Scabies Mites Alter the Skin Microbiome and Promote Growth of Opportunistic Pathogens in a Porcine Model

PLoS Neglected Tropical Diseases

Volumn 8, Issue 5, 2014, Pages

  Swe, Pearl M ^a   Zakrzewski, Martha ^a   Kelly, Andrew ^b   Krause, Lutz ^a   Fischer, Katja ^a  

^a QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^b UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ACARICIDE; DEXAMETHASONE; DORAMECTIN;

ANIMAL MODEL; ARTICLE; BACTERIAL SKIN DISEASE; CONTROLLED STUDY; DNA EXTRACTION; FEMALE; LACTOBACILLUS; MICROBIOME; MITE; MITE INFESTATION; NONHUMAN; NUCLEOTIDE SEQUENCE; OPPORTUNISTIC INFECTION; PATHOGENESIS; SCABIES; SECONDARY INFECTION; SKIN; STAPHYLOCOCCUS; STREPTOCOCCUS; SWINE; UNINDEXED SEQUENCE; ANIMAL; BACTERIA; BACTERIAL INFECTION; CLASSIFICATION; COMPLICATION; DISEASE MODEL; EXTERNAL EAR; GENETICS; HOST PARASITE INTERACTION; ISOLATION AND PURIFICATION; MICROBIOLOGY; MICROFLORA; PARASITOLOGY;

ANIMALS; BACTERIA; BACTERIAL INFECTIONS; DISEASE MODELS, ANIMAL; EAR AURICLE; HOST-PARASITE INTERACTIONS; MICROBIOTA; OPPORTUNISTIC INFECTIONS; SCABIES; SKIN; STAPHYLOCOCCUS; SWINE;

EID: 84901767891     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0002897     Document Type: Article

References (70)

1. Engelman D, Kiang K, Chosidow O, McCarthy J, Fuller C, et al. (2013) Toward the Global Control of Human Scabies: Introducing the International Alliance for the Control of Scabies. PLoS Negl Trop Dis 7(8): e2167 doi:10.1371/journal.pntd.0002167.
2. Hay RJ, Steer AC, Engelman D, Walton S, (2012) Scabies in the developing world-its prevalence, complications, and management. Clin Microbiol Infect 18: 313-323.
3. Fuller LC, (2013) Epidemiology of scabies. Curr Opin Infect Dis 26: 123-126.
4. Hicks MI, Elston DM, (2009) Scabies. Dermatol Ther 22: 279-292.
5. Makigami K, Ohtaki N, Ishii N, Yasumura S, (2009) Risk factors of scabies in psychiatric and long-term care hospitals: a nationwide mail-in survey in Japan. J Dermatol 36: 491-498.
6. Lassa S, Campbell MJ, Bennett CE, (2011) Epidemiology of scabies prevalence in the U.K. from general practice records. Br J Dermatol 164: 1329-1334.
7. Mahe A, Hay RJ (2005) Epidemiology and management of common skin diseases in childern in developing countries. World Health Organization Discussion papers on child health.
8. Whitehall J, Kuzulugil D, Sheldrick K, Wood A, (2013) Burden of paediatric pyoderma and scabies in North West Queensland. J Paediatr Child Health 49: 141-143.
9. Clucas DB, Carville KS, Connors C, Currie BJ, Carapetis JR, et al. (2008) Disease burden and health-care clinic attendances for young children in remote aboriginal communities of northern Australia. Bull World Health Organ 86: 275-281.
10. Hay RJ, Steer AC, Chosidow O, Currie BJ, (2013) Scabies: a suitable case for a global control initiative. Curr Opin Infect Dis 26: 107-109.
11. Hengge UR, Currie BJ, Jager G, Lupi O, Schwartz RA, (2006) Scabies: a ubiquitous neglected skin disease. Lancet Infect Dis 6: 769-779.
12. Andrews RM, Kearns T, Connors C, Parker C, Carville K, et al. (2009) A regional initiative to reduce skin infections amongst aboriginal children living in remote communities of the Northern Territory, Australia. PLoS Negl Trop Dis 3: e554.
13. Steer AC, Jenney AW, Kado J, Batzloff MR, La Vincente S, et al. (2009) High burden of impetigo and scabies in a tropical country. PLoS Negl Trop Dis 3: e467.
14. Carapetis J, Steer AC, Mulholland EK (2005) The current evidence for the burden of group A streptococcal diseases. World Health Organization Discussion papers of child health.
15. McCarthy JS, Kemp DJ, Walton SF, Currie BJ, (2004) Scabies: more than just an irritation. Postgrad Med J 80: 382-387.
16. Bergstrom FC, Reynolds S, Johnstone M, Pike RN, Buckle AM, et al. (2009) Scabies mite inactivated serine protease paralogs inhibit the human complement system. J Immunol 182: 7809-7817.
17. Mika A, Reynolds SL, Mohlin FC, Willis C, Swe PM, et al. (2012) Novel scabies mite serpins inhibit the three pathways of the human complement system. PLoS One 7: e40489.
18. Mika A, Reynolds SL, Pickering D, McMillan D, Sriprakash KS, et al. (2012) Complement inhibitors from scabies mites promote streptococcal growth-a novel mechanism in infected epidermis? PLoS Negl Trop Dis 6: e1563.
19. Kong HH, (2011) Skin microbiome: genomics-based insights into the diversity and role of skin microbes. Trends Mol Med 17: 320-328.
20. Morsy GH, Turek JJ, Gaafar SM, (1989) Scanning electron microscopy of sarcoptic mange lesions in swine. Vet Parasitol 31: 281-288.
21. Steinstraesser L, Vranckx JJ, Mohammadi-Tabrisi A, Jacobsen F, Mittler D, et al. (2006) A novel titanium wound chamber for the study of wound infections in pigs. Comp Med 56: 279-285.
22. Sullivan TP, Eaglstein WH, Davis SC, Mertz P, (2001) The pig as a model for human wound healing. Wound Repair Regen 9: 66-76.
23. Hollander DA, Erli HJ, Theisen A, Falk S, Kreck T, et al. (2003) Standardized qualitative evaluation of scar tissue properties in an animal wound healing model. Wound Repair Regen 11: 150-157.
24. Vodicka P, Smetana K Jr, Dvorankova B, Emerick T, Xu YZ, et al. (2005) The miniature pig as an animal model in biomedical research. Ann N Y Acad Sci 1049: 161-171.
25. Salvesen B, Mollnes TE, (2009) Pathway-specific complement activity in pigs evaluated with a human functional complement assay. Mol Immunol 46: 1620-1625.
26. Jiang H, Zhang HM, Frank MM, (2010) Subcutaneous infusion of human C1 inhibitor in swine. Clin Immunol 136: 323-328.
27. Meurens F, Summerfield A, Nauwynck H, Saif L, Gerdts V, (2012) The pig: a model for human infectious diseases. Trends Microbiol 20: 50-57.
28. Mounsey K, Ho MF, Kelly A, Willis C, Pasay C, et al. (2010) A tractable experimental model for study of human and animal scabies. PLoS Negl Trop Dis 4: e756.
29. Lo DY, Lee WM, Chien MS, Lin CC, Lee WC, (2005) Effects of dexamethasone on peripheral blood mononuclear cell phenotype in weanling piglets. Comp Immunol Microbiol Infect Dis 28: 251-258.
30. Marliere V, Roul S, Labreze C, Taieb A, (1999) Crusted (Norwegian) scabies induced by use of topical corticosteroids and treated successfully with ivermectin. J Pediatr 135: 122-124.
31. Dowd SE, Callaway TR, Wolcott RD, Sun Y, McKeehan T, et al. (2008) Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP). BMC Microbiol 8: 125.
32. Hooda S, Vester Boler BM, Kerr KR, Dowd SE, Swanson KS, (2013) The gut microbiome of kittens is affected by dietary protein:carbohydrate ratio and associated with blood metabolite and hormone concentrations. Br J Nutr 109: 1637-1646.
33. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, et al. (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7: 335-336.
34. Haas BJ, Gevers D, Earl AM, Feldgarden M, Ward DV, et al. (2011) Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res 21: 494-504.
35. Wang Q, Garrity GM, Tiedje JM, Cole JR, (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73: 5261-5267.
36. Edgar RC, (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26: 2460-2461.
37. Cole JR, Wang Q, Cardenas E, Fish J, Chai B, et al. (2009) The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37: D141-145.
38. Eddy SR, (1998) Profile hidden Markov models. Bioinformatics 14: 755-763.
39. Eddy SR, (2008) A probabilistic model of local sequence alignment that simplifies statistical significance estimation. PLoS Comput Biol 4: e1000069.
40. Price MN, Dehal PS, Arkin AP, (2009) FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol 26: 1641-1650.
41. Yazwinski TA, Tucker C, Featherston H, Johnson Z, Wood-Huels N, (1997) Endectocidal efficacies of doramectin in naturally parasitized pigs. Vet Parasitol 70: 123-128.
42. Grice EA, Kong HH, Conlan S, Deming CB, Davis J, et al. (2009) Topographical and temporal diversity of the human skin microbiome. Science 324: 1190-1192.
43. Tran TV, Weisman LE, (2004) Dexamethasone effects on group B streptococcal infection in newborn rats. Pediatr Infect Dis J 23: 47-52.
44. Hazarika RA, Mahanta PN, Dutta GN, Devriese LA, (1991) Cutaneous infection associated with Staphylococcus hyicus in cattle. Res Vet Sci 50: 374-375.
45. Andresen LO, Ahrens P, Daugaard L, Bille-Hansen V, (2005) Exudative epidermitis in pigs caused by toxigenic Staphylococcus chromogenes. Vet Microbiol 105: 291-300.
46. Foster AP (2012) Staphylococcal skin disease in livestock. Vet Dermatol 23: 342-351, e363.
47. Roberts S, Chambers S, (2005) Diagnosis and management of Staphylococcus aureus infections of the skin and soft tissue. Intern Med J 35 Suppl 2: S97-105.
48. Nagase N, Sasaki A, Yamashita K, Shimizu A, Wakita Y, et al. (2002) Isolation and species distribution of staphylococci from animal and human skin. J Vet Med Sci 64: 245-250.
49. Capone KA, Dowd SE, Stamatas GN, Nikolovski J, (2011) Diversity of the human skin microbiome early in life. J Invest Dermatol 131: 2026-2032.
50. Hogg JC, Lehane MJ, (1999) Identification of bacterial species associated with the sheep scab mite (Psoroptes ovis) by using amplified genes coding for 16S rRNA. Appl Environ Microbiol 65: 4227-4229.
51. Savini V, Catavitello C, Bianco A, Balbinot A, D'Antonio D, (2009) Epidemiology, pathogenicity and emerging resistances in Staphylococcus pasteuri: from mammals and lampreys, to man. Recent Pat Antiinfect Drug Discov 4: 123-129.
52. Rudolf I, Mendel J, Sikutová S, Svec P, Masaríková J, et al. (2009) 16S rRNA gene-based identification of cultured bacterial flora from host-seeking Ixodes ricinus, Dermacentor reticulatus and Haemaphysalis concinna ticks, vectors of vertebrate pathogens. Folia Microbiol (Praha) 54: 419-428.
53. Kloos WE, Schleifer KH, (1983) Staphylococcus auricularis sp. nov.: an Inhabitant of the human external ear. International journal of systematic bacteriology 33 (1): 9-14 doi:10.1099/00207713-33-1-9.
54. Kluytmans JA, (2010) Methicillin-resistant Staphylococcus aureus in food products: cause for concern or case for complacency? Clin Microbiol Infect 16: 11-15.
55. Carapetis JR, Connors C, Yarmirr D, Krause V, Currie BJ, (1997) Success of a scabies control program in an Australian aboriginal community. Pediatr Infect Dis J 16: 494-499.
56. Jackson A, Heukelbach J, Filho AF, Junior Ede B, Feldmeier H, (2007) Clinical features and associated morbidity of scabies in a rural community in Alagoas, Brazil. Trop Med Int Health 12: 493-502.
57. Worth C, Heukelbach J, Fengler G, Walter B, Liesenfeld O, et al. (2012) Acute morbidity associated with scabies and other ectoparasitoses rapidly improves after treatment with ivermectin. Pediatr Dermatol 29: 430-436.
58. Adjei O, Brenya RC, (1997) Secondary bacterial infection in Ghanaian patients with scabies. East Afr Med J 74: 729-731.
59. Mahe A, (2001) Bacterial skin infections in a tropical environment. Curr Opin Infect Dis 14: 123-126.
60. Lawrence G, Leafasia J, Sheridan J, Hills S, Wate J, et al. (2005) Control of scabies, skin sores and haematuria in children in the Solomon Islands: another role for ivermectin. Bull World Health Organ 83: 34-42.
61. Otto M, (2009) Staphylococcus epidermidis-the 'accidental' pathogen. Nat Rev Microbiol 7: 555-567.
62. Duguid IG, Evans E, Brown MR, Gilbert P, (1992) Growth-rate-independent killing by ciprofloxacin of biofilm-derived Staphylococcus epidermidis; evidence for cell-cycle dependency. J Antimicrob Chemother 30: 791-802.
63. Foster TJ, (2005) Immune evasion by staphylococci. Nat Rev Microbiol 3: 948-958.
64. Tong SY, McDonald MI, Holt DC, Currie BJ, (2008) Global implications of the emergence of community-associated methicillin-resistant Staphylococcus aureus in Indigenous populations. Clin Infect Dis 46: 1871-1878.
65. Devriese LA, Hommez J, Pot B, Haesebrouck F, (1994) Identification and composition of the streptococcal and enterococcal flora of tonsils, intestines and faeces of pigs. J Appl Bacteriol 77: 31-36.
66. Hojberg O, Canibe N, Poulsen HD, Hedemann MS, Jensen BB, (2005) Influence of dietary zinc oxide and copper sulfate on the gastrointestinal ecosystem in newly weaned piglets. Appl Environ Microbiol 71: 2267-2277.
67. Wertheim HF, Nghia HD, Taylor W, Schultsz C, (2009) Streptococcus suis: an emerging human pathogen. Clin Infect Dis 48: 617-625.
68. Gottschalk M, Xu J, Calzas C, Segura M, (2010) Streptococcus suis: a new emerging or an old neglected zoonotic pathogen? Future Microbiol 5: 371-391.
69. Figueiro AR, Nunes ZG, Silvia AAL, Giordano-Dias CMG, Conra JR, et al. (1995) Isolation of microorganisms of triatomines maintained in artificial and sylvatic conditions. Memorias do Instituto Oswaldo Cruz (Rio de Janeiro) 90.
70. Durvasula RV, Sundaram RK, Kirsch P, Hurwitz I, Crawford CV, et al. (2008) Genetic transformation of a Corynebacterial symbiont from the Chagas disease vector Triatoma infestans. Exp Parasitol 119: 94-98.