e01364–e01314.Google Scholar
Hurd, HS, Vaughn, MB, Holtkamp, D, Dickson, J and Warnick, L (2010). Quantitative risk from fluoroquinolone-resistant Salmonella and Campylobacter due to treatment of dairy heifers with enrofloxacin for bovine respiratory disease. Foodborne Pathogens and Disease 7: 1305–1322.Google Scholar
Jackson, BR, Zegarra, JA, Lopez-Gatell, H, Sejvar, J, Arzate, F, Waterman, S, Nunez, AS, Lopez, B, Weiss, J, Cruz, RQ, Murrieta, DY, Luna-Gierke, R, Heiman, K, Vieira, AR, Fitzgerald, C, Kwan, P, Zarate-Bermudez, M, Talkington, D, Hill, VR and Mahon, B, Team GBSOI (2014). Binational outbreak of Guillain-Barre syndrome associated with Campylobacter jejuni infection, Mexico and USA, 2011. Epidemiology and Infection 142: 1089–1099.Google Scholar
Janssen, R, Krogfelt, KA, Cawthraw, SA, van Pelt, W, Wagenaar, JA and Owen, RJ (2008). Host-pathogen interactions in Campylobacter infections: the host perspective. Clinical Microbiology Reviews 21: 505–518.Google Scholar
Jerome, JP, Bell, JA, Plovanich-Jones, AE, Barrick, JE, Brown, CT and Mansfield, LS (2011). Standing genetic variation in contingency loci drives the rapid adaptation of Campylobacter jejuni to a novel host. PLoS ONE 6: e16399.Google Scholar
Johnson, TJ, Shank, JM and Johnson, JG (2017). Current and potential treatments for reducing campylobacter colonization in animal hosts and disease in humans. Frontiers in Microbiology 8: 487–000.Google Scholar
Jones, MA, Marston, KL, Woodall, CA, Maskell, DJ, Linton, D, Karlyshev, AV, Dorrell, N, Wren, BW and Barrow, PA (2004). Adaptation of Campylobacter jejuni NCTC11168 to high-level colonization of the avian gastrointestinal tract. Infection and Immunity 72: 37693776.Google Scholar
Kaakoush, NO, Castano-Rodriguez, N, Mitchell, HM and Man, SM (2015). Global epidemiology of campylobacter infection. Clinical microbiology reviews 28: 687–720.Google Scholar
Kaida, K and Kusunoki, S (2010). Antibodies to gangliosides and ganglioside complexes in Guillain-Barre syndrome and Fisher syndrome: mini-review. Journal of Neuroimmunology 223: 5–12.Google Scholar
Karmali, MA and Fleming, PC (1979). Campylobacter enteritis in children. Journal of Pediatrics 94: 527–533.Google Scholar
Keithlin, J, Sargeant, J, Thomas, MK and Fazil, A (2014). Systematic review and meta-analysis of the proportion of Campylobacter cases that develop chronic sequelae. BMC Public Health 14: 1203.Google Scholar
Ketley, J, Guerry, P and Panigrahi, P (1996). Pathogenic mechanisms. In: Newell, DG, Ketley, JM, Feldman, RA (eds) Campylobacters, Helicobacters, and Related Organisms. New York: Plenum Press, pp. 537–544.Google Scholar
Ketley, JM (1997). Pathogenesis of enteric infection by Campylobacter. Microbiology 143(Pt 1): 5–21.Google Scholar
Kim, JS, Artymovich, KA, Hall, DF, Smith, EJ, Fulton, R, Bell, J, Dybas, L, Mansfield, LS, Tempelman, R, Wilson, DL and Linz, JE (2012). Passage of Campylobacter jejuni through the chicken reservoir or mice promotes phase variation in contingency genes Cj0045 and Cj0170 that strongly associates with colonization and disease in a mouse model. Microbiology 158: 1304–1316.Google Scholar
Kivistö, RI, Kovanen, S, Skarp-de Haan, A, Schott, T, Rahkio, M, Rossi, M and Hänninen, ML (2014). Evolution and comparative genomics of Campylobacter jejuni ST-677 clonal complex. Genome Biol Evol 6: 2424–2438.Google Scholar
Klancnik, A, Mozina, SS and Zhang, Q (2012). Anti-Campylobacter activities and resistance mechanisms of natural phenolic compounds in Campylobacter. PLoS ONE 7: e51800.Google Scholar
Knudsen, KN, Bang, DD, Nielsen, EM and Madsen, M (2005). Genotyping of Campylobacter jejuni strains from Danish broiler chickens by restriction fragment length polymorphism of the LPS gene cluster. Journal of Applied Microbiology 99: 392–399.Google Scholar
Koga, M, Takahashi, M, Masuda, M, Hirata, K and Yuki, N (2005). Campylobacter gene polymorphism as a determinant of clinical features of Guillain-Barre syndrome. Neurology 65: 1376–1381.Google Scholar
Kurz, M, Pischel, H, Hartung, HP and Kieseier, BC (2005). Tumor necrosis factor-alpha-converting enzyme is expressed in the inflamed peripheral nervous system. Journal of the Peripheral Nervous System 10: 311–318.Google Scholar
Landers, TF, Cohen, B, Wittum, TE and Larson, EL (2012). A review of antibiotic use in food animals: perspective, policy, and potential. Public Health Reports 127: 4–22.Google Scholar
Lehmann, HC, Lopez, PH, Zhang, G, Ngyuen, T, Zhang, J, Kieseier, BC, Mori, S and Sheikh, KA (2007). Passive immunization with anti-ganglioside antibodies directly inhibits axon regeneration in an animal model. Journal of Neuroscience 27: 27–34.Google Scholar
Li, CY, Xue, P, Tian, WQ, Liu, RC and Yang, C (1996). Experimental Campylobacter jejuni infection in the chicken: an animal model of axonal Guillain-Barre syndrome. Journal of Neurology, Neurosurgery, and Psychiatry 61: 279–284.Google Scholar
Linton, D, Gilbert, M, Hitchen, PG, Dell, A, Morris, HR, Wakarchuk, WW, Gregson, NA and Wren, BW (2000). Phase variation of a beta-1,3 galactosyltransferase involved in generation of the ganglioside GM1-like lipo-oligosaccharide of Campylobacter jejuni. Molecular Microbiology 37: 501–514.Google Scholar
Luangtongkum, T, Shen, Z, Seng, VW, Sahin, O, Jeon, B, Liu, P and Zhang, Q (2012). Impaired fitness and transmission of macrolide-resistant Campylobacter jejuni in its natural host. Antimicrobial Agents and Chemotherapy 56: 1300–1308.Google Scholar
Luo, N, Pereira, S, Sahin, O, Lin, J, Huang, S, Michel, L and Zhang, Q (2005). Enhanced in vivo fitness of fluoroquinolone-resistant Campylobacter jejuni in the absence of antibiotic selection pressure. Proceedings of the National Academy of Sciences of the United States of America 102: 541–546.Google Scholar
Malik, A, Sharma, D, St Charles, J, Dybas, LA and Mansfield, LS (2014). Contrasting immune responses mediate Campylobacter jejuni-induced colitis and autoimmunity. Mucosal Immunology 7: 802–817.Google Scholar
Mansfield, LS and Urban, JF (1996). The pathogenesis of necrotic proliferative colitis in swine is linked to whipworm induced suppression of mucosal immunity to resident bacteria. Veterinary Immunology and Immunopathology 50: 1–17.Google Scholar
Mansfield, LS, Bell, JA, Wilson, DL, Murphy, AJ, Elsheikha, HM, Rathinam, VA, Fierro, BR, Linz, JE and Young, VB (2007). C57BL/6 and congenic interleukin-10-deficient mice can serve as models of Campylobacter jejuni colonization and enteritis. Infection and Immunity 75: 1099–1115.Google Scholar
Mansfield, LS, Patterson, JS, Fierro, BR, Murphy, AJ, Rathinam, VA, Kopper, JJ, Barbu, NI, Onifade, TJ and Bell, JA (2008a). Genetic background of IL-10(−/−) mice alters host-pathogen interactions with Campylobacter jejuni and influences disease phenotype. Microbial Pathogenesis 45: 241–257.Google Scholar
Mansfield, LS, Schauer, DB and Fox, JG (2008b). Chapter 21: animal models of Campylobacter jejuni infections. In: Nachamkin, I, Szymanski, CM, Blaser, MJ (eds) Campylobacter. Washington, DC: American Society for Microbiology Press, pp. 376–379.Google Scholar
Martini, R and Willison, H (2016). Neuroinflammation in the peripheral nerve: cause, modulator, or bystander in peripheral neuropathies? Glia 64: 475–486.Google Scholar
Maruyama, S, Tanaka, T, Katsube, Y, Nakanishi, H and Nukina, M (1990). Prevalence of thermophilic Campylobacters in crows (Corvus levaillantii, Corvus corone) and serogroups of the isolates. Nippon Juigaku Zasshi 52: 1237–1244.Google Scholar
McCrackin, MA, Helke, KL, Galloway, AM, Poole, AZ, Salgado, CD and Marriott, BP (2016). Effect of antimicrobial use in agricultural animals on drug-resistant foodborne campylobacteriosis in humans: a systematic literature review. Critical Reviews in Food Science and Nutrition 56: 2115–2132.Google Scholar
McGonigal, R, Rowan, EG, Greenshields, KN, Halstead, SK, Humphreys, PD, Rother, RP, Furukawa, K and Willison, HJ (2010). Anti-GD1a antibodies activate complement and calpain to injure distal motor nodes of ranvier in mice. Brain 133: 1944–1960.Google Scholar
Mohawk, KL, Poly, F, Sahl, JW, Rasko, DA and Guerry, P (2014). High frequency, spontaneous motA mutations in Campylobacter jejuni strain 81–176. PLoS ONE 9: e88043.Google Scholar
Montrose, MS, Shane, SM and Harrington, KS (1985). Role of litter in the transmission of Campylobacter jejuni. Avian Diseases 29: 392–399.Google Scholar
Moore, JE, Barton, MD, Blair, IS, Corcoran, D, Dooley, JS, Fanning, S, Kempf, I, Lastovica, AJ, Lowery, CJ, Matsuda, M, McDowell, DA, McMahon, A, Millar, BC, Rao, JR, Rooney, PJ, Seal, BS, Snelling, WJ and Tolba, O (2006). The epidemiology of antibiotic resistance in Campylobacter. Microbes and Infection/Institut Pasteur 8: 1955–1966.Google Scholar
Moore, KW, Malefyt, RD, Coffman, RL and O'Garra, A (2001). Interleukin-10 and the interleukin-10 receptor. Annual Review of Immunology 19: 683–765.Google Scholar
Moxon, ER, Paul, BR, Martin, AN and Richard, EL (1994). Adaptive evolution of highly mutable loci in pathogenic bacteria. Current Biology 4: 2433.Google Scholar
Nachamkin, I, Yang, XH and Stern, NJ (1993). Role of Campylobacter jejuni flagella as colonization factors for three-day-old chicks: analysis with flagellar mutants. Applied and Environmental Microbiology 59: 1269–1273.Google Scholar
Nachamkin, I, Allos, BM and Ho, T (1998). Campylobacter species and Guillain-Barre syndrome. Clinical Microbiology Reviews 11: 555–567.Google Scholar
Nachamkin, I, Liu, J, Li, M, Ung, H, Moran, AP, Prendergast, MM and Sheikh, K (2002). Campylobacter jejuni from patients with Guillain-Barre syndrome preferentially expresses a GD(1a)-like epitope. Infection and Immunity 70: 5299–5303.Google Scholar
Newell, DG (2001). Animal models of Campylobacter jejuni colonization and disease and the lessons to be learned from similar Helicobacter pylori models. Journal of Applied Microbiology 90: 57S–67S.Google Scholar
Newell, DG, Elvers, KT, Dopfer, D, Hansson, I, Jones, P, James, S, Gittins, J, Stern, NJ, Davies, R, Connerton, I, Pearson, D, Salvat, G and Allen, VM (2011). Biosecurity-based interventions and strategies to reduce Campylobacter spp. on poultry farms. Applied and Environmental Microbiology 77: 8605–8614.Google Scholar
Nuijten, PJM, Berg, AJGvd, Formentini, I, Zeijst, Mvd and Jacobs, AAC (2000). DNA rearrangements in the flagellin locus of an flaA mutant of Campylobacter jejuni during colonization of chicken ceca. Infection and Immunity 68: 71377140.Google Scholar
Nurieva, RI and Chung, Y (2010). Understanding the development and function of T follicular helper cells. Cellular & Molecular Immunology 7: 190–197.Google Scholar
O'Loughlin, JL, Samuelson, DR, Braundmeier-Fleming, AG, White, BA, Haldorson, GJ, Stone, JB, Lessmann, JJ, Eucker, TP and Konkel, ME (2015). The intestinal microbiota influences Campylobacter jejuni colonization and extraintestinal dissemination in mice. Applied and Environmental Microbiology 81: 4642–4650.Google Scholar
Oh, E and Jeon, B (2015). Synergistic anti-Campylobacter jejuni activity of fluoroquinolone and macrolide antibiotics with phenolic compounds. Frontiers in Microbiology 6: 1129.Google Scholar
Oh, SJ, LaGanke, C and Claussen, GC (2001). Sensory Guillain-Barre syndrome. Neurology 56: 82–86.CrossRefGoogle ScholarPubMed
Oliver, SP, Patel, DA, Callaway, TR and Torrence, ME (2009). ASAS centennial paper: developments and future outlook for preharvest food safety. Journal of Animal Science 87: 419–437.Google Scholar
Ouyang, W, Rutz, S, Crellin, NK, Valdez, PA and Hymowitz, SG (2011). Regulation and functions of the IL-10 family of cytokines in inflammation and disease. Annual Review of Immunology 29: 71–109.Google Scholar
Parker, CT, Horn, ST, Gilbert, M, Miller, WG, Woodward, DL and Mandrell, RE (2005). Comparison of Campylobacter jejuni lipooligosaccharide biosynthesis loci from a variety of sources. Journal of Clinical Microbiology 43: 2771–2781.Google Scholar
Parkhill, J, Wren, BW, Mungall, K, Ketley, JM, Churcher, C, Basham, D, Chillingworth, T, Davies, RM, Feltwell, T, Holroyd, S, Jagels, K, Karlyshev, AV, Moule, S, Pallen, MJ, Penn, CW, Quail, MA, Rajandream, MA, Rutherford, KM, van Vliet, AH, Whitehead, S and Barrell, BG (2000). The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403: 665–668.Google Scholar
Pearson, AD, Greenwood, M, Healing, TD, Rollins, D, Shahamat, M, Donaldson, J and Colwell, RR (1993). Colonization of broiler chickens by waterborne Campylobacter jejuni. Applied and Environmental Microbiology 59: 987–996.Google Scholar
Perkins, DJ and Newstead, GL (1994). Campylobacter jejuni enterocolitis causing peritonitis, ileitis and intestinal obstruction. The Australian and New Zealand Journal of Surgery 64: 55–58.Google Scholar
Phongsisay, V, Perera, VN and Fry, BN (2006). Exchange of lipooligosaccharide synthesis genes creates potential Guillain-Barre syndrome-inducible strains of Campylobacter jejuni. Infection and Immunity 74: 1368–1372.Google Scholar
Pickett, CL, Pesci, EC, Cottle, DL, Russell, G, Erdem, AN and Zeytin, H (1996). Prevalence of cytolethal distending toxin production in Campylobacter jejuni and relatedness of Campylobacter sp. cdtB gene. Infection and Immunity 64: 2070–2078.Google Scholar
Prendergast, MM, Tribble, DR, Baqar, S, Scott, DA, Ferris, JA, Walker, RI and Moran, AP (2004). In vivo phase variation and serologic response to lipooligosaccharide of Campylobacter jejuni in experimental human infection. Infection and Immunity 72: 916–922.Google Scholar
Rathinam, VA, Hoag, KA and Mansfield, LS (2008). Dendritic cells from C57BL/6 mice undergo activation and induce Th1-effector cell responses against Campylobacter jejuni. Microbes and Infection 10: 1316–1324.Google Scholar
Rathinam, VA, Appledorn, DM, Hoag, KA, Amalfitano, A and Mansfield, LS (2009). Campylobacter jejuni-induced activation of dendritic cells involves cooperative signaling through TLR4-MyD88 and TLR4-TRIF axes. Infection and Immunity 77: 2499–2507.Google Scholar
Sahin, O, Plummer, PJ, Jordan, DM, Sulaj, K, Pereira, S, Robbe-Austerman, S, Wang, L, Yaeger, MJ, Hoffman, LJ and Zhang, Q (2008). Emergence of a tetracycline-resistant Campylobacter jejuni clone associated with outbreaks of ovine abortion in the United States. Journal of Clinical Microbiology 46: 1663–1671.Google Scholar
Sahin, O, Fitzgerald, C, Stroika, S, Zhao, S, Sippy, RJ, Kwan, P, Plummer, PJ, Han, J, Yaeger, MJ and Zhang, Q (2012). Molecular evidence for zoonotic transmission of an emergent, highly pathogenic Campylobacter jejuni clone in the United States. Journal of Clinical Microbiology 50: 680–687.Google Scholar
Scallan, E, Hoekstra, RM, Angulo, FJ, Tauxe, RV, Widdowson, MA, Roy, SL, Jones, JL and Griffin, PM (2011). Foodborne illness acquired in the United States--major pathogens. Emerging Infectious Diseases 17: 7–15.Google Scholar
Scott, AE, Timms, AR, Connerton, PL, Loc Carrillo, C, Adzfa Radzum, K and Connerton, IF (2007). Genome dynamics of Campylobacter jejuni in response to bacteriophage predation. PLoS Pathogens 3: e119.Google Scholar
Sestak, K, Merritt, CK, Borda, J, Saylor, E, Schwamberger, SR, Cogswell, F, Didier, ES, Didier, PJ, Plauche, G, Bohm, RP, Aye, PP, Alexa, P, Ward, RL and Lackner, AA (2003). Infectious agent and immune response characteristics of chronic enterocolitis in captive rhesus macaques. Infection and Immunity 71: 4079–4086.Google Scholar
Shimon, S (2000). Animal models of autoimmunity and their relevance to human diseases. Current Opinion in Immunology 12: 684690.Google Scholar
Shin, R, Suzuki, M and Morishita, Y (2002). Influence of intestinal anaerobes and organic acids on the growth of enterohaemorrhagic Escherichia coli O157:H7. Journal of Medical Microbiology 51: 201–206.Google Scholar
Stahl, M, Ries, J, Vermeulen, J, Yang, H, Sham, HP, Crowley, SM, Badayeva, Y, Turvey, SE, Gaynor, EC, Li, X and Vallance, BA (2014). A novel mouse model of Campylobacter jejuni gastroenteritis reveals Key Pro-inflammatory and tissue protective roles for toll-like receptor signaling during infection. PLoS Pathogens 10: e1004264.Google Scholar
St Charles, JL, Bell, JA, Gadsden, BJ, Malik, A, Cooke, H, Van de Grift, LK, Kim, HY, Smith, EJ and Mansfield, LS (2017). Guillain Barre syndrome is induced in Non-obese diabetic (NOD) mice following Campylobacter jejuni infection and is exacerbated by antibiotics. Journal of Autoimmunity 77: 11–38.Google Scholar
Stecher, B and Hardt, WD (2008). The role of microbiota in infectious disease. Trends in Microbiology 16: 107–114.Google Scholar
Suerbaum, S, Lohrengel, M, Sonnevend, A, Ruberg, F and Kist, M (2001). Allelic diversity and recombination in Campylobacter jejuni. Journal of Bacteriology 183: 2553–2559.Google Scholar
Tadesse, DA, Bahnson, PB, Funk, JA, Thakur, S, Morrow, WE, Wittum, T, DeGraves, F, Rajala-Schultz, P and Gebreyes, WA (2011). Prevalence and antimicrobial resistance profile of Campylobacter spp. Isolated from conventional and antimicrobial-free swine production systems from different U.S. Regions. Foodborne Pathogens and Disease 8: 367–374.Google Scholar
Tam, CC, O'Brien, SJ, Petersen, I, Islam, A, Hayward, A and Rodrigues, LC (2007). Guillain-Barre syndrome and preceding infection with Campylobacter, influenza and Epstein-Barr virus in the general practice research database. PLoS ONE 2: e344.Google Scholar
Ternhag, A, Torner, A, Svensson, A, Ekdahl, K and Giesecke, J (2008). Short- and long-term effects of bacterial gastrointestinal infections. Emerging Infectious Diseases 14: 143–148.Google Scholar
Thomas, DK, Lone, AG, Selinger, LB, Taboada, EN, Uwiera, RR, Abbott, DW and Inglis, GD (2014). Comparative variation within the genome of Campylobacter jejuni NCTC 11168 in human and murine hosts. PLoS ONE 9: e88229.Google Scholar
Vandenberg, O, Cornelius, AJ, Souayah, H, Martiny, D, Vlaes, L, Brandt, SM and On, SL (2013). The role of Epsilonproteobacteria in children with gastroenteritis. The Pediatric Infectious Disease Journal 32: 1140–1142.Google Scholar
van den Berg, B, Walgaard, C, Drenthen, J, Fokke, C, Jacobs, BC and van Doorn, PA (2014). Guillain-Barre syndrome: pathogenesis, diagnosis, treatment and prognosis. Nature Reviews Neurology 10: 469–482.Google Scholar
van der Waaij, D, Berghuis-de Vries, JM and Lekkerkerk-van der Wees, JEC (1971). Colonization resistance of the digestive tract in conventional and antibiotic-treated mice. The Journal of Hygiene (Lond) 69: 405–411.Google Scholar
van der Waaij, D, Berghuis-de Vries, JM and Lekkerkerk-van der Wees, JEC (1972). Colonization resistance of the digestive tract and the spread of bacteria to the lymphatic organs in mice. The Journal of Hygiene (Lond) 70: 335–342.Google Scholar
van der Woude, MW and Baumler, AJ (2004). Phase and antigenic variation in bacteria. Clinical Microbiology Reviews 17: 581–611.Google Scholar
Wassenaar, TM, Zeijst, BAMvd, Ayling, R and Newell, DG (1993). Colonization of chicks by motility mutants of Campylobacter jejuni demonstrates the importance of flagellin A expression. Journal of General Microbiology 139: 1171–1175.Google Scholar
Wassenaar, TM, Geilhausen, B and Newell, DG (1998). Evidence of genomic instability in Campylobacter jejuni isolated from poultry. Applied and environmental microbiology 64: 1816–1821.Google Scholar
Weis, AM, Storey, DB, Taff, CC, Townsend, AK, Huang, BC, Kong, NT, Clothier, KA, Spinner, A, Byrne, BA and Weimer, BC (2016). Genomic comparison of Campylobacter spp. and their potential for zoonotic transmission between birds, primates, and livestock. Applied and Environmental Microbiology 82: 7165–7175.Google Scholar
Wells, CL, Maddaus, MA, Jechorek, RP and Simmons, RL (1988). Role of intestinal anaerobic bacteria in colonization resistance. European Journal of Clinical Microbiology & Infectious Diseases 7: 107–113.Google Scholar
Willison, HJ and Plomp, JJ (2008). Anti-ganglioside antibodies and the presynaptic motor nerve terminal. Annals of the New York Academy of Sciences 1132: 114–123.Google Scholar
Willison, HJ, Jacobs, BC and van Doorn, PA (2016). Guillain-Barre syndrome. Lancet 388: 717–727.Google Scholar
Winter, SE, Thiennimitr, P, Winter, MG, Butler, BP, Huseby, DL, Crawford, RW, Russell, JM, Bevins, CL, Adams, LG, Tsolis, RM, Roth, JR and Bäumler, AJ (2010). Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature 467: 426–429.Google Scholar
Young, KT, Davis, LM and Dirita, VJ (2007). Campylobacter jejuni: molecular biology and pathogenesis. Nature Reviews. Microbiology 5: 665–679.Google Scholar
Young, VB and Mansfield, LS (2005). Campylobacter infection—clinical context. In: Ketley, JM, Konkel, ME (eds) Campylobacter: Molecular and Cellular Biology. London, UK: Horizon Bioscience, pp. 1–12.Google Scholar
Yuki, N, Taki, T, Inagaki, F, Kasama, T, Takahashi, M, Saito, K, Handa, S and Miyatake, T (1993). A bacterium lipopolysaccharide that elicits Guillain-Barré syndrome has a GM1 ganglioside-like structure. The Journal of Experimental Medicine 178: 1771–1775.Google Scholar
Zhang, Q, Lin, J and Pereira, S (2003). Fluoroquinolone-resistant Campylobacter in animal reservoirs: dynamics of development, resistance mechanisms and ecological fitness. Animal Health Research Reviews 4: 63–71.Google Scholar
Zhang, Q, Sahin, O, McDermott, PF and Payot, S (2006). Fitness of antimicrobial-resistant Campylobacter and salmonella. Microbes and Infection 8: 1972–1978.Google Scholar
Zhou, K, Aertsen, A and Michiels, C (2014). The role of variable DNA tandem repeats in bacterial adaptation. FEMS Microbiology Reviews 38.Google Scholar