Genomic epidemiology of the Escherichia coli O104:H4 outbreaks in Europe, 2011

Yonatan H. Grad; Marc Lipsitch; Michael Feldgarden; Harindra M. Arachchi; Gustavo C. Cerqueira; Michael FitzGerald; Paul Godfrey; Brian J. Haas; Cheryl I. Murphy; Carsten Russ; Sean Sykes; Bruce J. Walker; Jennifer R. Wortman; Sarah Young; Qiandong Zeng; Amr Abouelleil; James Bochicchio; Sara Chauvin; Timothy DeSmet; Sharvari Gujja; Caryn McCowan; Anna Montmayeur; Scott Steelman; Jakob Frimodt-Møller; Andreas M. Petersen; Carsten Struve; Karen A. Krogfelt; Edouard Bingen; François Xavier Weill; Eric S. Lander; Chad Nusbaum; Bruce W. Birren; Deborah T. Hung; William P. Hanage

doi:10.1073/pnas.1121491109

Genomic epidemiology of the Escherichia coli O104:H4 outbreaks in Europe, 2011

Yonatan H. Grad, Marc Lipsitch, Michael Feldgarden, Harindra M. Arachchi, Gustavo C. Cerqueira, Michael FitzGerald, Paul Godfrey, Brian J. Haas, Cheryl I. Murphy, Carsten Russ, Sean Sykes, Bruce J. Walker, Jennifer R. Wortman, Sarah Young, Qiandong Zeng, Amr Abouelleil, James Bochicchio, Sara Chauvin, Timothy DeSmet, Sharvari GujjaCaryn McCowan, Anna Montmayeur, Scott Steelman, Jakob Frimodt-Møller, Andreas M. Petersen, Carsten Struve, Karen A. Krogfelt, Edouard Bingen, François Xavier Weill, Eric S. Lander^*, Chad Nusbaum, Bruce W. Birren, Deborah T. Hung, William P. Hanage

^*Corresponding author for this work

Functional Genomics

190 Citations (Scopus)

Abstract

The degree to which molecular epidemiology reveals information about the sources and transmission patterns of an outbreak depends on the resolution of the technology used and the samples studied. Isolates of Escherichia coli O104:H4 from the outbreak centered in Germany in May-July 2011, and the much smaller outbreak in southwest France in June 2011, were indistinguishable by standard tests. We report a molecular epidemiological analysis using multiplatform whole-genome sequencing and analysis of multiple isolates from the German and French outbreaks. Isolates from the German outbreak showed remarkably little diversity, with only two single nucleotide polymorphisms (SNPs) found in isolates from four individuals. Surprisingly, we found much greater diversity (19 SNPs) in isolates from seven individuals infected in the French outbreak. The German isolates form a clade within the more diverse French outbreak strains. Moreover, five isolates derived from a single infected individual from the French outbreak had extremely limited diversity. The striking difference in diversity between the German and French outbreak samples is consistent with several hypotheses, including a bottleneck that purged diversity in the German isolates, variation in mutation rates in the two E. coli outbreak populations, or uneven distribution of diversity in the seed populations that led to each outbreak.

Original language	English
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	109
Issue number	8
Pages (from-to)	3065-3070
Number of pages	6
ISSN	0027-8424
DOIs	https://doi.org/10.1073/pnas.1121491109
Publication status	Published - 21 Feb 2012

Keywords

Enteroaggregative E. Coli
Enterohemorrhagic E. Coli
Food-borne outbreak
Shiga toxin

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Grad, Y. H., Lipsitch, M., Feldgarden, M., Arachchi, H. M., Cerqueira, G. C., FitzGerald, M., Godfrey, P., Haas, B. J., Murphy, C. I., Russ, C., Sykes, S., Walker, B. J., Wortman, J. R., Young, S., Zeng, Q., Abouelleil, A., Bochicchio, J., Chauvin, S., DeSmet, T., ... Hanage, W. P. (2012). Genomic epidemiology of the Escherichia coli O104:H4 outbreaks in Europe, 2011. Proceedings of the National Academy of Sciences of the United States of America, 109(8), 3065-3070. https://doi.org/10.1073/pnas.1121491109

Grad, YH, Lipsitch, M, Feldgarden, M, Arachchi, HM, Cerqueira, GC, FitzGerald, M, Godfrey, P, Haas, BJ, Murphy, CI, Russ, C, Sykes, S, Walker, BJ, Wortman, JR, Young, S, Zeng, Q, Abouelleil, A, Bochicchio, J, Chauvin, S, DeSmet, T, Gujja, S, McCowan, C, Montmayeur, A, Steelman, S, Frimodt-Møller, J , Petersen, AM, Struve, C, Krogfelt, KA, Bingen, E, Weill, FX, Lander, ES, Nusbaum, C, Birren, BW, Hung, DT & Hanage, WP 2012, 'Genomic epidemiology of the Escherichia coli O104:H4 outbreaks in Europe, 2011', Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 8, pp. 3065-3070. https://doi.org/10.1073/pnas.1121491109

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abstract = "The degree to which molecular epidemiology reveals information about the sources and transmission patterns of an outbreak depends on the resolution of the technology used and the samples studied. Isolates of Escherichia coli O104:H4 from the outbreak centered in Germany in May-July 2011, and the much smaller outbreak in southwest France in June 2011, were indistinguishable by standard tests. We report a molecular epidemiological analysis using multiplatform whole-genome sequencing and analysis of multiple isolates from the German and French outbreaks. Isolates from the German outbreak showed remarkably little diversity, with only two single nucleotide polymorphisms (SNPs) found in isolates from four individuals. Surprisingly, we found much greater diversity (19 SNPs) in isolates from seven individuals infected in the French outbreak. The German isolates form a clade within the more diverse French outbreak strains. Moreover, five isolates derived from a single infected individual from the French outbreak had extremely limited diversity. The striking difference in diversity between the German and French outbreak samples is consistent with several hypotheses, including a bottleneck that purged diversity in the German isolates, variation in mutation rates in the two E. coli outbreak populations, or uneven distribution of diversity in the seed populations that led to each outbreak.",

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AU - Cerqueira, Gustavo C.

AU - FitzGerald, Michael

AU - Godfrey, Paul

AU - Haas, Brian J.

AU - Murphy, Cheryl I.

AU - Russ, Carsten

AU - Sykes, Sean

AU - Walker, Bruce J.

AU - Wortman, Jennifer R.

AU - Young, Sarah

AU - Zeng, Qiandong

AU - Abouelleil, Amr

AU - Bochicchio, James

AU - Chauvin, Sara

AU - DeSmet, Timothy

AU - Gujja, Sharvari

AU - McCowan, Caryn

AU - Montmayeur, Anna

AU - Steelman, Scott

AU - Frimodt-Møller, Jakob

AU - Petersen, Andreas M.

AU - Struve, Carsten

AU - Krogfelt, Karen A.

AU - Bingen, Edouard

AU - Weill, François Xavier

AU - Lander, Eric S.

AU - Nusbaum, Chad

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AU - Hung, Deborah T.

AU - Hanage, William P.

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N2 - The degree to which molecular epidemiology reveals information about the sources and transmission patterns of an outbreak depends on the resolution of the technology used and the samples studied. Isolates of Escherichia coli O104:H4 from the outbreak centered in Germany in May-July 2011, and the much smaller outbreak in southwest France in June 2011, were indistinguishable by standard tests. We report a molecular epidemiological analysis using multiplatform whole-genome sequencing and analysis of multiple isolates from the German and French outbreaks. Isolates from the German outbreak showed remarkably little diversity, with only two single nucleotide polymorphisms (SNPs) found in isolates from four individuals. Surprisingly, we found much greater diversity (19 SNPs) in isolates from seven individuals infected in the French outbreak. The German isolates form a clade within the more diverse French outbreak strains. Moreover, five isolates derived from a single infected individual from the French outbreak had extremely limited diversity. The striking difference in diversity between the German and French outbreak samples is consistent with several hypotheses, including a bottleneck that purged diversity in the German isolates, variation in mutation rates in the two E. coli outbreak populations, or uneven distribution of diversity in the seed populations that led to each outbreak.

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KW - Food-borne outbreak

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JF - Proceedings of the National Academy of Sciences of the United States of America

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Genomic epidemiology of the Escherichia coli O104:H4 outbreaks in Europe, 2011

Abstract

Keywords

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