Literature DB >> 21749783

Worldwide distribution of major clones of Listeria monocytogenes.

Viviane Chenal-Francisque1, Jodie Lopez, Thomas Cantinelli, Valerie Caro, Coralie Tran, Alexandre Leclercq, Marc Lecuit, Sylvain Brisse.   

Abstract

Listeria monocytogenes is worldwide a pathogen, but the geographic distribution of clones remains largely unknown. Genotyping of 300 isolates from the 5 continents and diverse sources showed the existence of few prevalent and globally distributed clones, some of which include previously described epidemic clones. Cosmopolitan distribution indicates the need for genotyping standardization.

Entities:  

Mesh：

Year:  2011        PMID： 21749783      PMCID： PMC3358213          DOI： 10.3201/eid/1706.101778

Source DB:  PubMed          Journal:  Emerg Infect Dis        ISSN： 1080-6040            Impact factor:   6.883


Listeria monocytogenes is a foodborne pathogen that can cause listeriosis, a severe invasive infection in humans with a particularly high case-fatality rate. Listeriosis is a major public health concern in all world regions, with an increasing incidence in Europe, especially among elderly persons (,). L. monocytogenes is genetically heterogeneous (–). To help epidemiologic investigation and to define clones, i.e., groups of genetically similar isolates descending from a common ancestor, a variety of typing methods have been used, including pulsed-field gel electrophoresis (,), single nucleotide polymorphism typing (), and multiple housekeeping and virulence gene sequencing (,). Some clones implicated in multiple outbreaks have been defined as epidemic clones (EC) (,,–). ECI and ECIV have been described in several countries (,), but because of the lack of standardization of genotyping, a definition of clones is not widely accepted, and current knowledge on the global distribution of L. monocytogenes clones is virtually absent. Multilocus sequence typing (MLST) is a reference method for global epidemiology and population biology of bacteria, and its application to L. monocytogenes () effectively allows isolate comparisons across laboratories (www.pasteur.fr/mlst). The aim of this study was to investigate the global distribution of L. monocytogenes MLST-defined clones.

The Study

Three hundred L. monocytogenes isolates were collected from different sources from 42 countries on 5 continents (Table A1). The isolates derived from 1) the collection of the World Health Organization Collaborating Center for Listeria and 2) the Seeliger Listeria Culture Collection. When available, up to 10 countries per continent were included. Only 1 isolate per documented outbreak was kept, and the isolates from a given country were selected from various sources, years, and serotypes. A total of 117 isolates were from humans, 107 from food, 28 from animals, 32 from the environment and vegetation, and 16 of undocumented origin. The relative proportion of isolates from distinct sources was similar among world regions (Table A1), except that no animal isolate was available from the Western Hemisphere and that the ratio of human to food isolates was lower from this continent.
Table A1

Sources and characteristics of Listeria monocytogenes isolates analyzed

KeyWorld regionCountryYearSourceLineageCC*ST†Serotype‡
LM13415AfricaAlgeria1985Human1CC114b
LM13417AfricaAlgeria1987Human1CC224b
LM10976AfricaAlgeria1988Animal1CC224b
LM76305AfricaAlgeria1998Human1CC224b
LM05-00105AfricaAlgeriaUnknownHuman1CC22724b
LM8818AfricaAlgeria1988Animal2CC21211/2a
LM13419AfricaAlgeria1987Human1CC32731/2b
LM68629AfricaAlgeria1991Human2CC881/2a
LM68625
Africa
Algeria
1992
Human
2
CC8
8
1/2a
LM86423
Africa
Madagascar
Unknown
Food
2
CC121
121
1/2a
LM77185AfricaMoroccoUnknownFood1CC114b
LM86525AfricaMoroccoUnknownFood2CC1011011/2a
LM07-00231AfricaMoroccoUnknownFood1CC224b
LM20800AfricaMoroccoUnknownHuman1CC224b
LM75327AfricaMoroccoUnknownHuman1CC22774b
LM86505AfricaMoroccoUnknownFood1CC32871/2b
LM75325AfricaMoroccoUnknownHuman1CC331/2b
LM75328AfricaMoroccoUnknownHuman1CC331/2b
LM18327AfricaMorocco1990Human1CC3411/2b
LM77479AfricaMoroccoUnknownVegetal1CC3681/2b
LM77195AfricaMoroccoUnknownFood1CC592821/2b
LM85273AfricaMorocco2000Environment1CC592851/2b
LM86481AfricaMoroccoUnknownFood1CC592861/2b
LM07-00586
Africa
Morocco
Unknown
Food
1
CC59
59
1/2b
LM89984AfricaSenegalUnknownUnknown1CC21454b
LM09-00263AfricaSenegal2007Food1CC59591/2b
LM09-00264
Africa
Senegal
2009
Food
1
CC59
59
1/2b
LM09-00277AfricaTunisia2007Food2CC1011011/2a
LM58204AfricaTunisia1994Human1CC224b
LM09-00290AfricaTunisia2005Human1CC224b
LM09-00291AfricaTunisia2007Human1CC224b
LM20490AfricaTunisiaUnknownEnvironment1CC224b
LM71962AfricaTunisiaUnknownFood1CC22764b
LM42224
Africa
Tunisia
1993
Human
2
CC9
9
1/2c
LM21416Eastern AsiaChina1991Human1CC114b
LM12980Eastern AsiaChina1987Unknown1CC12434b
LM22261Eastern AsiaChina1992Food2CC1211211/2a
LM21413Eastern AsiaChina1991Human2CC1551551/2a
LM21436
Eastern Asia
China
Unknown
Food
1
CC2
2
4b
SLCC875
Eastern Asia
Russia
1948
Food
2
126
1/2a
LM12872EuropeAustria1986Human2CC14911/2a (s)
LM8792EuropeAustria1987Food2CC18181/2a (s)
LM83291EuropeAustria2000Human1CC1951951/2b (s)
LM8789EuropeAustria1987Food2CC1991991/2a (s)
LM8800EuropeAustria1988Food2CC1991991/2a (s)
LM8806EuropeAustria1988Food2CC1991991/2a (s)
LM8785EuropeAustria1987Food1CC224b (s)
LM8736EuropeAustria1986Food1CC331/2b (s)
LM8742EuropeAustria1986Food2CC991/2c (s)
LM8796
Europe
Austria
1988
Food
2
CC9
9
1/2c
LM11971EuropeBelgium1987Animal21771/2a
LM07-00578EuropeBelgium1990Food22221/2a
LM17434EuropeBelgium1988Food1CC1104b (s)
LM07-00581EuropeBelgium1990Food2CC1211211/2a
LM17416EuropeBelgium1988Food2CC18181/2a (s)
LM23000EuropeBelgium1990Food2CC1992301/2a (s)
LM17413EuropeBelgium1988Human1CC224b (s)
LM17559EuropeBelgium1989Human1CC224b (s)
LM17571EuropeBelgium1989Human1CC331/2b (s)
LM83769EuropeBelgium1999Human1CC444b (s)
LM11970EuropeBelgium1986Human1CC592411/2b (s)
LM17431EuropeBelgium1988Food1CC59591/2b (s)
SLCC2298
Europe
Bulgaria
1965
Animal
1
CC1
1
4b (s)
LM83919EuropeCroatia<2000Animal1CC224b (s)
LM80112EuropeCroatia<2000Animal1CC32351/2b (s)
LM78358EuropeCroatia<1999Animal2CC372341/2a (s)
LM83916
Europe
Croatia
<2000
Animal
2
CC8
120
1/2a (s)
LM07-00288EuropeCzech Republic<2007Unknown2CC14141/2a
LM69539EuropeCzech Republic1995Environment1CC1951951/2b
LM05-01034EuropeCzech Republic<2005Unknown1CC21454b
LM69522EuropeCzech Republic1995Food1CC551/2b
LM05-01033
Europe
Czech Republic
<2005
Unknown
2
CC7
12
1/2a
LM82202EuropeDenmark1999Human1CC1794b (s)
SLCC1531EuropeDenmark1962Human1CC224b
SLCC1686EuropeDenmark1963Human1CC224b (s)
LM10791EuropeDenmark1988Human1CC224b
SLCC1533EuropeDenmark1962Human1CC22574b (s)
SLCC2399EuropeDenmark1966Animal1CC2484b (s)
LM10378EuropeDenmark1988Food1CC59591/2b
LM12832EuropeDenmark1989Human2CC771/2a
SLCC69EuropeDenmark1937Human2CC7981/2a
LM14228
Europe
Denmark
1989
Food
2
CC9
9
1/2a
LM15178EuropeFinland1989Human2CC1211211/2a
LM15142EuropeFinland1986Human1CC224b (s)
LM8013EuropeFinland1987Food1CC331/2b
LM15208EuropeFinland1988Environment1CC331/2b
LM8017EuropeFinland1974Human1CC3152534b
LM8169EuropeFinland1987Animal1CC62544b
LM15256EuropeFinland1988Animal2CC72271/2a
LM8077EuropeFinland1987Food2CC771/2a
LM15183
Europe
Finland
1989
Human
2
CC9
9
1/2c
SLCC1612EuropeFrance1963Human1CC1734b
LM23187EuropeFrance1992Food1CC224b
SLCC546EuropeFrance1956Human1CC31171/2b
LM15262EuropeFrance1990Human1CC32281/2b (s)
SLCC206EuropeFrance1950Food1CC3151024b
LM12519EuropeFrance1989Human1CC42424b (s)
LM21131EuropeFrance1992Food1CC444b (s)
LM62444EuropeFrance1995Food2CC72311/2a
LM12485EuropeFrance1988Food2CC991/2c
LM06-00139
Europe
France
2006
Environment
2
CC9
9
1/2c
LM71759EuropeGermany<1996Unknown1CC114b (s)
LM65123EuropeGermany1994Human1CC114b
LM65127EuropeGermany1995Human1CC114b
SLCC39EuropeGermany1953Human2CC1011131/2a
SLCC1023EuropeGermany1960Animal2CC1011431/2a
LM82806EuropeGermany<2000Food2CC1211211/2a (s)
SLCC2EuropeGermany1953Human1CC21454b
LM74698EuropeGermany<1997Unknown1CC224b
LM82901EuropeGermany<2000Human2CC21211/2a (s)
LM18662EuropeGermany1990Human1CC331/2b
LM82900EuropeGermany<2000Animal1CC551/2b (s)
LM71758EuropeGermany1996Unknown2CC7121/2a (s)
SLCC1EuropeGermany1951Human2CC7231/2a
SLCC2864EuropeGermany1968Food2CC771/2a (s)
LM78008
Europe
Germany
<1999
Unknown
2
CC9
9
1/2c (s)
LM70960EuropeGreece<1996Animal11911/2b (s)
LM93187EuropeGreece<2003Human1CC114b (s)
LM70927EuropeGreece<1996Animal1CC12524b (s)
LM93191EuropeGreece<2003Human2CC1552371/2a (s)
LM70940EuropeGreece<1996Animal1CC224b (s)
LM70290EuropeGreece<1996Human1CC42514b (s)
LM67774EuropeGreece<1995Environment1CC664b
LM67783EuropeGreece<1995Food1CC664b
LM67781EuropeGreece<1995Food2CC91151/2c
LM70956
Europe
Greece
<1996
Animal
2
CC9
9
1/2c (s)
LM9414EuropeItaly1988Animal11911/2b
LM15852EuropeItaly1990Human1CC114b
LM7616EuropeItaly1987Human1CC12524b
LM13394EuropeItaly1989Food2CC1211211/2a
LM41103EuropeItaly1993Food2CC18181/2a
LM61388EuropeItaly1994Food1CC22464b
LM86834EuropeItaly<2001Food1CC331/2b (s)
LM68619EuropeItaly1995Human2CC81201/2a
LM07-01172EuropeItaly2003Animal2CC991/2c
LM06-00810
Europe
Italy
2005
Environment
2
CC9
9
1/2c
SLCC1457EuropeThe Netherlands1962Animal1CC114b (s)
LM07-01127EuropeThe Netherlands<2007Food1CC664b
LM07-01124
Europe
The Netherlands
<2007
Human
2
CC9
223
1/2c
SLCC2280
Europe
Poland
1965
Human
2
CC21
238
1/2a
LM08-00013EuropePortugal2000Human12241/2b
LM08-00002EuropePortugal2003Human1544b
LM70125EuropePortugal<1996Environment1CC114b (s)
LM84790EuropePortugal<2000Environment1CC12554b (s)
LM08-01095EuropePortugal<2005Human2CC1211211/2a
LM70124EuropePortugal<1996Environment2CC1211211/2a (s)
LM08-00024EuropePortugal2004Human2CC16161/2a
LM76641EuropePortugal1998Food1CC224b (s)
LM71637EuropePortugal<1996Food1CC2882331/2b (s)
LM70140EuropePortugal<1996Food1CC32281/2b (s)
LM70139EuropePortugal<1996Food1CC331/2b (s)
LM08-00016EuropePortugal1998Human1CC59591/2b
LM71634EuropePortugal<1996Food2CC991/2c (s)
LM05-01099
Europe
Portugal
<2005
Human
2
CC9
9
1/2c
LM87422EuropeSpain2000Human1CC12564b (s)
LM13478EuropeSpain<1989Animal1CC224b
LM13479EuropeSpain<1989Human1CC224b
LM13608EuropeSpain1989Food1CC224b
LM59597EuropeSpain1991Human1CC224b
LM38931EuropeSpain1992Human1CC224b
LM65719EuropeSpain1995Human1CC224b
LM9134
Europe
Spain
1988
Food
2
CC9
9
1/2c
LM68804EuropeSweden1973Human1CC114b
LM68807EuropeSweden1974Human1CC114b
LM68853EuropeSweden1995Environment1CC114b
LM68828EuropeSweden1987Human1CC12484b
LM68833EuropeSweden1988Human1CC224b
LM68834EuropeSweden1994Human1CC224b
LM68802EuropeSweden1975Human1CC22474b
LM68856EuropeSweden1991Human1CC331/2b
LM68846EuropeSweden1994Environment1CC3152494b
LM68865
Europe
Sweden
Unknown
Food
1
CC315
250
4b
SLCC792EuropeSwitzerland1958Human12404b (s)
SLCC2570EuropeSwitzerland1967Animal3201L
LM51770EuropeSwitzerland1994Food1CC114b (s)
SLCC1849EuropeSwitzerland1964Animal1CC12584b
SLCC243EuropeSwitzerland1954Animal2CC1552391/2a
LM60557EuropeSwitzerland1994Animal2CC18181/2a (s)
LM74493EuropeSwitzerland1997Environment1CC224b (s)
LM51415EuropeSwitzerland1993Human1CC22454b (s)
SLCC796EuropeSwitzerland1959Animal1CC22594b (s)
LM16587
Europe
Switzerland
1990
Animal
1
CC59
59
1/2b (s)
LM14569EuropeTurkey1989Food22261/2a (s)
LM14571EuropeTurkey1988Food22261/2a (s)
LM14574EuropeTurkey1988Food22261/2a (s)
LM13903EuropeTurkey1989Food1CC32251/2b (s)
LM13904
Europe
Turkey
<1989
Food
1
CC3
3
1/2b (s)
SLCC125EuropeUnited Kingdom1954Human1544b
LM10453EuropeUnited Kingdom<1988Food1CC114b
LM42629EuropeUnited Kingdom1993Unknown1CC1734b
SLCC1419EuropeUnited Kingdom1962Human1CC224b (s)
SLCC1616EuropeUnited Kingdom1963Human1CC224b (s)
SLCC2524EuropeUnited Kingdom1966Human1CC224b (s)
LM8720EuropeUnited Kingdom1988Human1CC224b (s)
LM24902EuropeUnited Kingdom1992Food2CC771/2a
SLCC21
Europe
United Kingdom
1935
Human
2
CC9
122
1/2c
LM19700Middle EastIraqUnknownFood1CC21454b
LM19695
Middle East
Iraq
Unknown
Food
1
CC3
66
1/2b
LM71350
Middle East
Iran
Unknown
Food
2
CC7
12
1/2a (s)
LM89979Middle EastIsraelUnknownHuman1CC224b (s)
LM89980Middle EastIsraelUnknownFood1CC3681/2b (s)
LM56346
Middle East
Israel
1993
Animal
2
CC7
7
1/2a
LM77966Middle EastQatarUnknownHuman1CC114b (s)
LM80419Middle EastQatarUnknownFood2CC1212361/2a (s)
LM80415
Middle East
Qatar
Unknown
Food
1
CC2
2
4b (s)
SLCC665North AmericaCanada1958Human1CC114b
SLCC183North AmericaCanada1954Human2CC1011011/2a
SLCC907North AmericaCanada1953Food2CC141601/2a
SLCC537North AmericaCanadaUnknownHuman1CC22574b
SLCC357North AmericaCanada1950Human1CC22904b
SLCC236North AmericaCanada1954Human2CC21221/2a
SLCC100
North America
Canada
1951
Human
2
CC7
98
1/2a
LM88502North AmericaMexico1999Vegetal1324b
LM88513North AmericaMexico1999Environment1CC224b
LM88519North AmericaMexico2000Vegetal1CC224b
LM88520North AmericaMexico2000Environment1CC2484b
LM88454North AmericaMexico1999Environment1CC2882881/2b
LM88455North AmericaMexico1999Vegetal1CC2882881/2b
LM88458North AmericaMexico1999Environment1CC2882881/2b
LM88461North AmericaMexico1999Environment1CC2882881/2b
LM88469North AmericaMexico1999Vegetal1CC2882881/2b
LM88491North AmericaMexico2000Vegetal1CC2882881/2b
LM88493North AmericaMexico2000Environment1CC2882881/2b
LM88500North AmericaMexico2000Environment1CC2882881/2b
LM88501
North America
Mexico
1999
Environment
1
CC6
6
4b
SLCC422North AmericaUnited States1956Food3294L
SLCC63North AmericaUnited States1933Human1CC11194b
SLCC65North AmericaUnited States1933Human1CC11194b
SLCC83North AmericaUnited States1937Food1CC11194b
SLCC299North AmericaUnited States1955Human1CC224b
SLCC527North AmericaUnited States1957Human1CC22914b
SLCC459
North America
United States
Unknown
Unknown
1
CC59
292
1/2b
LM13007OceaniaAustralia<1989Unknown1CC224b
LM21475
Oceania
Australia
<1992
Environment
2
CC204
204
1/2a
LM19717OceaniaNew Zealand1991Food22291/2a
LM11309OceaniaNew Zealand1987Human1CC114b
LM18429OceaniaNew Zealand1991Food1CC114b
LM70327OceaniaNew Zealand1995Human1CC12484b (s)
LM18427OceaniaNew Zealand1991Human2CC1551551/2a
LM70320OceaniaNew Zealand1995Human1CC224b (s)
LM18354OceaniaNew Zealand1989Human1CC22444b
LM13044OceaniaNew Zealand1981Human1CC331/2b (s)
LM18357OceaniaNew Zealand1990Human1CC331/2b
LM40964OceaniaNew Zealand1993Human1CC59591/2b
LM62719OceaniaNew Zealand1994Human2CC82321/2a
LM11308
Oceania
New Zealand
1988
Human
2
CC9
9
1/2c
LM66720South and Central AmericaArgentina1995Unknown1CC114b
LM77778South and Central AmericaArgentina1998Food1CC114b
LM77638South and Central AmericaArgentina1997Food2CC1992831/2a
LM69877South and Central AmericaArgentinaUnknownHuman1CC224b
LM80547South and Central AmericaArgentina1999Food1CC31171/2b
LM75973South and Central AmericaArgentina1997Food1CC331/2b
LM77713South and Central AmericaArgentina1998Food1CC331/2b
LM89775South and Central AmericaArgentina2001Food1CC331/2b
LM80503South and Central AmericaArgentina1999Food1CC3661/2b
LM78899South and Central AmericaArgentina1998Food2CC991/2c
LM80539South and Central AmericaArgentina1999Food2CC991/2c
LM89220
South and Central America
Argentina
2001
Food
2
CC9
9
1/2c
LM16678South and Central AmericaBrazil1989Human12184b
LM16713South and Central AmericaBrazil1989Food3293L
LM71345South and Central AmericaBrazilUnknownHuman1CC1734b
LM71338South and Central AmericaBrazilUnknownVegetal2CC1212751/2a
LM71346South and Central AmericaBrazilUnknownHuman1CC1951951/2b (s)
LM16722South and Central AmericaBrazil1990Human1CC1952741/2b
LM16728
South and Central America
Brazil
Unknown
Vegetal
2
CC9
9
1/2c
LM77137South and Central AmericaChileUnknownFood12794b
LM70662South and Central AmericaChileUnknownHuman1CC114b
LM90287South and Central AmericaChileUnknownFood1CC114b
LM77135South and Central AmericaChileUnknownHuman1CC12784b
LM77141South and Central AmericaChileUnknownFood1CC32801/2b
LM77152South and Central AmericaChileUnknownFood1CC32811/2b
LM77145South and Central AmericaChileUnknownFood1CC551/2b
LM77157South and Central AmericaChileUnknownFood1CC551/2b
LM90283South and Central AmericaChileUnknownFood1CC551/2b
LM77123South and Central AmericaChileUnknownHuman2CC771/2a
LM90291South and Central AmericaChileUnknownFood2CC82891/2a
LM70681South and Central AmericaChileUnknownFood2CC991/2c
LM77132South and Central AmericaChileUnknownHuman2CC991/2c
LM77150
South and Central America
Chile
Unknown
Food
2
CC9
9
1/2c
LM84996South and Central AmericaColombia1997Food1CC114b
LM85003South and Central AmericaColombia1998Food1CC12484b
LM85008South and Central AmericaColombia1999Food2CC1211211/2a
LM06-01614South and Central AmericaColombiaUnknownEnvironment2CC1991991/2a
LM85020South and Central AmericaColombia1999Food1CC224b
LM85058South and Central AmericaColombia2000Food1CC224b
LM06-01589South and Central AmericaColombiaUnknownFood1CC224b
LM84999South and Central AmericaColombia1998Food1CC59591/2b
LM85044South and Central AmericaColombia2000Food2CC771/2a
LM06-01598South and Central AmericaColombiaUnknownFood1CC87871/2b
LM84995South and Central AmericaColombia1997Food2CC991/2c
LM06-01615
South and Central America
Colombia
Unknown
Food
2
CC9
9
1/2c
LM06-00547South and Central AmericaFrench Guiana2006Human1CC114b
LM78969South and Central AmericaFrench Guiana1999Vegetal2CC1211211/2a
LM17308
South and Central America
French Guiana
1990
Human
2
CC155
155
1/2a
LM16656South and Central AmericaGuatemalaUnknownHuman1CC114b
LM18311South and Central AmericaGuatemalaUnknownHuman1CC114b
LM18351
South and Central America
Guatemala
Unknown
Human
1
CC1
1
4b
LM84817South and Central AmericaPeruUnknownUnknown12844b
LM84813South and Central AmericaPeruUnknownUnknown1CC331/2b
LM84810South and Central AmericaPeruUnknownUnknown2CC991/2c

*Strains with no clonal complex (CC) assignation correspond to singletons, i.e. genotypes that are not closely related to any other genotype.
†ST, sequence type.
‡Determined by classical serotyping (s) or by PCR serotyping; for the latter, the indicated serotype corresponds to the most common serotype of the PCR group.

Each isolate was hemolytic when streaked for isolation on blood agar. Genomic DNA was extracted by using Promega Wizard Genomic DNA purification kit (Promega, Madison, WI, USA). Serotype information was confirmed by PCR serogrouping (). MLST was performed as described (). Alleles and sequence types (STs) are publicly available at www.pasteur.fr/mlst. Clonal complexes (CC) were defined as groups of STs differing by only 1 gene from another member of the group () and were considered as clones. The θ estimator of the Fst statistic, which measures population differentiation, was determined on the basis of ST frequency by using FSTAT (www2.unil.ch/popgen/softwares/fstat.htm). The 300 isolates represented 111 STs (diversity index 95.4%) grouped into 17 CCs (Figure A1). Phylogenetic analysis of the concatenated genes (not shown) indicated that 199, 98, and 3 isolates belonged to lineages I, II, and III, respectively (). In lineage I, 3 CCs were highly prevalent: CC1 (47 isolates, serotype 4b), CC2 (64 isolates, 4b,) and CC3 (32 isolates, 1/2b). The remaining isolates of lineage I were of serotype 4b or 1/2b (Table). In lineage II, CC9 (28, all with serotype 1/2c, except one 1/2a isolate) was the most frequent, followed by CC7 (15 1/2a isolates). All other lineage II isolates had serotype 1/2a.
Figure A1

Genetic relationships among 660 Listeria monocytogenes isolates. The graph is a minimum spanning tree based on allelic profiles by using BioNumerics version 6.1 (Applied-Maths, Sint-Martens-Latem, Belgium). The 300 isolates of this study are in blue; the 360 L. monocytogenes isolates and reference strains of our earlier study () are in white and gray, respectively. Each circle represents a multilocus sequence typing genotype (ST), the size of which is related to the number of isolates (see legend). Clones, defined as clonal complexes [CC], are composed of groups of STs linked with a single gene difference, denoted as bold lines (see legend); clone number is indicated for the major clones. Links with >2 mismatches are unreliable because many alternatives may exist; links with 7 mismatches are not shown.

Comparisons of populations from different sources (Table) showed a clear partitioning of genotypic diversity between clinical isolates on the one hand and food or environmental isolates on the other (θ = 0.033 and 0.050, respectively; p<0.0002). Consistent with common knowledge (,), and even though recent outbreaks in Canada and Austria/Germany were caused by 1/2a strains, isolates of serotype 4b were, compared with other serotypes, relatively more frequent in human cases than in food. This difference in source distribution was further demonstrated for individual clones because the human/food ratio of both CC1 (2.6) and CC2 (2.8) differed significantly from those of CC3 (0.65) and CC9 (0.5) (χ2 p<0.01 for the 4 comparisons). A global distribution of L. monocytogenes clones was evident (Figure). Frequent clones were found in many countries (up to 30 countries for CC2; Table A1) and were globally distributed. Remarkably, CC1 and CC2 were predominant in all world regions except northern Africa for CC1 (Figure). CC3 ranked among the 4 most common clones in all regions, whereas CC9 ranked third in Europe and the Western Hemisphere. Altogether, these 4 clones represented 54 (50%) food isolates and 80 (68%) clinical isolates. Our results show that the same few clones account for a large fraction of nonepidemic L. monocytogenes isolates in distant world regions. However, continents and sources were not equally represented in our sample, and larger studies are needed to confirm our hypothesis that the clonal composition is similar across world regions and countries. Consistent with their cosmopolitan distribution, 15 of the 17 clones found herein (except CC199 and CC315, with only 6 and 3 isolates, respectively) included isolates from our previous analysis of 360 isolates, mostly from France ().

Conclusions

This study provides the first global view of L. monocytogenes clonal diversity. Our results clearly demonstrate the worldwide distribution and high prevalence of a few frequent clones in distinct world regions. In the current debate on the phylogeography of bacterial species (), major L. monocytogenes clones clearly fit in the “everything is everywhere” group, as do other pathogens in the environment, e.g., Pseudomonas aeruginosa (). Dispersal by human travel, animal or food trade, wild animal migration, or wind and dust all might contribute to the global diffusion of L. monocytogenes clones. However, finer phylogenetic resolution will possibly subdivide widespread MLST-defined clones into subclades that might exhibit phylogeographic partitioning and will better clarify the rate and patterns of strain dispersal. Remarkably, some ECs correspond with highly prevalent clones. ECII, described relatively recently (), and ECIII, involved in outbreaks from a single plant, correspond to 2 clones (CC6 and ST11, respectively []), that were rare herein (5 and 0 isolates, respectively), suggesting that both clones experienced particular conditions that favored their diffusion on specific occasions. In contrast, the outbreaks caused by ECI and ECIV, reference strains of which belong to CC1 and CC2, respectively (), could have been favored by their high prevalence in sources. One important question for future research is whether ECs correspond entirely to MLST-defined clones (i.e., CCs) or whether, on the contrary, they represent a genotypic subset thereof. The cosmopolitan distribution of clones, which protects them against extinction resulting from local disturbances, further highlights the crucial need to standardize L. monocytogenes genotyping to improve global epidemiologic knowledge and monitoring of current emergence trends.
Table

Distribution of the major Listeria monocytogenes clonal complexes in lineages I and II among sources

Lineage or clonal complexesNo. (%), by source
Human/food ratio
TotalHumanFoodAnimalEnvironmentUnknown
Lineage I, total199 (100)88 (44)60 (30)16 (8)24 (12)11 (6)1.60:1
CC1 (4b)47 (100)26 (55)10 (21)4 (9)3 (6)4 (9)2.60:1
CC2 (4b)64 (100)36 (56)13 (20)6 (9)5 (8)4 (6)2.77:1
CC3 (1/2b)32 (100)11 (34)17 (53)1 (3)2 (6)1 (3)0.65:1
Other 4b20 (100)8 (40)6 (30)1 (5)4 (20)1 (5)1.33:1
Other 1/2b
36 (100)
7 (19)
14 (39)
4 (11)
10 (28)
1 (3)
0.50:1
Lineage II, total98 (100)29 (30)45 (46)11 (11)8 (8)5 (5)0.64:1
CC9 (1/2c)28 (100)7 (25)14 (50)2 (7)3 (11)2 (7)0.50:1
Other, lineage II (1/2a)70 (100)22 (31)31 (44)9 (13)5 (71)3 (4)0.71:1
  14 in total

1.  A targeted multilocus genotyping assay for lineage, serogroup, and epidemic clone typing of Listeria monocytogenes.

Authors:  Todd J Ward; Thomas Usgaard; Peter Evans
Journal:  Appl Environ Microbiol       Date:  2010-08-13       Impact factor: 4.792

Review 2.  Microbial biogeography: putting microorganisms on the map.

Authors:  Jennifer B Hughes Martiny; Brendan J M Bohannan; James H Brown; Robert K Colwell; Jed A Fuhrman; Jessica L Green; M Claire Horner-Devine; Matthew Kane; Jennifer Adams Krumins; Cheryl R Kuske; Peter J Morin; Shahid Naeem; Lise Ovreås; Anna-Louise Reysenbach; Val H Smith; James T Staley
Journal:  Nat Rev Microbiol       Date:  2006-02       Impact factor: 60.633

3.  Multi-virulence-locus sequence typing identifies single nucleotide polymorphisms which differentiate epidemic clones and outbreak strains of Listeria monocytogenes.

Authors:  Yi Chen; Wei Zhang; Stephen J Knabel
Journal:  J Clin Microbiol       Date:  2007-01-10       Impact factor: 5.948

Review 4.  Listeria monocytogenes virulence and pathogenicity, a food safety perspective.

Authors:  Sophia Kathariou
Journal:  J Food Prot       Date:  2002-11       Impact factor: 2.077

5.  Global Pseudomonas aeruginosa biodiversity as reflected in a Belgian river.

Authors:  Jean-Paul Pirnay; Sandra Matthijs; Huri Colak; Patrice Chablain; Florence Bilocq; Johan Van Eldere; Daniel De Vos; Martin Zizi; Ludwig Triest; Pierre Cornelis
Journal:  Environ Microbiol       Date:  2005-07       Impact factor: 5.491

6.  Differentiation of the major Listeria monocytogenes serovars by multiplex PCR.

Authors:  Michel Doumith; Carmen Buchrieser; Philippe Glaser; Christine Jacquet; Paul Martin
Journal:  J Clin Microbiol       Date:  2004-08       Impact factor: 5.948

7.  Human Listeria monocytogenes infections in Europe--an opportunity for improved European surveillance.

Authors:  Justin Denny; Jim McLauchlin
Journal:  Euro Surveill       Date:  2008-03-27

8.  Multilocus sequence typing of outbreak-associated Listeria monocytogenes isolates to identify epidemic clones.

Authors:  Henk C den Bakker; Esther D Fortes; Martin Wiedmann
Journal:  Foodborne Pathog Dis       Date:  2010-03       Impact factor: 3.171

9.  Analysis of additional virulence genes and virulence gene regions in Listeria monocytogenes confirms the epidemiologic relevance of multi-virulence-locus sequence typing.

Authors:  Sara Lomonaco; Yi Chen; Stephen J Knabel
Journal:  J Food Prot       Date:  2008-12       Impact factor: 2.077

10.  Increasing incidence of listeriosis in France and other European countries.

Authors:  Véronique Goulet; Craig Hedberg; Alban Le Monnier; Henriette de Valk
Journal:  Emerg Infect Dis       Date:  2008-05       Impact factor: 6.883
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  77 in total

1.  Optimized Multilocus variable-number tandem-repeat analysis assay and its complementarity with pulsed-field gel electrophoresis and multilocus sequence typing for Listeria monocytogenes clone identification and surveillance.

Authors:  Viviane Chenal-Francisque; Laure Diancourt; Thomas Cantinelli; Virginie Passet; Coralie Tran-Hykes; Hélène Bracq-Dieye; Alexandre Leclercq; Christine Pourcel; Marc Lecuit; Sylvain Brisse
Journal:  J Clin Microbiol       Date:  2013-04-10       Impact factor: 5.948

2.  "Epidemic clones" of Listeria monocytogenes are widespread and ancient clonal groups.

Authors:  Thomas Cantinelli; Viviane Chenal-Francisque; Laure Diancourt; Lise Frezal; Alexandre Leclercq; Thierry Wirth; Marc Lecuit; Sylvain Brisse
Journal:  J Clin Microbiol       Date:  2013-09-04       Impact factor: 5.948

3.  Sequence typing confirms that a predominant Listeria monocytogenes clone caused human listeriosis cases and outbreaks in Canada from 1988 to 2010.

Authors:  Stephen J Knabel; Aleisha Reimer; Bindhu Verghese; Mei Lok; Jennifer Ziegler; Jeffrey Farber; Franco Pagotto; Morag Graham; Celine A Nadon; Matthew W Gilmour
Journal:  J Clin Microbiol       Date:  2012-02-15       Impact factor: 5.948

4.  Examination of food chain-derived Listeria monocytogenes strains of different serotypes reveals considerable diversity in inlA genotypes, mutability, and adaptation to cold temperatures.

Authors:  Jovana Kovacevic; Carolina Arguedas-Villa; Anna Wozniak; Taurai Tasara; Kevin J Allen
Journal:  Appl Environ Microbiol       Date:  2013-01-11       Impact factor: 4.792

5.  Listeria monocytogenes associated with New Zealand seafood production and clinical cases: unique sequence types, truncated InlA, and attenuated invasiveness.

Authors:  Cristina D Cruz; Andrew R Pitman; Sally A Harrow; Graham C Fletcher
Journal:  Appl Environ Microbiol       Date:  2013-12-20       Impact factor: 4.792

6.  Determination of Evolutionary Relationships of Outbreak-Associated Listeria monocytogenes Strains of Serotypes 1/2a and 1/2b by Whole-Genome Sequencing.

Authors:  Teresa M Bergholz; Henk C den Bakker; Lee S Katz; Benjamin J Silk; Kelly A Jackson; Zuzana Kucerova; Lavin A Joseph; Maryann Turnsek; Lori M Gladney; Jessica L Halpin; Karen Xavier; Joseph Gossack; Todd J Ward; Michael Frace; Cheryl L Tarr
Journal:  Appl Environ Microbiol       Date:  2015-11-20       Impact factor: 4.792

7.  Genetic determinants for cadmium and arsenic resistance among Listeria monocytogenes serotype 4b isolates from sporadic human listeriosis patients.

Authors:  Sangmi Lee; M Rakic-Martinez; L M Graves; T J Ward; R M Siletzky; S Kathariou
Journal:  Appl Environ Microbiol       Date:  2013-02-01       Impact factor: 4.792

8.  Clonogrouping, a Rapid Multiplex PCR Method for Identification of Major Clones of Listeria monocytogenes.

Authors:  Viviane Chenal-Francisque; Mylène M Maury; Morgane Lavina; Marie Touchon; Alexandre Leclercq; Marc Lecuit; Sylvain Brisse
Journal:  J Clin Microbiol       Date:  2015-07-29       Impact factor: 5.948

9.  Reservoirs of listeria species in three environmental ecosystems.

Authors:  Kristina Linke; Irene Rückerl; Katharina Brugger; Renata Karpiskova; Julia Walland; Sonja Muri-Klinger; Alexander Tichy; Martin Wagner; Beatrix Stessl
Journal:  Appl Environ Microbiol       Date:  2014-07-07       Impact factor: 4.792

Review 10.  Importance of Listeria monocytogenes in food safety: a review of its prevalence, detection, and antibiotic resistance.

Authors:  E Shamloo; H Hosseini; Z Abdi Moghadam; M Halberg Larsen; A Haslberger; M Alebouyeh
Journal:  Iran J Vet Res       Date:  2019       Impact factor: 1.376
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