The Epidemiology of 2056 Remote Site Infections and 1966Surgical Wound Infections Occurring in 1865 Patients:

A Four Year Study of 40,923 Operations atRush-Presbyterian-St. Luke's Hospital, Chicago

L. D. EDWARDS, M.D.*

Over a 4-year period 40,923 operations and 44,716 surgical admis-sions were monitored for both community and hospital onsetinfections. One thousand eight hundred sixty-five patients had1966 surgical wound infections and 2056 remote infections in-cluding 1652 hospital onset and 404 community onset infections.One thousand one hundred forty-four patients with multipleinfections averaged 40 days in the hospital contrasted with 24days for 721 patients with a single wound infection. The totalexcess cost of hospitalization for these patients was $951,150.A statistically significant reduction occurred for urinary tract in-fections, lower respiratory infections and clean and contaminatedsurgical wound infections. It is suggested that these are all inter-related and a significant reduction in surgical wound infectionscan be achieved through control of infections at remote sites,particularly those associated with medical devices. The coagulasepositive staphylococcus is still the most important single bacterialspecies in the primary etiology of surgical wound infections.When the gastrointestinal tract is entered or "supra" infectingorganisms appear, gram negative bacteria and mixed gram nega-tive and gram positive infections are dominant. Reduction inremote site infections occurring in surgical patients is necessaryto reduce the incidence of surgical wound infections, suggest pre-ventive and control measures, and document the effectivenessof such measures.

N UMEROUS STUDIES on surgical wound infection haveappeared in the literature. Perhaps the most

thorough and comprehensive study in this country was a

Submitted for publication February 16, 1976.* Director, Infectious Disease Service, Rockford School of Medicine,

1601 Parkview Avenue, Rockford, Illinois 61101. Formerly HospitalEpidemiologist and Assistant Director, Infectious Disease Section,Rush Medical College and Rush-Presbyterian-St. Luke's Hospital,Chicago, Illinois.

From the Rush Medical College andRush-Presbyterian-St. Luke's Hospital,

Chicago, Illinois

cooperative study between five university centers on 14,854patients with 15,613 operative wounds reported in thisjournal over a decade ago.'

Results of that study indicated that use of ultravioletlight did not significantly alter the wound infection rate(7.5% in the study group versus 7.4% in the control group).Variables shown to adversely affect wound infection rateswere: hospital involved (3.0-11.7%), age, obesity, useof steroids, prolonged preoperative hospitalization andprophylactic antimicrobial use.An additional variable noted in that study as well as one

reported from South Africa, that adversely affected thewound infection rate, was infection at a site remote fromthe wound. With such an infection at a remote site theformer study reported an increased rate of 2.7 times(18.4% versus 6.7%) and the latter study an increasedrate of 5.3 times (31.6% versus 6.0%o).17

Results reported here from our ongoing monitoringsystem of all infections in hospitalized patients at Rush-Presbyterian-St. Luke's Hospital from 1969 through 1972may shed some light on this problem. This report de-scribes an analysis of 2056 remote infections occurring in1865 patients with 1966 surgical wound infections duringthe four-year study period.10,11

758

EPIDEMIOLOGY OF REMOTE SITE INFECTIONS

Methodology

Standardized criteria were used for all sites of infec-tion.10"1 Data were continuously collected while the pa-tient was in the hospital by three full-time nurse epidemi-ologists who surveyed all infections in this 840-bedhospital. Before embarking on the surveillance study astudy designed to validate the ability of the nurse epi-demiologists to collect and record such data found them tobe as accurate as physicians with training in infectiousdiseases, i.e., no significant difference when subjected toChi Square analysis.10

Classical signs and symptoms were used to evaluatewound infections including the type and character ofdrainage, warmth and erythema. Stitch abscesses were

included when they were recorded on the chart, an infre-quent occurrence. Such lesions were deemed importantbecause of their potential for spread to other more suscep-tible hosts even though they may not be detrimental tothe patient in question.

Operations were classified as: Refined-Clean -thoseoperations where no risk of infection was encounteredother than incision through clean skin; Clean-thoseoperations where an added risk such as removal of a non-

infected organ occurred; Contaminated-those opera-

tions involving transection in the respiratory, gastro-intestinal or genitourinary tract; and Dirty -those opera-

tions involving a known infected site or ruptured viscus.Community Onset Infections (COI) were defined as

those present on admission or which became clinicallymanifest in the first 72 hours and were not related to a

hospital procedure. Hospital Onset Infections (HOI) were

defined as those which became clinically manifest after72 hours or were related to a hospital procedure in thefirst 72 hours. Prophylactic antimicrobials were thosegiven for the purpose of preventing an infection. Empiricantimicrobials were those given for poorly defined rea-

sons. Therapeutic antimicrobials were those given forspecific treatment of a clinically documented infection.Diseases and therapeutic modalities known to predisposeto infection were also monitored.

Results

Of 44,716 adult and pediatric surgical admissions7.3% had COI and 11.5% had HOI. The HOI rate (infec-tions/admissions x 100) was 16.6 or an average of 1.4HOI per infected patient (Table 1).COI (infected patients/admissions x 100), HOI (in-

fected patients/admissions x 100) and HOI (infections/admissions x 100) declined significantly during the studyperiod (Chi Square = 57.6, 27.9 and 119.3 respectively;all three P values were <0.001).One thousand one hundred forty-four patients of the

1865 with surgical wound infections (61.3%) had 1652

TABLE 1. Infection rates

Community Onset Hospital Onset Hospital OnsetYear Infections* Infections* Infectionst

1969 7.9 12.4 18.61970 8.4 12.0 18.21971 6.9 1 1.5 15.91972 6.0 10.3 13.9

Average 7.3 11.5 16.6

* Infected patients/admission x 100.t Infections/admissions x 100.

other HOI and 404 COI. Seventy-five per cent of theseremote sites of infection were broken down as follows:urinary tract-29.8%, lower respiratory tract- 24.9%,gastrointestinal tract 10.9%, and bacteremia-9.4%(Table 2). A statistically significant decline in urinarytract infections (Chi Square = 33.8, P < 0.001), lowerrespiratory infections (Chi Square = 8.5, P < 0.05) andgastrointestinal infections (Chi Square = 33.9, P< 0.001) occurred over the 4-year period.The site of origin of 27.5% of the bacteremias could

not be determined. The site of origin of other quantita-tively significant HOI bacteremias were: urinary tract-

TABLE 2. Remote Site of Infection in 1144 Patients Wit/i /652Hospital Onset Infections and 404 Community Onset Infe(ctions

in Addition to the Primary Suirgical Wound Inj'ection

Place of Onset ofInfection

Remote Site of Infection Hospital Community Total

Urinary tract 493 120 613 (29.8)*Lower respiratory tract 461 51 512 (24.9)Gastrointestinal tract 141 83 244 (10.9)Bacteremia from:

Site undetermined 50 3 53Gastrointestinal tract 41 6 47Surgical wound 39 39Urinary tract 21 2 23Intravenous cathetersand cutdowns 21 21

Lower respiratorytract 9 0 9

Mu sculoskeletalsystem 0 1 1

Total bacteremia 181 12 193 (9.4)Cutaneous (other than

surgical wound) 65 47 112 (5.4)Eye,ear,noseandthroat 80 32 112 (5.4)Additional surgicalwound 101 101 (4.9)

Genital 35 42 77 (3.7)Cardiovascular 72 2 74 (3.6)Musculoskeletal 11 6 17 (0.8)Central nervous system 7 2 9 (0.4)Miscellaneous 5 7 12 (0.6)

Total 1652 404 2056 (100.0)

* Numbers in parentheses indicate per cent of total infection.

759VOl. 184.o NO. 6

Ann. Surg. * December 1976

FIG. 1. Average age bydecade of patients withsurgical wound infectionscompared with all in-patients 1969-1972. Thefirst year of life is analyzedalso.

4.26%, intravenous cutdowns and catheters-3.72%,gastrointestinal tract-2.91%, lower respiratory tract-2.02% and surgical wounds- 1.98%. The sites of originof the other quantitatively significant COI bacteremiaswere: gastrointestinal tract 7.23%, and the urinary tract1.67% (Table 2).One thousand three hundred nine patients with surgical

wound infections were treated with 2151 medical devices,an average of 1.64 devices per patient. The urinary tract

infections associated with medical devices accounted for57.7% of the total. Septic phlebitis occurred in 6.83% ofpatients with intravenous catheters and 16.21% of cut-down sites. Of the patients with lower respiratory infec-tions 94.3% had various medical devices associated withthese infections. The rate for respirators was 56.6%, fortracheostomies- 19.1%, and for thoracotomy tubes27.3%. Of the patients with lower respiratory infections70.2% were cases of pneumonia, 26.2% were acute ex-

TABLE 3. Infection Rates Associated with the Use of2151 Medical Devices in 1309 Patients with SurgicalWound Infections from 1969 Through 1972

Medical Devices Infection Rate*

Urinary Tract Devices 855 Urinary Tract 57.66Indwelling catheter 694 Bacteremia from urinary tract 4.26tSupra-pubic catheter 81 Bacteremia from urinary tractSingle catheterization 51 associated with devices 2.46Cystoscopy 29

Intravenous Devices 565 Septic PhlebitisIntravenous catheter 483 From cutdown 16.21Umbilical catheter 8 From catheters 6.83Intravenous cutdown 74 Bacteremia from intravenous

catheters and cutdowns 3.72Respiratory Devices 489 Lower Respiratory 94.27

Respirator 261 Bacteremia from lower respiratoryThoracotomy tube 126 tract 2.02tTracheostomies 88 Bacteremia from lower respiratoryForeign bodies 8 tract associated with devices 1.84Intubation > 72 hours 6

Prostheses 242 ProsthesesSkeletal 97 Skeletal 5.15Vascular 82 Vascular 6.10Cardiac 50 Cardiac 4.00Cerebrospinal fluid shunts 13 Cerebrospinal fluid shunts 7.69

* Infections -i x 100Devices Used

Bacteremia x 100Infections at Site

76025

20

EDWARDS

AGE IN YEARS90

EPIDEMIOLOGY OF REMOTE SITE INFECTIONS

acerbations of bronchitis, and the remaining 3.5% weredue to abscesses or empyemas. Implanted prostheseswere associated with deep infection sites around theprostheses in 4.00W to 7.69W (Table 3).One thousand nine hundred sixty-six surgical wound

infections occurred in 1865 patients. Seven hundredtwenty-one patients with a single surgical wound averageda stay of 24 days in the hospital contrasted with anaverage stay of 40 days in those with a COI and/or HOIat a remote site. The average stay for all patients atour hospital during this study was 11 days.The incidence of surgical wound infections was greater

for the 40-80 age group compared with the overallinpatient population (Fig. 1).The ratio of infections for Caucasian females to Cau-

casian males was 0.9 and for Negro females to Negromales the ratio was 1.5. The overall population hadcomparative rates of 1.2 and 1.9 respectively (Table 4).The average preoperative stay for patients with surgical

wound infections was 7.9 days with an average of 8.8 daysfrom operation to clinical presentation of the infection.When separated into weekly intervals, infections ap-peared in approximately one-half ofthe patients in the firstweek after operation and 7.4% of the patients showedinfection more than 4 weeks after operation (Fig. 2).

Surgical Wound infection rates were as follows: Re-fined-Clean -4.2%, Clean -4.6%, Contaminated-6.0%O and Dirty- 10.1%. The overall surgical wound in-fection rate was 4.8%. There was no significant declineover the 4-year period for Refined-Clean and DirtyWounds (Chi Square = 5.6 n.s. and 6.5 n.s. respectively.)There was, however, a significant decline in Clean andContaminated Wound Infections predominately in the lasttwo years of the study. (Chi Square = 16.4 and 14.3respectively; both P values <0.01) (Table 5).The same specialty and general surgeons operated on

both adult and pediatric patients. Surgical wound infec-tion rates were higher in pediatrics for cardiovascularsurgery, neurosurgery and thoracic surgery. The reversewas true for orthopedic surgery and general surgery.Plastic surgery and urology had slightly lower rates forpediatric patients (Table 6).

In 383 patients that had cultures taken from the surgicalwound and the remote sites of infection, 596 isolatesof the same bacterial species were isolated at both sites.In 54.9o the same bacterial species was isolated at aclinically infected remote site prior to its isolation fromthe surgical wound, in 16.4% the isolation occurredsimultaneously and in 28.7% the organism was isolatedfrom a clinically infected remote site of infection afterbeing isolated from the surgical wound. Similar figuresfor bacteremias were 28.2% before, 34.6% simultaneouslyand 37.2% after isolation from the surgical wound(Table 7).

761TABLE 4. Race and Sex of 1865 Patients with Surgical

Wound Infections from 1969 Through 1972

Year Race and Sex

1969- 1972 CaucasianMale 726 (38.9%o)Female 687 (36.8%)

NegroMale 179 (9.6%)Female 269 (14.4%)

OrientalMealeale 31 (0.3%)FemaleI

Five hundred two of 1865 patients (26.9%o) withsurgical wounds were not cultured. An additional 40specimens revealed no growth and 23 were reported as"lab accidents". One thousand four hundred bacterialcultures were evaluable for positive results.Twenty-seven and two-tenths per cent of gram posi-

tive bacteria, contrasted with 10.1% of gram negativebacteria, were isolated as single isolates. Coagulase posi-tive staphylococci (232), coagulase negative staphylo-cocci (109), Klebsiella-Enterobacter species (45) andEscherichia coli (39) accounted for 78.3% of the totalnumber of single isolates (543). Gram positive bacteriawere responsible for 74.0%o of the single isolates. Thegram positive/gram negative ratio for all isolates was 1.06.Fungi were isolated 43 times (3.1%) but only 7 times(0.5%) as the sole isolate (Candida species-5 and Asper-gillus species-2) (Tables 8 and 9).

504.

40

zci 301

20 1

ioL

4 ,4A

WEEKS AFTER SURGERY

FIG. 2. Interval from surgery in weeks to onset of surgical woundinfections.

Vol. 184oNo. 6

762 EDWTABLE 5. Refined-Clean, Clean, Contaminated and Dirty Suirgical

Wound Infection Rates For 1966 Surgical Wound InfectionsOccurring After 40,923 Operations from

1969 Through 1972

Surgical Wound Infection Rates*

Refined- Contami-Year Clean Clean nated Dirty Total

1969 4.0 5.3 6.6 12.0 5.11970 4.5 5.2 7.2 12.6 5.41971 4.4 5.0 5.1 10.6 4.81972 3.7 3.2 5.0 5.9 3.9

4-Year Average 4.2. 4.7 6.0 10.1 4.8

* Rates calculated as percent:( fectionsxOperations

Four hundred sixty-nine of 1865 patients (25. 1%)with surgical wound infections were not treated with sys-

temic antimicrobials. The remaining 1396 patients re-

ceived 946 prophylactic and/or empiric antimicrobialcourses and 2166 therapeutic antimicrobial courses.

Ampicillin accounted for 28.0% of all prescriptions andled the list for both prophylactic and/or empiric andtherapeutic prescriptions. Of all antimicrobials prescribed55.8% were accounted for by ampicillin, the cephalo-sporins and other antipenicillinase penicillins. Of thedrugs prescribed 59.1% were for single antimicrobials,10.0% for dual combinations and 30.9%7 for courses insequence (Tables 10 and I1).

Forty-eight (2.6%) of the patients received immuno-suppressive drugs other than steroids, 6.8% (126) re-

ceived steroids and 4.7% (88) underwent radiotherapy.Overall 14.0% of the patients received one or more ofthese therapeutic modalities.

Several patients (37.9%O) had some form of cancer,

37.8% -cardiovascular diseases, 21.0%-gastroin-testinal diseases, 17.3%-genitourinary diseases, 13.7%-endocrine disorders, 10.8% -respiratory diseases,7.6% -central nervous system diseases, 5.3%-obesity

TABLE 6. Risk by Surgical Specialty of Ac-quiring a Suirgical WoundInfection for 38,818 Adu,lt and 5968 Pediatric Suirgical

Patients* from 1969 Throuigh 19721,

Surgical Patients

Surgical Specialty Adult Pediatric

Cardiovascular surgery 5.92 10.80Orthopedic surgery 5.61 2.31Plastic surgery 3.22 2.25Neurosurgery 2.56 9.09Urology 2.32 1.64Thoracic surgery 1.60 3.85Gynecology 1.56 0.00Otolaryngology 1.20 0.00Opthalmology 0.05 0.00

Specialty surgery 2.94 2.64General surgery 7.13 4.07

* Additive total of 44.786 patients. The excess of 70 is due to patientsbeing operated on by more than one specialty.

No. Surgical Wound Infections1 Rates calculated as No Adisin x 100No. Admissions

and 12.4% other miscellaneous diseases. These resultsare based on 2306 diseases in 1408 of the 1865 patients(75.5%) prospectively monitored because of their knownor possible potential for predisposing to an infectiouscomplication.

Discussion

The number of variables involved in the productionof a single surgical wound infection are multitudinous.Several articles have described transfer of bacteria tothe wound by exogenous airborne spread, exogenous con-tact spread and endogenous contamination.13,4,7,9,14,17,1920Likewise host determinants that predispose to infectionhave been discussed at length.1 2'4'7'8'15 As in these latterstudies, this present study also found age, steroids, otherimmunosuppressives, radiotherapy and diseases likecancer, cardiovascular diseases and diabetes mellitus to

TABLE 7. Time of Isolation of the Same Bacterial Species from Other Remote Sites of Infection in Relationship toits Isolation from the Surgical Wound in 383 Patients with 596 such Isolates from 1969 Through 1972*

Time of Isolation of the Same Bacterial Species in Relationship to itsIsolation From the Surgical Wound

Simultane-Remote Site of Infection Before ously After Total

Urinary Tract 108 (59.3)t 22 (12.1) 52 (28.6) 182 (100.0)Lower respiratory tract 104 (64.6) 15 (9.3) 42 (26.1) 161 (100.0)Gastrointestinal tract 54 (58.1) 14 (15.0) 25 (26.9) 93 (100.0)Bacteremia 22 (28.2) 27 (34.6) 29 (37.2) 78 (100.0)All other sites 39 (47.6) 20 (24.4) 23 (28.0) 82 (100.0)

Total 327 (54.9) 98 (16.4) 171 (28.7) 596 (100.0)

* Excluded are 33 additional surgical wounds infected with the same bacterial species as occurred in the primary wound; 9 were isolatedsimultaneously and 24 after isolation at the primary wound site.

t All numbers in parentheses indicate per cent in the row, i.e. per cent of total isolated before, simultaneously or after at any given site.

'ARDS Ann. Surg. o December 1976

EPIDEMIOLOGY OF REMOTE SITE INFECTIONS

TABLE 8. Gram Positiv e Bacteria Isolated from 1400 SuirgicalWolnds from 1969 throlugh 1972

IsolatesGram Positive

Bacteria Single Multiple Total

Coagulase positivestaphylococci 232 (57.7)* 216 (20.1)* 448 (30.3)*

Coagulase negativestaphylococci 109 (27.1) 208 (19.3) 317 (21.5)

Enterococci 13 (3.2) 321 (29.8) 334 (22.6)All other gram posi-

tive cocci 37 (13.9) 229 (86.1) 266 (100.0)All gram positive

bacilli 11 (9.7) 102 (90.3) 113 (100.0)

Total 402 (100.0) 1076 (100.0) 1478 (100.0)

* Numbers in parentheses indicate per cent of the total within thecolumn.

be risk factors present in a significant proportion of ourpatients. Some reports in the literature have indicatedthe importance of various medical devices and infectionsremote from the surgical wound as being significantrisk factors.1l4'5'7'12'13'15'16"19The present study indicates that it is in the control of

remote infections and medical devices that the greatestimpact can be made in reducing the incidence of surgicalwound infections as well as these other infections oc-curring in surgical patients. A statistically significantreduction occurred in our clean and contaminated surgicalwound rates. This paralleled a statistically significantreduction in the number of admissions to surgery withCOI and similar declines in the incidence of HOI in theurinary tract, lower respiratory tract and gastrointestinaltract.

Infections at remote sites have resulted in highersurgical wound infection rates by as much as 2.7 to 5.3times. '7 Although comparative rates in controls were notascertained during this study, 61.3% of the surgicalwound infections were associated with a remote site ofinfection, a rate between the 12.9% observed in the five-university study and that of 75.8% observed in the studyby Birkenstock."7Whereas recovery of the same bacterial species from

several sites does not indicate how many specific typeswithin the species are present, it is certain that suchbacterial types must come from within this group. There-fore the isolation of the same bacterial species by timeof clinical presentation at the infected sites is suggestiveof the direction of spread. The data reported herein indi-cate the major route of spread of bacteria is from theremote site to the surgical wound. Confirmation of thisfinding will require prospective laboratory studies donewith typing of bacteria, e.g. phage typing of coagulasepositive staphylococci. This finding is further confirma-tion that a reduction in surgical wound infection may

TABLE 9. Granm Negative Bacteria Isolatedfrom 1400 SurgicalWounds from 1969 through 1972

IsolatesGram Negative

Bacteria Single Multiple Total

E. coli 39 (27.7)* 348 (27.8)* 387 (27.8)*Klebsiella-Entero-

bacter species 45 (31.9) 283 (22.6) 328 (23.5)Proteus mirabilis 13 (9.2) 190 (15.2) 203 (14.6)Pseudomonas species 18 (12.8) 175 (13.9) 193 (13.8)All other gram nega-

tive bacilli 26 (9.2) 257 (90.8) 283 (20.3)

Total 141 (100.0) 1253 (100.0) 1394 (100.0)

* Numbers in parentheses indicate per cent of the total within thecolumn.

have occurred because infection at remote sites werereduced in incidence. Additionally, as the incidence ofsurgical wound infection decreases, a lesser salutaryeffect may occur on infections at remote sites.There are two important methods of control implicit

in this finding. First of all, patients with known sitesof infection should not undergo elective surgery until theinfection is eradicated or under appropriate control. Theimportance of this can be illustrated by the higher inci-dence of postoperative endocarditis following open heartsurgery in patients with chronic periodontal disease,chronic urinary tract infections and chronic prostatitis.'6Thus, a decrease in patients admitted to surgery withCOI will result in a decrease in HOI including a decreasedchance for spread from remote sites to the surgical wound.Secondly, greater attention must be given to the control

TABLE 10. Prophylactic and/or Empiric Prescription of 946Antimicrobial Colurses in Patients ivith Surgical

Wound Infections from 1969 throlugh 1972

Prophylactic and/or Empiric Prescriptions

DualCombina-

Antimicrobial Single tion Sequential Total

Ampicillin 113 7 85 205 (21.7)tCephalosporins 91 9 81 181 (19.1)Non-absorbable

sulfonamides 129 1 X* 130 (13.7)Anti-penicillin-

ase penicillins 32 4 75 111 (11.7)Short-acting

sulfonamides 63 1 0 64 (6.8)Penicillin 23 16 9 48 (5.1)All other anti-

microbialst 138 41 28 207 (21.9)

Total 589 (62.2)t 79 (8.4)t 278 (29.4)t 946 (100.0)

* X-Not included in the data collection system.t Number in parentheses indicates the per cent of all prophylactic/em-

piric antimicrobials prescribed.t Each of the other antimicrobials accounted for less than 5% of the

total.

763Vol. 184 * No. 6

764TABLE 11. Therapeutic Prescription of 2166 Antimicrobial Courses inPatients with Surgical Wound Infections, from 1969 through 1972

Therapeutic Prescriptions

DualCombina-

Antimicrobial Single tion Sequential Total

Ampicillin 358 24 284 666 (30.8)*Cephalosporins 161 18 149 328 (15.1)Anti-penicillin-

ase penicillins 170 18 57 245 (11.3)Penicillin 69 26 60 155 (7.2)Gentamicin 67 33 31 131 (6.0)Tetracyclines 89 3 33 125 (5.8)All other anti-

microbialst 337 111 68 516 (23.8)Total 1251 (57.7)t 233 (10.8)t 682 (31.5)t 2166 (100.0)

* Number in parentheses indicates the per cent of all therapeuticantimicrobials prescribed.

t Each of the remaining antimicrobials accounted for less than 5%of the total.

of medical devices and, whenever possible, a decrease intheir use.The rates of infection associated with medical devices

depicted in Table 3 are high. This association infersthat these devices were either etiologic or used after theinfection started, in which case they may have accen-tuated and prolonged the infection. It is recognized thatsometimes this may be unavoidable.

Implantation of prostheses foreign to the human bodyto replace a deficient part with resulting increase ininfection rates may be the price of progress. Neverthe-less, our studies of total hip replacements with the useof acrylic cement and prosthetic valve endocarditis hasprompted us to suggest that an interdisciplinary approachto these patients may lower the infection rates."2"16Most urinary, respiratory and intravenous devices are

placed or used just prior to or after surgery. With urinaryor respiratory devices it is necessary for the referringphysician or surgeon to document the presence of chronicinfected foci such as bronchitis, prostatitis or asympto-matic bacteriuria. If not, the use of these devices at aclinically quiescent, chronically infected focus almostensures a flare-up of the infection, or the introduction ofa hospital strain of bacteria. If such an infection is docu-mented by bacterial culture and sensitivity tests beforeoperation, specific antimicrobial therapy can be institutedin an effort to eradicate or, at least, control the infectionby preventing extension of the infection to other sites.15When a medical device is used, well-known control meas-ures such as the closed-urinary drainage system, propersterilization of respirators and changing the intravenoussite every 48 hours are indicated.5'5 Also, the deviceshould be removed at the earliest possible time as most ofthese control methods are temporizing measures only.

Emphasis on these control measures has resulted in thedecrease in infection rates observed in this study. Furtherreductions should be possible.The importance of these devices in the etiology of

bacteremia can be illustrated by two of the findings de-picted in Tables 2 and 3. Bacteremia (HOI) from theurinary tract occurred in 4.26% of cases contrasted with arate of 1.67% for bacteremia (COI) from the urinary tract.The difference between these two rates of 2.59% is strik-ingly similar to the bacteremia rate (HOI) of 2.46% asso-ciated with the use of urinary tract devices. The bac-teremia rate (HOI) from intravenous devices of 3.72%was nearly twice the rate observed in a previous studyfrom our institution.6 Except for one episode, bac-teremia was observed from intravenous devices eithersimultaneously or after the same bacterial species iso-lated from the surgical wound infection. Contrary to theresults from other remote sites reported herein, thisargues for spread from the surgical wound to the intra-venous site. Thus, the patient with a surgical woundinfection has nearly twice the chances of developingbacteremia from an intravenous device as do patients ingeneral.Another approach to decreasing the rate of HOI is to

decrease the time the patient is in the hospital or optfor outpatient surgery when feasible. One study on appro-priately selected operations on outpatients with homenursing followup has been reported.18 A prolonged pre-operative stay with exposure to the hospital environ-ment and its ubiquitous diagnostic procedures, therapiesand microflora have been repeatedly shown to increasethe rate of HOI.1'3"2 A shift in insurance programs toallow more outpatient, preadmission evaluation wouldhelp alleviate this problem and reduce the overall costs ofhealth care.

Patients with multiple infections averaged a stay of 3.6times as long in the hospital compared to 2.2 times aslong for patients with single surgical wound infections.The average stay for all inpatients during this study periodwas 1-1 days and the average cost per day was $150. Thus,the average excess cost for any patient with a surgicalwound infection was $5100. The total excess cost duringthe 4-year period for all 1865 patients was $951,150. Alte-meier estimated the cost of surgical wound infections in1967 to be $9.83 billion. He has adequately discussedthis and the related spiraling increase in malpracticeawards.4The higher rate of surgical wound infections on cardio-

vascular surgery, neurosurgery and thoracic surgery inpediatrics may represent differences in hosts with con-genital malformations or cancer at these sites. The lowerrate in pediatric orthopedic surgery may be accountedfor by the high incidence of trauma in this age groupin patients who are excellent hosts and possess excellent

EDWARDS Ann. Surg. o December 1976

EPIDEMIOLOGY OF REMOTE SITE INFECTIONS 765immune responses. In general surgery the higher inci-dence of chronic disease of the colon in adults (cancerand diverticulitis) contrasted with appendectomies,intussusceptions, etc., in youngsters may account for thehigher infection rate in adults. Similar reasoning wouldapply to the 7.23% COI and 29.1% HOI rates for bac-teremia from the gastrointestinal tract in this group ofpatients. Since the same surgeons operated on both adultand pediatric patients, it is unlikely that the techniquesof individual surgeons accounted for the different rates.

Jepsen, by phage typing coagulase positive staphylo-cocci, found the wards and not the operative rooms tobe the primary site of acquisition in the majority of suchwound infections. Acquisition was related to infectedpatients disseminating the same types of staphylococciinto their environment.14 In that light it is important tonote that over one-half of our surgical wound infectionsbecome manifest more than one week after surgery. The7.4% that presented more than 4 weeks after surgery maybe largely accounted for by infections around prostheseswhich often have a delayed clinical presentation. 12'16Therefore, our findings are in accord with the more de-tailed study by Jepsen and suggest, as his did, that a goodpart of the battle against surgical wound infectionsshould be fought in the intensive care units and on thesurgical wards.14Approximately one-fourth of patients with clinically

documented infections were not cultured and a similarproportion were not treated with systemic antimicrobials.Unfortunately, overlap in these two groups was notstudied. Whereas, it is understandable that certain pa-tients may do well without cultures or systemic anti-microbials, it must be emphasized that these patients are arisk factor to other patients. Patients or medical personnelwith minor staphylococcal lesions have been responsiblefor spread to other patients and resulting serious infec-tions.19 It is incumbent on the surgeon to view his patientas part ofa community. Interruption in the flow ofbacteriafrom one patient to another either by the patient directlyor through the intermediary of medical personnel wouldindicate the need for taking more cultures and givingspecific antimicrobial therapy. Thus, at one extreme thereis a need for more antimicrobial use; at the other extremeit is absolutely necessary that we reduce the use of "shot-gun regimens" and the ensuing breeding ofmultiply resist-ant hospital strains.2'3The prolific use of ampicillin is particularly difficult to

understand. Escherichia coli resistant to ampicillin isquite common in our institution and ampicillin is notusually effective against hospital strains of most of theother gram negative bacteria (except Proteus mirabilis)and coagulase positive staphylococci. The surgical serv-ice outdistances other services in our institution in theprolific use of prophylactic and/or empiric antimicrobials

(40.25% of patients) with no decline in HOI rates. Otherstudies support this finding.1'2'3'15The increasing incidence of gram negative infections

in surgical patients has been clearly documented.2Altemeier has also shown that the primary sources ofgram negative infections are the urinary and respiratorytracts and the many medical devices used in these areas.2The finding ofa predominance ofgram positive bacteria inthis study appears to be at variance with such reports.However, enterococci (344 isolates), peptostreptococci(8 isolates) and Clostridia species (35 isolates) havetheir primary habitat in the gastrointestinal tract andtheir epidemiology is quite similar to that of the gramnegative bacteria. Furthermore, a special anaerobelaboratory was not operational during this study. Hoffmanhas reported anaerobes to be the most common isolatesin surgical wound infections following gastrointestinalsurgery when special anaerobic collection, transport andprocessing techniques are used. 13 When the gastro-intestinal tract is entered during operation gram negativebacteria predominate in the wound whereas in othersurgery the staphylococci predominate.9'17

Virulence is often suggested by isolation ofa single bac-terial species from an infection. Coagulase positivestaphylococci were isolated as a single isolate morethan twice as many times as its closest competitor, thecoagulase negative staphylococci. The prominent associa-tion of this latter bacterial species in infections aroundprostheses makes one a little cautious at dismissing it asa contaminant, particularly if such a prosthesis ispresent.12'16 Coagulase positive staphylococci were indi-cated as a single isolate nearly 6 times more often as itsclosest single gram negative competitor, Escherichia coli.

Therefore, in operations not involving the gastroin-testinal tract, the coagulase positive staphylococci arelikely to be dominant in surgical wound infections,whereas in surgery involving the gastrointestinal tract,multiple isolates of gram negative and gram positivebacteria are likely. It has been our clinical impressionthat many surgical wound infections initiated by acoagulase positive staphylococcus often subsequentlybecome colonized or "supra' infected with gram negativebacteria. The data also support this, as coagulase positivestaphylococci (216 isolates) were the fourth most commonisolates found in mixed infections behind Escherichiacoli (348 isolates), Enterococci (321 isolates) and Kleb-siella-Enterobacter (283 isolates).

In conclusion, surgical wound infections are often asso-ciated with remote site infections. Control of the remotesite of infection has the potential oflowering the incidenceof surgical wound infections.A monitoring system such as we have described for

COI and HOI, including surgical wound infections, isnecessary to suggest preventive and control measures

Vol. 184 -No. 6

Ann. Surg. * December 1976

which can result in a lowering of the infection rateseven before all ofthe "hard data" have been accumulated.It can provide baseline data to document the effective-ness of control measures and also will suggest appropriateprospective studies to further unravel other variables in-volved in the etiology of surgical wound infections.

References1. Ad Hoc Committee of the Committee on Trauma, Division of

Medical Sciences, National Academy of Sciences-National Re-search Council: Postoperative Wound Infections: The Influenceof Ultraviolet Irradiation of the Operating Room and of VariousOther Factors. Ann. Surg. 160:2: (Supplement) 1964.

2. Altemeier, W. A., Todd, J. C., and Inge, W. W.: Gram-NegativeSepticelnia: A Growing Threat. Ann. Surg., 166:530, 1967.

3. Altemeier, W. A., Culbertson, W. R., and Hummel, R. P.: SurgicalConsiderations of Endogenous Infections-Sources, Types, andMethods of Control. Surg. Clin. North Am., 48:227, 1968.

4. Altemeier, W. A.: Current Infection Problems in Surgery, in theProceedings of the International Conference on NosocomialInfections. Chicago, American Hospital Association, 1971;pp. 82-87.

5. Altemeier, W. A., McDonough, J. J., and Fullen, W. D.: ThirdDay Surgical Fever, Arch. Surg., 103:158, 1971.

6. Bentley, D. W. and Lepper, M. H.: Septicemia Related to In-dwelling Venous Catheters, JAMA, 206:1749, 1968.

7. Birkenstock, W. E.: Surgical Sepsis. S. Afr. Med. J., 47:436,1973.

8. Burke, J. F.: Clinical Determinants of Host Susceptibility toInfection in Surgical Patients, in the Proceedings of the Inter-national Conference on Nosocomial Infections. Chicago, Ameri-can Hospital Association, 1971; pp. 169-172.

9. Davis, N. C., Cohen, J., and Rao, A.: The Incidence of SurgicalWound Infection: A Prospective Study of 20,822 Operations.Aust. N. Z. J. Surg., 43:75, 1973.

10. Edwards, L. D., Balagtas, R. C., Lawrence, R., et al.: Anti-microbials, Infections, and the Nurse-Epidemiologist atPresbyterian-St. Luke's Hospital. Rush-Presbyterian St. Luke'sMedical Bulletin, 9:132, 1970.

11. Edwards, L. D., Levin, S., and Lepper, M. H.: DescriptiveEpidemiology. Hospitals, J. Am. Hosp. Assoc. 43:75, 1971.

12. Edwards, L. D., Levin, S.: Complications From Total Hip Replace-ment With the Use of Acrylic Cement. Health. Serv. Rep.,88:857, 1973.

13. Hoffmann, K. and Gierhake, F. W.: Postoperative Infection ofWounds by Anaerobes. Ger. Med. Mon., XIV:31, 1969.

14. Jepsen, 0. B.: Post-Operative Wound Sepsis in General Surgery,VII. Staphylococcal Wound Sepsis, Acta. Chir. Scand.. 138:343, 1972.

15. Levin, S.: Acute Surgical Infections, In Intensive Care of theSurgical Patient, Marshall D. Goldin (Ed.), Chicago, Year BookMedical Publishers, 1971, Chapter 10.

16. Quenzer, R. W., Edwards, L. D., and Levin, S.: A ComparativeStudy of 48 Host Valve and 24 Prosthetic Valve EndocarditisCases. Am. Heart J.. 92:15, 1976.

17. Raahave, D.: Bacterial Density in Operation Wounds. Acta.Chir. Scand., 140:585, 1974.

18. Ruckley, C. V., MacLean, M., Smith, A. N., et al.: Team Approachto Early Discharge and Outpatient Surgery. Lancet, 1: 177, 1971.

19. Sub-Committee on Aseptic Methods in Operating Theatres ofTheir Committee on Hospital Infection, Medical ResearchCouncil, "Aseptic Methods in the Operative Suite." Lancet,Vol. 1: Pt. 1, 705-709; Pt. II, 763-768; Pt. III, 831-839, 1968.

20. Walter, C. W. and Kundsin, R. B.: The Airborne Component ofWound Contamination and Infection. Arch. Surg., 107:588,1973.

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