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Concentration of bacteria passing through puncture holes in surgical gloves
Concentration of bacteria passing through puncture holes in surgical gloves Julian-Camill Harnoß,a,b Lars-Ivo Partecke, MD,b Claus-Dieter Heidecke, MD, PhD,b Nils-Olaf Hu¨bner, MD,a Axel Kramer, MD, PhD,a and Ojan Assadian, MD, DTMHc Greifswald, Germany, and Vienna, Austria
Background: The reasons for gloving-up for surgery are to protect the surgical field from microorganisms on the surgeon’s hands and protect the surgeon from the patient’s microorganisms. This study measured the concentration of bacteria passing through glove punctures under surgical conditions. Methods: Double-layered surgical gloves were worn during visceral surgeries over a 4-month period. The study included 128 outer gloves and 122 inner gloves from 20 septic laparotomies. To measure bacterial passage though punctures, intraoperative swabs were made, yielding microorganisms that were compared with microorganisms retrieved from the inner glove layer using a modified Gaschen bag method. Results: Depending on the duration of glove wear, the microperforation rate of the outer layer averaged 15%. Approximately 82% of the perforations went unnoticed by the surgical team. Some 86% of perforations occurred in the nondominant hand, with the index finger being the most frequently punctured location (36%). Bacterial passage from the surgical site through punctures was detected in 4.7% of the investigated gloves. Conclusion: Depending on the duration of wear, surgical gloves develop microperforations not immediately recognized by staff. During surgery, such perforations allow passage of bacteria from the surgical site through the punctures. Possible strategies for preventing passage of bacteria include strengthening of glove areas prone to punctures and strict glove changing every 90 minutes. Key Words: Surgical glove; double-gloving; (micro-) perforation; bacterial transmission; crossinfection. Copyright ª 2010 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved. (Am J Infect Control 2010;38:154-8.)
Wearing sterile gloves is the most effective method of preventing the transmission of bacteria from hospital personnel to patients and vice versa. The latter aspect has become more important since the beginning of the human immunodeficiency virus pandemic in the 1980s.1 Staff safety is paramount, and the reliability and efficacy of surgical gloves are crucial to this. Yet the glove perforation rate is as high as 78% in high-risk procedures.2-8 Previous studies have shown that glove puncture rates and bacterial counts of hands increase with increasing operation time.3 Therefore, it is recommended From the Institute for Hygiene and Environmental Medicine,a Department for General and Visceral Surgery,b Ernst Moritz Arndt University, Greifswald, Germany; and Clinical Institute for Hygiene and Medical Microbiology, Division for Hospital Hygiene, Vienna General Hospital, Medical University of Vienna, Vienna, Austria.c Address correspondence to Prof. Ojan Assadian, MD, DTMH, Clinical Institute for Hygiene and Medical Microbiology, Medical University Vienna, General Hospital Vienna, Waehringer Guertel 18-20, 1090 Vienna, Austria. E-mail: [email protected]. 0196-6553/$36.00 Copyright ª 2010 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved. doi:10.1016/j.ajic.2009.06.013
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that both gloves be changed when a puncture is detected. Before new gloves are donned, hands should be disinfected. Although laboratory-based methods have been published that support the identification of the inoculation volume involving needles9 or the evidence of viruses released through puncture holes in gloves,10 surprisingly little is known about the amount of bacteria passing trough puncture holes in surgical gloves. The aim of the present study was to develop a repeatable method that allows direct measurement of the amount of bacteria passing through punctures caused by microperforations under practical surgical conditions. In contrast to the use of an electronic device that produces an alarm signal following a puncture of a surgical glove or simple bacterial sampling from surgeons’ hands after surgical procedures, in this study we identified bacteria directly originating from the patient passing through puncture holes to the hands of the surgical team.
METHODS The passage of bacteria from patients to the hands of surgical staff through puncture holes in gloves was investigated using a modified Gaschen bag method.11 Two glove layers were used, an unpunctured inner
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Fig 1. Location of artificial perforations in the laboratory-based in vitro test. glove and a punctured outer glove. Microorganisms obtained from the surface of the inner glove after removal of the outer glove were regarded as originating from the patient or the surgical field. Peha-taft powder-free gloves (Hartmann, Vienna, Austria) and Biogel doublegloving gloves (Mo¨lnlycke, Gothenburg, Sweden) were used for this study. We first established and evaluated the method as a controlled, laboratory-based in vitro study, then investigated the passage of bacteria from patients to the inner glove under practical conditions during 20 elective and emergency visceral laparotomies.
In vitro test First, 1 mL of a test suspension adjusted to 1.7 3 109 colony-forming units (cfu)/mL of Escherichia coli was applied to he hands of volunteers wearing sterile Peha-taft Powderfree gloves. The volunteers rubbed both hands thoroughly and let the test suspension dry for 5 minutes. To determine the recovery rate from the prepared gloves, gloved hands were shaken out for 15 seconds in a sterile plastic bag (‘‘Gaschen bag’’) containing 50 mL of physiological saline. The Gaschen bag fluid was retrieved, and serial dilutions at dilution steps of 1025 and 1027 were incubated on CSA (Caseinpepton-sojapepton) agar plates (105458, MERCK, Darmstadt, Germany) for 48 hours at 378C. The cfu/mL retrieved from the Gaschen bag fluid was counted and compared with the initial concentration of the organisms.
In the second step, Biogel double-gloving gloves were used. The outer layers of both gloved hands were perforated repeatedly with a 22 G needle using the same technique at defined locations (Fig 1).1 After 20 minutes, 1 mL of the E coli suspension at a concentration of 8.48 3 108 was applied in 100-mL consecutive increments onto the outer glove and rubbed in. Then the outer glove was removed, and the inner glove was shaken out in a Gaschen bag as described above. Each hand was sampled separately. Serial dilutions of 1021 and 1023 were prepared with the filtered content of the Gaschen bags. After an incubation period of 48 hours at 378C, the cfu/mL was calculated, quantified, and compared with the initial concentration of the organisms.
Testing under practical surgical conditions Over a 4-month period, Biogel double-gloving gloves were consecutively used at the Department for General and Visceral Surgery, Ernst Moritz Arndt University for all septic laparotomies and subsequently investigated. A total of 20 elective and emergency surgical laparotomies were followed up, including perforations and resections of the gastrointestinal tract, septic pancreas surgeries, abdominal lavages for underlying peritonitis, and explorative laparotomies. Similar to the laboratory-based model, the inner glove was examined after the outer glove was removed during glove changes between procedures, using the modified Gaschen bag procedure. The person wearing the glove, his or her role on the surgical team, the type of surgery, date,
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Fig 2. Comparison of the bacterial concentrations applied to artificially perforated outer layers and bacterial concentrations retrieved in the Gaschen bag. The figure shows passage of bacteria at a concentration of up to 6 log10 through perforated surgical gloves. More bacteria were found on the left inner gloves than on the right inner gloves. Because the left outer gloves had more perforations than the right outer gloves, it can be concluded that the number of bacteria transferred was correlated with the number of glove punctures. duration of glove wearing, and condition of surgery (emergency or elective) were documented. All members of the surgical team were right-handed. Gloves were grouped according to the duration of wear time: group I, ,90 minutes; group II, between 91 and 150 minutes; group III, .151 minutes. The gloves were then examined for perforations using the impermeability test according to DIN EN 455-1.12 Each inner and outer layer was evaluated separately. Perforations reported by staff were compared with the true microperforations detected immediately after each surgical procedure using the impermeability test, and numbers and locations were recorded. Surgical sites were examined by obtaining swabs, which were processed following standard microbiological methods. The collected Gaschen bag fluid was microbiologically processed by membrane filtration. Examination of microorganisms did not include anaerobic bacteria, spores, or viruses.
RESULTS For the first part of the laboratory-based in vitro tests, 5 volunteers with a total of 10 Gaschen bag examinations yielded E coli retrieval of 1.36 3 108/mL after an initial inoculation of 1.7 3 109/mL. The bacterial loss was only 1 log10 step. The second part of the test, with artificial perforation of the outer glove of double-gloving surgical gloves, showed that the quantity of detected bacteria can be analyzed more exactly by filtration of the physiological saline than by quantification in dilutions. An average of 4.04 3 102/mL of E coli out of the initial inoculation of 8.48 3 108/mL applied organisms passed though the artificial perforations in 3 volunteers (Fig 2). The amount of retrieved E coli
Fig 3. Examined gloves stratified by duration of wear. correlated with the number of artificial perforations (Fig 2); the outer glove of the right hand had 6 microperforations, while the outer glove of the left hand had 10 microperforations in 2 volunteers and 12 microperforations in 1 volunteer. In the investigation, under practical surgical conditions, 128 outer gloves and 122 corresponding inner gloves from 20 surgical procedures were examined. The average duration of wear time was 128 minutes (125 minutes for outer gloves and 131 minutes for inner gloves; range for all gloves, 25 to 285 minutes; Fig 3). Overall, 21.1% of the outer gloves (27/128) and 14.8% of the inner gloves (18/122) were perforated. The frequency of perforation correlated with the duration of
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Table 1. Correlation between duration of glove wear and frequency of glove perforation Duration of wear, minutes ,90 minutes (group 1) 91 to 150 minutes (group 2) .151 minutes (group 3) Total
Examined gloves
Inner gloves
Outer gloves
Perforated gloves, n (%)
Perforated inner layers, n (%)
Perforated outer layers, n (%)
86 84 80 250
40 42 40 122
46 42 40 128
4 (4.7%) 20 (23.8%) 21(26.3%) 45 (18.0%)
0 8 (19.0%) 10 (25.0%) 18 (14.8%)
4 (8.7%) 12 (28.6%) 11 (27.5%) 27 (21.1%)
Table 2. Bacterial passage from the operative site through punctures No.
Hand
Duration, minutes
Perforation (location/size)
1 2 3 4
Left Left Left Left
105 105 90 205
Index finger/medium Palm/medium Index finger/medium Thumb/large
5
Right
255
Thumb/large
6 7
Left Right
125 125
Index finger/large Not detected
Identical organisms found on inner glove and in operative site S lentus S lentus S xylosus E coli, K pneumoniae, Enterococcus faecium, Micrococcus spp E faecium, Acinetobacter lwoffii, aerobic spore-forming bacteria K pneumoniae, E faecium K pneumoniae, E faecium
NOTE. All retrieved bacteria were identified by morphology, biochemical properties, and resistance profile.
glove wear (Table 1). Of these 45 microperforations, 82.2% (37/45) went unnoticed by the surgical staff. In 37.5% of the cases (3/8), a least 1 perforation already existed at the time when the puncture was noticed. In 48.1% (13 of 27) of the perforated outer gloves, a perforation of the inner glove was found at the corresponding site. In the outer gloves, a single perforation was found in 13.3% (17/128), 2 perforations were found in 3.1% (4/128), and 3 perforations were found in 4.7% (6/128); 86% (37/43) of the perforations occurred in the outer left glove. The index finger of the nondominant hand was the most commonly affected location for all perforations of the outer glove (32.6%; 14/43). The passage of microorganisms through the puncture hole was demonstrated in 4.7% (6/128) of the outer gloves examined. The index finger of the nondominant hand was the entry point in 50.0% (3/6) of these passages (Table 2). The bacteria retrieved from the inner gloves included staphylococci (2 and 4 cfu/mL S lentus and 1 cfu/mL S xylosus), enterococci (18, 7, and .1000 cfu/mL), Klebsiella spp (2 and .1000 cfu/mL after 24 hours), aerobic spore-forming bacteria (2 cfu/mL), Micrococcus spp (1 cfu/mL), and E coli (2 cfu/mL).
DISCUSSION Our study, performed under practical surgical conditions in the operating theatre, showed that direct bacterial passage from the patient through a glove puncture on the hand occurred in almost 5% (6/128) of all gloves
worn. This observation is important for staff safety, as the spectrum of microorganisms passing through punctures on the hand is not limited to bacteria, but certainly includes viruses as well.10,13 Furthermore, our study reconfirms that the frequency of microperforation is correlated with the duration of glove wearing, supporting results obtained previously by others3 and our group.14 Also, the higher frequency of perforations observed on the index finger of the nondominant hand is in agreement with previous results.14-18 Another finding that can be concluded from our study is that even in heavily contaminated septic laparotomies, a single glove prevented bacterial transmission in .95% (122/128) of cases through a glove puncture site. Because ,50% (13/27) of these outer glove perforations have corresponding inner glove perforations, double gloves should be mandatory in all major surgical procedures, especially those involving heavy contamination or of long duration. It is tempting to speculate that wearing an additional glove in the course of this study reduced the risk of perforation of the inner glove. This speculation is supported by findings of Tanner et al.19 The frequency of microbial passage through perforation of the outer and inner gloves in our study, 4.7% (6/128), was also similar that reported by Ganczak et al,15 who reported a 4.1% rate of viral passage. Thomas et al20 and Caillot et al21 also reported a comparable frequency of undetected microperforation of about 80%, in agreement with our results (82%; 37/45). Even in defects noticed by the surgical team,
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37.5% (3/8) of the gloves had been perforated earlier in at least at one other location. This indicates that a reduced barrier function of the gloves already existed before a member of the surgical team even noticed a puncture. Because most of the perforations occurred at the palmar side of the hand, they were easily missed. Other studies have show that using an indicator glove can significantly improve the detection of perforations.5,21-23 But because in 48.1% (13/27) of perforations of the outer glove, a perforation of the inner glove was found at the corresponding site, simply changing the outer glove would appear to be insufficient to protect staff. In this study, staphylococci, micrococci, and enterococci in particular were found to pass from the operation site through punctures. This finding is in line with results reported by Al-Maiyah et al24 and with other studies in which a similar microbial spectrum was retrieved.25,26 However, other bacteria originating from the gastrointestinal tract obtained in the Gaschen bag have not been identified as organisms penetrating the punctured glove. Because swabbing is a sampling technique with low sensitivity, the missing correlation might be explained by the limits of the method. Interestingly, in one case, identical bacteria were found both on the inner glove and at the surgical site (Table 2). In this case, either the organisms were transferred due to insufficiently tight gloves or the size of the perforation was below our detection limit using the impermeability test according to DIN EN 455-1.
CONCLUSION With increasing duration of wear, surgical gloves develop microperforations that are not immediately detectable by staff. Our findings show that under practical conditions during surgery, such perforations allow the passage of bacteria from the operative site through the punctured glove. Possible strategies for preventing punctures include improving the gloves’ barrier function by double-gloving, strengthening puncture-prone sites, or strict glove changing every 90 minutes. References 1. Hansen KN, Korniewicz DM, Hexter DA, Kornilow JR, Kelen GD. Loss of glove integrity during emergency department procedures. Ann Emerg Med 1998;31:65-72. 2. Eckford SD, James M, Jackson SR, Hamer AJ, Browning JJ. Detection of glove punctures and skin contamination during caesarean section. Br J Obstet Gynaecol 1997;104:1209-11. 3. Eklund AM, Ojaja¨rvi J, Laitinen K, Valtonen M, Werkkala KA. Glove punctures and postoperative skin flora of hands in cardiac surgery. Ann Thorac Surg 2002;74:149-53. 4. Godin MS, Lavernia C, Harris JP. Occult surgical glove perforations in otolaryngology head and neck surgery. Arch Otolaryngol Head Neck Surg 1991;117:910-3.
American Journal of Infection Control March 2010 5. Laine T, Kaipia A, Santavirta J, Aarnio P. Glove perforations in open and laparoscopic abdominal surgery: the feasibility of double-gloving. Scand J Surg 2004;93:73-6. 6. Marin-Bertolin S, Gonza´les-Martinez R, Gime´nez CN, Marquina Vila P, Amorrortu-Velayos J. Does double-gloving protect surgical staff from skin contamination during plastic surgery? Plast Reconstr Surg 1997; 99:956-60. 7. Schiffner U. Defect rate of disposable gloves after longer treatment duration. Dtsch Zahnarztl Z 1989;44:661-3. 8. Pitten FA, Herdemann G, Kramer A. The integrity of latex gloves in clinical dental practice. Infection 2000;28:388-92. 9. Lefebvre DR, Strande LF, Hewitt CW. An enzyme-mediated assay to quantify inoculation volume delivered by suture needlestick injury: two gloves are better than one. J Am Coll Surg 2008;206:113-22. 10. O’Connell KP, El-Masri M, Broyles JB, Korniewicz DM. Testing for viral penetration of non-latex surgical and examination gloves: a comparison of three methods. Clin Microbiol Infect 2004;10:322-6. 11. Gaschen M. Comparative study on 2 methods for sampling the microbial flora of hands. Helv Chir Acta 1968;35:372-7. 12. European Committee for Standardization. EN 455: medical gloves for single use. Brussels: European Committee for Standardization; 2000. 13. Krikorian R, Lozach-Perlant A, Ferrier-Rembert A, Hoerner P, Sonntag P, Garin D, et al. Standardization of needlestick injury and evaluation of a novel virus-inhibiting protective glove. J Hosp Infect 2007;66:339-45. 14. Partecke LI, Goerdt AM, Langner I, Jaeger B, Assadian O, Heidecke CD, et al. The incidence of microperforation in surgical gloves depends on duration of wearing. Infect Control Hosp Epidemiol 2009;30:409-14. 15. Ganczak M, Bialecki P, Bohatyrewicz A. Double-gloving in reducing the interoperative risk of bloodborne pathogens. Chir Narzadow Ruchu Ortop Pol 2004;69:249-54. 16. Chan KY, Singh VA, Oun BH, To BH. The rate of glove perforations in orthopaedic procedures: single-versus double-gloving. A prospective study. Med J Malaysia 2006;61:S3-7. 17. Thanni LO, Yinusa W. Incidence of glove failure during orthopedic operations and the protective effect of double gloves. J Natl Med Assoc 2003;95:1184-8. 18. Punyatanasakchai P, Chittacharoen A, Ayudhya NI. Randomized controlled trial of glove perforation in single- and double-gloving in episiotomy repair after vaginal delivery. J Obstet Gynaecol Res 2004;30: 354-7. 19. Tanner J, Parkinson H. Double-gloving to reduce surgical crossinfection. Cochrane Database Syst Rev 2006;3:CD003087. 20. Thomas S, Agarwal M, Mehta G. Intraoperative glove perforation: single- versus double-gloving in protection against skin contamination. Postgrad Med J 2001;77:458-60. 21. Caillot JL, Paparel P, Arnal E, Schreiber V, Voiglio EJ. Anticipated detection of imminent surgeon–patient barrier breaches: a prospective randomized controlled trial using an indicator underglove system. World J Surg 2006;30:134-8. 22. Florman S, Burgdorf M, Finigan K, Slakey D, Hewitt R, Nicols RL. Efficacy of double gloving with an intrinsic indicator system. Surg Infect (Larchmt) 2005;6:385-95. 23. Laine T, Aarnio P. Glove perforation in orthopaedic and trauma surgery: a comparison between single, double indicator gloving and double gloving with two regular gloves. J Bone Joint Surg Br 2004;86: 898-900. 24. Al-Maiyah M, Bajwa A, Mackenney P, Port A, Gregg PJ, Hill D, et al. Glove perforation and contamination in primary total hip arthroplasty. J Bone Joint Surg Br 2005;87:556-9. 25. Davis N, Curry A, Gambhir AK, Panigrahi H, Walker CR, Wilkins EG, et al. Intraoperative bacterial contamination in operations for joint replacement. J Bone Joint Surg Br 1999;81:886-9. 26. Cole RP, Gault DT. Glove perforation during plastic surgery. Br J Plast Surg 1989;42:481-3.
Background: The reasons for gloving-up for surgery are to protect the surgical field from microorganisms on the surgeon’s hands and protect the surgeon from the patient’s microorganisms. This study measured the concentration of bacteria passing through glove punctures under surgical conditions. Methods: Double-layered surgical gloves were worn during visceral surgeries over a 4-month period. The study included 128 outer gloves and 122 inner gloves from 20 septic laparotomies. To measure bacterial passage though punctures, intraoperative swabs were made, yielding microorganisms that were compared with microorganisms retrieved from the inner glove layer using a modified Gaschen bag method. Results: Depending on the duration of glove wear, the microperforation rate of the outer layer averaged 15%. Approximately 82% of the perforations went unnoticed by the surgical team. Some 86% of perforations occurred in the nondominant hand, with the index finger being the most frequently punctured location (36%). Bacterial passage from the surgical site through punctures was detected in 4.7% of the investigated gloves. Conclusion: Depending on the duration of wear, surgical gloves develop microperforations not immediately recognized by staff. During surgery, such perforations allow passage of bacteria from the surgical site through the punctures. Possible strategies for preventing passage of bacteria include strengthening of glove areas prone to punctures and strict glove changing every 90 minutes. Key Words: Surgical glove; double-gloving; (micro-) perforation; bacterial transmission; crossinfection. Copyright ª 2010 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved. (Am J Infect Control 2010;38:154-8.)
Wearing sterile gloves is the most effective method of preventing the transmission of bacteria from hospital personnel to patients and vice versa. The latter aspect has become more important since the beginning of the human immunodeficiency virus pandemic in the 1980s.1 Staff safety is paramount, and the reliability and efficacy of surgical gloves are crucial to this. Yet the glove perforation rate is as high as 78% in high-risk procedures.2-8 Previous studies have shown that glove puncture rates and bacterial counts of hands increase with increasing operation time.3 Therefore, it is recommended From the Institute for Hygiene and Environmental Medicine,a Department for General and Visceral Surgery,b Ernst Moritz Arndt University, Greifswald, Germany; and Clinical Institute for Hygiene and Medical Microbiology, Division for Hospital Hygiene, Vienna General Hospital, Medical University of Vienna, Vienna, Austria.c Address correspondence to Prof. Ojan Assadian, MD, DTMH, Clinical Institute for Hygiene and Medical Microbiology, Medical University Vienna, General Hospital Vienna, Waehringer Guertel 18-20, 1090 Vienna, Austria. E-mail: [email protected]. 0196-6553/$36.00 Copyright ª 2010 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved. doi:10.1016/j.ajic.2009.06.013
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that both gloves be changed when a puncture is detected. Before new gloves are donned, hands should be disinfected. Although laboratory-based methods have been published that support the identification of the inoculation volume involving needles9 or the evidence of viruses released through puncture holes in gloves,10 surprisingly little is known about the amount of bacteria passing trough puncture holes in surgical gloves. The aim of the present study was to develop a repeatable method that allows direct measurement of the amount of bacteria passing through punctures caused by microperforations under practical surgical conditions. In contrast to the use of an electronic device that produces an alarm signal following a puncture of a surgical glove or simple bacterial sampling from surgeons’ hands after surgical procedures, in this study we identified bacteria directly originating from the patient passing through puncture holes to the hands of the surgical team.
METHODS The passage of bacteria from patients to the hands of surgical staff through puncture holes in gloves was investigated using a modified Gaschen bag method.11 Two glove layers were used, an unpunctured inner
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Fig 1. Location of artificial perforations in the laboratory-based in vitro test. glove and a punctured outer glove. Microorganisms obtained from the surface of the inner glove after removal of the outer glove were regarded as originating from the patient or the surgical field. Peha-taft powder-free gloves (Hartmann, Vienna, Austria) and Biogel doublegloving gloves (Mo¨lnlycke, Gothenburg, Sweden) were used for this study. We first established and evaluated the method as a controlled, laboratory-based in vitro study, then investigated the passage of bacteria from patients to the inner glove under practical conditions during 20 elective and emergency visceral laparotomies.
In vitro test First, 1 mL of a test suspension adjusted to 1.7 3 109 colony-forming units (cfu)/mL of Escherichia coli was applied to he hands of volunteers wearing sterile Peha-taft Powderfree gloves. The volunteers rubbed both hands thoroughly and let the test suspension dry for 5 minutes. To determine the recovery rate from the prepared gloves, gloved hands were shaken out for 15 seconds in a sterile plastic bag (‘‘Gaschen bag’’) containing 50 mL of physiological saline. The Gaschen bag fluid was retrieved, and serial dilutions at dilution steps of 1025 and 1027 were incubated on CSA (Caseinpepton-sojapepton) agar plates (105458, MERCK, Darmstadt, Germany) for 48 hours at 378C. The cfu/mL retrieved from the Gaschen bag fluid was counted and compared with the initial concentration of the organisms.
In the second step, Biogel double-gloving gloves were used. The outer layers of both gloved hands were perforated repeatedly with a 22 G needle using the same technique at defined locations (Fig 1).1 After 20 minutes, 1 mL of the E coli suspension at a concentration of 8.48 3 108 was applied in 100-mL consecutive increments onto the outer glove and rubbed in. Then the outer glove was removed, and the inner glove was shaken out in a Gaschen bag as described above. Each hand was sampled separately. Serial dilutions of 1021 and 1023 were prepared with the filtered content of the Gaschen bags. After an incubation period of 48 hours at 378C, the cfu/mL was calculated, quantified, and compared with the initial concentration of the organisms.
Testing under practical surgical conditions Over a 4-month period, Biogel double-gloving gloves were consecutively used at the Department for General and Visceral Surgery, Ernst Moritz Arndt University for all septic laparotomies and subsequently investigated. A total of 20 elective and emergency surgical laparotomies were followed up, including perforations and resections of the gastrointestinal tract, septic pancreas surgeries, abdominal lavages for underlying peritonitis, and explorative laparotomies. Similar to the laboratory-based model, the inner glove was examined after the outer glove was removed during glove changes between procedures, using the modified Gaschen bag procedure. The person wearing the glove, his or her role on the surgical team, the type of surgery, date,
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Fig 2. Comparison of the bacterial concentrations applied to artificially perforated outer layers and bacterial concentrations retrieved in the Gaschen bag. The figure shows passage of bacteria at a concentration of up to 6 log10 through perforated surgical gloves. More bacteria were found on the left inner gloves than on the right inner gloves. Because the left outer gloves had more perforations than the right outer gloves, it can be concluded that the number of bacteria transferred was correlated with the number of glove punctures. duration of glove wearing, and condition of surgery (emergency or elective) were documented. All members of the surgical team were right-handed. Gloves were grouped according to the duration of wear time: group I, ,90 minutes; group II, between 91 and 150 minutes; group III, .151 minutes. The gloves were then examined for perforations using the impermeability test according to DIN EN 455-1.12 Each inner and outer layer was evaluated separately. Perforations reported by staff were compared with the true microperforations detected immediately after each surgical procedure using the impermeability test, and numbers and locations were recorded. Surgical sites were examined by obtaining swabs, which were processed following standard microbiological methods. The collected Gaschen bag fluid was microbiologically processed by membrane filtration. Examination of microorganisms did not include anaerobic bacteria, spores, or viruses.
RESULTS For the first part of the laboratory-based in vitro tests, 5 volunteers with a total of 10 Gaschen bag examinations yielded E coli retrieval of 1.36 3 108/mL after an initial inoculation of 1.7 3 109/mL. The bacterial loss was only 1 log10 step. The second part of the test, with artificial perforation of the outer glove of double-gloving surgical gloves, showed that the quantity of detected bacteria can be analyzed more exactly by filtration of the physiological saline than by quantification in dilutions. An average of 4.04 3 102/mL of E coli out of the initial inoculation of 8.48 3 108/mL applied organisms passed though the artificial perforations in 3 volunteers (Fig 2). The amount of retrieved E coli
Fig 3. Examined gloves stratified by duration of wear. correlated with the number of artificial perforations (Fig 2); the outer glove of the right hand had 6 microperforations, while the outer glove of the left hand had 10 microperforations in 2 volunteers and 12 microperforations in 1 volunteer. In the investigation, under practical surgical conditions, 128 outer gloves and 122 corresponding inner gloves from 20 surgical procedures were examined. The average duration of wear time was 128 minutes (125 minutes for outer gloves and 131 minutes for inner gloves; range for all gloves, 25 to 285 minutes; Fig 3). Overall, 21.1% of the outer gloves (27/128) and 14.8% of the inner gloves (18/122) were perforated. The frequency of perforation correlated with the duration of
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Table 1. Correlation between duration of glove wear and frequency of glove perforation Duration of wear, minutes ,90 minutes (group 1) 91 to 150 minutes (group 2) .151 minutes (group 3) Total
Examined gloves
Inner gloves
Outer gloves
Perforated gloves, n (%)
Perforated inner layers, n (%)
Perforated outer layers, n (%)
86 84 80 250
40 42 40 122
46 42 40 128
4 (4.7%) 20 (23.8%) 21(26.3%) 45 (18.0%)
0 8 (19.0%) 10 (25.0%) 18 (14.8%)
4 (8.7%) 12 (28.6%) 11 (27.5%) 27 (21.1%)
Table 2. Bacterial passage from the operative site through punctures No.
Hand
Duration, minutes
Perforation (location/size)
1 2 3 4
Left Left Left Left
105 105 90 205
Index finger/medium Palm/medium Index finger/medium Thumb/large
5
Right
255
Thumb/large
6 7
Left Right
125 125
Index finger/large Not detected
Identical organisms found on inner glove and in operative site S lentus S lentus S xylosus E coli, K pneumoniae, Enterococcus faecium, Micrococcus spp E faecium, Acinetobacter lwoffii, aerobic spore-forming bacteria K pneumoniae, E faecium K pneumoniae, E faecium
NOTE. All retrieved bacteria were identified by morphology, biochemical properties, and resistance profile.
glove wear (Table 1). Of these 45 microperforations, 82.2% (37/45) went unnoticed by the surgical staff. In 37.5% of the cases (3/8), a least 1 perforation already existed at the time when the puncture was noticed. In 48.1% (13 of 27) of the perforated outer gloves, a perforation of the inner glove was found at the corresponding site. In the outer gloves, a single perforation was found in 13.3% (17/128), 2 perforations were found in 3.1% (4/128), and 3 perforations were found in 4.7% (6/128); 86% (37/43) of the perforations occurred in the outer left glove. The index finger of the nondominant hand was the most commonly affected location for all perforations of the outer glove (32.6%; 14/43). The passage of microorganisms through the puncture hole was demonstrated in 4.7% (6/128) of the outer gloves examined. The index finger of the nondominant hand was the entry point in 50.0% (3/6) of these passages (Table 2). The bacteria retrieved from the inner gloves included staphylococci (2 and 4 cfu/mL S lentus and 1 cfu/mL S xylosus), enterococci (18, 7, and .1000 cfu/mL), Klebsiella spp (2 and .1000 cfu/mL after 24 hours), aerobic spore-forming bacteria (2 cfu/mL), Micrococcus spp (1 cfu/mL), and E coli (2 cfu/mL).
DISCUSSION Our study, performed under practical surgical conditions in the operating theatre, showed that direct bacterial passage from the patient through a glove puncture on the hand occurred in almost 5% (6/128) of all gloves
worn. This observation is important for staff safety, as the spectrum of microorganisms passing through punctures on the hand is not limited to bacteria, but certainly includes viruses as well.10,13 Furthermore, our study reconfirms that the frequency of microperforation is correlated with the duration of glove wearing, supporting results obtained previously by others3 and our group.14 Also, the higher frequency of perforations observed on the index finger of the nondominant hand is in agreement with previous results.14-18 Another finding that can be concluded from our study is that even in heavily contaminated septic laparotomies, a single glove prevented bacterial transmission in .95% (122/128) of cases through a glove puncture site. Because ,50% (13/27) of these outer glove perforations have corresponding inner glove perforations, double gloves should be mandatory in all major surgical procedures, especially those involving heavy contamination or of long duration. It is tempting to speculate that wearing an additional glove in the course of this study reduced the risk of perforation of the inner glove. This speculation is supported by findings of Tanner et al.19 The frequency of microbial passage through perforation of the outer and inner gloves in our study, 4.7% (6/128), was also similar that reported by Ganczak et al,15 who reported a 4.1% rate of viral passage. Thomas et al20 and Caillot et al21 also reported a comparable frequency of undetected microperforation of about 80%, in agreement with our results (82%; 37/45). Even in defects noticed by the surgical team,
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37.5% (3/8) of the gloves had been perforated earlier in at least at one other location. This indicates that a reduced barrier function of the gloves already existed before a member of the surgical team even noticed a puncture. Because most of the perforations occurred at the palmar side of the hand, they were easily missed. Other studies have show that using an indicator glove can significantly improve the detection of perforations.5,21-23 But because in 48.1% (13/27) of perforations of the outer glove, a perforation of the inner glove was found at the corresponding site, simply changing the outer glove would appear to be insufficient to protect staff. In this study, staphylococci, micrococci, and enterococci in particular were found to pass from the operation site through punctures. This finding is in line with results reported by Al-Maiyah et al24 and with other studies in which a similar microbial spectrum was retrieved.25,26 However, other bacteria originating from the gastrointestinal tract obtained in the Gaschen bag have not been identified as organisms penetrating the punctured glove. Because swabbing is a sampling technique with low sensitivity, the missing correlation might be explained by the limits of the method. Interestingly, in one case, identical bacteria were found both on the inner glove and at the surgical site (Table 2). In this case, either the organisms were transferred due to insufficiently tight gloves or the size of the perforation was below our detection limit using the impermeability test according to DIN EN 455-1.
CONCLUSION With increasing duration of wear, surgical gloves develop microperforations that are not immediately detectable by staff. Our findings show that under practical conditions during surgery, such perforations allow the passage of bacteria from the operative site through the punctured glove. Possible strategies for preventing punctures include improving the gloves’ barrier function by double-gloving, strengthening puncture-prone sites, or strict glove changing every 90 minutes. References 1. Hansen KN, Korniewicz DM, Hexter DA, Kornilow JR, Kelen GD. Loss of glove integrity during emergency department procedures. Ann Emerg Med 1998;31:65-72. 2. Eckford SD, James M, Jackson SR, Hamer AJ, Browning JJ. Detection of glove punctures and skin contamination during caesarean section. Br J Obstet Gynaecol 1997;104:1209-11. 3. Eklund AM, Ojaja¨rvi J, Laitinen K, Valtonen M, Werkkala KA. Glove punctures and postoperative skin flora of hands in cardiac surgery. Ann Thorac Surg 2002;74:149-53. 4. Godin MS, Lavernia C, Harris JP. Occult surgical glove perforations in otolaryngology head and neck surgery. Arch Otolaryngol Head Neck Surg 1991;117:910-3.
American Journal of Infection Control March 2010 5. Laine T, Kaipia A, Santavirta J, Aarnio P. Glove perforations in open and laparoscopic abdominal surgery: the feasibility of double-gloving. Scand J Surg 2004;93:73-6. 6. Marin-Bertolin S, Gonza´les-Martinez R, Gime´nez CN, Marquina Vila P, Amorrortu-Velayos J. Does double-gloving protect surgical staff from skin contamination during plastic surgery? Plast Reconstr Surg 1997; 99:956-60. 7. Schiffner U. Defect rate of disposable gloves after longer treatment duration. Dtsch Zahnarztl Z 1989;44:661-3. 8. Pitten FA, Herdemann G, Kramer A. The integrity of latex gloves in clinical dental practice. Infection 2000;28:388-92. 9. Lefebvre DR, Strande LF, Hewitt CW. An enzyme-mediated assay to quantify inoculation volume delivered by suture needlestick injury: two gloves are better than one. J Am Coll Surg 2008;206:113-22. 10. O’Connell KP, El-Masri M, Broyles JB, Korniewicz DM. Testing for viral penetration of non-latex surgical and examination gloves: a comparison of three methods. Clin Microbiol Infect 2004;10:322-6. 11. Gaschen M. Comparative study on 2 methods for sampling the microbial flora of hands. Helv Chir Acta 1968;35:372-7. 12. European Committee for Standardization. EN 455: medical gloves for single use. Brussels: European Committee for Standardization; 2000. 13. Krikorian R, Lozach-Perlant A, Ferrier-Rembert A, Hoerner P, Sonntag P, Garin D, et al. Standardization of needlestick injury and evaluation of a novel virus-inhibiting protective glove. J Hosp Infect 2007;66:339-45. 14. Partecke LI, Goerdt AM, Langner I, Jaeger B, Assadian O, Heidecke CD, et al. The incidence of microperforation in surgical gloves depends on duration of wearing. Infect Control Hosp Epidemiol 2009;30:409-14. 15. Ganczak M, Bialecki P, Bohatyrewicz A. Double-gloving in reducing the interoperative risk of bloodborne pathogens. Chir Narzadow Ruchu Ortop Pol 2004;69:249-54. 16. Chan KY, Singh VA, Oun BH, To BH. The rate of glove perforations in orthopaedic procedures: single-versus double-gloving. A prospective study. Med J Malaysia 2006;61:S3-7. 17. Thanni LO, Yinusa W. Incidence of glove failure during orthopedic operations and the protective effect of double gloves. J Natl Med Assoc 2003;95:1184-8. 18. Punyatanasakchai P, Chittacharoen A, Ayudhya NI. Randomized controlled trial of glove perforation in single- and double-gloving in episiotomy repair after vaginal delivery. J Obstet Gynaecol Res 2004;30: 354-7. 19. Tanner J, Parkinson H. Double-gloving to reduce surgical crossinfection. Cochrane Database Syst Rev 2006;3:CD003087. 20. Thomas S, Agarwal M, Mehta G. Intraoperative glove perforation: single- versus double-gloving in protection against skin contamination. Postgrad Med J 2001;77:458-60. 21. Caillot JL, Paparel P, Arnal E, Schreiber V, Voiglio EJ. Anticipated detection of imminent surgeon–patient barrier breaches: a prospective randomized controlled trial using an indicator underglove system. World J Surg 2006;30:134-8. 22. Florman S, Burgdorf M, Finigan K, Slakey D, Hewitt R, Nicols RL. Efficacy of double gloving with an intrinsic indicator system. Surg Infect (Larchmt) 2005;6:385-95. 23. Laine T, Aarnio P. Glove perforation in orthopaedic and trauma surgery: a comparison between single, double indicator gloving and double gloving with two regular gloves. J Bone Joint Surg Br 2004;86: 898-900. 24. Al-Maiyah M, Bajwa A, Mackenney P, Port A, Gregg PJ, Hill D, et al. Glove perforation and contamination in primary total hip arthroplasty. J Bone Joint Surg Br 2005;87:556-9. 25. Davis N, Curry A, Gambhir AK, Panigrahi H, Walker CR, Wilkins EG, et al. Intraoperative bacterial contamination in operations for joint replacement. J Bone Joint Surg Br 1999;81:886-9. 26. Cole RP, Gault DT. Glove perforation during plastic surgery. Br J Plast Surg 1989;42:481-3.