Keeping the operating room contamination at the

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1 Glove Punctures and Postoperative Skin Flora of Hands in Cardiac Surgery Anne M. Eklund, MD, Juhani Ojajärvi, MD, PhD, Kirsi Laitinen, PhD, Matti Valtonen, MD, PhD, and Kalervo A. Werkkala, MD, PhD Department of Cardiothoracic Surgery, and Division of Infectious Diseases, Department of Medicine, Helsinki University Central Hospital, and Department of Public Health, University of Helsinki, Helsinki, Finland Background. Surgical gloves are frequently perforated during operations, including heart operations. This infection risk factor is inadequately studied. Methods. After preoperative hand disinfection and at the end of 116 heart operations, bacterial samples from hands of surgeons, altogether 800 samples, were taken. Glove punctures were examined with water test. Results. Surgeons changed 70 gloves because of breakage during operations. Additionally, 154 of 400 (39%) gloves had holes in postoperative testing. The breakage rate of gloves increased from 30% in operations shorter than 3 hours to 65% when operations were longer than 5 hours. High bacterial counts of the hands were also more common after prolonged operations. Conclusions. Glove puncture rates and bacterial counts of hands increase with increasing operation time. We recommend changing of both gloves when a puncture is detected. Before donning new gloves, hands should be disinfected. (Ann Thorac Surg 2002;74:149 53) 2002 by The Society of Thoracic Surgeons Keeping the operating room contamination at the lowest possible level is essential in heart surgery in which deep wound infections or prosthetic valve endocarditis lead to prolonged hospital stay and increased morbidity and mortality. One possible contamination route is a perforated glove. The purpose of surgical gloves is to create a barrier between the operating staff and the patient and thus to protect them both from microbial infections. In unused surgical gloves the puncture rate varies between 1.4% and 5.5% [1 3]. Studies conducted during surgical procedures have demonstrated glove perforation rates ranging from 10% in ophthalmologic surgery to 50% in general surgery [1, 4 7]. A great deal of punctures is not noticed by the operating staff [1, 3, 8]. Dodds and colleagues [5] showed that glove perforation did not influence bacterial counts on surgeons hands. They concluded that after standard preoperative hand preparation, glove perforations are of no clinical significance to the patient. However, the study was conducted in general surgery, in which the operation times are shorter than in heart surgery. The purpose of our study was to find out how often surgical gloves are punctured and how often it happens without the knowledge of the surgical staff, and to examine the correlation between punctures of surgical gloves and the bacterial counts of fingertips after operation. Accepted for publication April 8, Address reprint requests to Dr Eklund, Helsinki University Central Hospital, Jorvi Hospital, Turuntie 150, Espoo FIN-02740, Finland; anne.eklund@fimnet.fi. Material and Methods Study Population The study was conducted in the Department of Cardiothoracic Surgery of the Helsinki University Central Hospital. The consecutive 116 open heart procedures consisted mostly of coronary artery bypass grafting operations with cardiopulmonary bypass. One hundred six procedures were done through median sternotomy incision. Ten operations were redo procedures with previous heart operations. In total, 200 pairs of gloves from 23 participating surgeons were checked for holes, and their hands were cultured before and after operations. The surgeons had previously participated in similar studies and were thus well accustomed to the preoperative hand disinfection methods used in the clinic. Hand Washing and Disinfection Preoperatively, the hands and arms were first washed with liquid soap for 1 minute and subsequently dried with disposable paper towels. The hands were then disinfected by rubbing with alcoholic chlorhexidine (5 mg/ml chlorhexidine in 80% ethanol) into all surfaces of the hands in the standardized manner for 2 minutes. The skin of the hands was kept wet during the time of rubbing and additional solution was applied on the skin when necessary. Bacterial Samples Eight hundred bacterial samples (both hands of 200 surgeons, both before and after operation) from the hands of surgeons were taken both after the preoperative hand washing and disinfection and postoperatively immediately after the removal of the gloves. The samples 2002 by The Society of Thoracic Surgeons /02/$22.00 Published by Elsevier Science Inc PII S (02)

2 150 EKLUND ET AL Ann Thorac Surg GLOVE PUNCTURES AND BACTERIA IN SURGERY 2002;74: were taken by rubbing the fingertips for 1 minute against the bottom of two Petri dishes, one for each hand, containing 10 ml of sterile physiologic saline solution with appropriate inactivators to neutralize possible remnants of the disinfectant. This method is recommended by CEN (European Committee for Standardization) standard EN 1500 for testing of surgical hand disinfectants. Thereafter, the samples were transferred into test tubes and brought immediately to the laboratory for incubation and analysis. After incubation, the colony-forming units (cfu) of bacteria from the 1-mL aliquots of the sampling fluid and its 10-fold dilutions were counted. Negative growth in 10 ml of fluid thus indicated the presence of less than 9 cfu on the fingertips. Testing of Gloves The gloves were changed during the operation if the surgeon noticed a perforation in the glove. Their practice was to change only the damaged glove. The punctures reported by the surgeons during the operation were registered, and all gloves were analyzed for punctures. This was done by filling the gloves with 1 L of water (European standard EN 455 1). Dripping of water was recorded as a puncture. Glove perforation with a diameter of more than 0.5 cm was defined as large. The sites of the punctures were also recorded. Three types of surgical gloves were used during the study by the surgeons: Biogel (Regent Hospital Products, Broxbourne, UK), Ansell Medical Gammex (Ansell Medical, Surbiton, Surrey, UK), and Neutralon (Johnson & Johnson Medical Inc, Arlington, TX). Surveillance of Infections For surgical site infections, we used the criteria published by the Centers for Disease Control and Prevention in 1992 [9]. They classify surgical site infections as superficial incisional, deep incisional, or organ/space surgical site infections. The information about infections was gathered after 3 and 6 months from the hospital patient records and hospital infection registry. One hundred sixteen patient records were examined for diagnosis, surgical procedure, previous cardiac operation, other diseases such as pulmonary disease, hypertension, or diabetes mellitus, antibiotic prophylaxis and treatment, signs of infection (eg, state of wound, fever, C-reactive protein), and the notes of the medical staff in the records on wound healing. Statistical Analysis The results are mainly reported with descriptive statistics. For the assessment of observed differences in frequency of glove perforations, the uncorrected 2 test was used. For comparison of the length of the operations, Student s t test was used. A probability value of 0.05 was considered significant. Cochran-Armitage trend test (StatXact 5.0, CYTEL Software Corporation, Cambridge, MA) was used to compare the bacterial distributions when the gloves were intact, or had small or large holes (Table 1). Table 1. Bacterial Counts (cfu/ml) of Surgeons Hands After Preoperative Scrubbing and at the End of Operation by Integrity of Gloves Colony Count After Preoperative Disinfection All Hands (n 400) At the End of the Operation by Integrity of Gloves Gloves Intact (n 246) Small Punctures (n 87) Large Punctures (n 67) (95%) 131 (53%) 51 (59%) 34 (51%) (4%) 61 (25%) 18 (21%) 13 (19%) (1%) 43 (17%) 15 (17%) 11 (16%) (5%) 3 (3%) 9 (13%) cfu/ml colony-forming unit per milliliter of sampling solution. Results Glove Perforations During operations, the surgeons had punctured and changed altogether 53 left hand and 17 right hand gloves. From 400 gloves, removed at the end of operations, 154 were found punctured in the postoperative water test. Thus the total rate of punctured gloves during operations was 224 (48% of all the gloves used). Left hand gloves were punctured more often, in 54% (136 of 253 gloves), than right hand gloves that were punctured in 41% (88 of 217 gloves). The surgeons noticed the glove hole in 70 of 224 gloves (31%). At the end of the operation, holes in gloves were found in left-hand gloves more often (84 times) than in righthand gloves (70 times). The majority of all punctures (50%) were on the first three fingers of the left hand. Of the large punctures, 73% were located in the first two fingers of the gloves. The gloves of principal surgeons were found perforated at the end of operations more often (100 of 192 gloves, or 52%) than those of assistant surgeons (54 of 208 gloves, or 26%). The difference is statistically significant (p 0.01, 2 test). In only 20 (17%) operations both gloves were found unpunctured, and the chief surgeon had at least one glove perforated in 61% of the operations. No differences were found in the perforation rates of the three glove trademarks used in the study. Bacterial Counts After the preoperative disinfection of the hands, the bacterial counts were low. No colony counts were found in 84% of the hand samples, and in 95% of the hands the colony count was less than 10 cfu. No samples showed more than 1,000 cfu (Table 1). In the samples taken from the surgeons hands immediately after the operation, the variation in the bacterial counts was much wider; 36% (144 of 400) of all samples showed no bacteria and 54% (216 hands) had bacterial counts between 0 and 9 cfu. More than 1,000 bacterial colonies/ml of sampling fluid were found in 6% of hands (23 of 400 hand samples). When the gloves were intact at the end of operation,

3 Ann Thorac Surg EKLUND ET AL 2002;74: GLOVE PUNCTURES AND BACTERIA IN SURGERY 151 Fig 1. Rate of punctured gloves by duration of operation. The actual number of broken gloves in each group is presented within its respective column. high numbers of bacterial counts, more than 1,000 colonies, occurred in 5% of hand samples (Table 1). When the gloves had small punctures, the corresponding figure was 3%, and 13% when the punctures were large. However, these three groups (intact gloves and small and large punctures) did not differ significantly from each other (intact gloves versus small punctures, p ; intact gloves versus large punctures, p ; small versus large punctures, p ; Cochran-Armitage trend test). The postoperative colony counts of individual surgeons varied widely. Some of them showed no or only a few bacteria on fingertips before or after the operation, whereas the bacterial counts of some surgeons hands were remarkably high after the operation. Three surgeons had constantly high numbers of bacteria on either their right or left hand. However, for all the surgeons, no clear difference existed between the bacterial counts of the right and left hands. Operation Time The average duration of the operations was 3 hours 14 minutes (range, 62 to 500 minutes). With the increasing duration of the operation, the frequency of glove perforations as well as the occurrence of large holes also increased (Fig 1). The bacterial counts of hands taken after operations increased with the increasing operation time. The correlation is statistically significant at the 0.05 Fig 2. Colony counts in the surgeons hands (cfu/ml) at the end of operation grouped by the duration of operation. level (Pearson correlation coefficient 0.119, two-tailed; Fig 2). Infections In the 116 operations involved there were 7 (6%) sternal wound infections: one of which was mediastinitis, one deep, and five superficial sternal wound infections according to the criteria by the Centers for Disease Control and Prevention [9]. All of these patients received antibiotics. Only in one of these seven operations, gloves remained intact, and in three, there was at least one large glove perforation. Of the seven cases, six were coronary artery bypass grafting procedures, and one patient with superficial infection had aortic valve replacement with coronary artery bypass grafting. The operations were clearly longer than average (194 minutes) in these seven cases (Table 2). Comment In this study we have measured the rate of glove breakage and bacterial counts on the hands of 24 surgeons both after their preoperative washing and disinfection and immediately after 116 open heart procedures. In 154 of 400 gloves (39%) holes were detected postoperatively by the 1-L water test. However, 70 gloves were punctured and changed already during operations, which increases the glove breakage rate up to 48%. Table 2. Seven Cases With Sternal Wound Infection: Type of Procedure, Cultured Bacteria, and Duration of Operation Patient Number Type of Infection Type of Procedure Bacteriology Length of Operation (min) 1 Superficial CABG S. epidermidis Superficial CABG S. epidermidis Deep incisional CABG S. epidermidis Superficial CABG S. epidermidis Mediastinitis CABG Pseudomonas aeruginosa and S. epidermidis Superficial CABG none Superficial CABG AVR none 215 AVR aortic valve reconstruction; CABG coronary artery bypass grafting; S. epidermidis Staphylococcus epidermidis.

4 152 EKLUND ET AL Ann Thorac Surg GLOVE PUNCTURES AND BACTERIA IN SURGERY 2002;74: High tear rates have been described in heart operations [10, 11]. In other types of surgical procedures, the glove perforation rate varies from 10% to 50% [6, 7, 12]. Higher than 50% leak rates have been presented from cardiovascular, orthopaedic, and abdominal surgery [1]. The puncture rate no doubt depends on the type of operation as well as the diligence and skill of the surgeon. The risk of glove tears in orthopaedic operations may be especially high because of both sharp instruments and bone fragments [8]. It is a common practice to change the glove when it is punctured. However, the difficulty is that the surgeons may not notice the breakage. In our study, the surgeons noticed glove holes and subsequently changed the glove 70 times during operations. However, the gloves removed after operations were often punctured: in 154 of 400 gloves holes were detected in the water test. The surgeons thus detected punctures in 31% (70 of 224 punctured gloves). In previous studies the detection rates of tears have varied from 3% to 30% [4, 11]. Left hand gloves were punctured more often than those of the right hand when the gloves changed during operations were also taken into account. Half of the holes were found in the first three fingers of the left hand glove. Of the large punctures, 73% were located in the first two glove fingers. This is not hardly surprising nor is the finding that the gloves of principal surgeons were perforated more often than those of assistant surgeons. This is in agreement with the study of Whyte and associates [13] in which the surgeons gloves puncture rate was 47% and that of the assistant surgeons, 22%. More attention is deserved for our result that despite the development of glove materials, the gloves were found unpunctured in only 17% of all operations and the chief surgeon had at least one glove perforated in 61% of the operations. The glove holes were even rated large in 46% of the operations. It seems logical to assume that such a high glove breakage rate would considerably increase the infection risk. This study does not, however, support that assumption because the glove holes did not seem to have a straightforward influence on the infection rates. Today, the skin of the patient is diligently disinfected, in Europe most often with efficient alcoholic preparations, the patients receive preoperative antibiotic treatment, and the operation is elective, whenever possible. The infection is a consequence of multiple causative factors, and the bacteria from the surgeons hands are only one of these. Tammelin and coworkers [14] have shown that the patients sternal skin is the main source for wound contamination with epidemic methicillin-resistant Staphylococcus epidermidis bacteria. The same bacteria on the hands of the operating staff were not a risk factor for their occurrence in the wound at the end of the operation. This is consistent with statements from two other studies in which glove punctures did not increase the risk for postoperative wound infection [15] or wound contamination [13]. Dodds and associates [5] found glove perforations in 35% of operations and concluded that after standard preoperative hand preparation, glove perforations are of no clinical significance to the patient, and that protection of the surgeon is the main indication for a perioperative change of damaged gloves. However, the operations were general surgery and the operation times shorter than in heart surgery. We were not surprised that we were not able to confirm the correlation between glove holes and elevated infection risk. The development of a wound infection is a complex and multifactorial issue, and our material was not large enough to thoroughly study various factors predisposing to surgical site infection. It is claimed that the most common source of microorganisms responsible for surgical infections is with high probability the patient himself, and secondly the personnel [16, 17]. Changing of gloves punctured during the operation is an old custom, although there is not much scientific evidence to support this practice. Well-controlled studies with sufficiently accurate methods on the effects of the glove punctures on the operative and hand hygiene are rare. Although we were not able to prove in this study the increased infection risk, we could confirm that the bacterial counts of the hands increased with increasing length of the operation. The glove breakage rate also increased. Protecting the health-care workers from infectious diseases such as hepatitis B, hepatitis C, and acquired immune deficiency syndrome has become more and more important during the past years. Kjaergard and colleagues [18] have shown that open heart procedures carry a high risk of injury and frequent exposure to blood, which increases the risk of the surgical team to acquire viral infections from the patient. On the other hand, recent reports have indicated that surgeons may transmit hepatitis B or C to patients [19, 20]. Avoidance of glove holes and their quick detection during operation is also therefore of utmost importance. It is not known how large the hole must be so that it would be enough for microorganisms to enter or exit the glove. Small pinholes may be safe, because they may close immediately and may even avoid detection in the water test. On the other hand, large holes are a risk factor for both the patient and the staff. Because the bacteria on the skin of the hands increase with time, it is not unreasonable to suggest that when gloves are changed because of tear, the hands should also be disinfected before donning new gloves. Also, as the glove holes seem to avoid detection, changing both gloves when one glove is torn should be the practice of choice. If the disinfection is done properly, and the disinfection time is long enough, modern preoperative hand washing and disinfection techniques efficiently reduce bacterial counts of the hands. Some microbes may remain on the skin, but wearing of surgical gloves probably prevents their escape into the wound. In our study more than half of the hands were recolonized toward the end of the operation, which is probably owing to bacteria multiplying in the crypts of sebaceous glands and hair follicles. In our study we found that some doctors had no or only

5 Ann Thorac Surg EKLUND ET AL 2002;74: GLOVE PUNCTURES AND BACTERIA IN SURGERY 153 a few bacteria on their hands either before or after the operation, whereas the postoperative bacterial counts of some others were considerably high. This is probably because of personal skin problems, such as dermatitis, dry skin, or small scratches. In addition, in long and complex procedures surgeons may injure their skin when tying sutures. Those small wounds may potentially become the source for small amounts of serum and extracellular fluid being released under the glove and, in case of leakage, may become a possible route for microbes from surgeon to the patient or vice versa. Glove perforations occur in a majority of heart operations, and the number of perforated gloves is considerable. The frequency of glove perforations and the bacteria counts of the hands increase with operation time. Our study failed to show that the breakage of gloves during heart operations causes increased risk of infection. However, we could show that increasing number of gloves are punctured when the operation time increases and, simultaneously, bacterial counts of the hands increase. It seems reasonable to recommend that when a puncture is detected, both gloves are changed. Before donning a new pair of gloves, renewed disinfection of the hands will help to keep their bacterial counts lower even toward the end of a long operation. This study was supported by Grants from Helsinki University Hospital, Helsinki, Finland, and SSL Healthcare/Regent Medical. References 1. Albin MS, Bunegin L, Duke ES, Ritter RR, Page CP. Anatomy of a defective barrier: sequential glove leak detection in a surgical and dental environment. Crit Care Med 1992;20: Paulssen J, Eidem T, Kristiansen R. Perforations in surgeons gloves. J Hosp Inf 1988;11: Russell TR, Roque FE, Miller FA. A new method for detection of the leaky glove. Arch Surg 1966;93: Chapman S, Duff P. Frequency of glove perforations and subsequent blood contact in association with selected obstetric surgical procedures. Am J Obstet Gynecol 1993;168: Dodds RDA, Guy PJ, Peacock AM, Duffy SR, Barker SGE, Thomas MH. Surgical glove perforation. Br J Surg 1988;75: Brough SJ, Hunt TM, Barrie WW. Surgical glove perforations. Br J Surg 1988;75: Nakazawa M, Sato K, Mizuno K. Incidence of perforations in rubber gloves during ophthalmic surgery. Ophthalmic Surg 1984;15: Laine T, Aarnio P. How often does glove perforation occur in surgery? Comparison between single gloves and a doublegloving system. Am J Surg 2001;181: Horan TC, Gaynes RP, Martone WJ, Jarvis WR, Emori GT. CDC definitions of nosocomial surgical site infections. Infect Control Hosp Epidemiol 1992;13: Wong PS, Young VK, Youhana A, Wright JE. Surgical glove punctures during cardiac operations. Ann Thorac Surg 1993; 56: Berg GA, Kirk AJB, Bain WH. Punctured surgical gloves and bacterial re-colonisation of hands during open heart surgery: implications for prosthetic valve replacement. Br J Clin Pract 1987;41: Maffulli N, Capasso G, Testa V. Glove perforation in elective orthopedic surgery. Acta Orthop Scand 1989;60: Whyte W, Hambraeus A, Laurell G, Hoborn J. The relative importance of routes and sources of wound contamination during general surgery. I. Non-airborne. J Hosp Infect 1991; 18: Tammelin A, Hambraeus A, Ståhle E. Source and route of methicillin-resistant Staphylococcus epidermidis transmitted to the surgical wound during cardio-thoracic surgery. Possibility of preventing wound contamination by use of special scrub suits. J Hosp Infect 2001;47: Cruse PJE, Foord R. The epidemiology of wound infection. A 10 year prospective study of 62,939 wounds. Surg Clin North Am 1980;60: Drake CT, Goldman E, Nichols RL, Piatruszka K Nyhus LM. Environmental air and airborne infections. Ann Surg 1977; 185: Bitkover CY, Marcusson E, Ransjö U. Spread of coagulasenegative staphylococci during cardiac operations in a modern operating room. Ann Thorac Surg 2000;69: Kjaergard HK, Thiis J, Wiinberg N. Accidental injuries and blood exposure to cardiothoracic surgical teams. Eur J Cardiothorac Surg 1992;6: Esteban JI, Gómez J, Martell M, et al. Transmission of hepatitis C virus by a cardiac surgeon. N Engl J Med 1996; 334: Harpaz R, Von Seidlein L, Averhoff FM, et al. Transmission of hepatitis B virus to multiple patients from a surgeon without evidence of inadequate infection control. N Engl J Med 1996;334: