- Email: [email protected]
Bacteriology of abdominal wounds in elective open colon surgery: a prospective study of 100 surgical wounds
Research Note 155
than would have been expected, and the prevalence rates in the institution appeared to have risen significantly since the previous study [7]. Seasonality has been suggested as a factor that determines Strep. pyogenes colonisation of the oropharynx [6,8,9]. However, when the historically reported high prevalence season (late winter ⁄ early spring) was compared with the low prevalence season (autumn), no significant association was found. However, it is important to note that these historical rates are those of symptomatic subjects, whereas the present study included both symptomatic and asymptomatic subjects. In addition, the present study was not powered to find a small difference in prevalence between the two seasons studied, and a difference of 3.5% (11.5– 8.0%) is unlikely to be clinically significant. Overall, the present study demonstrated that individuals of university age had increased carriage rates of Strep. pyogenes and Staph. aureus compared with previous reports [2,3,5,7]. The precise reasons for these increased carriage rates are unknown. These findings, and those from a previous study [1], indicate that Strep. pyogenes may now be more prevalent in the oropharynx in university age populations (both with and without acne) and in acne patients taking long-term antibiotics. This may impact the health status of both carriers and their close contacts. Given the increased concern about antibiotic overuse, as well as numerous reports of severe streptococcal diseases, these findings may have important public health implications with respect to the treatment and diagnosis of bacterial pharyngitis. Further investigation is required to elucidate the possible clinical significance. ACKNOWLEDGEMENTS This study was supported by an Agency for Healthcare Research and Quality (AHRQ) Centers for Education and Research on Therapeutics cooperative agreement (grant HS10399), Rockville, MD, USA, and grants K24-AR02212 (D. Margolis) and T32-AR07465-18 (awarded to R. Lavker and used to support R. Levy) from the National Institute of Arthritis and Musculoskeletal and Skin Diseases, Bethesda, MD, USA.
2. Bridges-Webb C. A bacteriological study of the upper respiratory tract in normal families. Med J Austral 1971; 1: 735–738. 3. Feery BJ, Forsell P, Gulasekharam J. Streptococcal sore throat in general practice – a controlled study. Med J Austral 1976; 1: 989–991. 4. Morita JY, Kahn E, Thompson T et al. Impact of azithromycin on oropharyngeal carriage of group A Streptococcus and nasopharyngeal carriage of macrolide-resistant Streptococcus pneumoniae. Pediatr Infect Dis 2000; 19: 41–46. 5. Ramı´rez-Ronda CH, Fuxench-Lo´pez Z, Neva´rez M. Increased pharyngeal bacterial colonisation during viral illness. Arch Intern Med 1981; 141: 1599–1603. 6. Kaplan EL, Wotton JT, Johnson DR. Dynamic epidemiology of group A streptococcal serotypes associated with pharyngitis. Lancet 2001; 358: 1334–1337. 7. Collins M, Fleisher GR, Fager SS. Incidence of beta hemolytic streptococcal pharyngitis in adolescent with infectious mononucleosis. J Adolesc Health Care 1984; 5: 96–100. 8. Winther FO, Horthe K, Lystad A, Vellar OD. Pathogenic bacterial flora in the upper respiratory tract of healthy students. J Laryngol Otol 1974; 88: 407–412. 9. Brimblecombe FSW, Cruickshank R, Masters FL, Reid DD. Family studies of respiratory infections. BMJ 1958; 119– 128.
RESEARCH NOTE
Bacteriology of abdominal wounds in elective open colon surgery: a prospective study of 100 surgical wounds P. R. Fa-Si-Oen1, F. Kroeze1, L. H. M. Verhoef2, C. Verwaest3 and R. M. H. Roumen1 1
Department of Surgery, 2Department of Microbiology, Maxima Medical Centre, Veldhoven, The Netherlands and 3Department of Intensive Care Medicine, University Hospital Gasthuisberg, Leuven, Belgium ABSTRACT This article describes a prospective bacteriological study designed to assess the value of bacterial sampling during elective open colon surgery. Swabs of the subcutaneous tissue were taken after closure of the abdominal fascia, but before closure of the skin, in 100 patients during elective
REFERENCES 1. Levy RM, Huang EY, Roling D, Leyden JJ, Margolis DJ. Effect of antibiotics on the oropharyngeal flora in patients with acne. Arch Dermatol 2003; 139: 467–471.
Corresponding author and reprint requests: R. M. H. Roumen, Maxima Medical Centre, Department of Surgery, PO Box 7777, 5500 MB Veldhoven, The Netherlands E-mail: [email protected]
2005 Copyright by the European Society of Clinical Microbiology and Infectious Diseases, CMI, 11, 145–163
156 Clinical Microbiology and Infection, Volume 11 Number 2, February 2005
colon surgery. Of the 100 swabs, 52 were sterile with no resulting wound infection, while ten of the remaining 48 contaminated swabs were associated with a wound infection caused by colonic pathogens and nosocomial microorganisms. Bacterial sampling seems to be a useful method for the prediction of wound infection following elective colon surgery. Keywords Colon surgery, elective surgery, infections, surgery, wound infection Original Submission: 15 December 2003; Revised Submission: 27 July 2004; Accepted: 15 August 2004
Clin Microbiol Infect 2005; 11: 155–157 10.1111/j.1469-0691.2004.01011.x A persisting problem in colorectal surgery is the occurrence of wound infections, with infection rates following laparotomy of 10–15% [1]. Wound infection prolongs healing and increases the risk of poor cicatrisation, the duration of hospitalisation, and the subsequent costs of medical care [2–4]. Prevention of wound infection in elective open colorectal surgery includes antibiotic prophylaxis and mechanical bowel preparation. The advantages of the latter approach are currently being debated [5]. Antibiotic prophylaxis in colorectal surgery consists of a regimen directed at the endogenous flora of the large intestine, which mainly comprises Gram-negative and Gram-positive aerobes and anaerobes [6]. In order to improve our understanding of the dynamics of abdominal wound infection after colon surgery, this report describes a prospective bacteriological study of abdominal wounds in 100 patients undergoing elective open colon surgery during the period October 1998 to May 2000. Indications for surgery were recurrent diverticular disease or colon malignancy. All patients underwent colon resection with primary anastomosis without a deviating stoma. All surgical interventions were classified as clean or contaminated [7]. Intravenous antibiotic prophylaxis (2 g of cefuroxime and 1.5 g of metronidazole) was given to all patients 30 min before surgery. In addition, 43 patients underwent mechanical bowel preparation with 4 L of oral polyethyleneglycol before surgery. After closure of the abdominal fascia, and just before closure of the skin, a swab was taken of the subcutaneous tissue of each abdominal wound. Post-operative
follow-up was performed by surgeons and surgical residents who were unaware of the bacteriological results. The occurrence of wound infection was documented during hospital stay and for up to 4 weeks post-surgery in the outpatient setting. Infection was defined as discharge of pus from the wound, or a clinical suspicion of wound infection, based on inflammatory signs such as raised temperature, redness and tenderness of the wound. When it was deemed necessary to open an infected wound, an additional swab was taken of the drained area. Swabs were cultured, aerobically and anaerobically, at 37C for 48 h, and any microorganisms were identified with standard laboratory techniques. The study was approved by the local hospital ethics committee. Of the 100 initial swabs taken, 52 yielded no microorganisms following culture. Of the remaining 48 swabs, 21 yielded facultative aerobic bacteria only, 13 yielded anaerobic bacteria only, and 14 yielded a mixture of anaerobic and facultative aerobic bacteria (Table 1). The most common aerobes were Escherichia coli (18 swabs) and Streptococcus spp. (eight swabs), and the commonest anaerobe was Bacteroides fragilis (17 swabs). The 43 patients who received mechanical bowel preparation were distributed equally between the groups with positive and negative swabs. There were no wound infections among the 52 patients from whom an initial sterile swab was
Table 1. Microorganisms isolated from wounds following elective open colon surgery Organism isolated Streptococcus, viridans group Escherichia coli Bacteroides fragilis Bacteroides uniformis Streptococcus, b-haematolytic group C Actomyocines viscosus Enterococcus faecalis Endobacterium lentum Staphylococcus spp. Corynebacterium spp. Peptostreptococcus Lactobacillus spp. Actinomyces israeli Bacteroides vulgatus Bacteroides ovatus Enterobacter aerogenes Klebsiella pneumoniae Bacteroides melaninogenicus Streptococcus bovis Proteus mirabilis Stenotrophomonas maltophilia Propionibacterium Bacteroides buccae
No. of positive swabs taken No. of positive wound before skin closure infection swabs 5 18 17 1 2
2 4 2 0 0
2 3 4 3 2 2 1 3 1 1 1 1 1 1 1 1 1 1
0 3 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0
2005 Copyright by the European Society of Clinical Microbiology and Infectious Diseases, CMI, 11, 145–163
Research Note 157
taken. In the group of 48 patients with a contaminated initial swab, ten developed a clinically relevant wound infection. All ten of these patients yielded B. fragilis (six swabs), E. coli or Streptococcus spp. For seven of these ten patients, a swab of the opened wound was taken. In four cases, the swab from the opened wound yielded an organism that corresponded with at least one species cultured from the initial swab. All seven swabs from the opened wounds yielded potentially pathogenic microorganisms (Pseudomonas aeruginosa, Enterobacter cloacae, E. coli, Morganella morganii or Candida albicans) (Table 1). Thus, a positive swab of the surgical wound taken before skin closure seemed to be a valuable predictor for a subsequent clinically significant wound infection following elective open colon surgery, while the negative predictive value of a negative swab was 100% in this study. The highest wound infection rate in abdominal surgery probably occurs following colorectal procedures. It has been suggested that there is an increased bacterial load before wound closure following colorectal surgery in comparison with other abdominal operations. This is explained by the high numbers of aerobic and anaerobic organisms that are released when the abdominal viscera are opened [8,9]. In the present study, swabs were taken from the subcutaneous fat after fascial closure, as it has been suggested that this may be the best method of detecting organisms likely to cause a subsequent abdominal wound infection [10,11]. Organisms involved in infections following colorectal surgery are mainly endogenous microorganisms such as E. coli, B. fragilis, Proteus spp. and Klebsiella spp. [12–14]. The present study confirmed that these pathogens were the main causative pathogens of wound infections, but other nosocomial microorganisms were also cultured from all seven wound infections. It seems that contamination of the wound with colonic flora during surgery may cause a polymicrobial infection caused by commensals and other potentially pathogenic microorganisms. When systemic antibiotic prophylaxis was not common practice, swabs taken during surgery seemed to have the best predictive value for
assessing the likelihood of subsequent wound infection [15,16]. The present data demonstrate that the predictive value of such swabs remains high, even when systemic antibiotic prophylaxis and mechanical bowel preparation are undertaken before surgery. These findings raise the question of whether there may be a place for targeted antibiotic treatment in cases where swabs taken during surgery grow colonic or other potentially pathogenic microorganisms. REFERENCES 1. Johnston D. Bowel preparation for colorectal surgery. Br J Surg 1987; 74: 553–554. 2. Smith M, Enquist I. A quantitative study of the impaired healing resulting from infection. Surg Gynecol Obstet 1967; 125: 965. 3. Tenorio A, Jindrak K. Accelerated healing in infected wounds. Surg Gynecol Obstet 1976; 77: 537–543. 4. Kapur BM. Role of intraoperative wound contamination in post-operative wound infection in laparotomy. Ind J Med Res 1985; 81: 508–513. 5. Platell C, Hall J. What is the role of mechanical bowel preparation in patients undergoing colorectal surgery? Dis Colon Rectum 1998; 41: 875–883. 6. Keighley MRB. Prevention of wound sepsis in gastrointestinal surgery. Br J Surg 1977; 64: 315–318. 7. National Research Council, Division of Medical Sciences. Ad hoc Committee of the Committee on Trauma. Postoperative wound infection: the influence of ultraviolet irradiation of the operating room and other factors. Ann Surg 1964; 160(suppl): 1. 8. Raahave D. Bacterial density in laparotomy wounds during gastro-intestinal operations. Scand J Gastroenterol 1976; 37: 135–142. 9. Nandi PL, Soundara Rajan S. Surgical wound infection. Hong Kong Med J 1999; 5: 82–86. 10. Kippax PW, Thomas ET. Surgical wound sepsis in a general hospital. Lancet 1966; 2: 1297–1300. 11. Polk HC. Postoperative wound infection: prediction of some responsible organisms. Am J Surg 1973; 126: 592–594. 12. Davidson AIG, Smith G. A bacterial study of the immediate environment of a surgical wound. Br J Surg 1971; 58: 326–333. 13. Cruse PJE. A five year prospective study of 23,648 surgical wounds. Arch Surg 1973; 107: 206–210. 14. Gorbach SL, Bartlett JG. Anaerobic infections. N Engl J Med 1974; 290: 1177–1184. 15. Saksena DS, Block MA. Bacterioidaceae: anaerobic organisms encountered in surgical infections. Surgery 1968; 63: 261–267. 16. Raahave D. New technique for quantitative bacteriological sampling of wounds by velvet pads: clinical sampling trial. J Clin Microbiol 1975; 2: 277–280.
2005 Copyright by the European Society of Clinical Microbiology and Infectious Diseases, CMI, 11, 145–163
than would have been expected, and the prevalence rates in the institution appeared to have risen significantly since the previous study [7]. Seasonality has been suggested as a factor that determines Strep. pyogenes colonisation of the oropharynx [6,8,9]. However, when the historically reported high prevalence season (late winter ⁄ early spring) was compared with the low prevalence season (autumn), no significant association was found. However, it is important to note that these historical rates are those of symptomatic subjects, whereas the present study included both symptomatic and asymptomatic subjects. In addition, the present study was not powered to find a small difference in prevalence between the two seasons studied, and a difference of 3.5% (11.5– 8.0%) is unlikely to be clinically significant. Overall, the present study demonstrated that individuals of university age had increased carriage rates of Strep. pyogenes and Staph. aureus compared with previous reports [2,3,5,7]. The precise reasons for these increased carriage rates are unknown. These findings, and those from a previous study [1], indicate that Strep. pyogenes may now be more prevalent in the oropharynx in university age populations (both with and without acne) and in acne patients taking long-term antibiotics. This may impact the health status of both carriers and their close contacts. Given the increased concern about antibiotic overuse, as well as numerous reports of severe streptococcal diseases, these findings may have important public health implications with respect to the treatment and diagnosis of bacterial pharyngitis. Further investigation is required to elucidate the possible clinical significance. ACKNOWLEDGEMENTS This study was supported by an Agency for Healthcare Research and Quality (AHRQ) Centers for Education and Research on Therapeutics cooperative agreement (grant HS10399), Rockville, MD, USA, and grants K24-AR02212 (D. Margolis) and T32-AR07465-18 (awarded to R. Lavker and used to support R. Levy) from the National Institute of Arthritis and Musculoskeletal and Skin Diseases, Bethesda, MD, USA.
2. Bridges-Webb C. A bacteriological study of the upper respiratory tract in normal families. Med J Austral 1971; 1: 735–738. 3. Feery BJ, Forsell P, Gulasekharam J. Streptococcal sore throat in general practice – a controlled study. Med J Austral 1976; 1: 989–991. 4. Morita JY, Kahn E, Thompson T et al. Impact of azithromycin on oropharyngeal carriage of group A Streptococcus and nasopharyngeal carriage of macrolide-resistant Streptococcus pneumoniae. Pediatr Infect Dis 2000; 19: 41–46. 5. Ramı´rez-Ronda CH, Fuxench-Lo´pez Z, Neva´rez M. Increased pharyngeal bacterial colonisation during viral illness. Arch Intern Med 1981; 141: 1599–1603. 6. Kaplan EL, Wotton JT, Johnson DR. Dynamic epidemiology of group A streptococcal serotypes associated with pharyngitis. Lancet 2001; 358: 1334–1337. 7. Collins M, Fleisher GR, Fager SS. Incidence of beta hemolytic streptococcal pharyngitis in adolescent with infectious mononucleosis. J Adolesc Health Care 1984; 5: 96–100. 8. Winther FO, Horthe K, Lystad A, Vellar OD. Pathogenic bacterial flora in the upper respiratory tract of healthy students. J Laryngol Otol 1974; 88: 407–412. 9. Brimblecombe FSW, Cruickshank R, Masters FL, Reid DD. Family studies of respiratory infections. BMJ 1958; 119– 128.
RESEARCH NOTE
Bacteriology of abdominal wounds in elective open colon surgery: a prospective study of 100 surgical wounds P. R. Fa-Si-Oen1, F. Kroeze1, L. H. M. Verhoef2, C. Verwaest3 and R. M. H. Roumen1 1
Department of Surgery, 2Department of Microbiology, Maxima Medical Centre, Veldhoven, The Netherlands and 3Department of Intensive Care Medicine, University Hospital Gasthuisberg, Leuven, Belgium ABSTRACT This article describes a prospective bacteriological study designed to assess the value of bacterial sampling during elective open colon surgery. Swabs of the subcutaneous tissue were taken after closure of the abdominal fascia, but before closure of the skin, in 100 patients during elective
REFERENCES 1. Levy RM, Huang EY, Roling D, Leyden JJ, Margolis DJ. Effect of antibiotics on the oropharyngeal flora in patients with acne. Arch Dermatol 2003; 139: 467–471.
Corresponding author and reprint requests: R. M. H. Roumen, Maxima Medical Centre, Department of Surgery, PO Box 7777, 5500 MB Veldhoven, The Netherlands E-mail: [email protected]
2005 Copyright by the European Society of Clinical Microbiology and Infectious Diseases, CMI, 11, 145–163
156 Clinical Microbiology and Infection, Volume 11 Number 2, February 2005
colon surgery. Of the 100 swabs, 52 were sterile with no resulting wound infection, while ten of the remaining 48 contaminated swabs were associated with a wound infection caused by colonic pathogens and nosocomial microorganisms. Bacterial sampling seems to be a useful method for the prediction of wound infection following elective colon surgery. Keywords Colon surgery, elective surgery, infections, surgery, wound infection Original Submission: 15 December 2003; Revised Submission: 27 July 2004; Accepted: 15 August 2004
Clin Microbiol Infect 2005; 11: 155–157 10.1111/j.1469-0691.2004.01011.x A persisting problem in colorectal surgery is the occurrence of wound infections, with infection rates following laparotomy of 10–15% [1]. Wound infection prolongs healing and increases the risk of poor cicatrisation, the duration of hospitalisation, and the subsequent costs of medical care [2–4]. Prevention of wound infection in elective open colorectal surgery includes antibiotic prophylaxis and mechanical bowel preparation. The advantages of the latter approach are currently being debated [5]. Antibiotic prophylaxis in colorectal surgery consists of a regimen directed at the endogenous flora of the large intestine, which mainly comprises Gram-negative and Gram-positive aerobes and anaerobes [6]. In order to improve our understanding of the dynamics of abdominal wound infection after colon surgery, this report describes a prospective bacteriological study of abdominal wounds in 100 patients undergoing elective open colon surgery during the period October 1998 to May 2000. Indications for surgery were recurrent diverticular disease or colon malignancy. All patients underwent colon resection with primary anastomosis without a deviating stoma. All surgical interventions were classified as clean or contaminated [7]. Intravenous antibiotic prophylaxis (2 g of cefuroxime and 1.5 g of metronidazole) was given to all patients 30 min before surgery. In addition, 43 patients underwent mechanical bowel preparation with 4 L of oral polyethyleneglycol before surgery. After closure of the abdominal fascia, and just before closure of the skin, a swab was taken of the subcutaneous tissue of each abdominal wound. Post-operative
follow-up was performed by surgeons and surgical residents who were unaware of the bacteriological results. The occurrence of wound infection was documented during hospital stay and for up to 4 weeks post-surgery in the outpatient setting. Infection was defined as discharge of pus from the wound, or a clinical suspicion of wound infection, based on inflammatory signs such as raised temperature, redness and tenderness of the wound. When it was deemed necessary to open an infected wound, an additional swab was taken of the drained area. Swabs were cultured, aerobically and anaerobically, at 37C for 48 h, and any microorganisms were identified with standard laboratory techniques. The study was approved by the local hospital ethics committee. Of the 100 initial swabs taken, 52 yielded no microorganisms following culture. Of the remaining 48 swabs, 21 yielded facultative aerobic bacteria only, 13 yielded anaerobic bacteria only, and 14 yielded a mixture of anaerobic and facultative aerobic bacteria (Table 1). The most common aerobes were Escherichia coli (18 swabs) and Streptococcus spp. (eight swabs), and the commonest anaerobe was Bacteroides fragilis (17 swabs). The 43 patients who received mechanical bowel preparation were distributed equally between the groups with positive and negative swabs. There were no wound infections among the 52 patients from whom an initial sterile swab was
Table 1. Microorganisms isolated from wounds following elective open colon surgery Organism isolated Streptococcus, viridans group Escherichia coli Bacteroides fragilis Bacteroides uniformis Streptococcus, b-haematolytic group C Actomyocines viscosus Enterococcus faecalis Endobacterium lentum Staphylococcus spp. Corynebacterium spp. Peptostreptococcus Lactobacillus spp. Actinomyces israeli Bacteroides vulgatus Bacteroides ovatus Enterobacter aerogenes Klebsiella pneumoniae Bacteroides melaninogenicus Streptococcus bovis Proteus mirabilis Stenotrophomonas maltophilia Propionibacterium Bacteroides buccae
No. of positive swabs taken No. of positive wound before skin closure infection swabs 5 18 17 1 2
2 4 2 0 0
2 3 4 3 2 2 1 3 1 1 1 1 1 1 1 1 1 1
0 3 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0
2005 Copyright by the European Society of Clinical Microbiology and Infectious Diseases, CMI, 11, 145–163
Research Note 157
taken. In the group of 48 patients with a contaminated initial swab, ten developed a clinically relevant wound infection. All ten of these patients yielded B. fragilis (six swabs), E. coli or Streptococcus spp. For seven of these ten patients, a swab of the opened wound was taken. In four cases, the swab from the opened wound yielded an organism that corresponded with at least one species cultured from the initial swab. All seven swabs from the opened wounds yielded potentially pathogenic microorganisms (Pseudomonas aeruginosa, Enterobacter cloacae, E. coli, Morganella morganii or Candida albicans) (Table 1). Thus, a positive swab of the surgical wound taken before skin closure seemed to be a valuable predictor for a subsequent clinically significant wound infection following elective open colon surgery, while the negative predictive value of a negative swab was 100% in this study. The highest wound infection rate in abdominal surgery probably occurs following colorectal procedures. It has been suggested that there is an increased bacterial load before wound closure following colorectal surgery in comparison with other abdominal operations. This is explained by the high numbers of aerobic and anaerobic organisms that are released when the abdominal viscera are opened [8,9]. In the present study, swabs were taken from the subcutaneous fat after fascial closure, as it has been suggested that this may be the best method of detecting organisms likely to cause a subsequent abdominal wound infection [10,11]. Organisms involved in infections following colorectal surgery are mainly endogenous microorganisms such as E. coli, B. fragilis, Proteus spp. and Klebsiella spp. [12–14]. The present study confirmed that these pathogens were the main causative pathogens of wound infections, but other nosocomial microorganisms were also cultured from all seven wound infections. It seems that contamination of the wound with colonic flora during surgery may cause a polymicrobial infection caused by commensals and other potentially pathogenic microorganisms. When systemic antibiotic prophylaxis was not common practice, swabs taken during surgery seemed to have the best predictive value for
assessing the likelihood of subsequent wound infection [15,16]. The present data demonstrate that the predictive value of such swabs remains high, even when systemic antibiotic prophylaxis and mechanical bowel preparation are undertaken before surgery. These findings raise the question of whether there may be a place for targeted antibiotic treatment in cases where swabs taken during surgery grow colonic or other potentially pathogenic microorganisms. REFERENCES 1. Johnston D. Bowel preparation for colorectal surgery. Br J Surg 1987; 74: 553–554. 2. Smith M, Enquist I. A quantitative study of the impaired healing resulting from infection. Surg Gynecol Obstet 1967; 125: 965. 3. Tenorio A, Jindrak K. Accelerated healing in infected wounds. Surg Gynecol Obstet 1976; 77: 537–543. 4. Kapur BM. Role of intraoperative wound contamination in post-operative wound infection in laparotomy. Ind J Med Res 1985; 81: 508–513. 5. Platell C, Hall J. What is the role of mechanical bowel preparation in patients undergoing colorectal surgery? Dis Colon Rectum 1998; 41: 875–883. 6. Keighley MRB. Prevention of wound sepsis in gastrointestinal surgery. Br J Surg 1977; 64: 315–318. 7. National Research Council, Division of Medical Sciences. Ad hoc Committee of the Committee on Trauma. Postoperative wound infection: the influence of ultraviolet irradiation of the operating room and other factors. Ann Surg 1964; 160(suppl): 1. 8. Raahave D. Bacterial density in laparotomy wounds during gastro-intestinal operations. Scand J Gastroenterol 1976; 37: 135–142. 9. Nandi PL, Soundara Rajan S. Surgical wound infection. Hong Kong Med J 1999; 5: 82–86. 10. Kippax PW, Thomas ET. Surgical wound sepsis in a general hospital. Lancet 1966; 2: 1297–1300. 11. Polk HC. Postoperative wound infection: prediction of some responsible organisms. Am J Surg 1973; 126: 592–594. 12. Davidson AIG, Smith G. A bacterial study of the immediate environment of a surgical wound. Br J Surg 1971; 58: 326–333. 13. Cruse PJE. A five year prospective study of 23,648 surgical wounds. Arch Surg 1973; 107: 206–210. 14. Gorbach SL, Bartlett JG. Anaerobic infections. N Engl J Med 1974; 290: 1177–1184. 15. Saksena DS, Block MA. Bacterioidaceae: anaerobic organisms encountered in surgical infections. Surgery 1968; 63: 261–267. 16. Raahave D. New technique for quantitative bacteriological sampling of wounds by velvet pads: clinical sampling trial. J Clin Microbiol 1975; 2: 277–280.
2005 Copyright by the European Society of Clinical Microbiology and Infectious Diseases, CMI, 11, 145–163