Wound infection under occlusive dressings

Journal

of Hospital

Infection

(1991)

17, 83-94

REVIEW

Wound

infection

ARTICLE

under

J. J. Hutchinson

occlusive

dressings

and J. C. Lawrence*

Wound Healing Research Institute, Newtech Square, Deeside Industrial Park, Deeside, Clwyd CH5 2NU and *The Burns Research Group, Birmingham Accident Hospital, Bath Row, Birmingham B15 1NA Accepted for publication

12 October 1990

Summary: It is often supposed that occlusive dressings potentiate wound infection. However, even though heavy colonization by skin and wound flora is often seen under certain types of occlusion, clinical infection is not a frequent occurrence. Commensal wound flora consists of a variety of Grampositive and Gram-negative organisms and fungi which do not appear to be detrimental to healing. Certain aspects of wound healing may in fact be promoted by bacterial colonization, although clinical infection can lead to wound breakdown and systemic infection. Wounds compromised by devitalized tissue, drains or sutures are more susceptible than clean wounds to clinical infection. Occlusive dressings may help prevent infection by presenting a barrier to potential pathogens, and hydrocolloid occlusive dressings have been shown to prevent dissemination of methicillin-resistant Staphylococcus aureus. The rate of clinical infection as deduced from published trials of dressings is lower under occlusion than when non-occlusive dressings are used, and this is likely to be a result of normal activity of the host defences under occlusive dressings. Keywords:

Wound

healing;

occlusive

dressings;

infection.

Introduction

It is generally assumed that covering wounds with occlusive dressings potentiates the risk of infection’s2 and the work of Evans3 appeared to substantiate this concern. However, it is important to realize that the presence of bacteria within a wound is not indicative of infection4 and diagnosis should be based on the classical clinical signs together with supportive microbiology. Improved healing in occluded wounds was first reported by Bull, Squire 8-zTopley,’ and Schilling, Roberts & Goodman,6 but the classical work of Winte.r7 which demonstrated that occluded wounds re-epithelialized faster than those left exposed eventually led to the introduction of a wide variety of Correspondence

to: J. J. Hutchinson.

0195-6701/91/020083

112 $03.00/O

0 1991 The Hospital

83

Infectmn

Society

J. J. Hutchinson

84

Table Dressing Hydrocolloids

Hydrogels

(HCD)

(HG)

Polyurethane

Films

(PUF)*

Foams

* PUF also called semi-occlusive ** ‘DuoDERM’

is also known

and J. C. Lawrence

I. Examples

of occlusive

Proprietary

name

dressings Manufacturers

‘DuoDERM’** ‘Comfeel’ ‘Restore’ ‘Vigilon’ ‘Geliperm’ ‘OpSite’ ‘Tegaderm’ ‘Omiderm’ ‘Synthaderm’ ‘Lyofoam’ ‘Silastic foam’ or vapour-permeable as ‘Granuflex’

membrane and ‘Varihesive’.

Squibb ConvaTec Coloplast Hollister Bard Geistlich Smith and Nephew 3M Health Care Omikron Scientific Derma-Lock Ultra Labs Inc. Dow Corning (VPM).

occlusive dressings. Occlusive dressings may be defined as those which prevent uninhibited passage of water vapour, and which therefore maintain wounds in a moist state. Healing which takes place under them is often referred to as ‘moist wound healing’. Dressings which induce such a state include simple plastic films, polyurethane-backed hydrocolloids, foams and hydrogels (Table I). In addition to the effects on reepithelialization,s,9 occluded wounds exhibit altered collagen metabolism,” enhanced granulation tissue formation” and enhanced neovascularization.‘2 Occlusive dressings have been applied to virtually all wound types including burns, donor sites, ulcers, abrasions, incisions and excisions. Varicjus authors’3,‘4 have described the properties of an ‘ideal’ dressing-the more important factors are shown in Table II. Many current occlusive dressings (Table I) fulfil most of these criteria; moreover, in clinical use they appear to be associated with lower wound infection rates than traditional dressings. This review considers the effects of occlusion on the microbiology of normal skin and wounds, the distinction between wound colonization and infection and the role of microorganisms in wound healing. General factors relevant to the likelihood of wound infection developing are discussed together with the effect occlusive dressings have on this possibility. By reviewing the numerous publications concerning the use of occlusive dressings on a variety of wounds, it can be demonstrated that wound infection rates are lower than with conventional dressings. The reasons for the lower infection rates associated with occlusive wound cover are considered. The

effects

of occlusion

on commensal

flora

of normal

skin

The normal resident commensal flora of intact human skin is composed mainly of Gram-positive organisms such as Staphylococcus epidermidis, Streptococcus spp. and Corynebacterium spp. Occasionally Candida spp. may be isolated. The precise nature of the flora, i.e. species and number is

Infection Table

under

occlusive

II. Some characteristics

dressings

of the ‘ideal’

85

wound dressing”,14

Handling of excess exudate Removal of toxic substances Maintenance of moist environment over the wound Permit gaseous exchange Present a barrier to microorganisms Provide thermal insulation Demonstrate freedom from particulate contaminants Removal without trauma to new tissue

dependent upon: body site and subject;” antagonism between microorganisms;16 skin lipids and desiccation;‘7,‘8 and the degree of hydration or maceration of the skin. 19v2’There is also considerable variation between individuals21 and transient bacteria may also be encountered. The degree of hydration of the skin can be altered by occlusion and such changes in the microbial flora are described by Marples,” Bibel & LeBrum,20 Aly et uZ.,~* Easmon23 and Lawrence & Lilly.24~25 Total occlusion, as for instance provided by Saran Wrap, polyvinylchloride (PVC) sheets and impervious plastic tapes, causes the normal flora to proliferate22-24 and the viable count may increase up to 50 000 fold.22 Changes in the proportion of species isolated can occur; Gram-negative bacilli and lipophilic diphtheroids may increase whilst non-lipophilic diphtheroids decline.22’26 Occlusion with hydrocolloid24 and polyurethane film dressings23 has not led to changes in the resident flora. Lawrence & Lilly24 compared the occlusive hydrocolloid dressing ‘DuoDERM’ (also known as ‘Granuflex’ and ‘Varihesive’), with a conventional tulle gras/absorbent gauze dressing, and found that the flora remained unaltered under both dressings. The

effects

of occlusion

on wound

flora

Irrespective of the dressing, the flora isolated from wounds is often similar to that of normal skin and may include S. epidermidis, S. aureus, P-haemolytic streptococci of Lancefield groups A, B and C, diphtheroids and Micrococcus. Gram-negative organisms are usually isolated, and may include Pseudomonas aeruginosa, Klebsiella spp. and other ‘coliform’ bacteria. Furthermore, anaerobes such as Clostridium welchii, Bacteroides spp. and anaerobic cocci are often seen. Fungi may be isolated in burns, but rarely from venous ulcers. Use of a dressing alters the wound environment resulting in a specific sub-dressing ecology.27,28 As with normal skin, the most pronounced effects occur under dressings that prevent desiccation.29 Early concerns that occlusive dressings would promote wound infection retarded their widespread use3,3632 despite the healing benefits seen in both acute* and chronic wounds.33 Early investigations using dressings that permit fluid to accumulate

86

J. J. Hutchinson

and J. C. Lawrence

(‘Silastic’) appeared to support the claim that their use predisposed to infection34z35 such that P. aeruginosa numbers increased and caused clinical infection. The subsequent development of more advanced occlusive dressings which are either water vapour permeable and/or capable of holding exudate has reduced the risk of infection. Studies of these advanced occlusive dressings (discussed fully under clinical trial results) show that the colonizing flora of wounds is similar to that noted with ‘conventional’ dressings. These studies also show that the presence of microorganisms is not necessarily indicative of infection. It is essential to distinguish between colonization and infection when interpreting results of clinical trials.

Colonization

or infection?

Because of similarities in the inflammatory response to wound healing and infection36 confusion can arise between colonization and infection.37,38 Some authorities diagnose infection if the bacterial count is greater than lo5 colony forming units (cfu) g-’ of tissue.39,40 However, in burns, healing can occur in the presence of much larger numbers4i although numbers greater than 1O’cfu g-’ may be associated with a higher risk of infection42 and impaired graft take.43 . The importance of microbiological findings in diagnosing infection must be evaluated in conjunction with clinical signs such as local pain, cellulitis, lymphangitis, heat, erythema, oedema and purulent exudate.30 Histologically, infection, as distinct from colonization, can be characterized by invasion of viable tissue by pathogens. 36,44Organisms present in wound exudate are not necessarily invading tissue thus their presence can only be indicative, but not diagnostic, of infection. The role

of microorganisms

in wound

healing

Although it is generally accepted that clinical infection impairs wound healing, the effect of any colonizing microorganisms on the healing process is yet to be determined. The effects that organisms may exert on wound healing range from detrimental to stimulatory. Numerous publications suggest that commensal organisms do not usually adversely influence wound healing.4~29~45~46The study of sterile wounds is not usually practical since contamination rapidly occurs from the normal surrounding skin; thus a definitive answer concerning the real influence of contamination on healing is difficult to obtain. However, some evidence suggests that a relationship exists between colonization and the rate and quality of healing. The effect of bacterial numbers on healing remains controversial.47,48 However, some authors have established links between necrotic non-healing ulceration and the presence of specific organisms such as Proteus mirabilis, P. aeruginosa and Bacteroides ~pp.~~ Topical application of chlorhexidine and gentamicin” was shown to reduce the carriage of

Infection

under

occlusive

dressings

87

microorganisms in ulcers prior to grafting, although the use and effects of topical or systemic antibacterial administration remain controversial.5~47~4s,5’ Work by Greenhalgh, Gamelli & Fosters2 suggests that killed cells of the immunomodulating organism Corynebacterium parvum injected intraperitoneally into mice impair wound healing in a dorsal incision wound. This contrasts with the stimulating effect of this organism on host defence against sepsis, and could be due to the activation of inhibitory macrophages. Wound healing has also been shown to be adversely affected by a wide range of bacterial metabolites including those from S. aureus, P. aeruginosa53-55 and Lancefield Group A P-haemolytic streptococci.s4 Bacteria in wounds are not necessarily detrimental to the healing process, and can aid desloughing34 and possibly enhance wound healing by stimulating inflammation.56-58 Very early observations suggested that wounds may heal faster if contaminated.59,60 In conclusion it appears likely that the bacterial species37 and change in number of organisms detected31 are more important in wound healing than the total bacterial count.

Factors

affecting

wound

infection

The consequences of a wound becoming clinically infected as distinct from simply colonized must be regarded as detrimental to the healing process. Healing may stop and, occasionally, regress; sutured wounds may dehisce. Systemic infection can be a consequence of infection in necrotic undebrided wounds; bacteraemia has been reported in 76% of patients with decubitus ulcers.61 Local wound factors which predispose to infection include: the presence of devitalized tissue, haematoma, foreign bodies and method of wound closure used. Foreign bodies, such as suture$j2 and drains63,64 are reported to increase wound infection. Sutures have also been shown to harbour a dense surface population of adherent organisms, particularly Staphylococcus epidermid@ and to increase the pus forming ability of S. azweus lo3 to 104-fold.‘j6 Wounds close d p rimarily show a lower wound strength than those allowed to heal by secondary intention over a prolonged period,67 and are more likely to become infected than open granulating wounds. Haematoma in a wound may also potentiate infection.68 Systemic factors also affect the likelihood of infection; these include age, diabetes, steroid therapy, gross obesity, malnutrition and infection of other body sites. Inhibition of wound healing, as measured by the breaking strength of incision wounds, has been shown in rats with transient bacteraemia resulting from a distal site of infection.69 Measures aimed at preventing wound infection should include debridement of all dead tissue7’ and meticulous wound cleansing. Foreign materials must be removed and the use of drains in uninfected wounds kept

88

J. J. Hutchinson

and J. C. Lawrence

Tape closures instead of sutures reduce infective to a minimum. develop, complications of surgical wounds. 70,71 Should wound infection systemic antibiotic treatment may be required together with debridement and topical antisepsis. Occlusive

dressings

in wound

healing

Currently available occlusive dressings include hydrocolloids (HCD), hydrogels (HG), foams and polyurethane films (PUF) (Table I). These dressings do not alter the wound flora such that endogenous infection is potentiated (vi& +a). They also provide a barrier to exogenous pathogens. Endogenous and exogenous infection is therefore minimized. Clinical trials show that wound infection rates using occlusive dressings are lower than those observed with conventional dressings. Occlusive dressings as bacterial barriers In-vitro studies of the polyurethane-backed HCDs, ‘DuoDERM’, ‘Comfeel Ulcus’ and ‘Dermiflex’ and the PUFs, ‘OpSite’ and ‘Tegaderm’ show that these dressings are bacteria-proof. By contrast, a non-woven fibre-backed HCD, ‘Biofilm’ is readily permeated by P. aeruginosa and S. aureus.25 Studies by Mertz, Marshall & Eaglstein,27 in which partial thickness wounds on pigs were challenged with 10’ S. aureus and P. aeruginosa, showed that no wound contamination was detected in wounds dressed with ‘DuoDERM’ even if repeatedly challenged. The in-vitro effectiveness of ‘OpSite’ was not confirmed. The authors suggest that as skin moves, channel formation occurs under ‘OpSite’ leading to bacterial contamination. The HG, ‘Vigilon’, also showed protection from S. aUYeUs in 50% of wounds but no protection from P. aeruginosa; however, no barrier function is claimed for this dressing. Preliminary work by Wilson, Burroughs & Dunn,72 using the HCDs ‘DuoDERM’ and ‘Dermiflex’, suggests that they are effective in preventing the spread of epidemic methicillin-resistant S. aUYeUs (MRSA). Seven patients with MRSA-contaminated ulcers were managed with these HCDs to prevent contamination of the wound environment. Distal sites of MRSA contamination were treated with antibacterial measures. Despite wound colonization with MRSA there was continued absence of this organism from the outer surface of the dressing. This important clinical finding has implications not only on the epidemiology of MRSA but also on the costs involved in barrier nursing. Clinical trial results Collated data from 50 controlled trials on a variety of wounds yielded infection rates of 5.37% and 3.25% (P
Infection Table

III.

Overall

rate of clinical

under

occlusive

infection in wounds dressings Controlled

Conventional No. studies No. wounds % Infection P < 0.001 for a vs b (Chi-square

50 1787 5.37”

dressings treated

studies Occlusive 50 2064 3.2Sb

89 by conventional

OY occlusive

All studies Occlusive 103 5374 2.08b

test).

occlusive dressings, therefore, virtually halved the infection rate. If non-controlled studies are also included (N = 103), infection rates of 5.37% and 2.08% (PC 0.001) are obtained for conventional and occlusive dressings respectively (Table III). Occlusive dressings were associated with lower rates of infection for all types of wound studied; the greatest difference being with ulcers and donor sites (Table IV). A comparison of the.occlusive dressings studied showed that the HCDs were associated with the lowest infection rates (Table V). All but two of the studies involved the HCD ‘DuoDERM’. All infection rate differences calculated from these pooled data are statistically significant but the possibility of ‘publication bias’ cannot be excluded. This data review also established that the colonizing flora of wounds was similar irrespective of dressing type. Reports which included details of microbiology appeared to confirm that the presence of most bacteria did not inhibit healing. 28,38,73-75 The presence of high levels of aerobic and anaerobic bacteria did not impede the healing of chronic venous ulcers under the HCD ‘DuoDERM’.~~~~~ Katz et uZ.,~~ Varghese et aL2* and Gilchrist & Reed,77 reported a reduction in numbers of P. aeruginosa and S. aUreUS under this HCD. This may be due to the antibacterial effect of the reduced of fungal pathogens was pH measured using HCD treatment. ‘s Potentiation not observed.79 Defence against infection under occlusion The normal host defence mechanisms against invading organisms can be categorized as non-specific and specific. ‘* The specific defences include the humoral and associated cell-mediated responses and are of importance after infection is established in tissues. The non-specific defences are, however, of particular importance in the prevention of infectious complications in wounds. Normal skin provides an excellent bacterial barrier; wounds disrupt this barrier but it can be temporarily restored with dressings such as HCDs. Certain occlusive dressings have also been shown to provide other possible defence mechanisms such as inhibition of bacterial growth by the reduced antibacterial pH created under HCD dressings28 and by the inherent activity of PUF dressings.‘*

IV.

Infection

Ulcers

2.07

7::

5;;

4.7

OCCL

CONV

Burns”

5.85

39;

7 298 5.0

22% 0.82

OCCL

CONV

OCCL 5:: 5.2

OCCL

All studies

13 437 1.1

3;:

abrasions, lacerations,

5.9

OCCL

sites

partial

15 511 4.7

OCCL

experimental

14 591 5.75

22 829 2.05

incisions,

CONV

controlled Others” Controlled studies

N = 50 for

OCCL

All studies

to indication.

CONV

Controlled studies

Donor

and occlusive dressings according N = 103 for all studies

Controlled studies

(conventional)

All studies

non-occlusive

Controlled studies

rates for

CONV, Conventional dressings; OCCL, Occlusive dressings. ’ Mainly partial thickness. ’ Includes moist skin desquamation, blisters, epidermolysis bullosa, sports injuries, wounds, granulating wounds, finger tip injuries and amputations.

No. studies No. wounds % Infections

Table

2.66

thickness

17:;

OCCL

All studies

studies,

Infection Table

V. Infection

under

rates for non-occlusive

occlusive

and occlusive category Controlled

dressings dressings according

studies

Conventional HCD” Films?

Foams and Hydrogels’ aPredominantly b Predominantly c Predominantly

No. studies No. wounds % Infection No. studies No. wounds % Infection No. studies No. wounds % infection ulcers; donor sites; miscellaneous

wounds

29 1104 1.9 17 743 4.44

21; 10.0

(See note ‘b’ Table

to occlusive dressing

All studies

Occlusive

29 823 3.9 16 754 5.7

91

21:

Occlusive 54 2548 0.98 32 1364 5.0 14:;

6.0

1.3

IV).

A particularly important role of some occlusive dressings is enhancement of host-derived non-specific mechanisms, complement and polymorphonuclear leukocytes (PMNs). The complement system, which is activated in normally under occlusive any wound containing bacteria,s2 functions dressings. The important host-derived factor in controlling wound sepsis is which provides immediate non-specific phagocytic PMN infiltrations3 antibacterial cover for the wound.82 Under occlusive dressings efficient PMN infiltration of the wound occurs together with enhanced bactericidal in occluded wounds has been confirmed.28,85,s6 activity.s4 PMN activity Examination of wound fluid has confirmed that this activity is equivalent to that of circulating blood.” Conclusion

Occlusive dressings are not only able to provide an optimum environment for re-epithelialization and angiogenesis 7,12but also create an environment which enables the host non-specific phagocytic defence mechanism to function efficiently. These factors together with lack of maceration of tissuess7 and careful wound management, are probably major contributors to the low rate of infection noted under occlusive dressings. References 1. Laforet EG. Wound dressing or window dressing? Arch Surg 1974; 109: 457. 2. Bennett RG. The debatable benefit of occlusive dressings for wounds. Dermatol Surg Oncol 1982; 8: 166-167. 3. Evans AJ. Treatment of burns today. Proc Roy Sot Med 1971; 64: 21-22. 4. Eaglstein WH. Experiences with biosynthetic dressings. r Am Acad Dermatol 1985; 12: 434440.

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5. Bull JP, Squire JR, Topley E. Experiments with occlusive dressings of new plastic. Lancet 1948; 1: 213-215. 6. Schilling RSF, Roberts M, Goodman N. Clinical trial of occlusive plastic dressings. Lancet 1950; 1: 293-296. 7. Winter GD. Formation of the scab and the rate of epithelialisation of superficial wounds in the skin of the young domestic pig. Nature 1962; 193: 293-294. 8. Hinman CC, Maibach HI, Winter CD. Effect of air exposure and occlusion on experimental human skin wounds. Nature 1963; 200: 377-379. 9. Madden MR, Finkelstein JL, Hefton JM, Yurt RW. Optimal healing of donor site wounds with hydrocolloid dressings. In: Ryan TJ, Ed. An Environment for Healing: the Role of Occlusion. Proceedings of the First International Symposium on Occlusion. London: Royal Society of Medicine 1985; 133-137. 10. Alvarez OM, Mertz PM, Eaglstein WH. The effect of occlusive dressings on collagen synthesis and re-epithelialization in superficial wounds. J Surg Res 1983; 35: 142-148. 11. Cherry GW, Ryan TJ, McGibbon D. Trial of a new dressing in venous leg ulcers. The Practitioner 1984; 228: 1175-1178. 12. Lydon MJ, Hutchinson JJ, Rippon M et al. Dissolution of wound coagulum and promotion of granulation tissue under DuoDERMTM. Wounds 1989; 1: 95-106. 13. Lawrence JC. What materials for dressings? Injury 1982; 13: 500-512. 14. Turner TD. Current and future trends in wound management 1: wound healing and traditional surgical dressings. Pharm Internat 1985; May: 117-119. 15. Holland KT, Kearney JN. Microbiology of skin. In: Skerrow D, Skerrow CJ, Eds. Methods in Skin Research. Chichester: John Wiley & Sons 1985; 433474. 16. Marsh PD. Selwvn S. Studies on antagonism between human skin bacteria. Med Microbial 1977; ld: 161-169. 17. Rebel1 G, Pillsbury DM, Phalle G, de Saint M, Ginsberg D. Factors affecting the rapid disanvearance of bacteria nlaced on the normal skin. Invest Dermatoll950: 14: 247-263. 18. Aly R, Maibach HI, Shinefield H, Strauss W. Survival of pathogenic microorganisms on human skin. Invest Dermatol 1972; 58: 205-210. 19. Marples RR. The effect of hydration on the bacterial flora of the skin. In: Skin Bacteria and their Role in Infection. New York: McGraw-Hill Book Company 1965; 33-41. 20. Bibel DJ, LeBrum JR. Changes in cutaneous flora after wet occlusion. CanJ Microbial 1975; 21: 496-500. 21. Selwyn S, Ellis H. Skin bacteria and skin disinfection reconsidered. Br MedJ 1972; 1: 136-140. 22. Aly R, Shirley C, Cunico B, Maibach HI. Effect of prolonged occlusion on the microbial flora, pH, carbon dioxide and transepidermal water loss on human skin. J Innvest Dermatol 1978; 71: 378-381. 23. Easmon CSF. Skin flora under chest dressings. In: Ryan TJ, Ed. An Environment for Healing: the Role of Occlusion. Proceedings of the First International Symposium on Occlusion. London: Royal Society of Medicine 1985: 42-44. 24. Lawrence JC, Lilly HA. Bacteriological properties of a new hydrocolloid dressing on intact skin of normal volunteers. In: Ryan TJ, Ed. An Environment for Healing: the Role of Occlusion. Proceedings of the First International Symposium on Occlusion. London: Royal Society of Medicine 1985: 51-55. 25. Lawrence JC, Lilly HA. Are hydrocolloid dressings bacteria-proof? PharmJ 1987; 239: 184. 26. Henning DR, Griffin TB, Maibach HI. Studies on changes in skin surface bacteria in induced miliaria and associated hypohydrosis. Acta Derm Venereal (Stockh) 1972; 52: 371-37s. 27. Mertz PM, Marshall DA, Eaglstein WH. Occlusive wound dressings to prevent bacterial invasion and wound infection. J Am Acad Dermatol 1985; 12: 662-668. 28. Varghese MC, Balin AK, Carter DM, Caldwell D. Local environment of chronic wounds under synthetic dressings. Arch Dermatol 1986; 122: 52-57. 29. Mertz PM, Eaglstein WH. The effect of a semiocclusive dressing on the microbial population in superficial wounds. Arch Surg 1984; 119: 287-289. 30. Eaglstein WH. Current wound management: a symposium. Clin Dermatol 1984; 2: 134-142. 31. Eaglstein WH. Effect of occlusive dressings on wound healing. Clin Dermatol 1984; 2: 107-111.

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32. Eaglstein WH, Mertz PM. Dressings and wound healing. In: Hunt TK, Heppenstall RB, Pines E, Rovee D, Eds. Soft and Hard Tissue Repair. Biological and Clinical Aspects, New York: Praeger, 1984; 316--325. 33. Alper JC, Welch EA, Ginsberg M, Bogaars H, Maguire P. Moist healing under a vapour permeable membrane. J Am Acad Dermatol 1983; 8: 347-353. 34. Harrison HN, Lindberg RB, Mason AD. Bacteriological and histological response of excised rat wounds to synthetic grafts. In: Wallace AB, Wilkinson AW, Eds. Research in Burns. Edinburgh: Livingstone 1966; 327-343. 3.5. Harris DR, Filarski SA, Hector RE. The effect of silastic sheet dressings on the healing of split skin graft donor sites. Plast Reconst Surg 1973; 52: 189-190. 36. Bucknall TE. Factors affecting healing. In Bucknall TE, Ellis H, Eds. Wound Healing for Surgeons. London: Bailhere-Tindall 1984; 42-74. 37. Lowbury EJL. Wit versus genes: the continuing battle against infection. 3’ Trauma 1979;

19: 33-45. 38. Alper JC, Vittimberga G. How and when to apply membrane dressings. Consultant 1988; 28: 142-150. 39. Bornside GH, Bornside BB. Comparison between moist swab and tissue biopsy methods for quantitation of bacteria in experimental incision wounds. J Trauma 1979; 19: 103-10s. 40. Pruitt BA. The diagnosis and treatment of infection in the burned patient. Burns 1984;

11: 79-81. 41. Lawrence JC. The bacteriology of burns. J Hosp infect 1985; 6 (Suppl. B): 3-17. 42. Robson MC, Duke WF, Krizek TJ. Rapid bacterial screening in the treatment of civilian wounds. r Surg Res 1973; 14: 426430. 43. Krizek TJ, Robson MC, Kho E. Bacterial growth and skin graft survival. Surg Forum 1967; 18: 518. 44. Goodwin CW. Current burn treatment. Advances in Surgery 1984; 18: 1455176. 45. Eriksson G, Eklund A-E, Kallings LO. The clinical significance of bacterial growth in venous leg ulcers. Stand J Infect Dis 1984; 16: 175-180. 46. van Rijswijk L, Brown D, Friedman S et al. Multicentre clinical evaluation of a hydrocolloid dressing for leg ulcers. Cutis 1985; 35: 173-176. 47. Lookingbill DP, Miller SH, Knowles RC. Bacteriology of chronic leg ulcers. Arch Dermatol 1978; 114: 1765-1768. 48. Alinovi A, Bassissi P, Pini M. Systemic administration of antibiotics in the management of venous ulcers. J Am Acad Dermatol 1986; 15: 186-l 91. 49. Daltrey DC, Rhodes B, Chattwood JG. Investigation into the microbial flora of healing and non-healing decubitus ulcers. J Clin Path01 1981; 34: 701-705. 50. Henderson HP, Marples RR, Richardson JF. Comparison of topical antibacterial agents in the preparation of varicose ulcers for skin grafting. J Hosp Infect 1980; 1: 141-147. 51. Mertz PM, Alvarez OM, Smerbeck RV, Eaglstein WH. A new in-vivo model for the evaluation of topical antiseptics on superficial wounds. The effect of 70% alcohol and povidone iodine solution. Arch Derm 1984; 120: 58862. 52. Greenhalgh D, Gamelli RL, Foster RS. Corynebacterium parvum impairs wound healing. Surg Forum 1983; 34: 616-619. 53. Cruickshank CND, Lowbury EJL. The effect of pyocyanin on human skin cells and leukocytes. BrJ Exp Path01 1953; 34: 583-587. 54. Lawrence JC. Some effects of staphylococcal and streptococcal toxins upon mammalian skin in tissue culture. BrJ Exp Path01 1959; 40: 8-14. 55. Lawrence JC. Laboratory studies of dressings. In: Lawrence JC, Ed. Proceedings of the Wound Healing Symposium. Oxford: Medicine Publishing Foundation 1983; 1155128. 56. Tenorio A, Jindrak K, Weiner M, Bella E, Enquist IF. Accelerated healing in infected wounds. Surg Gynaecol Obstet 1976; 142: 537-543. 57. Kan Gruber D, Gruber C, Seifter E, Molnar J, Levenson SM. Acceleration of wound healing by Staphylococcus aureus. Surg Forum 1981; 32: 76-78. 58. Laato M, Lehtonen O-P, Niinikoski J. Granulation tissue formation in experimental wounds inoculated with Staphylococcus aureus. Acta Chirurg Stand 1985; 151: 313-318. 59. Carrel1 A. Cicatrisation of wounds-XII, factors initiating regeneration. J Exp Med 1921; 24: 425-434. 60. Botsford T. The tensile strength of sutured skin wounds during healing. Surg Gynaecol Obstet 1941; 72: 690-697.

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