n Feature Article
Microbial Surface Contamination After Standard Operating Room Cleaning Practices Following Surgical Treatment of Infection Rishi Balkissoon, MD, MPH; Tariq Nayfeh, MD, PhD; Kerri L. Adams, MS, RN; Stephen M. Belkoff, PhD, MPH; Stefan Riedel, MD, PhD; Simon C. Mears, MD, PhD
abstract Full article available online at Healio.com/Orthopedics. Search: 20140401-53 At the authors’ institution, some joint arthroplasty surgeons require the operating room to be terminally cleaned before using the room after infected cases, in theory to decrease exposure to excessive microbial contamination for the subsequent patient. The authors found no guidance in the literature to support this practice. To test this theory, the authors measured microbial surface contamination from 9 surfaces in operating rooms after standard operating room turnover following 14 infected cases vs 16 noninfected cases. A check was made for an association between organisms isolated intraoperatively from infected surgical patients immediately preceding standard cleaning and organisms isolated from common operating room surfaces. Colony counts were made at 24 and 48 hours, and organisms were identified. No significant difference was noted in colony counts between infected and noninfected cases, and no relationship was found between organisms isolated from infected cases and those from operating room surfaces. Furthermore, the largest colony count from both groups (0.08 cfu/cm2) was an order of magnitude less than the recently proposed 5 cfu/cm2 threshold for surface hygiene in hospitals. This finding indicates that standard operating room turnover results in minimal surface contamination, regardless of the previous case’s infection status, and that there is no need for a more extensive terminal cleaning after an infected case. The authors are from the Department of Orthopaedic Surgery (RB, TN, SMB, SCM), The Johns Hopkins University/Johns Hopkins Bayview Medical Center, Baltimore; Infection Control (KLA), Johns Hopkins Bayview Medical Center, Baltimore; and the Department of Pathology (SR), Division of Microbiology, The Johns Hopkins University/Johns Hopkins Bayview Medical Center, Baltimore, Maryland. Drs Balkissoon, Belkoff, Riedel, and Mears and Ms Adams have no relevant financial relationships to disclose. Dr Nayfeh received a financial contribution to his Infection Study of less than $30,000 from a private individual. The authors thank Lisa Dam, MT (ASCP), for her support in the clinical microbiology laboratory during the processing and assessment of the bacterial cultures. Correspondence should be addressed to: Stephen M. Belkoff, PhD, MPH, c/o Elaine P. Henze, BJ, ELS, Medical Editor and Director, Editorial Services, Department of Orthopaedic Surgery, The Johns Hopkins University/Johns Hopkins Bayview Medical Center, 4940 Eastern Ave, #A665, Baltimore, MD 21224-2780 ([email protected]). Received: July 25, 2013; Accepted: November 8, 2013; Posted: April 15, 2014. doi: 10.3928/01477447-20140401-53
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oncern exists that contaminated environmental surfaces contribute to the transmission of infection in the health care setting. Antibiotic-resistant organisms, including methicillin-resistant Staphylococcus aureus (MRSA), vancomycin-resistant enterococci, and Clostridium difficile, can remain viable on dry surfaces for prolonged periods.1 Methicillin-resistant S aureus is a contaminant found in hospitals2,3 that is associated with transmission on hospital wards and intensive care units1,4-6 and is responsible for substantial periprosthetic joint infections after joint arthroplasty. The surgical patient is particularly vulnerable in the operating room with open wounds exposed to the environment. Some joint arthroplasty surgeons at the authors’ institution avoid using operating rooms after infected cases. Anecdotally, those surgeons require an extensive “terminal cleaning” before performing an arthroplasty after such a case. This practice stems from concern that these rooms may be excessively contaminated, potentially increasing the risk for subsequent surgical-site infection. However, the efficacy of this practice is untested and it likely requires higher operating costs and operating room scheduling strategies that complicate optimal patient care. Few studies have investigated environmental pathogenic contamination in the operating room. The level of operating room surface contamination that can influence surgical-site infection rates is not known, but a clean surgical environment is expected to reduce the number of pathogens available for potential transmission.7 Currently, operating room cleaning standards as outlined by the Association of periOperative Registered Nurses7 and the Centers for Disease Control and Prevention8 are not universal and in addition are vague in their description of goals. It has been recently recommended that “indicator organisms” (eg, MRSA, C difficile, multiply resistant Gram-negative bacilli, vancomycin-resistant enterococci, and Salmonella spp) should be found in less
e340
Table 1
Cases Enrolled Clean Cases (n=16)
Infected Cases (n=14)
THA
Knee infected prepatellar bursitis I&D and closure
TKA
Hip infected wound I&D, vac dressing application
TKA
Chronic leg infection I&D w/vac dressing application
TKA Revision TKA for periprosthetic fracture Conversion of hip resurfacing to THA Distal radius fracture ORIF I&D scrotal wound, split-thickness skin graft application TKA TKA Quadriceps tendon repair TKA Inguinal hernia repair Revision breast reconstruction
Infected TKA single-stage revision Second toe amputation for infection Hip infected wound I&D Hip removal of hardware, I&D, resection arthroplasty Perirectal abscess I&D Arm abscess and wound infection I&D Perirectal abscess I&D Laparotomy w/infected pancreatic pseudocyst I&D Revision infected hip hemiarthroplasty, Hickman catheter Septic elbow I&D Infected TKA I&D w/polyethylene exchange
Knee removal of hardware THA Abbreviations: I&D, incision and drainage; ORIF, open reduction internal fixation; THA, total hip arthroplasty; TKA, total knee arthroplasty; vac, negative pressure.
than 1 cfu/cm2 of the clinical environment.9 The purpose of the current study was to measure microbial surface contamination and test the hypotheses that: (1) microbial surface contamination in the operating room after standard operating room turnover following infected cases is not significantly greater than that following noninfected (clean) cases; and (2) the organisms found on the cleaned operating room surfaces do not correspond to those organisms isolated intraoperatively from the infected patient from the previous case.
Materials and Methods This study received institutional review board approval. The authors monitored 14 infected and 16 noninfected (clean) cases
undergoing open surgical treatment at an academic medical center with 14 operating rooms (Table 1). All surgical subspecialties (orthopedics, general surgery, vascular surgery, urology, obstetrics/gynecology, neurosurgery, otolaryngology, plastic surgery) were included. Unscheduled cases, video-assisted or percutaneous procedures, after-hour cases, and terminally cleaned rooms were excluded from data collection. Infected cases treated by open surgical debridement were confirmed as infected using intraoperative records and laboratory data (wound culture results). Using Replicate Organism Detection and Counting (RODAC) stamp plates (Becton, Dickinson and Company, BD Diagnostic Systems, Sparks, Maryland),
ORTHOPEDICS | Healio.com/Orthopedics
n Feature Article
Table 2
Comparison of Clean Cases and Infected Cases for All Variablesa Variable
Clean Cases (n=16)
Infected Cases (n=14)
Surgical time, min
169 (138-200)
136 (59-213)
Room humidity, %
47 (42-52)
53 (40-65)
Room temperature, °F
68 (65-71)
68 (66-69)
Air exchanges, no.
23.8 (22.5-25.2)
24.1 (20.7-27.5)
0.05 (0.028-0.067)
0.02 (-0.03-0.07)
22 (14.2-29.8)
27 (8-46)
Colony count at 24 h, cfu/ case
7.4 (5.4-9.4)
8.2 (5.3-11.1)
Colony count at 48 h, cfu/ case
10.6 (7.2-14.0)
15.6 (10.7-20.4)
Room pressure, inches of H20 Turnover time, min
Abbreviations: cfu, colony-forming units; h, hours; min, minutes. a Reported as mean values with 95% confidence intervals in parentheses.
9 different, reproducible operating room surfaces were sampled after standard cleaning practices (2 on the operating room table, 2 on the surgical instrument table, and 1 each on the arm board, Mayo stand, anesthesia cart, operating room light panel, and main operating room door handle) following the surgical treatment of 14 infected and 16 clean cases. Data were collected over approximately 2 months (February 15-21, 2012, and July 2-29, 2012, times of primary investigator availability). The use of RODAC plates is an established method for the evaluation of environmental surface contamination.10 Before the operating room was used for the next surgical case, all surfaces were sampled immediately after standard operating room turnover using standard RODAC sampling methods for any given sample collection. For each case, the following were recorded before the RODAC samples were collected: the type of surgical procedure; procedure time; room humidity, temperature, ambient air pressure, and air exchanges; and operating room turnover time. Infected and clean cases were compared for these potential confounders to ensure that cases were equally matched.
APRIL 2014 | Volume 37 • Number 4
Immediately after sampling operating room surfaces, the RODAC plates were transferred to the institution’s microbiology laboratory. All plates were incubated at 37°C for 48 hours. The RODAC agar plates were evaluated for bacterial growth at 24 and 48 hours, and those positive for growth were reported as colony-forming units (cfu)/(RODAC plate surface area or 33.2 cm2). At 48 hours, each colony was morphologically characterized, and a Gram stain was performed. No additional identification was obtained for Gram-positive rods with the characteristic microscopic appearance consistent with Bacillus spp or Corynebacterium spp. Gram-positive cocci were further characterized using standard bench-level identification methods as established by the clinical laboratory’s common procedure manual, the Clinical Microbiology Procedures Handbook.11 Gram-positive cocci in clusters that were catalase positive and further tested negative for coagulase using the Staphaurex test (Remel, Lenexa, Kansas) were recorded as coagulase-negative Staphylococcus spp (CoNS) and not further identified to species level. Gram-positive, catalase-positive cocci in clusters that tested positive for coagulase
were recorded as S aureus, and testing for the methicillin resistance was performed using MRSASelect agar (BioRad Laboratories, Redmond, Washington). Organism identification for Gram-negative bacilli was performed using the API20-E and API20-NE methods (bioMérieux, Durham, North Carolina). The organisms identified from the RODAC plates were compared to the clinical test and culture results of infected patients to evaluate concordance. The authors checked for significant (P
Microbial Surface Contamination After Standard Operating Room Cleaning Practices Following Surgical Treatment of Infection Rishi Balkissoon, MD, MPH; Tariq Nayfeh, MD, PhD; Kerri L. Adams, MS, RN; Stephen M. Belkoff, PhD, MPH; Stefan Riedel, MD, PhD; Simon C. Mears, MD, PhD
abstract Full article available online at Healio.com/Orthopedics. Search: 20140401-53 At the authors’ institution, some joint arthroplasty surgeons require the operating room to be terminally cleaned before using the room after infected cases, in theory to decrease exposure to excessive microbial contamination for the subsequent patient. The authors found no guidance in the literature to support this practice. To test this theory, the authors measured microbial surface contamination from 9 surfaces in operating rooms after standard operating room turnover following 14 infected cases vs 16 noninfected cases. A check was made for an association between organisms isolated intraoperatively from infected surgical patients immediately preceding standard cleaning and organisms isolated from common operating room surfaces. Colony counts were made at 24 and 48 hours, and organisms were identified. No significant difference was noted in colony counts between infected and noninfected cases, and no relationship was found between organisms isolated from infected cases and those from operating room surfaces. Furthermore, the largest colony count from both groups (0.08 cfu/cm2) was an order of magnitude less than the recently proposed 5 cfu/cm2 threshold for surface hygiene in hospitals. This finding indicates that standard operating room turnover results in minimal surface contamination, regardless of the previous case’s infection status, and that there is no need for a more extensive terminal cleaning after an infected case. The authors are from the Department of Orthopaedic Surgery (RB, TN, SMB, SCM), The Johns Hopkins University/Johns Hopkins Bayview Medical Center, Baltimore; Infection Control (KLA), Johns Hopkins Bayview Medical Center, Baltimore; and the Department of Pathology (SR), Division of Microbiology, The Johns Hopkins University/Johns Hopkins Bayview Medical Center, Baltimore, Maryland. Drs Balkissoon, Belkoff, Riedel, and Mears and Ms Adams have no relevant financial relationships to disclose. Dr Nayfeh received a financial contribution to his Infection Study of less than $30,000 from a private individual. The authors thank Lisa Dam, MT (ASCP), for her support in the clinical microbiology laboratory during the processing and assessment of the bacterial cultures. Correspondence should be addressed to: Stephen M. Belkoff, PhD, MPH, c/o Elaine P. Henze, BJ, ELS, Medical Editor and Director, Editorial Services, Department of Orthopaedic Surgery, The Johns Hopkins University/Johns Hopkins Bayview Medical Center, 4940 Eastern Ave, #A665, Baltimore, MD 21224-2780 ([email protected]). Received: July 25, 2013; Accepted: November 8, 2013; Posted: April 15, 2014. doi: 10.3928/01477447-20140401-53
APRIL 2014 | Volume 37 • Number 4
e339
n Feature Article
C
oncern exists that contaminated environmental surfaces contribute to the transmission of infection in the health care setting. Antibiotic-resistant organisms, including methicillin-resistant Staphylococcus aureus (MRSA), vancomycin-resistant enterococci, and Clostridium difficile, can remain viable on dry surfaces for prolonged periods.1 Methicillin-resistant S aureus is a contaminant found in hospitals2,3 that is associated with transmission on hospital wards and intensive care units1,4-6 and is responsible for substantial periprosthetic joint infections after joint arthroplasty. The surgical patient is particularly vulnerable in the operating room with open wounds exposed to the environment. Some joint arthroplasty surgeons at the authors’ institution avoid using operating rooms after infected cases. Anecdotally, those surgeons require an extensive “terminal cleaning” before performing an arthroplasty after such a case. This practice stems from concern that these rooms may be excessively contaminated, potentially increasing the risk for subsequent surgical-site infection. However, the efficacy of this practice is untested and it likely requires higher operating costs and operating room scheduling strategies that complicate optimal patient care. Few studies have investigated environmental pathogenic contamination in the operating room. The level of operating room surface contamination that can influence surgical-site infection rates is not known, but a clean surgical environment is expected to reduce the number of pathogens available for potential transmission.7 Currently, operating room cleaning standards as outlined by the Association of periOperative Registered Nurses7 and the Centers for Disease Control and Prevention8 are not universal and in addition are vague in their description of goals. It has been recently recommended that “indicator organisms” (eg, MRSA, C difficile, multiply resistant Gram-negative bacilli, vancomycin-resistant enterococci, and Salmonella spp) should be found in less
e340
Table 1
Cases Enrolled Clean Cases (n=16)
Infected Cases (n=14)
THA
Knee infected prepatellar bursitis I&D and closure
TKA
Hip infected wound I&D, vac dressing application
TKA
Chronic leg infection I&D w/vac dressing application
TKA Revision TKA for periprosthetic fracture Conversion of hip resurfacing to THA Distal radius fracture ORIF I&D scrotal wound, split-thickness skin graft application TKA TKA Quadriceps tendon repair TKA Inguinal hernia repair Revision breast reconstruction
Infected TKA single-stage revision Second toe amputation for infection Hip infected wound I&D Hip removal of hardware, I&D, resection arthroplasty Perirectal abscess I&D Arm abscess and wound infection I&D Perirectal abscess I&D Laparotomy w/infected pancreatic pseudocyst I&D Revision infected hip hemiarthroplasty, Hickman catheter Septic elbow I&D Infected TKA I&D w/polyethylene exchange
Knee removal of hardware THA Abbreviations: I&D, incision and drainage; ORIF, open reduction internal fixation; THA, total hip arthroplasty; TKA, total knee arthroplasty; vac, negative pressure.
than 1 cfu/cm2 of the clinical environment.9 The purpose of the current study was to measure microbial surface contamination and test the hypotheses that: (1) microbial surface contamination in the operating room after standard operating room turnover following infected cases is not significantly greater than that following noninfected (clean) cases; and (2) the organisms found on the cleaned operating room surfaces do not correspond to those organisms isolated intraoperatively from the infected patient from the previous case.
Materials and Methods This study received institutional review board approval. The authors monitored 14 infected and 16 noninfected (clean) cases
undergoing open surgical treatment at an academic medical center with 14 operating rooms (Table 1). All surgical subspecialties (orthopedics, general surgery, vascular surgery, urology, obstetrics/gynecology, neurosurgery, otolaryngology, plastic surgery) were included. Unscheduled cases, video-assisted or percutaneous procedures, after-hour cases, and terminally cleaned rooms were excluded from data collection. Infected cases treated by open surgical debridement were confirmed as infected using intraoperative records and laboratory data (wound culture results). Using Replicate Organism Detection and Counting (RODAC) stamp plates (Becton, Dickinson and Company, BD Diagnostic Systems, Sparks, Maryland),
ORTHOPEDICS | Healio.com/Orthopedics
n Feature Article
Table 2
Comparison of Clean Cases and Infected Cases for All Variablesa Variable
Clean Cases (n=16)
Infected Cases (n=14)
Surgical time, min
169 (138-200)
136 (59-213)
Room humidity, %
47 (42-52)
53 (40-65)
Room temperature, °F
68 (65-71)
68 (66-69)
Air exchanges, no.
23.8 (22.5-25.2)
24.1 (20.7-27.5)
0.05 (0.028-0.067)
0.02 (-0.03-0.07)
22 (14.2-29.8)
27 (8-46)
Colony count at 24 h, cfu/ case
7.4 (5.4-9.4)
8.2 (5.3-11.1)
Colony count at 48 h, cfu/ case
10.6 (7.2-14.0)
15.6 (10.7-20.4)
Room pressure, inches of H20 Turnover time, min
Abbreviations: cfu, colony-forming units; h, hours; min, minutes. a Reported as mean values with 95% confidence intervals in parentheses.
9 different, reproducible operating room surfaces were sampled after standard cleaning practices (2 on the operating room table, 2 on the surgical instrument table, and 1 each on the arm board, Mayo stand, anesthesia cart, operating room light panel, and main operating room door handle) following the surgical treatment of 14 infected and 16 clean cases. Data were collected over approximately 2 months (February 15-21, 2012, and July 2-29, 2012, times of primary investigator availability). The use of RODAC plates is an established method for the evaluation of environmental surface contamination.10 Before the operating room was used for the next surgical case, all surfaces were sampled immediately after standard operating room turnover using standard RODAC sampling methods for any given sample collection. For each case, the following were recorded before the RODAC samples were collected: the type of surgical procedure; procedure time; room humidity, temperature, ambient air pressure, and air exchanges; and operating room turnover time. Infected and clean cases were compared for these potential confounders to ensure that cases were equally matched.
APRIL 2014 | Volume 37 • Number 4
Immediately after sampling operating room surfaces, the RODAC plates were transferred to the institution’s microbiology laboratory. All plates were incubated at 37°C for 48 hours. The RODAC agar plates were evaluated for bacterial growth at 24 and 48 hours, and those positive for growth were reported as colony-forming units (cfu)/(RODAC plate surface area or 33.2 cm2). At 48 hours, each colony was morphologically characterized, and a Gram stain was performed. No additional identification was obtained for Gram-positive rods with the characteristic microscopic appearance consistent with Bacillus spp or Corynebacterium spp. Gram-positive cocci were further characterized using standard bench-level identification methods as established by the clinical laboratory’s common procedure manual, the Clinical Microbiology Procedures Handbook.11 Gram-positive cocci in clusters that were catalase positive and further tested negative for coagulase using the Staphaurex test (Remel, Lenexa, Kansas) were recorded as coagulase-negative Staphylococcus spp (CoNS) and not further identified to species level. Gram-positive, catalase-positive cocci in clusters that tested positive for coagulase
were recorded as S aureus, and testing for the methicillin resistance was performed using MRSASelect agar (BioRad Laboratories, Redmond, Washington). Organism identification for Gram-negative bacilli was performed using the API20-E and API20-NE methods (bioMérieux, Durham, North Carolina). The organisms identified from the RODAC plates were compared to the clinical test and culture results of infected patients to evaluate concordance. The authors checked for significant (P
