JOURNAL OF CLINICAL MICROBIOLOGY, Sept. 1987, p. 1668-16740095-1137/87/091668-07$02.00/0Copyright ©ç 1987, American Society for Microbiology

Epidemiologic Factors Affecting Antimicrobial Resistance ofCommon Bacterial Isolates

PAUL D. ELLNER,1* DANIEL J. FINK,' HAROLD C. NEU,2 AND MICHAEL F. PARRY3

Clinical Microbiology and Laboratory Information Services, The Presbyterian Hospital,' and Division of InfectiousDiseases, Department of Medicine, College of Physicians and Surgeons, Columbia University,2 New York, New York

10032, and The Stamford Hospital, Stamford, Connecticut 069023

Received 17 February 1987/Accepted 4 June 1987

The pattern of antimicrobial resistance ofcommon bacterial isolates obtained from various groups of patientsat a large tertiary-care center was compared with the pattern of resistance seen at a primary-care communityhospital. At the tertiary-care center, significant differences in susceptibility were seen between pediatric andadult groups. In the tertiary-care center, the inpatients were more likely than the outpatients to have resistantstaphylococcal and enterobacterial strains. Comparison of the overall resistance at the tertiary-care center andthe primary-care hospital showed that resistance to cephalosporins, piperacillin, and aminoglycosides wassignificantly higher at the tertiary-care hospital than at the community hospital. Striking differences were notedin the resistance of nosocomial Enterobacter and Citrobacter isolates. Hospitals should be cautious inextrapolating nationwide data to their particular institutions.

The antimicrobial resistance of common pathogenic bac-teria has been noted to vary from one hospital to another. Inone instance, a 6- to 14-fold difference in resistance toantibiotics was observed between a general hospital inBoston and a similar institution in Paris (9). However, arecent study by Atkinson and Lorian (2) suggested that therehas not been any major increase in bacterial resistance in thepast several years. Data from The National NosocomialInfections Study suggest that there are resistance differencesamong hospitals (5).

We- became interested in studying subgroups of the popu-lation of patients in our area of the northeastern UnitedStates, with reference to the role that age and inpatient oroutpatient status in a large tertiary-care hospital has onresistance patterns and what role attendance at a communityhospital versus a large tertiary-care center may play in theprevalence of resistance to frequently used antimicrobialagents.The present study compares differences in prevalence of

resistance among various groups of patients at The Presby-terian Hospital in New York, N.Y. (PH), a 1,200-bed urbantertiary care center, with patterns of resistance seen inpatients at The Stamford Hospital (SH), a primary-caregeneral community hospital of 318 beds in Stamford, Conn.It also analyzes the differences in susceptibility patternsencountered in the different departments of a large tertiary-care hospital.

MATERIALS AND METHODS

All organisms tested were fresh clinical isolates obtainedfrom patients at PH and SH. Specimens were processed on

commercially prepared media (Scott Laboratories, Fiske-ville, R.I.; BBL Microbiology Systems, Cockeysville, Md.),except for the broth used to prepare the inoculum for MICdetermination. This broth was prepared in-house from de-hydrated material (Scott Laboratories). Bacteria recoveredwere identified by standard recommended procedures (8).Isolates that were obvious contaminants were not included

* Corresponding author.

in this study (e.g., coagulase-negative staphylococci fromnormally colonized anatomic sites).Methods for the determination of the MICs for the bacte-

rial strains were identical in both hospitals and used frozen,prediluted microdilution trays containing antibiotics appro-priate for gram-positive or gram-negative organisms(MicroScan, Mahwah, N.J.). Control strains run at bothinstitutions to ensure similarity of results were Staph-ylococcus aureus ATCC 25923, Escherichia coli ATCC25922, and Pseudotnonas aeruginosa ATCC 27853. Purecultures of each isolate (2 to 10 colonies) were inoculatedinto 0.5 ml ofbrain heart infusion broth, incubated for 2 to 4h at 35°C, and then adjusted to a turbidity approximating the0.5 McFarland standard. A 0.5-ml quantity of this standardsuspension was added to 25 ml of sterile water with 0.02%Tween 80, and this suspension was used to inoculate thewells of the microdilution tray so that each well containedapproximately i05 CFU/ml of Mueller-Hinton broth. Brothin the methicillin wells was supplemented with 1.5% sodiumchloride. Trays were incubated for 15 to 18 h at 35°C, and theMICs were determined by reading the trays visually or byautomated densitometry using the Autoscan 3, an instrumentthat displays the identification of the organism as well as theMICs (1, 3, 7).Each tray contained sterility and growth control wells, and

stock cultures of control organisms were included in the runeach day.For the purposes of this report, organisms were consid-

ered resistant if MICs (in micrograms per milliliter) were

equal or greater than 0.25 for penicillin; 16 for methicillin; 4for clindamycin, erythromycin, and vancomycin; 8 forgentamicin and tobramycin; 16 for ampicillin, cephalothin,cefoxitin, cefamandole, and amikacin; 32 for cefotaxime; 128for carbenicillin and piperacillin; and 2/38 for trimethoprim-sulfamethoxazole (TMP-SMX). These are based on the Foodand Drug Administration (FDA)-approved concentrations as

listed in the package inserts for each antimicrobial agent.Cephalothin resistance was assumed for methicillin-resistantS. aureus. Organisms were considered to be community-acquired outpatient isolates if they were from cultures sentfrom the outpatient clinics. Isolates from replicate or multi-

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FACTORS AFFECTING RESISTANCE OF BACTERIAL ISOLATES 1669

ple cultures were scanned by the computer for genus,species, and antibiogram, and only the initial isolate wasused for analysis of the data.Data were collected during 1 year and were tested for

statistically significant differences by using a z test forcomparison of proportions when two groups were evaluatedand the chi-square test when more than two groups wereexamined (6).

RESULTS

S. aureus. S. aureus showed more resistance to penicillinamong the infants than in any other age group (Table 1).Only 10% of both inpatient and outpatient isolates weresusceptible to penicillin G (Table 2). Furthermore, 39% ofrespiratory S. aureus isolates were resistant to erythromy-cin, compared with less than 10% resistant to clindamycin.There were no statistically significant differences among thevarious age groups in susceptibility to the other drugs tested.Methicillin resistance was found for 6 to 10% of isolates.Resistance to methicillin, cephalothin, erythromycin, andclindamycin was greatest in the urine isolates (Table 3).Inpatient isolates showed more resistance to erythromycinthan did outpatient isolates. Cephalothin resistance did notvary between inpatient and outpatient isolates and wassimilar between PH and SH patients (Table 4).

Coagulase-negative staphylococci. Most strains of coagu-lase-negative staphylococci collected were probably etio-logic agents of nosocomial bacterial endocarditis, surgicalinfections of total hip replacements, sternotomy wounds,etc., and infected ventriculoatrial shunts. Obvious contami-nants were not included, and susceptibility data were notcollected on isolates from wounds unless the physicianbelieved that coagulase-negative staphylococci were a sig-nificant part of the-infection.

Significantly more resistance was seen to penicillin,methicillin, erythromycin, and clindamycin in the neonatalgroup than in other age groups. In contrast to S. aureus, thegreatest resistance of coagulase-negative staphylococci topenicillin, methicillin, and erythromycin occurred in upper-respiratory-tract isolates.

Strains from cerebrospinal fluid, other body fluids, andtissue biopsies had a high incidence of methicillin resistance,with 41% of cerebrospinal fluid isolates resistant to methicil-lin (Table 3). Inpatient strains were more resistant to all ofthe drugs tested than were outpatient isolates, and extremelyhigh resistance to clindamycin (41%) and erythromycin(53%) was noted for the inpatient isolates (Table 2). Eryth-romycin resistance was significantly higher in PH patientsthan in SH patients (Table 4).

E. coli. More ampicillin and carbenicillin resistance wasseen in younger subjects than in older patients (Table 1). OfE. coli samples isolated from children between the ages of 6months and 6 years, 58% were resistant to ampicillin and41% were resistant to cephalothin. Respiratory-tract isolateswere more resistant to these drugs than were strains fromother body sites (Table 3). There were no major differencesbetween outpatients and inpatients, but significantly moreresistance was seen in PH patients than in SH patients(Table 4). More than 30% of urinary isolates were resistantto ampicillin, and 27% were resistant to cephalothin, butresistance to ampicillin and cephalothin was found for iso-lates from all body sites (Table 2). Most E. coli isolates fromboth hospitals were susceptible to cefoxitin, and all weresusceptible to cefotaxime. A striking difference in piperacil-lin susceptibility was observed between PH (76%) and SH

(97%) patients, and for cefamandole, a difference was alsoobserved between PH (87%) and SH (100%) patients.

Infants showed the most resistance to gentamicin, andmore gentamicin resistance was seen in upper-respiratory-tract isolates collected in evaluation of pneumonitis in thispopulation of patients. But in general, the E. coli isolateswere susceptible to gentamicin, in contrast to the highbeta-lactam resistance.More resistance to cephalosporins was seen in the 6-

month to 6-year group than in any other age group, and themost resistance was found in respiratory-tract strains. Atboth institutions, there was minimal resistance of E. coli toTMP-SMX.

Klebsiella species. Klebsiella species studied includedKlebsiella pneumoniae and Klebsiella oxytoca. It was ofinterest that the infant group showed the greatest resistanceto gentamicin, with 24% of isolates from newborns andpatients less than 6 months of age. However, only 9% ofKlebsiella isolates from patients older than 65 years wereresistant to gentamicin. All age groups contained Klebsiellaisolates resistant to cephalothin, ranging from 19 to 29% ofisolates. Urinary and respiratory-tract isolates showed sim-ilar resistance patterns (Table 3). Resistance of Klebsiellaspp. to cefamandole at PH was as common as resistance toolder cephalosporins, with upper-respiratory-tract strainsmore resistant than those from other body sites. Overall,there were more gentamicin- and cephalothin-resistant iso-lates in inpatients. Klebsiella strains from SH were almostuniformly susceptible to cephalosporins and aminoglyco-sides, in contrast to the significant resistance of the PHisolates. For example, only 2% of SH isolates were resistantto piperacillin and 74% of PH isolates were resistant. Some13% of PH isolates were resistant to cefoxitin, and almost allSH isolates were susceptible. Furthermore, 13% of Klebsi-ella isolates at PH were resistant to TMP-SMX and only 2%at SH were resistant.

Enterobacter species. The Enterobacter isolates, whichincluded Enterobacter cloacae and Enterobacter aerogenes,at PH were extremely resistant, with 39% of isolates encoun-tered in children younger than 6 months resistant togentamicin and 56% resistant to carbenicillin (Table 1).Much less resistance to gentamicin was found in the Entero-bacter isolates from the patients more than 65 years old thanin the isolates from neonates, whereas resistance to carbeni-cillin and cefamnandole was similar for all age groups. Bloodisolates of Enterobacter spp. showed roughly as high orhigher resistance than did isolates from other sites (Table 3).The differences in susceptibility of Enterobacter spp. be-tween isolates from PH and SH were marked, with only 1%of isolates at SH resistant to piperacillin, 5% resistant tocefotaxime, and none resistant to gentamicin, whereas at PH33% of isolates were resistant to piperacillin, 32% wereresistant to cefotaxime, and 17% were resistant to genta-micin (Table 4). Very few strains were resistant to amikacinat either institution, but at PH many Enterobacter isolates(15%) were TMP-SMX resistant.

Serratia marcescens. The Serratia isolates showed signifi-cant resistance to beta-lactams and aminoglycosides (Table1). Gentamicin resistance was most common in the <6-month age group, and carbenicillin resistance was mostcommon in patients 6 to 16 years old. Outpatient isolateswere less commonly resistant than inpatient isolates, buteven in the outpatient isolates, 49% were resistant to car-benicillin and 98% were resistant to cefoxitin. Marked dif-ferences between the isolates at PH and SH were found forsusceptibility to carbenicillin, piperacillin, gentamicin, and

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1670 ELLNER ET AL.

TABLE 1. Susceptibility of common isolates in different PH age groups% Resistant at patient age:

Organisms) and drug <6 mo 6 mo-6 yr 6-16 yr 16-65 yr >65 yr

S. aureus(No. of strains) (281) (164) (291) (1,329) (355)Penicillin 98 93 89 89 88"Methicillin 6 8 7 8 7Cephalothin 3 3 3 5 3Erythromycin 22 19 18 19 19Clindamycin 6 4 8 7 7

Coagulase-negative staphylococci(No. of strains) (179) (107) (101) (530) (179)Penicillin 88 72 74 75 76aMethicillin 68 31 40 34 46"Cephalothin 8 3 7 7 12Erythromycin 60 39 50 45 50Clindamycin 44 24 36 29 39

E. coli(No. of strains) (231) (309) (676) (2,906) (1,371)Ampicillin 45 58 31 32 29aGentamicin 10 6 4 4 5c'Cephalothin 36 41 26 25 25aCarbenicillin 49 58 37 36 33"Cefoxitin 10 il 9 8 ilCefamandole 24 32 16 14 10"

Klebsiella spp.(No. of strains) (111) (104) (260) (715) (515)Ampicillin 95 97 94 96 93Gentamicin 24 20 18 10 9"Cephalothin 21 23 29 19 22Carbenicillin 99 98 97 98 97Cefoxitin 15 15 19 15 18Cefamandole 20 20 26 18 19

Enterobacter spp.(No. of strains) (65) (37) (191) (582) (390)Ampicillin 81 80 90 88 90Gentamicin 39 13 17 15 l0Cephalothin 93 87 96 92 94Carbenicillin 56 47 50 42 41Cefoxitin 93 93 93 94 949Cefamandole 59 40 55 50 54

Serratia marcescens(No. of strains) (24) (2) (100) (165) (150)Ampicillin 95 98 97 90"Gentamicin 37 il 15 15Cephalothin 100 98 99 99Carbenicillin 47 69 47 45aCefoxitin 89 95 97 93Cefamandole 84 95 94 92

Proteus mirabilis(No. of strains) (11) (33) (138) (495) (336)Ampicillin 0 19 15 10 10Gentamicin 0 12 2 6 5Cephalothin 0 16 10 8 10Carbenicillin 0 22 14 10 11Cefoxitin O 9 8 8 8a

Cefamandole 0 12 9 6 8

P. aeruginosa(No. of strains) (46) (60) (400) (895) (727)Gentamicin 45 46 55 54 52Carbenicillin 41 39 40 36 37Tobramycin 10 12 23 20 19Amikacin 23 16 24 22 19

" Significant difference, P < 0.01 by chi-square test.

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FACTORS AFFECTING RESISTANCE OF BACTERIAL ISOLATES 1671

TABLE 2. Comparison of susceptibilities of common isolatesfrom PH outpatients and inpatients

% ResistantOrganism(s) and drug Outpatient Inpatient

S. aureus

(No. of strains)PenicillinMethicillinCephalothinClindamycinErythromycin

(1,166)90

7

4

6

15

Coagulase-negative staphylococci(No. of strains)MethicillinCephalothinClindamycinErythromycin

E. coli(No. of strains)AmpicillinGentamicinCephalothinCarbenicillinCefoxitinCefamandole

Klebsiella spp.(No. of strains)AmpicillinGentamicinCephalothinCarbenicillinCefoxitinCefamandole

Enterobacter spp.(No. of strains)AmpicillinGentamicinCephalothinCarbenicillinCefoxitinCefamandole

Serratia marcescens(No. of strains)AmpicillinGentamicinCephalothinCarbenicillinCefoxitinCefamandole

Proteus mirabilis(No. of strains)AmpicillinGentamicinCephalothinCarbenicillinCefoxitinCefamandole

(351)2741738

(2,681)313

24358

13

(451)95

s

17981415

(184)803

86308933

(61)989

98499895

(333)8s

6il86

(1,254)90948

22a

(745)49`9a

4la

53a

(2,8 12)35"6a

29a39alia16"

(1,254)95la

24a

981822a

(1,081)goa

17a94a

47"95a56a

(380)94179966'9492

(680)13aEs10"

1288

P. aeruginosa(No. of strains) (427) (1,701)Gentamicin 48 55"Carbenicillin 36 38Tobramycin 16 21"Amikacin 17 22a

aSignificant difference, P < 0.01 by chi-square test.

cefoxitin. At both institutions, most organisms were suscep-tible to cefotaxime, amikacin, and TMP-SMX.

Proteus mirabilis. It was interesting that 19% of P. mirabilisisolates from children 6 months to 6 years old were resistantto ampicillin and that 13% of the inpatient isolates wereresistant to gentamicin (Tables 1 and 2). No statisticaldifferences in resistance by body site were noted, butinpatient isolates showed greater resistance to ampicillin andcephalothin. P. mirabilis isolates from SH were susceptibleto virtually all agents, in contrast to the resistance seen atPH, with the most important differences seen for ampicillinand piperacillin.The other Proteus species were infrequently encountered

at SH compared with PH, and marked differences in suscep-tibilities were seen for cefamandole and cephalothin.

P. aeruginosa. Resistance of P. aeruginosa to gentamicinwas found in all age groups at PH (Table 1). Few P.aeruginosa organisms were isolated from children, com-pared with the large numbers from adults; 45 to 55% ofisolates were resistant to both gentamicin and carbenicillin.Interestingly, resistance to gentamicin was noted for all bodysites (Table 3). Particularly high resistance was found amongthe respiratory-tract isolates; this finding was probably re-lated to the large cystic fibrosis population at PH and thelarge number of intensive-care-unit patients. A total of 25%of lower-respiratory-tract isolates and 22% of urinary iso-lates were resistant to amikacin. At PH, there was highresistance to gentamicin and carbenicillin for both the inpa-tient and the outpatient isolates (Table 2). At SH, 90% of theisolates were susceptible to all five agents tested, whereas atPH 21% were resistant to tobramycin, 38% were resistant tocarbenicillin, and 16% were resistant to piperacillin (Table4).

Other organisms. Differences in susceptibility of Ci-trobacter species were noted between PH and SH (Table 4).For example, at SH 99% of Citrobacter species were sus-ceptible to piperacillin, and only 50% were susceptible atPH. Similar differences were noted for other beta-lactamsand for gentamicin as well. Indeed, for Citrobacterfreundii,which was the most frequent isolate, all at SH were suscep-tible to cefotaxime, but 26% were resistant at PH, and 17%were resistant to TMP-SMX.

DISCUSSION

It is logical to question why the differences in susceptibil-ity noted in this article occurred. First, the high prevalenceof resistance among the infant population at PH probably isa reflection of the fact that the majority of these patientswere neonates in the intensive care unit who were receivingvarious antimicrobial agents. Increased resistance was alsonoted in coagulase-negative staphylococcal and enterobac-terial upper-respiratory-tract isolates, particularly in the6-month to 6-year group. This may be a reflection of the useof oral agents in the patients before they are admitted to thehospital. Respiratory-tract isolates of P. aeruginosa showedmore resistance to gentamicin than did strains from othersites. Most ofthese Pseuidomonas strains were from patientsin intensive-care units and patients with cystic fibrosis.

Inpatients were more likely to have resistant staphy-lococcal and enterobacterial strains than were outpatients.There were striking differences between community hospitalpatients and the population of the tertiary-care hospital; theprevalence of resistance was significantly higher in the latterinstitution to cephalosporins, piperacillin, aminoglycosides,and even to the broad-spectrum cephalosporin cefotaxime.

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TABLE 3. Susceptibility of common organisms by anatomic site in samples from PH

% Resistant in sample from:

Organism(s) and drug Upper Lower Body CerebrospinalUrine respiratory respiratory Blood fluids fluid Tissue

tract tract

S. aureus(No. of strains)PenicillinMethicillinCephalothinErythromycinClindamycin

Coagulase-negative staphylococci(No. of strains)PenicillinMethicillinCephalothinErythromycinClindamycin

E. coli(No. of strains)AmpicillinGentamicinCephalothinCarbenicillinCefoxitinCefamandole

Klebsiella spp.(No. of strains)AmpicillinGentamicinCephalothinCarbenicillinCefoxitinCefamandole

(310)9013133317

(385)7740125332

(4,495)334

27379

15

(1,016)961426981823

(165)96104186

(76)95797

6246

(65)57il38589

23

(44)983021100

726

(290)8763

217

(153)8841

153

(7) (271)69294

3827

(159)388

32451320

(280)946

15981814

(139)252

26287

13

(73) (42)84 957 10

16 1894 10012 2115 18

Enterobacter spp.(No. of strains)AmpicillinGentamicinCephalothinCarbenicillinCefoxitinCefamandole

(461)871892549160

Serratia marcescens

(No. of strains)AmpicillinGentamicinCephalothinCarbenicillinCefoxitinCefamandole

(133)991898509493

Proteus mirabilis(No. of strains)AmpicillinGentamicinCephalothinCarbenicillinCefoxitinCefamandole

(606)il7

1013109

P. aeruginosa(No. of strains)GentamicinCarbenicillinTobramycinAmikacin

(1,063)51403022

(29)85351004510043

(17)10017

100179292

(10)10OOOOO

(40)51331913

(327)91il97349541

(128)9516

100619898

(111)144121356

(573)62411325

(68) (41)88 6124 2988 7945 6195 9658 64

(50) (15)86 1004 il

96 10036 3389 10082 100

(20) (10)s oO O5 o5 105 10s o

(28) (43)46 5328 377 32

12 26" Significant difference, P < 0.01 by chi-square test.

1672

(10)100101010O

(925)906"2"'

18"6a

(13)7773

236

(28)8961145050

(87)348

30371323

(70)71414

4933

(6)

(0)

(122)81"43"6"

42"34

(330)29"6"

2133a6

11"

(156)94"13"20"97il17

(1)

(3)

(0)

(0)

(254)88"10'95"349748"

(56)92"il

10058"9294"

(198)il4610s4

(278)48"26"5"

15"

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FACTORS AFFECTING RESISTANCE OF BACTERIAL ISOLATES 1673

TABLE 4. Comparison of susceptibilities of common isolatesfrom a community hospital (SH) and a tertiary-care center (PH)

% Resistant from:Organism(s) and drug PH SH

S. aureus(No. of strains)PenicillinNafcillinCephalothinErythromycinClindamycinTMP-SMX

(1,418)9054

2185

Coagulase-negative staphylococci(No. of strains)PenicillinNafcillinCephalothinErythromycinClindamycinTMP-SMX

E. coli(No. of strains)AmpicillinCaraenicillinPiperacillinCephalothinCefoxitinCefamandoleCefotaximeGentamicinAmikacinTMP-SMX

Klebsiella spp.(No. of strains)AmpicillinCarbenicillinPiperacillinCephalothinCefoxitinCefamandoleCefotaximeGentamicinAmikacinTMP-SMX

Proteus mirabilis(No. of strains)AmpicillinCaraenicillinPiperacillinCephalothinCefoxitinCefamandoleCefotaximeGentamicinAmikacinTMP-SMX

Other Proteus spp.(No. of strains)AmpicillinCarbenicillinPiperacillinCephalothinCefoxitinCefamandoleCefotaxime

(852)79248

513916

(3,068)373624308

13o648

(1,361)9590742413175166

13

(704)137

27il57o675

(274)91158

941663o

(377)84"6O"13"7la

(201)61"2413'40"3514

(974)21"19"3"5'o"oa

0'0"la

(359)68"58a2"5"la

0"oa1'0"2"

(240)6a1"0"140"0"o0"1"1'

(14)100"

7O

29"

0"o

TABLE 4-Continiied

Organism(s) and drug

GentamicinAmikacinTMP-SMX

Acinetobacter spp.(No. of strains)AmpicillinCarbenicillinPiperacillinCephalothinCefoxitinCefamandoleCefotaximeGentamicinAmikacinTMP-SMX

% Resistant from:

PH SH

10 04 0

il 0

(193)7183

100939422228

12

Citrobacter spp.(No. of strains)AmpicillinCarbenicillinPiperacillinCephalothinCefoxitinCefamandoleCefotaximeGentamicinAmikacinTMP-SMX

(59)25"3O

978583"3a3"O2'

(407)8155508175342614617

P. aeruginosa(No. of strains)CarbenicillinPiperacillinGentamicinTobramycinAmikacin

(1,761)3816552122

Enterobacter spp.(No. of strains)AmpicillinCarbenicillinPiperacillinCephalothinCefoxitinCefamandoleCefotaximeGentamicinAmikacinTMP-SMX

(73)66"17"1"

44"46"13"0"0"o8

(318)11"1"

11"5"5"

(233)76"13"1"

81"89"20"5a0"0"1

(1,126)89363394945132173

15

Serratia marcescens(No. of strains)AmpicillinCarbenicillinPiperacillinCephalothinCefoxitinCefamandoleCefotaximeGentamicinAmikacinTMP-SMX

(398)9536149973916

1797

(70)71"15"2"

91"32"44"2"5"s0'

" Significant difference, P < 0.01 by chi-square test.

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1674 ELLNER ET AL.

It is extremely interesting that at a community hospital themajority of organisms remained susceptible to many of thecurrently used antimicrobial agents. Some important resis-tances at a community hospital are to be noted. For exam-ple, 21% of E. coli isolates were resistant to ampicillin at SH,compared with 37% that were resistant to ampicillin at PH.Twenty-four percent of the E. coli strains at PH wereresistant to piperacillin, whereas only three percent of the E.<oli isolates were resistant at SH. It is also interesting that13% of E. coli isolates at the university hospital wereresistant to cefamandole and 8% were resistant to cefoxitin,while none of the E. coli isolates at the community hospitalwere resistant to these agents.The Klebsiella isolates provide another example of

marked differences in susceptibility between communityhospitals and university centers. The university hospitalisolates showed a high resistance to broad-spectrum penicil-lins such as piperacillin, whereas most isolates at the com-munity hospital were susceptible. Resistance to broad-spectrum cephalosporins such as cefoxitin and cefamandolewas seen at the university hospital, whereas virtually allstrains were susceptible in the community hospital. Similardifferences were noted for the aminoglycosides and forTMP-SMX, with many Klebsiella isolates at the tertiary-carecenter resistant to gentamicin.

Respiratory-tract isolates of members of the Enterobac-teriaceae showed fairly high resistance at the universityhospital. This finding is probably related to the large numberof intensive-care units in the institution and the type ofpatients maintained in these units. These patients frequentlyhad received many antimicrobial agents, had often beentransferred from other institutions, and frequently remainedin the hospital for long periods.A striking example of differences in resistance between a

community hospital and the university hospital was notedfor species such as Enterobacter and Citrobacter. At thecommunity hospital, these important "new" pathogens wereuniformly susceptible to cefotaxime, a broad-spectrum ceph-alosporin, but at PH, for 40% of E. cloacae and 28% of E.aerogenes isolates cefotaxime MICs were greater than 8p.g/ml, and for 27% of C. freuIndii isolates cefotaxime MICswere greater than 8 1tg/ml. Furthermore, many of the En-terobacter and Citrobacter isolates at the university hospitalwere resistant to gentamicin and TMP-SMX. Recently, anEnterobacter outbreak was noted in a neonatal-intensive-care unit at another institution that had switched to cefotax-ime because of extensive resistance to gentamicin (4).

Whether these marked differences in resistance are causedby antibiotic usage or result from the type of patients is notestablished.

Surveillance studies such as this are beneficial to theindividual hospital. They can be used to select the antimi-crobial agents which should be included in the formulary ofthat hospital. It is also possible based on studies such as thisto point out to individual services that they may or may nothave a particular problem with resistant organisms and todevelop methods to alter resistance patterns. Hospitalsshould be cautious in interpreting nationwide data on resist-ance patterns or in extrapolating data frequently shown inadvertisements to their particular institution. The data fromthe National Nosocomial Surveillance Study (8) are ex-tremely helpful but may not reflect the resistance patterns ofa part or the whole institution because of local factors relatedto both antibiotic use and the type of patients.

LITERATURE CITED1. Aldridge, K. E., A. Janney, C. V. Sanders, and R. L. Marier.

1983. Interlaboratory variation of antibiograms of methicillin-resistant and methicillin-susceptible Siaphvlococcus aureusstrains with conventional and commercial testing systems. J.Clin. Microbiol. 18:1226-1236.

2. Atkinson, B. A., and V. Lorian. 1984. Antimicrobial agent sus-ceptibility patterns of bacteria in hospitals from 1971 to 1982. J.Clin. Microbiol. 20:791-796.

3. Boyce, J. M., L. S. Lytie, and D. A. Walsh. 1984. Detection ofmethicillin-resistant Staphl'/ococcus aureus by microdilution anddisk elution susceptibility systems. J. Clin. Microbiol. 20:1068-1075.

4. Bryan, C. S., J. F. John, Jr., M. S. Pai, and T. L. Austin. 1985.Gentamicin vs cefotaxime for therapy of neonatal sepsis: rela-tionship to drug resistance. Am. J. Dis. Child. 139:1086-1089.

5. Centers for Disease Control. 1985. National nosocomial infectionsstudy: 1984 study report (July 1985). Centers for Disease Control,Atlanta.

6. Colton, T. 1974. Statistics in medicine. Little, Brown, & Co..Boston.

7. DeGirolami, P. C., K. A. Eichelberger, L. C. Salfity, and M. F.Rizzo. 1983. Evaluation of the AutoSCAN-3, a device for readingmicrodilution trays. J. Clin. Microbiol. 18:1292-1295.

8. Lennette, E., A. Balows, W. A. Hausier, Jr., and H. J. Shadomy(ed.). 1985. Manual of clinical microbiology, 4th ed. AmericanSociety for Microbiology, Washington, D.C.

9. O'Brien, T. F., J. F. Acar, A. A. Medeiros, R. A. Norton, F.Goldstein, and R. L. Kent. 1978. International comparison ofprevalence of resistance to antibiotics. J. Am. Med. Assoc.239:1518-1523.

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