1887

Crowdsourced Data Indicate Widespread Multidrug Resistance in Skin Flora of Healthy Young Adults

    Authors: Scott Freeman1,*, Nnadozie O. Okoroafor1, Christopher M. Gast2, Mikhail Koval1, David Nowowiejski3, Eileen O’Connor1, Robert D. Harrington4, John W. Parks1, Ferric C. Fang3
    VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Department of Biology University of Washington, Seattle, WA 98195; 2: Interdisciplinary Program in Quantitative Ecology and Resource Management; currently Fred Hutchinson Cancer Research Center, University of Washington, Seattle, WA 98195; 3: Department of Laboratory Medicine and Harborview Medical Center, University of Washington, Seattle, WA 98195; 4: Department of Allergy and Infectious Diseases, University of Washington, Seattle, WA 98195
    AUTHOR AND ARTICLE INFORMATION AUTHOR AND ARTICLE INFORMATION
    • Published 01 March 2016
    • ©2016 Author(s). Published by the American Society for Microbiology.
    • [open-access] This is an Open Access article distributed under the terms of the Creative Commons Attribution-Noncommercial-NoDerivatives 4.0 International license (https://creativecommons.org/licenses/by-nc-nd/4.0/legalcode), which grants the public the nonexclusive right to copy, distribute, or display the published work.

    • Supplemental materials available at http://jmbe.asm.org
    • *Corresponding author. Mailing address: Department of Biology, Box 355320, University of Washington, Seattle, WA 98195. Phone: 206-300-4448. E-mail: srf991@uw.edu.
    Source: J. Microbiol. Biol. Educ. March 2016 vol. 17 no. 1 172-182. doi:10.1128/jmbe.v17i1.1008
MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.
  • XML
  • HTML
    80.78 Kb
  • PDF
    340.76 Kb

    Abstract:

    In a laboratory exercise for undergraduate biology majors, students plated bacteria from swabs of their facial skin under conditions that selected for coagulase-negative ; added disks containing the antibiotics penicillin, oxacillin, tetracycline, and erythromycin; and measured zones of inhibition. Students also recorded demographic and lifestyle variables and merged this information with similar data collected from 9,000 other students who had contributed to the database from 2003 to 2011. Minimum inhibitory concentration (MIC) testing performed at the Harborview Medical Center Microbiology Laboratory (Seattle, WA) indicated a high degree of accuracy for student-generated data; species identification with a matrix-assisted laser desorption ionization (MALDI) Biotyper revealed that over 88% of the cells analyzed by students were or The overall frequency of resistant cells was high, ranging from 13.2% of sampled bacteria resistant to oxacillin to 61.7% resistant to penicillin. Stepwise logistic regressions suggested that recent antibiotic use was strongly associated with resistance to three of the four antibiotics tested ( = 0.0003 for penicillin, << 0.0001 for erythromycin and tetracycline), and that age, gender, use of acne medication, use of antibacterial soaps, or makeup use were associated with resistance to at least one of the four antibiotics. Furthermore, drug resistance to one antibiotic was closely linked to resistance to the other three antibiotics in every case (all values << 0.0001), suggesting the involvement of multidrug–resistant strains. The data reported here suggest that citizen science could not only provide an important educational experience for undergraduates, but potentially play a role in efforts to expand antibiotic resistance (ABR) surveillance.

Key Concept Ranking

Antibacterial Agents
0.8687704
Antibiotics
0.51101357
Staphylococcus aureus
0.49737838
0.8687704

References & Citations

1. Alanis AJ2005Resistance to antibiotics: are we in the post-antibiotic era?Arch Med Res3669770510.1016/j.arcmed.2005.06.00916216651 http://dx.doi.org/10.1016/j.arcmed.2005.06.009
2. Alekshun MN, Levy SB2007Molecular mechanisms of antibacterial multidrug resistanceCell1281037105010.1016/j.cell.2007.03.00417382878 http://dx.doi.org/10.1016/j.cell.2007.03.004
3. American Association for the Advancement of Science2010Vision and change: a call to actionAAASWashington, DC[Online.] http://visionandchange.org/files/2011/03/Revised-Vision-and-Change-Final-Report.pdfAccessed 24 April 2012
4. Argudín MA, Mendoza MC, Martín MC, Rodicio MR2014Molecular basis of antimicrobial drug resistance in Staphylococcus aureus isolates recovered from healthy young carriers in SpainMicro Path7481410.1016/j.micpath.2014.06.005 http://dx.doi.org/10.1016/j.micpath.2014.06.005
5. Association of American Medical Colleges–Howard Hughes Medical Institute (AAMC-HHMI) Committee2009Scientific foundations for future physiciansAssociation of American Medical CollegesWashington, DC[Online.] www.aamc.org/download/271072/data/scientificfoundationsforfuturephysicians.pdfAccessed 24 April 2012
6. Barral AM, Makhluf H, Soneral P, Gasper B2014Small World Initiative: crowdsourcing research of new antibiotics to enhance undergraduate biology teachingFASEB J281(Suppl. 618.41).
7. Bascom-Slack C2015PARE undergraduate-high school citizen science partnership[Online.] http://campuspress.yale.edu/bascomslack/projectsAccessed 15 July 2015
8. Bonney R, et al2014Next steps for citizen scienceScience3431436143710.1126/science.125155424675940 http://dx.doi.org/10.1126/science.1251554
9. Brownell SE, Kloser MJ, Fukami T, Shavelson R2012Undergraduate biology lab courses: comparing the impact of traditionally based “cookbook” and authentic research-based courses on student lab experiencesJ Coll Sci Teach4143645
10. Casotti G, Rieser-Danner L, Knabb MT2008Successful implementation of inquiry-based physiology laboratories in undergraduate major and nonmajor coursesAdv Physiol Educ3228629610.1152/advan.00100.200719047505 http://dx.doi.org/10.1152/advan.00100.2007
11. Chiller K, Selkin BA, Murakawa GJ2001Skin microflora and bacterial infections of the skinJ Inv Dermatol Symp Proc617017410.1046/j.0022-202x.2001.00043.x http://dx.doi.org/10.1046/j.0022-202x.2001.00043.x
12. Cove JH, Eady EA, Cunliffe WJ1990Skin carriage of antibiotic-resistant coagulase-negative staphylococci in untreated subjectsJ Antimicrob Chemother2545946910.1093/jac/25.3.4592338422 http://dx.doi.org/10.1093/jac/25.3.459
13. Cresawn SG, et al2015Comparative genomics of cluster O mycobacteriophagesPLoS One103e011872510.1371/journal.pone.0118725257420164351075 http://dx.doi.org/10.1371/journal.pone.0118725
14. den Heijer CDJ, et al2013Prevalence and resistance of commensal Staphylococcus aureus, including meticillin-resistant S. aureus, in nine European countries: a cross-sectional studyLancet Infect Dis1340941510.1016/S1473-3099(13)70036-723473661 http://dx.doi.org/10.1016/S1473-3099(13)70036-7
15. Diekema DJ, et althe SENTRY Participants Group2001Survey of infections due to Staphylococcus species: frequency of occurrence and antimicrobial susceptibility of isolates collected in the United States, Canada, Latin America, Europe, and the Western Pacific Region for the SENTRY Antimicrobial Surveillance Program, 1997–1999Clin Infect Dis32Suppl. 2S114S13210.1086/320184 http://dx.doi.org/10.1086/320184
16. Ellis MW, Hospenthal DR, Dooley DP, Gray PJ, Murray CK2004Natural history of community-acquired methicillin-resistant Staphylococcus aureus colonization and infection in soldiersClin Infect Dis3997197910.1086/42396515472848 http://dx.doi.org/10.1086/423965
17. European Committee on Antimicrobial Susceptibility Testing2015Data from the EUCAST MIC distribution websitewww.eucast.org/mic_distributions_and_ecoffsAccessed 26 July 2015
18. Farrell DJ, Mendes RE, Ross JE, Jones RN2009Linezolid surveillance program results for 2008 (LEADER Program for 2008)Diagn Microbiol Infect Dis6539240310.1016/j.diagmicrobio.2009.10.01119913682 http://dx.doi.org/10.1016/j.diagmicrobio.2009.10.011
19. Fox R1996The post-antibiotic era beckonsJ Roy Soc Med8960260391355851295992
20. Fredheim EGA, et al2009Biofilm formation by Staphylococcus haemolyticusJ Clin Microbiol471172118010.1128/JCM.01891-08191447982668337 http://dx.doi.org/10.1128/JCM.01891-08
21. Garza-González E, Morfin-Otero R, Martínez-Vázquez MA, Gonzalez-Diaz E, González-Santiago O, Rodríguez-Noriega E2011Microbiological and molecular characterization of human clinical isolates of Staphylococcus cohnii, Staphylococcus hominis, and Staphylococcus sciuriScan J Infect Dis4393093610.3109/00365548.2011.598873 http://dx.doi.org/10.3109/00365548.2011.598873
22. Genereux DP, Bergstrom CT2005Evolution in action: understanding antibiotic resistance145153 Cracraft J, Bybee RWEvolutionary science and society: educating a new generationAIBSWashington, DC
23. Goossens H, Ferech M, Vander Stichele R, Elseviers M2005Outpatient antibiotic use in Europe and association with resistance: a cross-national database studyLancet36557958710.1016/S0140-6736(05)70799-615708101 http://dx.doi.org/10.1016/S0140-6736(05)70799-6
24. Hatfull GF2010Bacteriophage research: gateway to learning scienceMicrobe56243250
25. Hoa NQ, et al2010Decreased Streptococcus pneumoniae susceptibility to oral antibiotics among children in rural Vietnam: a community studyBMC Infect Dis10859610.1186/1471-2334-10-85203563992853544 http://dx.doi.org/10.1186/1471-2334-10-85
26. Jourdain S, et al2010Differences in nasopharyngeal bacterial carriage in preschool children from different socioeconomic originsClin Microbiol Infect1790791410.1111/j.1469-0691.2010.03410.x http://dx.doi.org/10.1111/j.1469-0691.2010.03410.x
27. Kanter DE, Smith HD, McKenna A, Rieger C, Linsenmeier RA2003Inquiry-based laboratory instruction throws out the “cookbook” and improves learningProc. 2003 Am Soc. Eng. Educ. Ann. Conf. Expos. Session 2230
28. Kennett R, Danielsen F, Silvius KM2015Conservation management: citizen science is not enough on its ownNature52116110.1038/521161d25971501 http://dx.doi.org/10.1038/521161d
29. Leung W, et al2015Drosophila Muller F elements maintain a distinct set of genomic properties over 40 million years of evolutionG3 (Bethesda)5571974010.1534/g3.114.0159664426361 http://dx.doi.org/10.1534/g3.114.015966
30. Levy SB, Marshall B2004Antibacterial resistance worldwide: causes, challenges, and responsesNat Med10S122S12910.1038/nm114515577930 http://dx.doi.org/10.1038/nm1145
31. Naci H, Ioannidis JPA2015Evaluation of wellness determinants and interventions by citizen scientistsJAMA314212112210.1001/jama.2015.616026068643 http://dx.doi.org/10.1001/jama.2015.6160
32. National Research Council1999Transforming undergraduate education in science, mathematics, engineering, and technologyThe National Academies PressWashington, DC
33. National Research Council2003Bio 2010: Transforming undergraduate education for future research biologistsThe National Academies PressWashington, DC
34. Pol M, Ruegg PL2007Relationship between antimicrobial drug usage and antimicrobial susceptibility of gram-positive mastitis pathogensJ Dairy Sci9026227310.3168/jds.S0022-0302(07)72627-9 http://dx.doi.org/10.3168/jds.S0022-0302(07)72627-9
35. President’s Council of Advisors on Science and Technology2012Engage to excel: producing one million additional college graduates with degrees in science, technology, engineering, and mathematicsPCASTWashington, DC[Online.] http://www.whitehouse.gov/sites/default/files/microsites/ostp/pcast-engage-to-excelfinal_2-25-12.pdfAccessed 24 April 2012
36. Price SB, Flournoy DJ1982Comparison of antimicrobial susceptibility patterns of coagulase-negative staphylococciAntimicrob Agents Chemother2143644010.1128/AAC.21.3.4367103446181911 http://dx.doi.org/10.1128/AAC.21.3.436
37. Queenan AM, Foleno B, Gownley C, Wira E, Bush K2004Effects of inoculum and β-lactamase activity in AmpC- and extended-spectrum β-lactamase (ESBL)-producing Escherichia coli and Klebsiella pneumonia clinical isolates tested by using NCCLS ESBL methodologyJ Clin Microbiol42126927510.1128/JCM.42.1.269-275.200414715764321709 http://dx.doi.org/10.1128/JCM.42.1.269-275.2004
38. Reardon S2014WHO warns against ‘post-antibiotic’ eraNature NewsNature Publishing Group[Online.] www.nature.com/news/who-warns-against-post-antibioticera-1.15135
39. Sauermann H, Franzoni C2015Crowd science user contribution patterns and their implicationsProc Natl Acad Sci U S A112367968410.1073/pnas.1408907112255615294311847 http://dx.doi.org/10.1073/pnas.1408907112
40. Shuttleworth S, Frampton S2015Constructing scientific communities: citizen scienceLancet385256810.1016/S0140-6736(15)61150-326122151 http://dx.doi.org/10.1016/S0140-6736(15)61150-3
41. Silvertown J2009A new dawn for citizen scienceTrends Ecol Evol24946747110.1016/j.tree.2009.03.01719586682 http://dx.doi.org/10.1016/j.tree.2009.03.017
42. Soltani B, et al2014Risk factors for methicillin resistant Staphylococcus aureus nasal colonization of healthy childrenJundishapur J Microbiol79e2002510.5812/jjm.20025254850714255386 http://dx.doi.org/10.5812/jjm.20025
43. Sommer MOA, Dantas G, Church GM2009Functional characterization of the antibiotic resistance reservoir in the human microfloraScience3251128113110.1126/science.1176950197135264720503 http://dx.doi.org/10.1126/science.1176950
44. Thomson KS, Moland ES2001Cefepime, piperacillin-tazobactam, and the inoculum effect in tests with extended-spectrum β-lactamase-producing enterobacteriaceaeAntimicrob Agents Chemo45123548355410.1128/AAC.45.12.3548-3554.2001 http://dx.doi.org/10.1128/AAC.45.12.3548-3554.2001
45. Varaldo PE, et al1984Identification, clinical distribution, and susceptibility to methicillin and 18 additional antibiotics of clinical Staphylococcus isolates: nationwide investigation in ItalyJ Clin Microbiol1968388436565709271195
46. Vianna GMS, Meekan MG, Bornovski TH, Meeuwig JJ2014Acoustic telemetry validates a citizen science approach for monitoring sharks on coral reefsPLoS One94e9556510.1371/journal.pone.0095565247600813997401 http://dx.doi.org/10.1371/journal.pone.0095565
47. Vignaroli C, Zandri G, Aquilanti L, Pasquaroli S, Biavasco F2011Multidrug-resistant enterococci in animal meat and faeces and co-transfer of resistance from an Enterococcus durans to a human Enterococcus faeciumCurr Microbiol621438144710.1007/s00284-011-9880-x21286720 http://dx.doi.org/10.1007/s00284-011-9880-x
48. Widerström M, Wiström J, Ek E, Edebro H, Monsen T2011Near absence of methicillin-resistance and pronounced genetic diversity among Staphylococcus epidermidis isolated from healthy persons in northern SwedenAPMIS11950551210.1111/j.1600-0463.2011.02757.x21749450 http://dx.doi.org/10.1111/j.1600-0463.2011.02757.x
49. World Health Organization2010The top 10 causes of death[Online.] www.who.int/mediacentre/factsheets/fs310/en/index.htmlAccessed 24 April 2012
50. World Health Organization2014Antimicrobial resistance: global report on surveillanceWorld Health OrganizationGeneva
51. Yazdankhah SP, et al2006Triclosan and antimicrobial resistance in bacteria: an overviewMicrob Drug Resist12839010.1089/mdr.2006.12.8316922622 http://dx.doi.org/10.1089/mdr.2006.12.83
jmbe.v17i1.1008.citations
jmbe/17/1
content/journal/jmbe/10.1128/jmbe.v17i1.1008
Loading

Citations loading...

Supplemental Material

Loading

Article metrics loading...

/content/journal/jmbe/10.1128/jmbe.v17i1.1008
2016-03-01
2017-09-26

Abstract:

In a laboratory exercise for undergraduate biology majors, students plated bacteria from swabs of their facial skin under conditions that selected for coagulase-negative ; added disks containing the antibiotics penicillin, oxacillin, tetracycline, and erythromycin; and measured zones of inhibition. Students also recorded demographic and lifestyle variables and merged this information with similar data collected from 9,000 other students who had contributed to the database from 2003 to 2011. Minimum inhibitory concentration (MIC) testing performed at the Harborview Medical Center Microbiology Laboratory (Seattle, WA) indicated a high degree of accuracy for student-generated data; species identification with a matrix-assisted laser desorption ionization (MALDI) Biotyper revealed that over 88% of the cells analyzed by students were or The overall frequency of resistant cells was high, ranging from 13.2% of sampled bacteria resistant to oxacillin to 61.7% resistant to penicillin. Stepwise logistic regressions suggested that recent antibiotic use was strongly associated with resistance to three of the four antibiotics tested ( = 0.0003 for penicillin, << 0.0001 for erythromycin and tetracycline), and that age, gender, use of acne medication, use of antibacterial soaps, or makeup use were associated with resistance to at least one of the four antibiotics. Furthermore, drug resistance to one antibiotic was closely linked to resistance to the other three antibiotics in every case (all values << 0.0001), suggesting the involvement of multidrug–resistant strains. The data reported here suggest that citizen science could not only provide an important educational experience for undergraduates, but potentially play a role in efforts to expand antibiotic resistance (ABR) surveillance.

Highlighted Text: Show | Hide
Loading full text...

Full text loading...

/deliver/fulltext/jmbe/17/1/jmbe-17-172.xml.a.html?itemId=/content/journal/jmbe/10.1128/jmbe.v17i1.1008&mimeType=html&fmt=ahah

Figures

Image of FIGURE 1

Click to view

FIGURE 1

Changes in the frequency of resistant bacteria over time.

Source: J. Microbiol. Biol. Educ. March 2016 vol. 17 no. 1 172-182. doi:10.1128/jmbe.v17i1.1008
Download as Powerpoint

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error