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JOURNAL OF CLINICALMICROBIOLOGY, Apr. 1989,p.622-627 0095-1137/89/040622-06$02.00/0

Copyright © 1989, American Society for Microbiology

Clonal

Groups

of

Salmonella typhimurium in

New

York State

PATRICK L. McDONOUGH,ît* JOHN F. TIMONEY,2 RICHARD H. JACOBSON,' AND RASIKKHAKHRIA3 Diagnostic Laboratory' andDepartmentof Veterinary Microbiology,2 New York State College of Veterinary Medicine,

Cornell University, Ithaca, New York14853, and Phage Typing Centre, Division ofEntericBacteriology, Bureauof' Microbiology, Laboratory Centre forDisease Control, Health and Welfare, Ottawa, Ontario K1A OL2, Canada3

Received 16September 1988/Accepted21 December1988

The epidemiology of 278 strains of Salmonellatyphimuriumisolatedfrom1973to 1981 fromanimals in New YorkStatewasstudiedbyusingfour"fingerprinting"techniques,bacteriophagetype(B. R. Callow, J. Hyg. 57:346-359, 1959), biotype (J. P. Duguid, E. S. Anderson, G. A. Alfredsson, R.Barker, and D. C. Old, J. Med. Microbiol. 8:149-166, 1975), plasmid profile, and antibiogram. Phagetype with biotypewasthe most usefulmarkerfor distinguishingclonalgroupsofS.typhimurium.Fourclonesof S.typhimuriumpredominated,

i.e.,phagetype/biotypes U275/26, 49/26, 10/3, and2/3. U275/26and49/26werecommonlyfound until 1976,

but clones 10/3 and2/3werepredominantafter1976.Comparisonofresultswith datafrom Canada suggested adissemination ofstrainsofS. typhimuriumbetween Canada and New York. Cattlewere a common sourceof phagetype49, ashas beenobserved inother countries.

Salmonellosis is a disease of great public health and economic significance. The ubiquity ofone serotype, Salmno-nella typhimurium, in human and animal reservoirs of infec-tion and in the environment is well established. After sero-typing, bacteriophage typing is often the first step in "fingerprinting" isolates of S. typhimuriainsothat theymay be distinguished from or identified as part of an epidemic strain (4, 23). Phage typing is then linked with biotyping (4, 5, 18, 21), plasmid profile analysis (32, 34), and other characterizations, suchasrestriction endonuclease analysis, incompatibility grouping, and analysis of antibiogram

pat-terns(10, 24, 35), to further define an epidemic strain.

The phage typing scheme of Callow (15) used in various countries has proven to be useful in epidemiological inves-tigations of S. typhimurium infections at both the local (9) andinternational (3, 26, 31) levels. Biotyping of S. typhimul-rium was developed by Duguid and co-workers (21) in Scotland from an earlier scheme by Kristensen (1, 27) and has proven to be useful in manyepidemiological investiga-tions of S. typhimurium infections (4, 5, 7, 21). Biotyping was anessential element inunderstanding the epidemic ofS. typhimurium phagetypes (PTs) 49-204-193 in Britain in the 1970s (6).

In thepresent epidemiological study, four characteristics were combined to fingerprint isolates of S. typhimurinum,

i.e., PT, biotype (BT), plasmid profile, and antibiogram

pattern.Theevolution of different PT/BTgroups orclonesin differentanimal populationswas analyzed. Thesignificance ofclonally distributed PT/BTgroupswasassessed inlight of

theavailable knowledge of theepidemiology of S.

typhimu-rium.

MATERIALS AND METHODS

Bacterial isolates. Twohundredseventy-eight isolates ofS. typhimurium, including subsp. Copenhagen, isolated during the period 1973 to 1981 from animal sources in New York

State were studied. For each strain, date of isolation, loca-tion, andsource were recorded. All strainsweremaintained

*Correspondingauthor.

tPresentaddress:School ofVeterinary Medicine,Tufts

Univer-sity,305South St., Boston,MA02130.

onDorsetEggMedium(Difco Laboratories, Detroit, Mich.) at roomtemperature.

Serotyping. Serotyping using established procedures for cellwall (O) andflagellar (H) antigen identification (22) was performed at the New York State College of Veterinary Medicine, Ithaca, and at the National Veterinary Service Laboratories, Animal and Plant Health Inspection Service, U.S. Department ofAgriculture, Ames, Iowa.

Phage typing. Strains were phage typed by using the updated scheme of Callow (3, 15), which included new phagesisolated in Canada by Khakhria and Lior (26).

Biotyping. Biotyping wasperformed by the procedures of Duguidet al.(21). Primary BTtests consisted of the follow-ing fermentation reactions: D-xylose in Bitter medium; L-rhamnose and ineso-inositol inpeptone water; theD-tartrate tube turbidity test; and the m-tartrate plate inhibition test. AllprimaryBTtestswereconductedat37°C.Thesecondary BT tests consisted ofassays fortype 1 fimbriaandflagella; fermentationreactions in peptone waterofD-xylose (37°C, 24h), trehalose (37°C, 24h), meso-inositol (25°C, 48 h),and glucose (gas formation, 37°C,24 h); l-tartrate tubeturbidity test (37°C, 24 h); fermentation ofglycerol in Stern medium (37°C, 24 h); fermentation ofL-rhamnose in Bitter medium (370C, 24h); testingforauxotrophsonminimal mediumplus nicotinamide, cysteine, or other amino acids. The tartaric acidturbiditytestswereadaptedtosemiautomatedtestingin 50-well Gilford nonbinding enzyme immunoassay cuvette packs. At the end ofincubation, packs were shaken for 1 min, and theA515 was readautomatically on aGilford EIA System(PR650 processing unit; Gilford Instrument Labora-tories, Inc., Oberlin, Ohio) interfaced with a PDP 11/34A

computer (Digital Equipment Corp., Maynard, Md.). Absorbance readings were interpreted in a computer pro-gramwhichgenerateda+, -,or"retest"resultfor eachd-,

1-, and m-tartaric acid test.

Control strains for the biotyping tests consisted of 12 strains of S. typhimurium representing different BTs

re-ceived from R. Barker, University of Dundee Medical School, Dundee, Scotland. These strains were

repre-sentative of the following BTs: la, lbc, lf, lg, lh, 2a, 3a, 17a, 26d, 26i, 31b,and 32b.

Plasmid profile. (i) Isolation of plasmid DNA. Bacterial strainswerescreened forplasmidDNAbyamodification of 622

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CLONAL GROUPS OF SALMONELLA FROM NEW YORK

TABLE 1. Salmonellafrequencydistribution by host animal

No. of

Species

strains(%)

Cattle ... ... 204 (73)

Calf ... ... 127(45.7)

AduIt ... ... 77(27.7)

Horses ... ... 49 (17.6)

PouItry... ... 6(2.2) Cats... 3(1.1)

Pigs... 5(1.8) Guinea pigs... 5(1.8)

Dogs ... ... 2(0.7)

Leopards... ... 1(0.35) Rabbits... 1 (0.35)

Goats... 1(0.35)

Opossums... ... 1(0.35)

theBirnboim-Doly extraction procedure (11). Control

plas-mids for determining the molecular sizes of test plasplas-mids consistedofRi (62megadaltons

[MDa])

and S-a(23 MDa). (ii) Plasmid DNA analysis. Plasmid DNA was examined by vertical agarose gelelectrophoresisby using thetechniqueof

Crosaand Falkow(19).

Antimicrobial susceptibility testing. The disk diffusion

technique ofBauer et al. (8) was used to assayresistance to

14antimicrobial agents by using Sensi-discs (BBL Microbi-ology Systems, Cockeysville, Md.) of the following drugs:

ampicillin(Am) (10 1tg), chloramphenicol (C)(30

F.g),

colis-tin(Cl) (10

ptg),

gantrisin (G) (300 p.g),gentamicin (Gm) (10

ptg),

kanamycin (K) (30

p.g),

neomycin (N) (30 ,ug),

nitrofu-rantoin(F/M) (300

fig),

polymyxin B (Pb) (300 ,ug),

strepto-mycin(S) (10

pug),

tetracycline(Te) (30

p.g),

triplesulfa(SSS)

(250

p.g),

trimethoprim (1.25 Ftg)-sulfamethoxazole (23.75

jig)

(SXT), and cephalothin (CF) (30 ,ug). Mueller-Hinton

agarplates (BBL) wereused. Control bacterial strains were

Escherichia coli ATCC 25922, Staphvlococcus aureus ATCC 25923, and Pseudomonas aeruginosa ATCC 27853.

For ease in data analysis, the resistance pattern or

anti-biogram of each bacterial strain was reduced to a number

scoreby usingamnemonic, i.e., four groups of three drugs

each andafifth groupoftwodrugswerecoded and scoredas

follows. Possiblescore:

AM C CI G GM K N F/M Pb S Te SSS SXT CF

4 2 1 4 2 1 4 2 1 4 2 1 4 2

ResistancetoAm, G, K, N, SSS would be scoredasfollows:

400 401 400 001 00

Adding

the

possible scores within each group produces a

five-digit antibiogram:

4 5 4 1 0 RESULTS

Strain distribution of S. typhimurium. Of the strains, 16% were isolated in 1973, 22% were isolated in 1974, 18% were isolated in 1975, 9%were isolated in 1976, 2% were isolated in 1977,2%wereisolatedin 1978, 7%wereisolated in 1979,

10% were isolated in 1980, and 13% were isolated in 1981. Table 1 lists the frequency of strains of S. typhimurium

isolatedfrom animalspecies from 1973 to 1981. Of the total,

73% (204/278) werefrom cattle.

PTsof S. typhimurium. Table 2 lists thefrequency

distri-bution of PTs of S. typhimurium isolated in the study

TABLE 2. PercentagefrequencyofPTs ofS. typhimuriumfrom

nonhumansources (1973to 1981)

PT No.of strains (%) Rank

U275" 66(23.7) 1

49 46(16.5) 2

10 28(10.1) 3

2; CR2b 19(6.8); 1 (0.4) 4

771' 13(4.7) 5

U276" 13(4.7) 5

191;CR191 9(3.2); 1 (0.4) 6

88 9(3.2) 7

93 7(2.5) 8

772' 4(1.4) 9

69 3(1.1) 10

186 2(0.7) il

40 2 (0.7) il

81 2 (0.7) il

1 1 (0.4) 12

1 Variant 1 (0.4) 12

3Aerogenic 1 (0.4) 12

12 1 (0.4) 12

17 1 (0.4) 12

105 1 (0.4) 12

108 1 (0.4) 12

124 1 (0.4) 12

146 1 (0.4) 12

164 1 (0.4) 12

172 1 (0.4) 12

204 1 (0.4) 12

Untypable'

10(3.6)

Rform' 5(1.8)

Atypicalf 19(6.8)

Nottested& 7(2.5)

"PTsU275andU276 areprovisionaltypedesignationsrecommendedby

B.Rowe,World HealthOrganisation Collaborating Centre for PhageTyping

andResistance of EntericBacteria,London, United Kingdom.

">CR,Closelyresemblingaknown PT.

PTs 771 and 772 are Laboratory Centre for Disease Control (Ottawa,

Ontario, Canada) designations, i.e.. typable byusing experimental phages

isolated inCanada.

"Untypable, Culture totally resistanttoail typing phages ofthe present

Callowscheme.

' Rform, Rough form.nottypable.

-fAtypical,Designatedthus because these strains react withS.typhimurium

typing phagesbut do notconformto arecognizabletype.

eNottested,Strains were notphagetyped because of loss ofviabilityat

typingcenter.

population. The

predominant

PT was U275

(23.7%),

fol-lowed by types49(16.5%), 10

(10.1%),

and 2 (7.2%).

PT/BTcombinations. The PTs andtheircombinationswith

BTs are shown in Table 3. Among the 278 strains of S.

typhimurium, 26differentPTsand 32fullBTsweredefined.

Up to 77 different combinations of PT/full BT were pro-duced.

Fourmajor epidemic clones:PT/BT. Ofthe 278 strains of

S. typhimurium, four major clones (same PT and BT)

emerged, makingup52%of all strains (Table4).

Plasmids. Table 5 shows the distribution of plasmids

among the four major PT/BT groups. Reference plasmids

ranged in size down to 23 MDa; extrapolation from the

standardcurve tocalculate the sizeof smallerplasmids may thus contain error. Also, very large plasmids were not

optimallyrecovered with theBirboim-DolyDNAextraction

methods,sothat insome strains of S. typhimurium alllarge

plasmids may not have been detected.

Combinationofallfingerprintcharactersforthefourclonal groups. (i) PT U275/BT 26. S. typhimurium PT U275

com-prised66strains ofonlyoneprimary BT,26(Table6). Four

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624 MCDONOUGH ET AL.

TABLE 3. BTs of S. typhimurium distributedamong PTs

PTa BT(no. of isolates)

1... 2a(1)

1 Variant... 25a (1)

2 ...la(1), 3a(11), 3f(1),4a(1), 17a(2), 17dg (1), î7dgj(1), 19a (1)

CR2... 3a(1)

3Aerogenic... 26ei(1)

10... la(1), 3a(21), 3y (1), 4a(3), 4f(1), 19e(1)

12... 17e(1)

17...17a(1)

40... 22be (1), 32bdh(1)

49... 18e(1), 26egi(1), 26ei (44)

69... 3a(3)

81... 3a(2)

88... la(1), 3a(6), 3y(1), 4f(1)

93... 3a(2), 26ei(4), 26i (1)

105...la(1) 108... 3a(1)

124... 32beghi (1)

146... 32beh(1)

164... 3a(1)

172... 3a(1)

186... 26ei (1), 26i (1)

191... 17a(9)

CR191... 3a(1)

204... 26ei(1)

771...la(2), 3a(6), 26ei(4), 26iy (1) 772... 3a(3), 26ei(1)

U275... 26e(1), 26egi(1), 26ei (63), 26i(1)

U276... la(1), 18a(1), 26ei(2). 26fi(1), 26i(7),

28iy (1) Untypable... 3a(3), 26ei(7)

Rform... l2f(1), 26ei (2),26i(2)

Atypical... ldg(1), 2a(1), 2f(1), 3a(6). 3y (1),9di

(1), 17a (1),26ei(7) Not tested... 3a(2), 26ei(4), 26eiy (1)

"See footnotesto Table 2 for explanations of CR, untypable. R form,

atypical, andnottested.

subtypes of BT 26werepresent, i.e., 26e (1 strain), 26egi (1 strain),26i (1 strain), and 26ei (63 strains). U275/26eiwasthe predominant PT/full BT and comprised about 24% of all strains of S. typhimurium of the study. U275 and the four subtypesmay beconsideredas oneclonecontainingmutant sublines.

U275 and its BTs were widely distributed in at least 10 NewYork counties in 1973, 13counties in1974, 1countyin

TABLE 4. Major epidemic PT/BTs (clones) ofS.

typhimrurium

PT/BT No. of

strains

U275/26ei... 63

U275/26e... 1

U275/26egi... 1

U275/26i... 1

49/26ei... 44

49/26egi... 1

10/3a... 21

10/3y... 1

2/3a... 11

CR2"/3a... 1

2/3f... 1 "CR, Closelyresemblingaknown PT.

TABLE 5. Distribution ofplasmidsamongthe fourmajor clonal groups of S. typhimnurium

No.ofplasmids in clonal group (PT/BT): Plasmid size

(MDa) U275/26 49/26 10/3 2/3

(n=66)" (n=45) (n =22) (n= 13)

s20 130 83 1 2

20-30 " 1

30-40 40-50

50-60

-60-70 61 44 3 2

-70 12 1

"n, Number ofstrains.

- Noplasmids detected. See thetext.

1975, and 2 countiesin 1976.Theywere not seenin 1977. In 1978 and 1979, they occurred inonlyonecountyeach year, after which they were not detected. U275/26ei was found predominantly in calves, especially veal calves, throughout the study period, but it also occurred in adult cattle, in horses, and on oneoccasionin pigs.

(ii) PT 49/BT 26. Forty-five strains of PT 49 that were of BT 26 occurred (Table 6). BT 26occurred as two subtypes, i.e., 26ei (44 strains) and 26egi (1 strain). Subtype 49/26ei wasfound in three counties in 1973,wasmorewidespread in six counties in 1974 and fourcounties eachin 1975 and1976, andwas seenonlyonceafter1976 in veal calves in 1979.As with U275, PT 49 occurred mainly in calves, mostly veal

calves, but was found also in adult cattle, horses, and on

occasion pigs and othersmallanimals.

(iii) PT 10/BT3.Twenty-two strainsof PT 10 that wereof BT3 occurred. BT3had twosubtypes, 3a (21 strains) and 3y (1strain). Subtype 10/3awasseen sporadically from 1975to 1976 in horsesand goats and wasnotseen atallfrom 1977 to 1978. Subtype10/3a was observed as a widespread clone in five counties by 1979, seven counties in 1980, and eight counties in 1981. Strains from adult cattle, not calves, accounted formostof the 10/3aisolates, but 10/3awas seen in horses andotherspeciesas well.

(iv) PT 2 and CR2/BT3. Thirteen strains ofPT 2 andCR (closely resembling) 2 wereofprimaryBT3 (Table 6). BT3 had twosubtypes, 3a(12isolates)and 3f(1isolate). Subtype 2/3a was isolated from 1975 to 1977 once each year in two counties from horses, adult cattle, and calves and was not encountered again until 1979, when it appeared in adult cattle in two counties. In 1980, it again occurred in adult cattle inonecounty. Subtype2/3fwas seeninadult cattle in a different county in 1980. In 1981, 2/3a occurred twice in adult cattle and twice in horses in four different counties.

Subtype 2/3a was isolated predominantly from adult cattle

and horses but not from calves, in which it occurred only once.

DISCUSSION

S.typhimnuriurn is the most commonSalmonella serotype

isolated from human and animalsourcesin New York State (14,20, 28) and the United States(12, 16);however, little is known about its epidemiological significance. The results presented here provide epidemiological information on the distribution ofPTsand clonal groups of strains of S.

typhi-murium fromanimals.

Cattle and horses were the predominant host animals in

the study and areprobably reflective more of the

composi-tion of submissions totheDiagnostic Laboratorythanof the J. CLIN. MICROBIOL.

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CLONAL GROUPS OF SALMONELLA FROM NEW YORK TABLE 6. Combined fingerprint characters of major clones

ofS. tv'philuii(i-initnl

Anti- No.of No. ofplasmids of size (MDa):

PT BT

biogram'

strains >70'> 62

20-30

<20

U275 26ei 05470 1

3 1

17 1 2

6 1 3

9 1 1 2

1 1 3

6 1 1

1 3

45472 1 1 1 3

1 1 1 4

3 1 2

6 1 3

1 1

04070 1 1

45470 1 1 3

05670 1 1 1

04050 1 1 1

26e 45472 1 1 3

26egi 05470 1 1 1

26i 45470 1 1 2

49 26ei 45472 5 1 3

4 1 4

5i2

5 1 1

i i i 6

i 1 5

05470 1 1 1 2

i 1

1 1 3

4 1

4 1 1

1 1

01460 5 1

24270 1 1

25470 1 1

44072 1 1 2

2 1 1

00000 i 1 2

26egi 04010 1 1 2

10 3a 00000 12

1 1

2 i

00040 5

1 1

3y 00040 1

2;CR2 3a 00000 1 1

5

00040 1 1

1 1

2

67070 1 1

65470 1

3f 00000 1

Antibiogramcode: 05470 = resistanceto gantrisin (G). kanamycin (K). neomycin(N),streptomycin(S),tetracycline(Te), triple sulfa(SSS);45472=

ampicillin (Am),G, K,N.S.Te,SSS,cephalothin(CF);04070=G.S.Te, SSS;

45470=Am,G.K. N.S.Te.SSS;05670=G. K.N.nitrofurantoin(F/M),S.

Te,SSS;04050=G. S.SSS;01460= K. N. S.Te; 24270=chloramphenicol

(C), G. F/M. S. Te, SSS;25470=C, G. K. N. S. Te, SSS;44072=Am.G. S. Te,SSS, CF;00000=noresistance;04010=G.SSS;00040=S:67070=Am,

C, G. gentamicin (Gm), K. S.Te,SSS;65470= Am. C. G. K. N.Te.SSS.

Birnboim-Doly plasmid extraction technique does not optimally recover verylarge plasmids.

real prevalence of Salmnonella infection among all animal

species, e.g., poultry andpigsarepoorly represented in the study. Our results, therefore, are most relevant in the context ofsalmonellosis in cattle and horses in New York State.

There are increasingly frequent examples of the clonal distribution ofplasmid-bearingentericpathogensthroughout

theworld(2, 24, 29-31, 33, 34). Ithas become apparentthat salmonellae or their plasmids, if present, may be clonal in nature. Although manyepidemiological studies of S. tvphi-mnuriumn have used PT, PT/BT, or plasmid profile in strain

differentiation,the present study combined fourphenotypic

and genotypic traits. PT, BT, plasmid profile, and antibio-gram,thatenabled ustoidentify widely dispersed clones of

S. typhilînuriuîn around New York State.

Clonal groups U275/26 and 49/26 were widespread and associated mainly with the cattle population. Evidence ofa clonalrelationship wasapparent from the matchingPT and

BT. The majority of strains within the U275/26 and 49/26

clones had similar plasmid profiles, but there was enough

variability in both plasmid profile and antibiogram to make thesetraits less usefulthan thecombination ofPTandBTin

supportingtheclonalnatureof the strains(Table6). Manyof

the U275/26 and 49/26 strains were isolated from calves,

especially veal calves. Perhaps the decline in

frequency

of

both of these clones after 1976 was associated with the decrease in veal calf salmonellosis observed in New York State after 1976 (17).

The

epidemiology

oftwoclones, 10/3 and 2/3. differed in many waysfrom that of both the U275/26 and 49/26 clones of S.

tîphiinuriuin.

The clonal natureof the strains of 10/3 and

2/3 was supportedbytheir common PTand BT characters.

Because most strains lacked

plasmids

andwere

susceptible

toantibiotics. thesefingerprintcharacterswereoflittle value

inestablishingaclonaldesignation.The absence ofplasmids

in the 10/3 and 2/3 clones may be attributed to the relative lackof antibiotics

given

toadultdairy cattle,whichwerethe

major sourcesof the 10/3clones and (along withhorses)the

2/3 clones. Incontrast. calves,whichwerethemajorsource of the U275/26 and 49/26

clones,

receive many more antimi-crobial agents at

prophylactic

levels in feed and also for

therapeuticreasons; the greater numberof

plasmids

and the

resistance antibiograms of these clones reflect this differ-ence.

Eightother different PT/BTcombinationswere of interest

because oftheirclonalnature. Theseclones

comprised

only

about 15% of the study isolates. Futuresurveillance should tell us whether they will become established in the animal

populations

in New York.

There is frequent traffic among animals and people be-tweenNew York and eastern Canada. Using methods simi-lartothose used inourstudy, Khakhria and Lior(26)phage

typed Canadian isolates of S.

tphlimuriuim

from humanand

animal sources

during

1969to 1976. PT 49, 10, 3 aerogenic, 6, and2 were mostcommonfrom human sources; and types

49, 123, 1, 3 aerogenic, and 10 were most common from

animals. All but4of the26 PTsfound inNew

York,

186. 771,

772, and U275, were commoninCanadian humanoranimal

isolates of S.

tvphimrnîriuni.

Until 1976, PT 49 was the most common typefrom animal andhuman sources inCanada; it

was then replacedby PT 10asthe most common Canadian

PT of S.

tvphlimîîriuni(

(25). A similar shift in

frequency

distribution occurred in New York, i.e., PTs 49 and U275 were verycommonupto 1976,whenthey were replaced by

types 10 and 2. PT U275 was not reported from animal sources in Canada.The occurrence ofthesame PTsinNew

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626 McDONOUGH ET AL.

York and Canada suggestsdissemination of the sametypes in thetworegions. It is unfortunate thatnodataareavailable from human isolates in New York during the time of this study tofurthershed lighton these observations.

Studies have noted that PT 49 was common throughout Britain and documented its spread from calvestothehuman population (7, 31, 33, 34). During the spread of PT 49, it acquired plasmids resulting in PT interconversion and the creation of PT 204 and, ultimately, PT 193. Biotyping showed that both PTs 49 and 204were regularly associated with asingle BT, 26, a fact that provided evidence that PT

interconversion had occurred in producing PT 204 from PT

49 (6, 7). It is unknown whether PT interconversion has occurred in any PTs of S. typhimurium from New York;

however, both PTs 49 and 204 have been found in New York Stateanimals.

In the Federal Republic of Germany, Brandis et al. (13) studied many strains of S. typhimurium from animals and humans. PTs 2 and 49were verycommoninhumans,as was

type49 in adult cattle, calves, and pigs. Also, Holmberget al.(24) usedanumberoftyping phagesof the Callowscheme tostudy strains of S. typhimurium from epidemics ofhuman disease in the United States. PTs 2 and CR10 (havingalysis

patternclosely resembling [CR] PT 10) accountedfor 15 and 21%, respectively, of the typable strains from humans. PTs 2 and 10 were themost common PTsin animals from New York in ourstudy after 1976. TheoccurrenceofthesePTs in

humanand animal disease outbreaks has important epidemi-ological implications.

Our studies of clonal groups of S. typhimurium found in animalpopulations in New Yorkcanthereforebecompared with those of othercountries and shouldserve as abasis for the study of future changes in the epidemiology of S. typhimurium infectionintheregion and forthefeasibilityof generating similar data on strains of S. typhimurium from humans.

ACKNOWLEDGMENTS

Thisresearchwassupported by funds provided bythe New York

State Department ofAgriculture and Markets through aGraduate

Research Assistantship awardedtoP.L.M. bythe Diagnostic Lab-oratory.

We thank D. Duck of the Phage Typing Centre, Laboratory Centre forDiseaseControl, Health andWelfare, Ottawa, Ontario, Canada, for phage typing; B. Blackburn and K. Sutch of the

NationalVeterinary Service Laboratories,Animal and Plant Health

Inspection Service, U.S. DepartmentofAgriculture, Ames, Iowa,

for serotyping Salmonella isolates; and D. Downing of the New

York StateDiagnostic Laboratoryfordesigningacomputerprogram

for theanalysisof thetartaric acidturbiditytestsof the BT studies. LITERATURECITED

1. Alfredsson, G.A.,R. M.Barker, D. C.Old,andJ.P.Duguid. 1972. Useof tartaric acid isomersandcitricacid in thebiotyping

ofSalmonella typhimurium. J. Hyg.70:651-666.

2. Anderson, E.S., E. J. Threlfall, J.M.Carr,M. M.McConnell,

and H.R. Smith. 1977.Clonal distributionof resistance plasmid-carryingSalmonellatyphimurium, mainlyin the Middle East. J.

Hyg. 79:425-448.

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