Environmental Air and Airborne Infections CHRISTOPHER T. DRAKE, M.D., F.A.C.S., EUGENE GOLDMAN, M.D., RONALD LEE NICHOLS, M.D., F.A.C.S., KATHLEEN PIATRUSZKA, LLOYD M. NYHUS, M.D., F.A.C.S.

The results of a study on the epidemiology of airborne (aerobic) surgical infections are presented. The first phase of the study was carried out in a surgical suite which contained no environmental or traffic control systems. The second phase of the study took place within a modern "up to date" operating room suite containing multiple air screens as well as an elaborate ventilation system utilizing HEPA type filters which provided the operating room with clinically sterile air. One hundred and fifty-six patients were studied. All patients underwent major procedures. The ratio of clean, clean-contaminated, and dirty cases was the same in both groups. Preoperatively, a nasal swab, clean voided urine (or vaginal swab) and a rectal swab were obtained on each patient. Daily nasal cultures and cultures of suspected sites of infection were obtained postoperatively. Daily nasal cultures and "glove sweat" cultures were obtained on all personnel attending the patient. Environmental cultures of the operating room, the operating room hallway, recovery room and patients' rooms were also taken. All samples were checked for the presence of staphylococci, streptococci, Eschericia coli, proteus species, enterobacter, klebsiella, and pseudomonas. In all, 15,000 cultures were taken during the study. The rate of infection was essentially the same in both phases of the study. Environmental air only occasionally served as the source of infecting organisms. The results of the study support the conclusion that the most common source of infecting organisms in surgical infections is the patient or those around him. The most common time of contamination is during the surgical procedure itself. Surgical infections can best be minimized by meticulous observation of fundamental principles of antisepsis rather than by dependence on elaborate and costly ventilation and air control systems.

ALTHOUGH the causes of surgical infection may not be precisely identifiable, there appears to be general agreement that the sources of infecting organisms include: the patient, surgical team, other attending person-

16

Submitted for publication April 19, 1976. Supported by H.E.W. Grant #HSOO 256. Reprint requests: Christopher T. Drake, M.D., F.A.C.S., Department of Surgery, Illinois Masonic Medical Center, 836 West Wellington Street, Chicago, Illinois 60657.

From the Department of Surgery, The Abraham Lincoln School of Medicine, University of Illinois and the Illinois Masonic Medical Center, Chicago, Illinois

nel, environmental air, walls and floors, material and equipment.1'6'13 Howe and others have demonstrated that more than half of all surgical incisions become contaminated with airborne organisms during operations.3 11 However, the role of these organisms in the genesis of surgical infection has not been established.5'8 Nonetheless, some investigators have concluded that airborne organisms do constitute a major cause of surgical infections.4'16'21 They have therefore proposed "clean air" operating room ventilation systems as a means of reducing such infections.4'15'16 To date, little controlled research has been carried out to assess the significance of such installations in effectively reducing postoperative infections in surgical units.9 Studies demonstrating a correlation between "clean air" systems and a reduction in infection rates have failed to show that the airborne organisms eliminated from the environment were in fact responsible for previous infections.4'18 In 1970 our institution began the construction of a new surgical suite. Our pre-existing operating room facility was of elementary design. It had a single central corridor through which all traffic, including street traffic, moved. Window air conditioners were used. A forced air heating system was employed, with minimal air filtration. The new surgical suite provided for strictly controlled surgical traffic and contained multiple air screens appropriately located so as to prevent airborne contamination of the suite. Its ventilation system filtered air through HEPA type filters* (99.97%) efficiency; 0.3 microns). The rate of

219

*

HEPA-Serfilco, Chicago, Illinois.

Ann. Surg. * February 1977

DRAKE AND OTHERS

220

TABLE 3. Surgical Procedures Studied

TABLE 1. Male:Female Distribution of Patients Studied

Male Female Total Age range Mean age

Phase I

Phase II

Type

Phase I

Phase II

41 42 83

22 51 73

14-71 40.5

16-73 37.3

General Orthopedic Gynecologic Other Total

37 23 16 7 83

18 37 18 0 73

C. Definitions of Infection The same criteria for infection were used as for general infection surveillance by our nurse epidemiologist. These criteria are those recommended by the Center for Infections and Disease Control. Each patient was observed carefully for classical symptoms and signs of postoperative infection up to the time he or she was released from the hospital. All patients were followed for a minimum of three weeks. Tables 1 and 2 show the age and sex distribution of patients studied, as well as the classification of procedures monitored. Table 3 indicates the type of surgical performed upon the patients studied. Table 4 procedures Methods and Materials outlines the number and distribution of cultures taken A. Sampling Procedures per case studied. Over 15,000 cultures were taken Preoperatively a nasal swab, clean voided urine (or throughout the entire study. vaginal swab) and a rectal swab were obtained from each Results patient. Postoperatively, daily nasal cultures and cultures Infections. During the first phase of our study we from any suspected site of infection were obtained. Nasal cultures were obtained from all personnel entering the encountered 6 wound infections. There were two wound operating room. "Glove sweat" was cultured from the infections noted in clean wounds, two in clean-consurgeon and each "scrubbed" attendant. All personnel taminated, and two in dirty wounds. The environment attending the patient postoperatively had daily nasal was implicated only once. In the second phase of the cultures taken. On the day of surgery, air sedimentation study we noted three wound infections. The wound incultures were obtained from the operating room hall, the fections were all in "clean" wounds. The environment operating room and the recovery room. Standard 150 mm was not implicated. Tables 5 and 6 provide further blood agar plates were exposed to the environment for one information on the infections experienced. hour and colony counts obtained. Also, daily sedimentaEnvironmental Sampling. Operating Room (Table 7)tion plates were obtained from each patient's room. The daily variation of col/hr obtained was related to the amount of "traffic" experienced in each area. Repeated environmental cultures during the early B. Bacteriologic Cultures prior to any traffic within the new All samples were cultured for strains of Staphylococcus morning hours and operating suite have yielded less than 2 col/hr growth. aureus, streptococci, Eschericia coli, proteus species, The level of environmental contamination was not inenterobacter, klebsiella and pseudomonas, using standard

air flow provided 20 air exchanges per room, per hour. Construction of such a unit provided us with an opportunity to study airborne infections as well as the effectiveness of included systems in reducing surgical infection rates. A project was therefore initiated to monitor persons, places and environmental air in order to determine the origin and spread of airborne micro-organisms causing surgical infections. Our study was divided into two phases. Phase I was carried out in the old physical plant to serve as a control and required 15 months. Phase II took place in the new surgical suite and lasted 9 months.

bacteriologic techniques.

TABLE 4. Type and Number of Cultures Taken per Patient Studied

Cultures/Case

TABLE 2. Classification of Procedures Studied

Clean Cleancontaminated

Dirty

Phase I

Phase II

57/83 (69o)

52/73 (71%)

14/83 (17%) 12/83 (14%)

14/3 (19%) 7/73 (10%)

Patient cultures Environmental cultures Personnel cultures Total

Phase I

Phase II

12 13 95 120

7 8 46 61

Vol. 185 a No. 2

AIRBORNE INFECTIONS

221

TABLE 5. Wound Infections -Phase I

Patient

Age, Sex

Procedure, Date

Infection Noted

B.M.

45, F

Abdominal Hysterectomy, 11/16/72

11/22/72

C.A.

43, F

Laminectomy, 2128/3

Organism Isolated Enterococcus P. mirabilis

3/8/73

Staph aureus (coagulase-)

Organism Source Roommate-wound surgeons, attendants - nares, environment Surgeon-glove sweat, anesthesiologistnares

G.A.

24, M

Colostomy closure, 5/25/72

5/30/72

E. coli, Staph aureus (coagu-

J.L.

41, M

Cholecystectomy, 7/11/72

7/14/72

Staph aureus

3/11/72

E. coli E. coli Pseudomonas Pseudomonas

lase+) (coagulase-) M.J.

63, M

Arthroplasty, 3/9/72

P.J.

27, M

Rotation flap, decubitus ulcer, 8/28/72

9/6/72

Patient-G.I. tract, patient, nursesnares

Surgeon-glove sweat O.R. nurse-glove sweat

Patient-G. I. tract, unknown Patient-urinary tract,

pre-existing

creased on the days of procedures which were followed by infection. The operating room hallway of the preexisting suite exhibited the highest levels of environmental contamination observed during the entire study (Table 8). The overall level of environmental contamination was at its lowest level in the recovery room of both suites reflecting the small amount of traffic in these areas (Table 9). The level of environmental contamination of patients' rooms also reflected the levels of traffic in this area (Table 10). The organisms isolated during the study consisted of the usual variety of airborne bacteria as reported by others. The most common pathogens were: a) Staphylococcus aureus, coagulase positive; b) Staphyloccocus albus; c) E. coli; d) Proteus mirabilis; e) Klebsiella; f) Enterobacter species; g) Pseudomonas; h) Bacillus species.

that all possible measures designed to reduce the incidence of surgical infection be undertaken.6'5 It seemed logical and was inevitable therefore that surgeons, architects and operating room designers would ultimately resort to NASA type technology in order to achieve germ free air within operating room suites.12,5 Little or no controlled research was carried out to substantiate the thesis that the environmental air is in fact the major source of infecting organisms in surgical patients.8'9'12'14 Some studies have correlated a reduction in post surgical sepsis with bacteriologic control of the environmental air.4 However, they have failed to demonstrate that the organisms causing the wound infections were organisms that were in fact being eliminated from the environment. Other authors have been able to demonstrate that surgical incisions are frequently contaminated by airDiscussion borne organisms during the surgical procedure.3'5'1' Few of these incisions developed postoperative infection and The introduction to surgery of implantable prosthetic when they did, the organisms isolated from such indevices markedly increased the need for infection con- cisions were found to be different from the organisms trol.9 The catastrophic sequeli to an infected hip prosthe- cultured from the same incisions at the time of operasis or infected artificial heart valve made it mandatory tion."1 TABLE 6. Wound Infections -Phase II

Infection

Patient

Age, Sex

C.R.

51, F

Procedure, Date

Hip replacement,

10/17/74

Noted

10/31/74

Organism Isolated

Organism Source

Staph. aureus (coagulase-),

Unknown Unknown O.R. nurse-nares, O.R. nurse-glove

Enterobacter

L.J.

51, F

Fusion wrist, 7/9/74

7/10/74

Staph. aureus (coagulase+)

sweat

S.M.

56, F

Hip replacement, 10/24/74

11/ 1/74

Pseudomonas

Unknown

DRAKE AND OTHERS

222

TABLE 7. Environmental Cultures-Operating Room

Range

Mean*

Samples

Unin- Infected fected

UninInfected fected

Phase I 71

1-204

collhr Phase II 52

4-90

collhr

12-117 col/hr

collhr

12-68 col/hr

39 col/hr

55

Ann.

Surg. February 1977

TABLE 9. Environmental Cultures -Recovery Room

Daily variation

Cultures TNTCt

61 col/hr

Marked

4

32

Moderate

None

Phase I 71 Phase II 51

collhr

Range

Mean*

UninInfected fected

Unin- Infected fected

0-234 40-116 col/hr col/hr

65 col/hr

3-65

col/hr

* Those too numerous to count were excluded.

8-65 col/hr

29

collhr

76

Marked

None

Moderate

None

collhr 31 col/hr

* Those too numerous to count were excluded. t Too numerous to count.

t Too numerous to count.

Some authors have suggested that contamination of the environmental air is more of a reflection of pre-existing, high human contamination rate in such an area rather than being the primary mode of transmission of organisms

and the "cleanliness" of the operating suite air. 3) To analyze the above in order to assess the need for extensive (and expensive) designs and installations for control of operating room traffic and air. Analysis of the to man.17 data gathered during the two phases of the investigation It has been shown that surgical patients who are nasal, reveals that only two of the infections noted in Phase I umbilical, or skin carriers of coagulase positive, staphylo- occurred in "clean" wounds. All three of the infections cocci have a higher incidence of postoperative staph- in Phase II were in "clean" incisions. The clean wound ylococcal sepsis than those who do not.19 At times a infection rate was 3.5% for Phase I (2/57) and 5.7% high proportion of staphylococci capable of producing (3/52) for Phase II. disease in surgical patients are harboured by these paIf one examines the overall "clean"-"clean-contamitients at the time of their admissions to the hospital.19'22 nated" infection rates, the corresponding values are 5.6% In addition to patient related sources of contamination, (4/71) for Phase I and 4.5% (3/66) for Phase II. there are reports implicating the surgeon and his attendAlthough the number of cases is small, it would ants as the source of infections.10 Especially important is appear from this study that introduction of an elaborate the presence of minor lesions of septic nature present in surgical suite and sophisticated ventilation system has no the skin of surgeons or attendants during the time of opera- perceptible effect on wound infection rates. tion. It also has been shown that during the postThe source of contamination in these cases was comoperative period, infection may be transferred to the pa- parable in both phases. Endogenous flora and cross tient by the individuals who change the surgical dressings contamination at the time of surgery appeared to be the and in so doing, contaminate the wound.20 predominant factors. Cross contamination from nasal The objectives of our study can be stated as follows: 1) carriers can and does occur but less frequently than To gather epidemiologic data concerning vectors of air- anticipated.1023 The organisms causing infection varied borne bacterial infection in surgical patients. 2) To relate but Staphylococcus aureus (coagulase+), E. coli, enterothe above data to the design of the operating room suite cocci, enterobacter, pseudomonas, and proteus forms TABLE 8. Environmental cultures-Operating Room Hallway

TABLE 10. Environmental Cultures -Patients' Rooms

Range

Mean*

Samples

Unin- Infected fected

Unin- Infected fected

variation

Cultures TNTCt

Samples

Phase I 72

24-257 49-208

134 130 col/hr col/hr

Marked

15

Phase I 709

1

Phase II 294

collhr collhr

Daily

Phase II 59

19-96 31-80 col/hr col/hr

59

54

Moderate

col/hr collhr

* Those too numerous to count were excluded.

t Too numerous to count.

Range

Mean*

UninInfected fected

Unin- Infected fected

Daily Variation

Cultures TNTCt

0-292 0-252 collhr col/hr

70 78 collhr collhr

Marked

74

Marked

10

0-150

collhr

0-120 col/hr

57

41

collhr collhr

* Those too numerous to count were excluded. t Too numerous to count.

Vol. 185 * No. 2

AIRBORNE INFECTIONS

were predominant (Table 5 and 6).11 Airborne infection did not appear to play a major role. An inspection of the results of the environmental studies indicates that environmental air is subject to marked fluctuation in the levels of "'contamination" as evidenced by the wide range of "col/hr" growth obtained. This has been noted by other investigators.23 The high contamination levels in the operating room hall are believed to be the result of the increased traffic and "shedding" that the area sustained.2 It is similarly believed that the peak levels of contamination noted in the other areas can also be related to increased traffic by floor personnel, visitors, lab technicians, etc. Wiley has reported col/hr counts increasing from 15 col/hr during quiet periods to over 100 col/hr during periods of heavy traffic.23 Environmental cultures taken in the new surgical suite during Phase II demonstrated the effectiveness of air and traffic control systems in maintaining an environment less impregnated with bacterial contamination. This reduction however was substantially less than anticipated. Although the air introduced into the O.R. suite was free of bacteria and exchanged at the rate of 20 times per hour, it is apparent that enough "shedding" occurred to maintain an airborne bacterial population of sizable proportions. Nonetheless, even if we had achieved 100o reduction of environmental bacterial contamination, the effect of this on the overall pattern of infections noted during this study would have been negligible. Conclusions We believe that the data gathered in this study and presented in this report support the following conclusions: The most common source of microorganisms causing surgical infections is the patient himself. The organisms implicated in such infections are among the "endogenous flora'' harboured by the patient. Sites such as vaginal and urinary tract, the skin, GI tract, and any infected areas serve as the topographic locus for the origin and spread of infecting microorganisms. The second most common source(s) of infecting microorganisms include the surgical room personnel, recovery room, and floor personnel. The most common "time" that bacterial contamination occurs is during the surgical procedure itself. Nasal carriers of pathogenic organisms are an infrequent source of infecting microorganisms in surgical infections. Environmental air, although often laden with pathogenic bacterial flora does not frequently serve as the source of infecting organisms. Control and reduction of surgical infections can best be achieved by meticulous attention to fundamental surgical principles such as: a) Preoperative antiseptic preparation of the patient; b) Thorough preparation of the surgical

223

site at the time of surgery; c) Careful observation of sterile technique during surgery and the postoperative handling of patient and wound dressing. Elaborate traffic control and air maintenance systems such as those employed in our new surgical facility are not likely of themselves to effect a significant reduction in surgical infections-especially if the above outlined steps are ignored. References 1. Alexander, J. W.: Emerging Concepts in the Control of Surgical Infections. Surgery, 75:934, 1974. 2. Bernard, H. R., Cole, W. R., and Gravens, D. L.: Reduction of latrogenic Bacterial Contamination in Operating Rooms. Ann. Surg., 165:609, 1969. 3. Burke, J. F.: Identification of the Sources of Staphylococci Contaminating the Surgical Wound During Operation. Ann. Surg., 158:898, 1963. 4. Charnley, J., and Eftekhar, N.: Post-operative Infection in Total Prosthetic Replacement Arthroplasty of the Hip Joint. Br. J. Surg., 56:641, 1969. 5. Dillon, M. F., Postlethwait, R. W., and Bowling, K. A.: Operative Wound Cultures and Wound Infections, A Study of 342 Patients. Ann. Surg., 170:1029, 1969. 6. Dineen, P.: Prevention of Infection in the Operating Room. Bull. Am. Coll. Surg. Dec., 1970. 7. Flower, M., Borden, G., and Kerstein, M.D.: The Role of the Nurse Epidemiologist in Infection Control and Continuing Education. Surg. Gynecol. Obstet., 141:552, 1975. 8. Goodrich, E. 0. and Whitfield, W. W.: Air Environment in the Operating Room. Bull. Am. Coll. Surg., June, 1970. 9. Herndon, C. H.: The Clean Air Operating Room at University Hospitals of Cleveland Cleveland Clin. Quart., 40:183, 1973. 10. Howe, C. W., and Marston, A. T.: A Study on Sources of Post-Operative Staphylococcal Infection. Surg. Gynecol. Obstet., 115:226, 1962. 11. Howe, C. W.: Bacterial Flora of Clean Wounds and Its Relation to Subsequent Sepsis Am. J. Surg., 107:696, 1964. 12. Laufman, H.: Confusion in Application of Clean Air Systems of Operating Rooms. Cleveland Clin. Quart., 40:203, 1973. 13. Laufman, H.: The Surgeon Views Environmental Controls in the Operating Room. Bull. Am. Coll. Surg., May, 1969. 14. Laufman, H.: Special Air Systems for Operating Rooms. Bull. Am. Coll. Surg., 57:18, 1972. 15. Nelson, C. L.: Clean Air and the Total Hip Arthroplasty. Orthop. Clin. North Am., 4:533, 1973. 16. Nelson, P. J., Glassburn, A. R., Talbott, R. D., and McElhinney, J. B.: Clean Room Operating Rooms. Clin. Orthop., 96:179, 1973. 17. Rammelkamp, C. H., Jr.: Epidemiology of Streptococcal Infections. The Harvey Lectures, 1955-56, New York, Academic Press, 1956. 18. Ritter, M. A., Hart, J. B., French, M. L. V., and Eitzen, H. E.: A Systems Analysis Approach to Post-Qperative Wound Infections. Cleveland Clin. Quart., 40:211, 1973. 19. Shooter, R. A., Thom, B. T., Dunkerly, D. R., and Taylor, G. W.: Pre-operative Segregation of Patients in a Surgical Ward. Br. Med. J. 2:1567, 1963. 20. Shooter, R. A., Smith, M. A., Griffiths, J. D., et al.: Spread of Staphylococci in a Surgical Ward. Br. Med. J., 1:607, 1958. 21. Walter, C. E., Kundsin, R. B., and Brubecker, M. M.: The Incidence of Airborne Wound Infection During Operation. JAMA, 186:122, 1963. 22. Weinstein, J. J.: The Relationship Between the Nasal-Staphylococcal-Carrier State and the Incidence of Post-Operative Complications. N. Engl. J. Med., 260:1303, 1959. 23. Wiley, A. M., and Barnet, M.: Clean Surgeons and Clean Air. Clin. Orthop., 96:168, 1973.

Environmental air and airborne infections.

Environmental Air and Airborne Infections CHRISTOPHER T. DRAKE, M.D., F.A.C.S., EUGENE GOLDMAN, M.D., RONALD LEE NICHOLS, M.D., F.A.C.S., KATHLEEN PIA...
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