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Public Health Microbiology

Multilocus Sequence Typing Supports the Hypothesis that Cow- and Human-Associated Salmonella Isolates Represent Distinct and Overlapping Populations

S. D. Alcaine, Y. Soyer, L. D. Warnick, W.-L. Su, S. Sukhnanand, J. Richards, E. D. Fortes, P. McDonough, T. P. Root, N. B. Dumas, Y. Gröhn, M. Wiedmann
S. D. Alcaine
Department of Food Science
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Y. Soyer
Department of Food Science
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L. D. Warnick
Department of Population Medicine and Diagnostic Sciences, Cornell University, Ithaca, New York 14853
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W.-L. Su
Department of Food Science
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S. Sukhnanand
Department of Food Science
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J. Richards
Department of Food Science
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E. D. Fortes
Department of Food Science
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P. McDonough
Department of Population Medicine and Diagnostic Sciences, Cornell University, Ithaca, New York 14853
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T. P. Root
Wadsworth Center, New York State Department of Health, Albany, New York
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N. B. Dumas
Wadsworth Center, New York State Department of Health, Albany, New York
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Y. Gröhn
Department of Population Medicine and Diagnostic Sciences, Cornell University, Ithaca, New York 14853
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M. Wiedmann
Department of Food Science
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  • For correspondence: mw16@cornell.edu
DOI: 10.1128/AEM.01174-06
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  • FIG. 1.
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    FIG. 1.

    Map of New York and Vermont counties where Salmonella isolates were obtained. The map was drawn using MapViewer 4.01 (Golden Sofware, Inc., Golden, CO). County codes are as follows: Alb, Albany; Brx, Bronx; Brm, Broome; Cat, Cattaraugus; Cay, Cayuga; Cha, Chautauqua; Cmg, Chemung; Cno, Chenango; Cvt, Chittenden, VT; Cli, Clinton; Cor, Cortland; Del, Delaware; Dut, Dutchess; Eri, Erie; Fra, Franklin; Fvt, Franklin, VT; Gen, Genesee; Kin, Kings; Lvt, Lamoille, VT; Lew, Lewis; Liv, Livingston; Mon, Monroe; Nas, Nassau; New, New York; Nia, Niagara; One, Oneida; Ono, Onondaga; Ont, Ontario; Ora, Orange; Orl, Orleans; Osw, Oswego; Ots, Otsego; Put, Putnam; Ren, Rensselaer; Sar, Saratoga; Sch, Schenectady; Sen, Seneca; Stl, St. Lawrence; Ste, Steuben; Suf, Suffolk; Tom, Tompkins; Uls, Ulster; Unk, Unkown; War, Warren; Was, Washington; Way, Wayne; Wes, Westchester; and Wyo, Wyoming.

  • FIG. 2.
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    FIG. 2.

    Phylogenetic trees based on Salmonella fimA (A) and mdh (B) gene sequences. Neighbor-joining trees were built in PAUP* using one representative isolate for each sequence type, including STs previously described by Sukhnanand et al. (49), which were not represented among the isolates found here (these STs are indicated by a *). ML trees (not shown) displayed similar clusterings and topologies. Bootstrap analyses were performed using 5,000 replications, and bootstrap values >50 are indicated. M indicates STs representing isolates that contain a manB gene duplication; the branch labeled as “clade 1” represents a number of related STs, including STs (ST52 to ST57, ST63, and ST67 in the mdh tree) that correspond to isolates with two manB copies, indicating a common ancestral event that was responsible for the two manB copies found in these isolates. D1, D2, and D3 indicate STs representing isolates that contain fimA deletion types D1 through D3 (Table 6). STs representing the two distinct Salmonella serotype Newport groups (designated types A and B) are marked by circles or boxes and the respective type.

Tables

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  • TABLE 1.

    Farms with multiple sample submission dates resulting in the isolation of Salmonella from clinically infected cattle

    FarmNo. of farm sample dates with positive Salmonella samplesSubtype(s) isolateda (no. of isolates)
    51020ST11/serotype Newport (20), ST6/serotype 4,5,12:i:- (1)
    26122ST6/serotype 4,5,12:i:- (18), ST17/serotype Kentucky (5), ST6/serotype Typhimurium (1)
    22315ST60/serotype Infantis (15)
    3295ST9/serotype Montevideo (1), ST44/serotype Muenster (3), ST62/serotype Thompson (1)
    1864ST75/serotype Adelaide (1), ST8/serotype Typhimurium (2), ST8/serotype Typhimurium var. Copenhagen (1)
    5245ST6/serotype 4,5,12:i:- (1), ST11/serotype Newport (4)
    1524ST11/serotype Newport (4)
    4904ST11/serotype Newport (4)
    1633ST60/serotype Infantis (1), ST11/serotype Newport (2)
    2593ST44/serotype Muenster (3)
    4883ST11/serotype Bardo (1), ST11/serotype Newport (3)
    5843ST2/serotype Agona (2), ST6/serotype Typhimurium (1)
    972ST8/serotype Typhimurium var. Copenhagen (2)
    1052ST11/serotype Newport (1), ST8/serotype Typhimurium (1)
    1252ST6/serotype Typhimurium (2)
    2082ST6/serotype Typhimurium (2)
    3032ST11/serotype Newport (2)
    3202ST11/serotype Newport (2)
    4152ST9/serotype Montevideo (1); ST6/serotype Typhimurium (1)
    7642ST6/serotype Typhimurium (2)
    • ↵a Subtype is represented as ST/serotype.

  • TABLE 2.

    Distribution of Salmonella serotypes among STs and human and bovine isolates

    SerotypeaST(s)No. of isolates from:
    HumansDairy cattleb
    Serotype 4,5,12:i:-6, 40123
    Serotype Agona1, 234
    Serotype Enteritidis***14, 36260
    Serotype Heidelberg*3, 26, 50100
    Serotype Mbandaka64, 65, 7341
    Serotype Montevideo9, 56, 57, 6743
    Serotype Muenster*4415
    Serotype Newport***11, 13, 33, 46, 76, 781825
    Serotype Saint Paul38, 8150
    Serotype Thompson43, 6253
    Serotype Typhimurium6, 7, 8, 47, 493019
    Serotype Urbana5250
    • ↵a Only serotypes that occurred more than five times are listed separately (for animal isolates, only one isolate with a given serotype and ST per farm was counted). Additional serotypes that occurred less than five times are as follows (numbers of human and unique bovine isolates per farm are included in parentheses): serotype 4,12:i:- (one bovine isolate), serotype Abony (two human isolates), serotype Adelaide (one human isolate and one bovine isolate), serotype Agbeni (one human isolate), serotype Anatum (three human isolates), serotype Arechavaleta (one human isolate), serotype 4,12:r:- (two human isolates), serotype Bardo (two bovine isolates), serotype Berta (two human isolates), serotype Blockley (one human isolate), serotype Braenderup (one human isolate), serotype 1,7:-:1,5 (three human isolates), serotype Cubana (one human isolate), serotype Dublin (two human isolates), serotype Give (one human isolate), serotype Hadar (two human isolates), serotype Hartford (one human isolate), serotype Havana (one bovine isolate), serotype Infantis (two human and two bovine isolates), serotype Javiana (four human isolates), serotype Kentucky (two bovine isolates), serotype Kintambo (one human isolate), serotype Litchfield (one human isolate), serotype Muenchen (three human isolates), serotype Nyanza (one human isolate), serotype Oranienburg (one human isolate and one bovine isolate), serotype Panama (three human isolates), serotype Paratyphi B (one human isolate), serotype Paratyphi B var. Java (two human isolates), serotype Paratyphi C (one human isolate), serotype Pomona (one human isolate), serotype Poona (two human isolates), serotype Rough o:i:1,2 (one bovine isolate), serotype Rublislaw (one human isolate), serotype Schwarzengrund (three human isolates), serotype Senftenberg (one human isolate), serotype Stanley (two human isolates), serotype Typhimurium var. Copenhagen (four bovine isolates), serotype Weltvreden (one human isolate), and serotype Worthington (one human isolate). Serotypes that differ significantly in frequency among human and animal isolates, as determined by chi-square test or Fisher's exact test, are marked with * (P < 0.05) or *** (P < 0.001).

    • ↵b Only one isolate representing each unique serotype/ST combination found on a given farm was counted; these numbers were used to avoid the overrepresentation of a subtype due to resampling on a given farm (e.g., when isolates with the same serotype/ST combination were isolated on different dates on the same farm) (Table 1).

  • TABLE 3.

    Distribution of Salmonella STs among human and bovine isolates and among different counties in New York state

    STaSerotype(s)No. of isolates from:County origin of isolates (no. of isolates) fromc:
    HumansCattlebHumansDairy cattleb
    3*Serotype Heidelberg, serotype 4,12:r:-100Dut (1), Eri (1), Fra (1), Mon (1), Nas (2), New (1), One (1), Suf (2)None
    6Serotype Typhimurium, serotype 4,12:i:-, serotype 4,5,12:i:-3820Alb (1), Brx (1), Cha (1), Cmg (1), Cor (1), Dut (1), Eri (3), Fra (1), Kin (1), Mon (1), Nas (4), Ono (2), Ora (1), Ots (1), Stl (1), Ste (2), Suf (7), Tom (1), War (1), Was (2), Wes (4)Cat (1), Cli (3), Cor (1), Gen (1), Nia (1), Ont (1), Orl (1), Ren (3), Stl (1), Tom (1), Was (1), Wyo (5)
    8***Serotype Typhimurium, serotype Rough o:i:1,2, serotype Typhimurium var. Copenhagen07NoneCay (1), Cno (1), Osw (2), Was (3)
    11***Serotype Newport, serotype Bardo927Cno (1), Nia (1), Put (1), Sar (1), Suf (1), Uls (1), Unk (1), Way (1), Wes (1)Cay (1), Cno (1), Cvt (2), Cli (2), Cor (1), Eri (1), Fvt (6), Gen (1), Lvt (1), Lew (1), Nia (3), One (2), Ono (1), Sen (1), Stl (1), Wyo (2)
    14**Serotype Enteritidis190Brm (1), Dut (1), Eri (3), Kin (1), Mon (2), Nas (3), Ono (2), Ora (1), Suf (2), Unk (1), Wes (2)None
    36Serotype Enteritidis70Alb (1), Del (1), Eri (1), Mon (1), Nas (1), Tom (1), Wes (1)None
    44**Serotype Muenster15Cmg (1)Fra (1), Liv (1), Orl (1), Wyo (2)
    52Serotype Urbana50Cli (2), Sch (3)None
    62Serotype Thompson42Nas (1), Sar (1), Uls (1), Way (1)Liv (1), Nia (1)
    Rare**Various serotypes8617NSNS
    • ↵a Only STs that occurred five or more times are listed separately; the STs with fewer than five isolates were grouped into a category termed “rare”; STs that differ significantly in frequency among human and bovine isolates, as determined by chi-square test or Fisher's exact test, are marked with * (P < 0.05), ** (P < 0.01), or *** (P < 0.001).

    • ↵b Only one isolate representing each unique serotype/ST combination found on a given farm was counted; these numbers were used to avoid the overrepresentation of a subtype due to resampling on a given farm (e.g., when isolates with the same serotype/ST combination were isolated on different dates on the same farm) (Table 1).

    • ↵c Counties are depicted in Fig. 1. County codes are as follows: Alb, Albany; Brx, Bronx; Brm, Broome; Cat, Cattaraugus; Cay, Cayuga; Cha, Chautauqua; Cmg, Chemung; Cno, Chenango; Cvt, Chittenden, VT; Cli, Clinton; Cor, Cortland; Del, Delaware; Dut, Dutchess; Eri, Erie; Fra, Franklin; Fvt, Franklin, VT; Gen, Genesee; Kin, Kings; Lvt, Lamoille, VT; Lew, Lewis; Liv, Livingston; Mon, Monroe; Nas, Nassau; New, New York; Nia, Niagara; One, Oneida; Ono, Onondaga; Ont, Ontario; Ora, Orange; Orl, Orleans; Osw, Oswego; Ots, Otsego; Put, Putnam; Ren, Rensselaer, Sar, Saratoga; Sch, Schenectady; Sen, Seneca; Stl, St. Lawrence; Ste, Steuben; Suf, Suffolk; Tom, Tompkins; Uls, Ulster; Unk, Unkown; War, Warren; Was, Washington; Way, Wayne; Wes, Westchester; Wyo, Wyoming. NS, not shown.

  • TABLE 4.

    Serotypes that include at least one isolate that carries two manB copiesa

    SerotypeST(s) of human isolates (no of isolates) within a given serotype that carry:ST(s) of cattle isolates (no. of isolates) within a given serotype that carryb:
    Two manB copiesOne manB copyTwo manB copiesOne manB copy
    Serotype Agbeni63 (1)NoneNoneNone
    Serotype Braenderup61 (1)NoneNoneNone
    Serotype 1,7:-:1,558 (1)42 (1), 43 (1)NoneNone
    Serotype Cubana71 (1)NoneNoneNone
    Serotype HavanaNoneNone69 (1)None
    Serotype Infantis60 (2)None60 (1)None
    Serotype Kintambo59 (1)NoneNoneNone
    Serotype Mbandaka64 (2)73 (2)65 (1)None
    Serotype Montevideo56 (2), 57 (1), 67 (1)NoneNone9 (3)
    Serotype Nyanza66 (1)NoneNoneNone
    Serotype Oranienburg53 (1)None53 (1)None
    Serotype Poona55 (1)28 (1)NoneNone
    Serotype Rublislaw54 (1)NoneNoneNone
    Serotype Thompson62 (4)43 (1)62 (2)43 (1)
    Serotype Urbana52 (5)NoneNoneNone
    Serotype Worthington68 (1)NoneNoneNone
    • ↵a Serotypes for which all isolates carry only a single manB copy are not included in this table.

    • ↵b Only one isolate representing each unique serotype/ST combination found on a given farm was counted; these numbers were used to avoid the overrepresentation of a subtype due to resampling on a given farm (e.g., when isolates with the same serotype/ST combination were isolated on different dates on the same farm) (Table 1).

  • TABLE 5.

    Serotypes that include at least one isolate that carries a deletion in the 3′ end of fimAa

    SerotypefimA deletion typeST(s) of human isolates (no. of isolates) within a given serotype that carry:ST of cattle isolates (no. of isolatesb) within a given serotype that carry:
    fimA deletionNo fimA deletionfimA deletionNo fimA deletion
    Serotype NewportD178 (3)11 (9), 13 (1), 33 (2), 46 (2), 76 (1)None11 (25)
    Serotype WeltvredenD279 (1)NoneNoneNone
    Serotype Paratyphi CD280 (1)NoneNoneNone
    Serotype Saint PaulD381 (1)38 (4)NoneNone
    Serotype BertaD382 (1), 83 (1)NoneNoneNone
    Serotype StanleyD384 (1)39 (1)NoneNone
    • ↵a Serotypes for which all isolates carry no deletion in the 3′ end of fimA are not included in this table.

    • ↵b Only one isolate representing each unique serotype/ST combination found on a given farm was counted; these numbers were used to avoid the overrepresentation of a subtype due to resampling on a given farm (e.g., when isolates with the same serotype/ST combination were isolated on different dates on the same farm) (Table 1).

  • TABLE 6.

    DNA and amino acid sequences of fimA deletion types D1, D2, and D3a

    Deletion typeDNA sequenceAmino acid sequence
    Wild typeGCACGCTATAAGGCAACCGCCGCCGCCACGACGCCAGGCCAGGCTAATARYKATAAATTPGQANADATFIMKYE
    D1GCACGCTATAAGGCAACCGCCGCCGCCGCGACGCCAGGC-----TAATARYKATAAAATPG
    D2GCACGCTATAAGGCAACCGCCGCC---ACGACGCCAGGCCAGGCTAATARYKATAA-TTPGQANADATFIMKYE
    D3GCACGCTATAAGGCAACCGCCGCCGCG---ACGCCAGGCCAGGCTAATARYKATAAA-TPGQANADATFIMKYE
    • ↵a Nucleotide sequences surrounding the deletions in the 3′ region of fimA and amino acid sequences surrounding the deletions in the 3′ region of fimA are shown. The first amino acid corresponds to the first codon shown in the DNA sequence. Whereas the amino sequence includes the stop codon, the nucleotide sequence shown is missing the nucleotides encoding the last 10 amino acids.

Additional Files

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    • Supplemental file 1 - Table S1 (Salmonella isolates included in the study)
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Multilocus Sequence Typing Supports the Hypothesis that Cow- and Human-Associated Salmonella Isolates Represent Distinct and Overlapping Populations
S. D. Alcaine, Y. Soyer, L. D. Warnick, W.-L. Su, S. Sukhnanand, J. Richards, E. D. Fortes, P. McDonough, T. P. Root, N. B. Dumas, Y. Gröhn, M. Wiedmann
Applied and Environmental Microbiology Dec 2006, 72 (12) 7575-7585; DOI: 10.1128/AEM.01174-06

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Multilocus Sequence Typing Supports the Hypothesis that Cow- and Human-Associated Salmonella Isolates Represent Distinct and Overlapping Populations
S. D. Alcaine, Y. Soyer, L. D. Warnick, W.-L. Su, S. Sukhnanand, J. Richards, E. D. Fortes, P. McDonough, T. P. Root, N. B. Dumas, Y. Gröhn, M. Wiedmann
Applied and Environmental Microbiology Dec 2006, 72 (12) 7575-7585; DOI: 10.1128/AEM.01174-06
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