Immuno-epidemiology of chronic bacterial and helminth co-infections: Observations from the field and evidence from the laboratory

International Journal for Parasitology

Volumn 42, Issue 7, 2012, Pages 647-655

  Pathak, Ashutosh K ^a   Pelensky, Chad ^a   Boag, Brian ^b   Cattadori, Isabella M ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

Author keywords

Bordetella bronchiseptica; Co infection; Field epidemiology; Graphidium strigosum; Immune response; Laboratory infection

Indexed keywords

BACTERIUM; EPIDEMIOLOGY; IMMUNE RESPONSE; INFECTIOUS DISEASE; LABORATORY METHOD; LAGOMORPH; NEMATODE;

AGE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL INFECTION; BACTERIAL INTENSITY; BORDETELLA BRONCHISEPTICA; BREEDING; CONTROLLED STUDY; DISEASE SEVERITY; EPIDEMIOLOGY; GRAPHIDIUM STRIGOSUM; HELMINTH INTENSITY; HELMINTHIASIS; HOST; HOST PARASITE INTERACTION; IMMUNE RESPONSE; IMMUNOEPIDEMIOLOGY; LOWER RESPIRATORY TRACT; MALE; MICROBIAL COLONIZATION; MICROBIOLOGICAL PARAMETERS; MIXED INFECTION; NEMATODE; NONHUMAN; NOSE CAVITY; ORYCTOLAGUS CUNICULUS; PARASITE PARASITE INTERACTION; PARASITISM; PREVALENCE; RABBIT; REINFECTION; SEASONAL VARIATION; WINTER;

ANIMALS; BACTERIAL LOAD; BORDETELLA BRONCHISEPTICA; BORDETELLA INFECTIONS; CHRONIC DISEASE; COINFECTION; MALE; PARASITE LOAD; PREVALENCE; RABBITS; RODENT DISEASES; SEASONS; TRICHOSTRONGYLOIDEA; TRICHOSTRONGYLOIDIASIS;

BACTERIA (MICROORGANISMS); BORDETELLA BRONCHISEPTICA; GRAPHIDIUM STRIGOSUM; ORYCTOLAGUS CUNICULUS; VERMES;

EID: 84862337543     PISSN: 00207519     EISSN: 18790135     Source Type: Journal    
DOI: 10.1016/j.ijpara.2012.04.011     Document Type: Article

References (47)

1. Abolins S.R., Pocock M.J., Hafalla J.C., Riley E.M., Viney M.E. Measures of immune function of wild mice, Mus musculus. Mol. Ecol. 2011, 20:881-892.
2. Allen J.E., Maizels R.M. Diversity and dialogue in immunity to helminths. Nat. Rev. Immunol. 2011, 11:375-388.
3. Babayan S.A., Read A.F., Lawrence R.A., Bain O., Allen J.E. Filarial parasites develop faster and reproduce earlier in response to host immune effectors that determine filarial life expectancy. PLoS Biol. 2010, 8:e1000525.
4. Baker D.G. Natural pathogens of laboratory mice, rats, and rabbits and their effects on research. Clin. Microbiol. Rev. 1998, 11:231-266.
5. Blaser M.J., Kirschner D. The equilibria that allow bacterial persistence in human hosts. Nature 2007, 449:843-849.
6. Boag B., Lello J., Fenton A., Tompkins D.M., Hudson P.J. Patterns of parasite aggregation in the wild European rabbit (Oryctolagus cuniculus). Int. J. Parasitol. 2001, 31:1421-1428.
7. Bourke C.D., Maizels R.M., Mutapi F. Acquired immune heterogeneity and its sources in human helminth infection. Parasitology 2011, 138:139-159.
8. Brady M.T., O'Neill S.M., Dalton J.P., Mills K.H. Fasciola hepatica suppresses a protective Th1 response against Bordetella pertussis. Infect. Immun. 1999, 67:5372-5378.
9. Brockmeier S.L., Loving C.L., Nicholson T.L., Palmer M.V. Coinfection of pigs with porcine respiratory coronavirus and Bordetella bronchiseptica. Vet. Microbiol. 2008, 128:36-47.
10. Brockmeier S.L. Prior infection with Bordetella bronchiseptica increases nasal colonization by Haemophilus parasuis in swine. Vet. Microbiol. 2004, 99:75-78.
11. Carmo A.M., Vicentini M.A., Dias A.T., Alves L.L., Alves C.C., Brandi J.S., De Paula M.L., Fernandes A., Barsante M.M., Souza M.A., Teixeira H.C., Negrão-Corrêa D., Ferreira A.P. Increased susceptibility to Strongyloides venezuelensis in mice due to Mycobacterium bovis co-infection which modulates production of Th2 cytokines. Parasitology 2009, 136:1357-1365.
12. Cattadori I.M., Boag B., Bjørnstad O.N., Cornell S.J., Hudson P.J. Peak shift and epidemiology in a seasonal host-nematode system. Proc. Biol. Sci. 2005, 272:1163-1169.
13. Cattadori I.M., Albert R., Boag B. Variation in host susceptibility and infectiousness generated by co-infection: the myxoma-Trichostrongylus retortaeformis case in wild rabbits. J. R. Soc. Interface 2007, 4:831-840.
14. Cattadori I.M., Boag B., Hudson P.J. Parasite co-infection and interaction as drivers of host heterogeneity. Int. J. Parasitol. 2008, 38:371-380.
15. Chalker V.J., Toomey C., Opperman S., Brooks H.W., Ibuoye M.A., Brownlie J., Rycroft A.N. Respiratory disease in kennelled dogs: serological responses to Bordetella bronchiseptica lipopolysaccharide do not correlate with bacterial isolation or clinical respiratory symptoms. Clin. Diagn. Lab. Immunol. 2003, 10:352-356.
16. Cooper P.J. Mucosal immunology of geohelminth infections in humans. Mucosal Immunol. 2009, 2:288-299.
17. Cox F.E. Concomitant infections, parasites and immune responses. Parasitology 2001, 122:S23-S38.
18. Diavatopoulos D.A., Cummings C.A., Schouls L.M., Brinig M.M., Relman D.A., Mooi F.R. Bordetella pertussis, the causative agent of whooping cough, evolved from a distinct, human-associated lineage of B. bronchiseptica. PLoS Pathog. 2005, 1:e45.
19. Dunne D.W., Riley E.M. Immunity, morbidity and immunoepidemiology in parasite infections. Parasite Immunol. 2004, 26:425-428.
20. Eira C., Torres J., Miquel J., Vingada J. The helminth parasites of the wild rabbit Oryctolagus cuniculus and their effect on host condition in Dunas de Mira. Portugal J. Helminthol. 2007, 81:239-246.
21. Fox J.G., Beck P., Dangler C.A., Whary M.T., Wang T.C., Shi H.N., Nagler-Anderson C. Concurrent enteric helminth infection modulates inflammation and gastric immune responses and reduces helicobacter-induced gastric atrophy. Nat. Med. 2000, 6:536-542.
22. Graham A.L. Ecological rules governing helminth-microparasite coinfection. Proc. Natl. Acad. Sci. USA 2008, 105:566-570.
23. Hellriegel B. Immunoepidemiology - bridging the gap between immunology and epidemiology. Trends Parasitol. 2001, 17:102-106.
24. Hewitson J.P., Grainger G.R., Maizels R.M. Helminth immunoregulation: the role of parasite secreted proteins in modulating host immunity. Mol. Biochem. Parasit. 2009, 167:1-11.
25. Huby F., Nano J.L., Mallet S., Hoste H. Effects of the excretory/secretory products of Trichostrongylus colubriformis on the growth of different cell lines. Int. J. Parasitol. 1999, 29:697-702.
26. Kirimanjeswara G.S., Mann P.B., Harvill E.T. Role of antibodies in immunity to Bordetella infections. Infect. Immun. 2003, 71:1719-1724.
27. Massoni J., Cassone J., Durette-Desset M.C., Audebert F. Development of Graphidium strigosum (Nematoda, Haemonchidae) in its natural host, the rabbit (Oryctolagus cuniculus) and comparison with several Haemonchidae parasites of ruminants. Parasit. Res. 2011, 25-36.
28. Meeusen E.N., Balic A., Bowles V. Cells, cytokines and other molecules associated with rejection of gastrointestinal nematode parasites. Vet. Immunol. Immunopathol. 2005, 18:121-125.
29. Monack D.M., Mueller A., Falkow S. Persistent bacterial infections: the interface of the pathogen and the host immune system. Nat. Rev. Microbiol. 2004, 2:747-765.
30. Murphy L., Nalpas N., Stear M., Cattadori I.M. Explaining patterns of infection in free-living populations using laboratory immune experiments. Parasite Immunol. 2011, 33:287-302.
31. Newey S., Shaw D.J., Kirby A., Montieth P., Hudson P.J., Thirgood S.J. Prevalence, intensity and aggregation of intestinal parasites in mountain hares and their potential impact on population dynamics. Int. J. Parasitol. 2005, 35:367-373.
32. O'Neill S.M., Mills K.H., Dalton J.P. Fasciola hepatica cathepsin l cysteine proteinase suppresses Bordetella pertussis-specific interferon-gamma production in vivo. Parasite Immunol. 2001, 23:541-547.
33. Page K.R., Scott A.L., Manabe Y.C. The expanding realm of heterologous immunity: friend or foe? Cell. Microbiol. 2006, 8:185-196.
34. Parker D., Prince A. Innate immunity in the respiratory epithelium. Am. J. Respir. Cell Mol. Biol. 2011, 45:189-201.
35. Pathak A.K., Boag B., Poss M., Harvill E.T., Cattadori I.M. Seasonal breeding drives the incidence of a chronic bacterial infection in a free-living herbivore population. Epidemiol. Infect. 2011, 139:1210-1219.
36. Pathak A.K., Biarnes M.C., Murphy L., Cattadori I.M. Snapshot of spatio-temporal cytokine responses to single and co-infections with helminths and bacteria. Results Immunol. 2011, 1:95-102.
37. Pathak A.K., Creppage K.E., Werner J.R., Cattadori I.M. Immune regulation of a chronic bacteria infection and consequences for pathogen transmission. BMC Microbiol. 2010, 10:226.
38. Perry S., Hussain R., Parsonnet J. The impact of mucosal infections on acquisition and progression of tuberculosis. Mucosal Immunol. 2011, 4:246-251.
39. Rastogi D., Ratner A.J., Prince A. Host-bacterial interactions in the initiation of inflammation. Paediatr. Respir. Rev. 2001, 2:245-252.
40. Rotchford K., Strum A.W., Wilkinson D. Effect of coinfection with STDs and of STD treatment on HIV shedding in genital tract secretions. Sex Transm. Dis. 2000, 27:243-248.
41. Rougier S., Galland D., Boucher S., Boussarie D., Vallé M. Epidemiology and susceptibility of pathogenic bacteria responsible for upper respiratory tract infections in pet rabbits. Vet. Microbiol. 2006, 115:192-198.
42. Schmittgen T.D., Livak K.J. Analyzing real-time PCR data by the comparative C(t) method. Nat. Protoc. 2008, 3:1101-1108.
43. Stewart G.R., Boussinesq M., Coulson T., Elson L., Nutman T., Bradley J.E. Onchocerciasis modulates the immune response to mycobacterial antigens. Clin. Exp. Immunol. 1999, 117:517-523.
44. Supali T., Verweij J.J., Wiria A.E., Djuardi Y., Hamid F., Kaisar M.M., Wammes L.J., van Lieshout L., Luty A.J., Sartono E., Yazdanbakhsh M. Polyparasitism and its impact on the immune system. Int. J. Parasitol. 2010, 40:1171-1176.
45. Tornatore M., Gonçalves C.V., Bianchi M.S., Germano F.N., Garcés A.X., Soares M.A., Machado E.S., Martinez A.M. Co-infections associated with human immunodeficiency virus type 1 in pregnant women from southern Brazil: high rate of intraepithelial cervical lesions. Mem. Inst. Oswaldo Cruz 2012, 107:205-210.
46. Thakar J., Pathak A.K., Murphy L., Albert R., Cattadori I.M. Network model of immune responses reveals key effectors to single and co-infection dynamics by a respiratory bacterium and a gastrointestinal helminth. PLoS Comput. Biol. 2012, 8:e1002345.
47. Zhu J., Yamane H., Paul W.E. Differentiation of effector CD4 T cell populations. Annu. Rev. Immunol. 2010, 28:445-489.