Within-host dynamics of mycoplasma infections: Conjunctivitis in wild passerine birds

Journal of Theoretical Biology

Volumn 306, Issue , 2012, Pages 73-92

  Hurtado, Paul J ^a  

^a Cornell University ^*  (United States)

Author keywords

House finch (Carpodacus mexicanus); Immune response; Mycoplasma gallisepticum; Ordinary differential equations; Virulence

Indexed keywords

HOST-PATHOGEN INTERACTION; IMMUNE RESPONSE; INFECTIOUS DISEASE; NUMERICAL MODEL; PASSERINE; VIRULENCE;

ARTICLE; BIRD; CONJUNCTIVITIS; CONTROLLED STUDY; GROWTH RATE; HOST PATHOGEN INTERACTION; IMMUNE RESPONSE; MYCOPLASMA; MYCOPLASMA GALLISEPTICUM; MYCOPLASMA GALLISEPTICUM INFECTION; MYCOPLASMOSIS; NONHUMAN; PRIORITY JOURNAL; SURVIVAL;

ANIMALS; ANTIBODIES, BACTERIAL; BIRD DISEASES; CONJUNCTIVITIS, BACTERIAL; FINCHES; HOST-PATHOGEN INTERACTIONS; IMMUNITY, INNATE; MODELS, IMMUNOLOGICAL; MYCOPLASMA GALLISEPTICUM; MYCOPLASMA INFECTIONS; VIRULENCE;

AVES; CARPODACUS MEXICANUS; MYCOPLASMA; MYCOPLASMA GALLISEPTICUM; MYCOPLASMATALES; PASSERIFORMES; VERTEBRATA;

EID: 84860830122     PISSN: 00225193     EISSN: 10958541     Source Type: Journal    
DOI: 10.1016/j.jtbi.2012.04.018     Document Type: Article

References (65)

1. Aldrich J.W., Weske J.S. Origin and evolution of the eastern house finch population. Auk 1978, 95(3):528-536.
2. Altizer S., Hochachka W.M., Dhondt A.A. Seasonal dynamics of mycoplasmal conjunctivitis in eastern north american house finches. J. Anim. Ecol. 2004, 73(2):309-322.
3. Altizer S., Davis A.K., Cook K.C., Cherry J.J. Age, sex, and season affect the risk of mycoplasmal conjunctivitis in a southeastern house finch population. Can. J. Zool. 2004, 82(5):755-763. 10.1139/Z04-050.
4. Altizer S., Dobson A., Hosseini P., Hudson P., Pascual M., Rohani P. Seasonality and the dynamics of infectious diseases. Ecol. Lett. 2006, 9(4):467-484. 10.1111/j.1461-0248.2005.00879.x.
5. Baseman J.B., Tully J.G. Mycoplasmas: sophisticated, reemerging, and burdened by their notoriety. Emerg. Infect. Dis. 1997, 3(1):21-32. 10.3201/eid0301.970103.
6. Mycoplasmas: Molecular Biology Pathogenicity and Strategies for Control 2005, Horizon Bioscience, Wymondham, Norfolk, U.K. A. Blanchard, G. Browning (Eds.).
7. Brown D.R., Zacher L.A., Wendland L.D., Brown M.B. Emerging mycoplasmoses in wildlife. Mycoplasmas Molecular Biology Pathogenicity and Strategies for Control 2005, 383-414. Horizon Bioscience, Wymondham, Norfolk, U.K, (Chapter 11). A. Blanchard, G. Browning (Eds.).
8. Brown D.R., Whitcomb R.F., Bradbury J.M. Revised minimal standards for description of new species of the class Mollicutes (division Tenericutes). Int. J. Syst. Evol. Microbiol. 2007, 57(11):2703-2719. 10.1099/ijs.0.64722-0.
9. Cecchini K.R., Gorton T.S., Geary S.J. Transcriptional responses of Mycoplasma gallisepticum strain R in association with eukaryotic cells. J. Bacteriol. 2007, 189(16):5803-5807. 10.1128/JB.00667-07.
10. Cherry J.J., Ley D.H., Altizer S. Genotypic analyses of Mycoplasma gallisepticum isolates from songbirds by random amplification of polymorphic DNA and amplified-fragment length polymorphism. J. Wildl. Dis. 2006, 42(2):421-428.
11. Citti C., Browning G.F., Rosengarten R. Phenotypic diversity and cell invasion in host subversion by pathogenic mycoplasmas. Mycoplasmas: Molecular Biology Pathogenicity and Strategies for Control 2005, 439-483. Horizon Bioscience, Wymondham, Norfolk, U.K., (Chapter 13). A. Blanchard, G. Browning (Eds.).
12. Cooper C.B., Hochachka W.M., Dhondt A.A. Contrasting natural experiments confirm competition between house finches and house sparrows. Ecology 2007, 88(4):864-870. 10.1890/06-0855.
13. Dhondt A., Tessaglia D., Slothower R. Epidemic mycoplasmal conjunctivitis in house finches from eastern North America. J. Wildl. Dis. 1998, 34(2):265-280.
14. Dhondt A., Badyaev A., Dobson A., Hawley D., Driscoll M., Hochachka W., Ley D. Dynamics of mycoplasmal conjunctivitis in the native and introduced range of the host. EcoHealth 2006, 3:95-102. 10.1007/s10393-006-0019-7.
15. Dhondt A.A., Altizer S., Cooch E.G., Davis A.K., Dobson A., Driscoll M.J., Hartup B.K., Hawley D.M., Hochachka W.M., Hosseini P.R., Jennelle C.S., Kollias G.V., Ley D.H., Swarthout E.C., Sydenstricker K.V. Dynamics of a novel pathogen in an avian host: mycoplasmal conjunctivitis in house finches. Acta Tropica 2005, 94(1):77-93. 10.1016/j.actatropica.2005.01.009.
16. Dhondt A.A., Dhondt K.V., Hawley D.M., Jennelle C.S. Experimental evidence for transmission of Mycoplasma gallisepticum in house finches by fomites. Avian Pathol. 2007, 36(3):205-208. 10.1080/03079450701286277.
17. Dhondt A.A., Dhondt K.V., McCleery B.V. Comparative infectiousness of three passerine bird species after experimental inoculation with Mycoplasma gallisepticum. Avian Pathol. 2008, 37(6):635-640. 10.1080/03079450802499100.
18. Dhondt K.V., Dhondt A.A., Ley D.H. Effects of route of inoculation on Mycoplasma gallisepticum infection in captive house finches. Avian Pathol. 2007, 36(6):475-479. 10.1080/03079450701642016.
19. Edward D.G.f., Freundt E.A. Proposal for Mollicutes as name of the class established for the order Mycoplasmatales. Int. J. Syst. Bacteriol. 1967, 17(3):267-268. 10.1099/00207713-17-3-267.
20. Edward D.G.f., Kanarek E.A. Organisms of the pleuropneumonia group of avian origin: their classification into species. Ann. N. Y. Acad. Sci. 1960, 79(10):696-702. 10.1111/j.1749-6632.1960.tb42744.x.
21. Elliott J.J., Aribib R.S. Origin and status of the eastern house finch in the eastern United States. Auk 1953, 70(1):31-37.
22. Farmer K.L., Hill G.E., Roberts S.R. Susceptibility of wild songbirds to the house finch strain of Mycoplasma Gallisepticum. J. Wildl. Dis. 2005, 41(2):317-325.
23. Faustino C.R., Jennelle C.S., Connolly V., Davis A.K., Swarthout E.C., Dhondt A.A., Cooch E.G. Mycoplasma gallisepticum infection dynamics in a house finch population: seasonal variation in survival,bb encounter and transmission rate. J. Anim. Ecol. 2004, 73(4):651-669. 10.1111/j.0021-8790.2004.00840.x.
24. Fischer J.R., Stallknecht D.E., Luttrell P., Dhondt A.A., Converse K.A. Mycoplasmal conjunctivitis in wild songbirds: the spread of a new contagious disease in a mobile host population. Emerg. Infect. Dis. 1997, 3(1):69-72. 10.3201/eid0301.970110.
25. Flindt R., Solomon N. Amazing Numbers in Biology 2006, Springer Berlin Heidelberg. first ed., 10.1007/3-540-30147-X.
26. Grodio J.L., Dhondt K.V., O'Connell P.H., Schat K.A. Detection and quantification of Mycoplasma gallisepticum genome load in conjunctival samples of experimentally infected house finches (Carpodacus mexicanus) using real-time polymerase chain reaction. Avian Pathol. 2008, 37(4):385-391. 10.1080/03079450802216629.
27. Grodio J.L., Hawley D.M., Osnas E.E., Ley D.H., Dhondt K.V., Dhondt A.A., Schat K.A. Pathogenicity and immunogenicity of three Mycoplasma gallisepticum isolates in house finches (Carpodacus mexicanus). Vet. Microbiol. 2011, 155(1):53-61. 10.1016/j.vetmic.2011.08.003.
28. Hartup B., Mohammed H., Kollias G., Dhondt A. Risk factors associated with mycoplasmal conjunctivitis in house finches. J. Wildl. Dis. 1998, 34(2):281-288.
29. Hartup B., Dhondt A., Sydenstricker K., Hochachka W., Kollias G. Host range and dynamics of mycoplasmal conjunctivitis among birds in North America. J. Wildl. Dis. 2001, 37(1):72-81.
30. Hartup B.K., Bickal J.M., Dhondt A.A., Ley D.H., Kollias G.V. Dynamics of conjunctivitis and Mycoplasma gallisepticum infections in house finches. Auk 2001, 118(2):327-333. 10.1642/0004-8038(2001)118[0327:DOCAMG]2.0.CO;2.
31. Hawley D.M., Sydenstricker K.V., Kollias G.V., Dhondt A.A. Genetic diversity predicts pathogen resistance and cell-mediated immunocompetence in house finches. Biol. Lett. 2005, 1(3):326-329. 10.1098/rsbl.2005.0303.
32. Hawley D.M., Lindström K., Wikelski M. Experimentally increased social competition compromises humoral immune responses in house finches. Horm. Behav. 2005, 49(4):417-424. 10.1016/j.yhbeh.2005.09.003.
33. Hawley D.M., Hanley D., Dhondt A.A., Lovette I.J. Molecular evidence for a founder effect in invasive house finch (Carpodacus mexicanus) populations experiencing an emergent disease epidemic. Mol. Ecol. 2006, 15(1):263-275. 10.1111/j.1365-294X.2005.02767.x.
34. Hawley D.M., Jennelle C.S., Sydenstricker K.V., Dhondt A.A. Pathogen resistance and immunocompetence covary with social status in house finches (Carpodacus mexicanus). Funct. Ecol. 2007, 21(3):520-527. 10.1111/j.1365-2435.2007.01254.x.
35. Hawley D.M., Dhondt K.V., Dobson A.P., Grodio J.L., Hochachka W.M., Ley D.H., Osnas E.E., Schat K.A., Dhondt A.A. Common garden experiment reveals pathogen isolate but no host genetic diversity effect on the dynamics of an emerging wildlife disease. J. Evol. Biol. 2010, 23:1680-1688. 10.1111/j.1420-9101.2010.02035.x.
36. Hickman-Davis J., Michalek S., Gibbs-Erwin J., Lindsey J. Depletion of alveolar macrophages exacerbates respiratory mycoplasmosis in mycoplasma-resistant C57BL mice but not mycoplasma-susceptible C3H mice. Infect. Immun. 1997, 65(6):2278-2282.
37. Hochachka W.M., Dhondt A.A. Density-dependent decline of host abundance resulting from a new infectious disease. Proc. Natl. Acad. Sci. USA 2000, 97(10):5303-5306. 10.1073/pnas.080551197.
38. Hochachka W.M., Dhondt A.A. House finch (Carpodacus mexicanus) population- and group-level responses to a bacterial disease. Ornithol. Monogr. 2006, 60:30-43.
39. Holt R.D., Barfield M. Within-host pathogen dynamics: some ecological and evolutionary consequences of transients. Disease Evolution: Models, Concepts, and Data Analyses, DIMACS Series in Discrete Mathematics and Theoretical Computer Science 2006, 45-66. American Mathematical Society. Z. Feng, U. Dieckmann, S. Levin (Eds.).
40. Hosseini P.R., Dhondt A.A., Dobson A. Seasonality and wildlife disease: how seasonal birth, aggregation and variation in immunity affect the dynamics of Mycoplasma gallisepticum in house finches. Proc. R Soc. Lond. B Biol. Sci. 2004, 271(1557):2569-2577. 10.1098/rspb.2004.2938.
41. Hotchkiss E.R., Davis A.K., Cherry J.J., Altizer S. Mycoplasmal conjunctivitis and the behavior of wild house finches (Carpodacus mexicanus) at bird feeders. Bird Behav. 2005, 17(1):1-8.
42. Hu, Z., Yin, J., Shen, K., Kang, W., Chen, Q., 2009. Outbreaks of Hemotrophic mycoplasma infections in China [letter], Emerg Infect Dis 15(7) . doi:10.3201/eid1507.090174.
43. Hurtado, P.J., Infectious disease ecology: immune-pathogen dynamics, and how trophic interactions drive prey-predator-disease dynamics, Ph.D. Thesis, Cornell University (August 2011).
44. Hurtado P. The potential impact of disease on the migratory structure of a partially migratory passerine population. Bull. Math. Biol. 2008, 70(8):2264-2282. 10.1007/s11538-008-9345-y.
45. Kollias G.V., Sydenstricker K.V., Kollias H.W., Ley D.H., Hosseini P.R., Connolly V., Dhondt A.A. Experimental infection of house finches with Mycoplasma gallisepticum. J. Wildl. Dis. 2004, 40(1):79-86.
46. Lange A., Ferguson N.M. Antigenic diversity transmission mechanisms and the evolution of pathogens. PLoS Comput. Biol. 2009, 5(10):e1000536. 10.1371/journal.pcbi.1000536.
47. Lee K.A. Linking immune defenses and life history at the levels of the individual and the species. Integr. Comp. Biol. 2006, 46(6):1000-1015. 10.1093/icb/icl049.
48. Lee K., Martin L., Wikelski M. Responding to inflammatory challenges is less costly for a successful avian invader, the house sparrow (Passer domesticus), than its less-invasive congener. Oecologia 2005, 145:243-250. 10.1007/s00442-005-0113-5.
49. Ley D.H., Sheaffer D.S., Dhondt A.A. Further western spread of Mycoplasma gallisepticum infection of house finches. J. Wildl. Dis. 2006, 42(2):429-431.
50. Lindström K.M., Hawley D.M., Davis A.K., Wikelski M. Stress responses and disease in three wintering house finch (Carpodacus mexicanus) populations along a latitudinal gradient. Gen. Comp. Endocrinol. 2005, 143(3):231-239. 10.1016/j.ygcen.2005.04.005.
51. Luttrell M., Stallknecht D., Fischer J., Sewell C., Kleven S. Natural Mycoplasma gallisepticum infection in a captive flock of house finches. J. Wildl. Dis. 1998, 34(2):289-296.
52. Luttrell M.P., Fischer J.R., Stallknecht D.E., Kleven S.H. Field investigation of Mycoplasma gallisepticum infections in house finches (Carpodacus mexicanus) from Maryland and Georgia. Avian Dis. 1996, 40(2):335-341. 10.2307/1592229.
53. Marco I., Mentaberre G., Ballesteros C., Bischof D.F., Lavín S., Vilei E.M. First report of Mycoplasma conjunctivae from wild caprinae with infectious keratoconjunctivitis in the Pyrenees (NE Spain). J. Wildl. Dis. 2009, 45(1):238-241. (arXiv:http://www.jwildlifedis.org/content/45/1/238.full.pdf+html).
54. Martin L.B., Pless M., Svoboda J., Wikelski M. Immune activity in temperate and tropical house sparrows: a common-garden experiment. Ecology 2004, 85(8):2323-2331. 10.1890/03-0365.
55. Mikaelian I., Ley D., Claveau R., Lemieux M., Berube J. Mycoplasmosis in evening and pine grosbeaks with conjunctivitis in Quebec. J. Wildl. Dis. 2001, 37(4):826-830.
56. Messick, J.B., 2004. Hemotrophic mycoplasmas (hemoplasmas): a review and new insights into pathogenic potential, Vet Clin Pathol 33(1), . doi:10.1111/j.1939-165X.2004.tb00342.x.
57. Osnas E.E., Dobson A.P. Evolution of virulence when transmission occurs before disease. Biol. Lett. 2010, 6(4):505-508. 10.1098/rsbl.2009.1019.
58. Papazisi L., Gorton T.S., Kutish G., Markham P.F., Browning G.F., Nguyen D.K., Swartzell S., Madan A., Mahairas G., Geary S.J. The complete genome sequence of the avian pathogen Mycoplasma gallisepticum strain Rlow. Microbiology 2003, 149(9):2307-2316. 10.1099/mic.0.26427-0.
59. Pepin K., Volkov I., Banavar J., Wilke C., Grenfell B. Phenotypic differences in viral immune escape explained by linking within-host dynamics to host-population immunity. J. Theor. Biol. 2010, 265(4):501-510. 10.1016/j.jtbi.2010.05.036.
60. Reynolds A., Rubin J., Clermont G., Day J., Vodovotz Y., Ermentrout G.B. A reduced mathematical model of the acute inflammatory response: I.Derivation of model analysis of anti-inflammation. J. Theor. Biol. 2006, 242(1):220-236. 10.1016/j.jtbi.2006.02.016.
61. Roberts S., Nolan P., Hill G. Characterization of Mycoplasma gallisepticum Infection in Captive House Finches (Carpodacus mexicanus) in 1998. Avian Dis. 2001, 45:70-75. 10.2307/1593013.
62. Segel L.A., Perelson A.S. Exploiting the diversity of time scales in the immune system: A B-cell antibody model. J. Stat. Phys. 1991, 63:1113-1131. 10.1007/BF01030002.
63. Simecka J.W. Immune responses following mycoplasma infection. Mycoplasmas: Molecular Biology Pathogenicity and Strategies for Control, Horizon Bioscience 2005, 485-534. Horizon Bioscience, Wymondham, Norfolk, U.K, (Chapter 14). A. Blanchard, G. Browning (Eds.).
64. Sydenstricker K.V., Dhondt A.A., Ley D.H., Kollias G.V. Re-exposure of captive house finches that recovered from Mycoplasma gallisepticum infection. J. Wildl. Dis. 2005, 41(2):326-333.
65. Sydenstricker K.V., Dhondt A.A., Hawley D.M., Jennelle C.S., Kollias H.W., Kollias G.V. Characterization of experimental Mycoplasma gallisepticum infection in captive house finch flocks. Avian Dis. 2006, 50(1):39-44. 10.1637/7403-062805R.1.