- Email: [email protected]
Comparative study of skin grafting with and without surgical removal of granulation tissue in chronic burn wounds
burns 33 (2007) 872–878
available at www.sciencedirect.com
journal homepage: www.elsevier.com/locate/burns
Comparative study of skin grafting with and without surgical removal of granulation tissue in chronic burn wounds Sanjay Dhar *, Rakesh Saraf, Anand K. Gupta, Bhavani Raina Department of Surgery, Govt. Medical College, Jammu, India
article info
abstract
Article history:
A prospective comparative study of skin grafting of chronic wounds with and without
Accepted 21 November 2006
surgical removal of granulation tissue was done on 51 patients with an objective of finding a better method of skin grafting objectively in the chronic burns wounds. Comparative study
Keywords:
was done on those patients who had wounds on both the sides of their body. Wounds
Chronic burn wound
present on the right side of the body labeled as Group A were skin grafted after removal of
Skin grafting
granulation tissue and wounds present on left side of the body labeled as Group B were skin
Graft uptake
grafted without removal of granulation tissue.
Cosmetic appearance
There was no significant difference in the comparative bacteriology, graft uptake and cosmetic appearance of the grafts. We found no effect of bacteriology and chronicity of the wounds on the uptake of grafts in the two groups. Serum albumin levels <4 g% was found to be associated with statistically significant decreased graft uptake only in Group A wounds. It was further observed that Group A wounds were associated with more blood loss, less secure haemostasis, prolonged surgical duration and thus more cost of surgery as compared to Group B wounds. # 2006 Elsevier Ltd and ISBI. All rights reserved.
1.
Introduction
The primary objective of any wound treatment is to achieve secure primary epithelial coverage of the defect rapidly and completely either by suturing or by application of graft or a flap. However, due to increased number of admissions in government hospitals as well as due to paucity of operative time, all these patients with tissue loss cannot be taken up for early wound closure. Moreover, in our center, many patients belonging to low socio economic status present quite late for treatment when their wounds are grossly infected, financial resources exhausted and morale down. Such patients are built up physiologically and psychologically and wound closure delayed till the dead tissue separates and granulation tissue is developed when the wound becomes ready for skin grafting.
The problem which now arises is, how to go about applying skin grafts on these chronic granulating wounds; whether to apply it on the granulation tissue per se; or to apply it after removal of granulation tissue. Opinions are divided on this issue. Some surgeons favour application of grafts after removal of granulation tissue in such wounds [1–4], while others favour application of grafts directly on the granulation tissue [5–8]. So far no controlled study has been reported in the literature, comparing the success of skin grafting by these two methods, that is, skin grafting with removal of granulation tissue and without removal of granulation tissue. Which of the two methods offered a better take of skin grafts was the object of our study so that these physically and psychologically scarred people could get a better treatment approach.
* Corresponding author at: 309-B, Sector-1, Durga Nagar, Jammu Tawi 180013, India. Tel.: +91 1912592156/9419194131. E-mail address: [email protected] (S. Dhar). 0305-4179/$32.00 # 2006 Elsevier Ltd and ISBI. All rights reserved. doi:10.1016/j.burns.2006.11.012
873
burns 33 (2007) 872–878
Fig. 1 – Granulation tissue on the wound sustained due to flame burns.
2.
Materials and methods
A prospective comparative study was carried out in the Department of Surgery on 51 patients in Government Medical College, Jammu, India. This study was done after being approved by the ethical committee of our institution and after taking written consent of the patients and their guardians. ‘Chronic burn wound’ for the purpose of this study meant a wound with skin loss which failed to heal or epithelise on its own within 3 weeks of the date of injury (Figs. 1 and 5). This study was done by dividing the wounds into Group A and Group B (Fig. 2). Group A included wounds on right side of the body in which granulation tissue was removed before skin grafting (right side remove granulations). Group B included wounds on left side of the body in which granulation tissue was not removed before grafting (left side leave granulations), instead it was cleansed with Ether (Rankem (diethyl ether 99%), manufactured by Fine Chemicals Ltd. an ISO 9001:2000 certified company of Ranbaxy) and Povidone iodine 5% (Betadine 5% w/v, manufactured by G.S. Pharmbutor Pvt. Ltd., Rajasthan, India and marketed by Win Medicare Pvt. Ltd.) followed by saline wash. Swabs for culture and sensitivity were taken using standard methods before removal of granulation tissue in Group A and after cleansing of granulation tissue with Ether and Betadine in Group B. Keeping in mind that removal of granulation tissue in Group A wounds might decrease skin graft uptake because of improper haemostasis and clot formation underneath the grafts, skin graft application was delayed for 24 h in both the groups for uniformity of comparison during which period partial thickness skin grafts were preserved in sterile saline gauze with dermal surfaces in apposition and refrigerated (not frozen). The skin grafts were meshed manually and placed on the wounds in the burn ward using sterile methods after giving injectible analgesics like diclofenac sodium or tramadol (Fig. 3). The grafted areas were dressed with tulle grass, adequately padded and splinted for immobility whenever necessary. The first post-graft dressing was done after 72 h which was followed by alternate day dressings (Fig. 6). Graft uptake was assessed on 16th post-grafting day (Fig. 7) and uptake was correlated with parameters like bacteriology,
Fig. 2 – Appearance of wound bed after excision of granulation on right side (black arrow) and after cleansing of granulation tissue on left side (white arrow).
chronicity and serum proteins. Cosmetic appearance of these grafted areas was assessed using Modified Scar Assessment Scale [9] after a minimum period of 3 months post-grafting (Fig. 4). This scar rating scale has three major categories of Colour, Texture and Symmetry.
Fig. 3 – Application of skin grafts.
874
burns 33 (2007) 872–878
Fig. 4 – Cosmetic appearance of the skin grafts 3 months after skin graft application (black arrow indicates right side and white arrow indicates left side).
Colour was further divided into (a) Pigmentation and (b) Vascularity. In Pigmentation a score of 1 and 2 was given to the graft for hypo or hyper pigmentation, respectively, in comparison to normal skin. Vascularity of the grafts was
Fig. 6 – Skin grafting after removal of granulation tissue on right leg and without removing granulation tissue on left leg. Bandage area shows the donor area.
Fig. 5 – Granulating wounds involving both legs following flame burns ready for grafting.
divided into three grades, i.e. Pink, Red and Purple which were given a score of 1, 2 and 3, respectively. Texture of the grafted area was divided into (a) Pliability and (b) Height above the normal surrounding skin. Pliability was further divided into Supple, Yields to pressure, Firm and flexible and Banding with a score of 1, 2, 3 and 4, respectively. Height of the grafted areas above normal skin was given a score of 1, 2, 3 depending on whether the graft was <2, <5, and >5 mm, respectively. Symmetry of the affected portion was judged comparing it to the normal skin and also with respect to the other affected side. Score of 1–3 depending on the asymmetry, i.e. mild, moderate or severe asymmetry, respectively, was given to the wounds. The design of the study was such as to enable us to achieve two important objectives. One was to control the variables like age, gender, duration of wounds, nutrition, etc. that may affect graft uptake, by doing both the types of grafting on the same patient. The other was to remove any bias in the selection of the patients by taking consecutive patients in the study and by randomizing wounds into right and left groups.
875
burns 33 (2007) 872–878
Table 2 – Comparative uptake of graft on 16th postgrafting day % uptake
Group A (n = 38)
91–100 81–90 71–80 <70
16 10 5 7
Group B (n = 38)
(42.09) (26.31) (13.15) (18.42)
12 16 5 5
(31.57) (42.10) (13.15) (13.15)
Figures in parenthesis indicate percentages ( p = 0.51).
Table 3 – Comparative distribution of isolates Organisms
Group A (n = 38)
Solitary isolates Twin isolates Nil
18 (47.36) 1 (7.89) 19 (50)
Group B (n = 38) 19 (50) 0 19 (50)
Figures in parenthesis indicate percentages.
Fig. 7 – Skin grafts on 16th post-grafting day.
Results were analysed statistically using Chi-square test.
3.
Observations
Fifty-one consecutive subjects were studied. These 38 subjects had wounds present on both sides of the body and presented a milieu for an ideal comparative study. Of the remaining 13 subjects, 5 had wounds only on right side and 8 had wounds only on left side of the body. The data obtained from these 13 provided additional information which helped in the formulation of the conclusion of the study. There was no statistically significant difference in the % body surface area of the wounds in the two groups (Table 1). Mean %BSA of wounds grafted in Group A was 4.65 2.35
Table 1 – Comparative distribution of %age of wounds grafted %BSA of wounds 1–5 6–10
(mean S.D.) and in Group B was 3.71 1.79 which again showed no significant difference. Only 68.40% of Group A against 73.67% of Group B wounds showed an uptake of 81–100% (Table 2). Mean graft uptake % in Group A was 83.74 16.74 (mean S.D.) and in Group B was 84.23 18.90. These differences were not statistically significant. Both the groups of wounds showed an almost similar bacteriological profile (Tables 3 and 4). Staph. epidermidis as a solitary isolate was the most common organism in both the groups followed by Pseudomonas, Staph. aureus, Escherchia coli and Klebsiella. There was further no statistically significant difference between the two groups of wounds when graft uptake was compared with the type of organisms cultured (Table 5). It was further observed that Gram negative organisms decreased the graft uptake against Gram positive organisms in either study groups. However, the total number of Gram negative organisms cultured was too small to assess
Group A (n = 38) 27 (71.05) 11 (28.94)
Figures in parenthesis indicate percentages.
Table 4 – Comparative distribution of organisms cultured Organisms cultured Staph. epidermidis Staph. aureus Pseudomonas E. coli Klebsiella
12 4 3 1 0
(60) (20) (15) (5)
Group B (n = 19) 11 3 3 1 1
(57.8) (15.7) (15.7) (5.2) (5.2)
Figures in parenthesis indicate percentages.
Table 5 – Comparative distribution of graft uptake in relation to organisms cultured Organisms cultured
Wounds
Gram+ve
Group A (n = 16) Group B (n = 14)
Gram ve
Group A (n = 4) Group B (n = 5)
Group B (n = 38) 32 (84.21) 6 (15.78)
Group A (n = 20)
Graft uptake Graft uptake (81–100%) (<81%) 10 (62.5) 11 (78.57) 2 (50) 3 (60)
Figures in parenthesis indicate percentages.
6 (37.5) 3 (21.42) 2 (50) 2 (40)
876
burns 33 (2007) 872–878
Table 6 – Comparative distribution of graft uptake in relation to the chronicity of wounds Chronicity (days)
% uptake
Group A
Table 9 – Comparative observations Factors
Group B
21–40 (n = 10)
81–100 <81
6 (60) 4 (40)
6 (60) 4 (40)
41–60 (n = 5)
81–100 <81
4 (80) 1 (20)
5 (100) 0
>60 (n = 23)
81–100 <81
15 (65.25) 8 (34.78)
15 (65.25) 8 (34.78)
Figures in parenthesis indicate percentages.
Graft uptake Cosmesis Blood loss Physiological insult Haemostasis Blood transfusions Operative time Cost of surgery Nutritional status (proteins)
Group A (excision) Same Same More More Less secure (takes more time) Required More More Affects uptake
Group B (non-excision) Same Same Minimal Minimal More secure (takes less time) Not required Less Less Does not affect
Table 7 – Comparative uptake of the graft in comparison to serum albumin concentration Serum albumin (g%)
Groups
% uptake of grafts 81–100
<81
4
A* (n = 20) B** (n = 20)
11 (55) 12 (60)
9 (45) 8 (40)
>4
A* (n = 23) B** (n = 26)
19 (82.60) 21 (80.76)
4 (17.39) 5 (19.23)
Figures in parenthesis indicate percentages. x2 = 3.87, d.f. = 1, p = 0.04 (significant). ** x2 = 2.41, d.f. = 1, p = 0.12 (not significant). *
its statistical significance. No statistically significant difference in graft uptake between two groups was noted when chronicity of the wounds was considered (Table 6). Table 7 reveals a comparison between two groups when 13 (5 + 8) subjects with unilateral wounds were added to 38 subjects. Thus, we had 43 wounds (38 + 5) in Group A and 46 wounds (38 + 8) in Group B for comparison. Our study revealed that when granulation tissue was removed (Group A) serum albumin conc. did affect the graft uptake significantly ( p = 0.04), meaning that when serum albumin levels were >4 g%, graft uptake was more than when serum albumin levels were 4 g%. Similar comparison in Group B wounds did not reveal any statistically significant results ( p = 0.12) meaning that graft uptake was better even when serum albumin levels were <4 g%. Cosmetic appearance using Modified Scar Assessment Scale revealed mean scar rating score of 4.93 1.43 (mean S.D.) in Group A wounds which was marginally better than Group B wounds which had a mean score of
Table 8 – Comparative cosmetic appearance score using Modified Scar Assessment Scale at 3 months postgrafting Score 3 4 5 6 7 8
Group A (n = 30) 5 7 10 3 3 2
(16.66) (23.33) (33.33) (10) (10) (6.66)
Figures in parenthesis indicate percentages.
Group B (n = 30) 4 10 3 6 6 1
(13.33) (33.33) (10) (20) (20) (3.33)
5.1 1.49 (Table 8). However, the difference was not statistically significant. In a subgroup of 13 subjects with unilateral wounds, all 5 in Group A were transfused blood because of blood loss during surgery as against no transfusions required in 8 of Group B, even though there was no statistically significant difference in the mean % of wounds grafted in two groups (Group A 4% and Group B 3.12%) (Table 9). Besides, operative time was also increased in Group A wounds because of the need to secure haemostasis before grafting.
4.
Discussion
After reviewing the literature we came across various studies either favouring excision of granulation tissue before application of grafts [1–4] or application of grafts directly on the granulation tissue without removal [5–8]. Some surgeons are of the view that if the granulations are fresh they can be grafted upon directly, but if granulations are long standing and fibrous they should be removed [3]. Some authors favouring excision of granulation tissue, however, state that if excision causes too much of bleeding the procedure can be omitted and grafts applied directly. All these views are very conflicting and present a very controversial picture of the status of granulation tissue. In all the studies mentioned the decision whether to or not to remove granulation tissue has been subjective based on surgeon’s experience and expertise. However, after searching the literature and Internet extensively we could not come across any controlled study comparing skin grafting with and without removal of granulation tissue. Our study was an attempt to objectively study the effect of granulation tissue on skin grafting. In our study a period of 3 weeks was kept as the criterion for labeling the wound as chronic because during this period the superficial wounds and small second degree burn wounds heal on their own [10]. Moreover during this period the slough and dead tissues in deep wounds get separated and granulation tissue is formed and wounds are considered fit for grafting [1–3].
4.1.
Bacteriology
We took 38 swabs from each group of wounds before grafting (Table 3). In Group A, we cultured solitary isolates from 18
burns 33 (2007) 872–878
swabs, twin isolates of Staph. aureus and Pseudomonas from 1 surface swab. From 19 swabs no organism could be cultured. In Group B wounds, only solitary isolates were cultured from 19 swabs and 19 swabs revealed no growth. There was comparable distribution of organisms cultured from both the groups (Table 4). Because of 1 twin culture in Group A total organisms present were 20 as against only 19 in Group B. There was predominance of Staph. epidermidis followed by Pseudomonas, Staph. aureus, E. coli and Klebsiella in both the groups. This is similar to observations from other studies [11–13]. However, in a few other studies Gram negative organisms have been found to be most prevalent with Klebsiella in some [14–16] and Pseudomonas in others [17–19]. Despite the fact that Staph. epidermidis was cultured from most of the wounds it was not found to affect graft uptake in our study [22]. Staph. epidermidis is considered to be a surface contaminant and non-pathogenic ordinarily but can cause disease when host defenses are breached and should be considered a significant pathogen in both burn patients and critically ill patients [20,21]. The decreased uptake of the grafts when Gram negative organisms were cultured in both the groups even though not significant (Table 5), could be attributed to Pseudomonas in our study. However, it requires further studies to uphold this view, since the total number of Gram negative organisms cultured in our study was less. Pseudomonas is a highly evolved nosocomial pathogen which is highly pathogenic in burn patients contributing considerably to morbidity and mortality and reduces the graft uptake by 5–10% [8] which may be the case in our study.
4.2.
Nutrition
Serum albumin can be considered an indicator of the nutritional state of the person as proteins are required by the body for wound healing and repair. Surgical removal of granulation tissue results in significant blood loss and adds physiological and operative insult to already compromised and catabolic patient. There is also more oozing of tissue fluids after surgical debridement (Group A) which also leads to protein loss. Proteins in such patient are needed for building up body reserves in the form of haemoglobin and tissue proteins in addition to skin graft uptake. When the granulation tissue is not removed (Group B) there is minimal blood loss and minimal physiological insult and more secure haemostasis and proteins are thus conserved for graft uptake only.
4.3.
877
thus causing stasis of the venous blood and more extraction of oxygen from the blood and hence the colour. As the graft matures, colour changes towards red and finally pink indicating that vascular network in the laid graft has achieved its peak. Usually after 6 months to 1 year, wound and scar maturation starts occurring resulting in decreased vascularity, and graft also becomes softer and flatter and colour of the graft may approach that of the normal skin. In our study at 3 months after skin grafting vascularity noted was usually pink which is consistent with colour changes of the scar at this time after injury. Most of the wounds had a pliability rating score of 1 or 2 with few showing a score of 3, i.e. firm and inflexible. Height of the graft was either the same as surrounding skin or in few cases <2 mm. In our study most of the cases showed mild asymmetry and few had moderate asymmetry.
5.
Conclusion
It is immaterial whether grafts are placed on granulation tissue or after scraping, however, it is better to graft the wounds without removing the granulation tissue for the reasons enumerated in Table 9. Graft uptake and cosmesis are the same in both the groups but other listed factors in the table tilt the balance strongly in favour of application of grafts without removal of granulation tissue. Scraping off of the granulation tissue entails loss of much blood and requires alertness on the part of attending doctors to detect hypotension which usually occurs suddenly. This causes more physiological instability in an already chronically ill patient if replacement by fluids and blood is not swift and adequate. The arrangement of blood preoperatively requires significant efforts and consumes much time and energy. This difficulty in arranging blood preoperatively is a great deterrent towards taking up the patients for surgery in our setup. Blood requirement for surgery can be virtually dispensed with in these patients if granulation tissue is not removed because minimal blood loss occurs. The base of the wound continues to ooze for a considerable period of time after removal of granulation tissue in Group A wounds, requiring much time and patience to achieve haemostasis. This increases time spent in surgery and also subjects the patient to potentially harmful anaesthetic drugs for more period of time. All these things also add to the increased cost of surgery.
Cosmesis
6. Out of the 38 subjects, 8 patients were lost to the follow up and only 30 patients were considered for comparative cosmetic appearance results which was found to be statistically similar (Table 8). In majority of cases in our study skin grafts observed were found to be hyperpigmented irrespective of the groups they belonged to. Purple colour is usually seen in the initial few weeks of the graft application because of immaturity of vascular system,
Suggestion
We strongly recommend grafting of chronic burn wounds without removing the granulation tissue and, thus, curtailing if not mitigating the misery of the patients.
Conflict of interest No conflicts of interests are involved in this study.
878
burns 33 (2007) 872–878
references
[1] Blair VP, Brown JB. The use and uses of large split skin grafts of intermediate thickness.. Surg Gynecol Obstretics 1929;49(1):82–97. [2] Brown JB, Byars Louis T, Blair VP. A study of ulcerations of lower extremity and their repair with thick split skin grafts. Surg Gynecol Obestretics 1936;63(3):331–40. [3] Brown JB, Mcdowell F. Massive repair of burns with thick split skin grafts. Ann Surg 1942;115(4):658–74. [4] Ackman D, Gerrie JW, Pritchard JE, Mills ES. A report on the management of burns using the occlusive compression with sulphathiazide emulsion. Ann Surg 1944;119(2):167–77. [5] Pollock William J, Parkes James C. Open skin grafting of war wounds. J Bone Joint Surg 1969;51-A(5):926–34. [6] Harlanstone H, Fabian Timothy C, Turklson Margaret L, et al. Management of acute full thickness losses of the abdominal wall. Ann Surg 1981;193(5):612–8. [7] Rudolph R, Ballantyne DL. Skin grafts. In: McCarthy Joseph G, editor. Plastic surgery, vol. 1. Philadephia: WB Saunders Company; 1990. p. 221–74. [8] McGregor Alan D. Free skin Grafts, chapter 3. In: McGregor Alan D, editor. Fundamental techniques of plastic surgery. 10th ed., Churchill Livingstone: Harcourt Publishers Ltd.; 2000. p. 35–59. [9] Fraulin Frankie OG, Illmayer SJ, Tredget EE. Assessment of cosmetic and functional results of conservative versus surgical management of facial burns. J Burn Care Rehabil 1996;17(1):19–29. [10] Larson DL. Closure of burn wound. J Trauma 1965;5(2): 254–66.
[11] Winkler M, Erbs G, Muller FE, Konig W. Epidemiology studies of microbial colonization of severely burned patients. Zentralbl Bakteriol Mikrobiol Hyg (B) 1987;184(3– 4):304–20. [12] Vindeness H, Bjerknes R. Microbial colonization of large wounds. Burns 1995;21(8):575–9. [13] Choudhary A, Rao TV. Bacteraemia in a tertiary care urban hospital in South India. Indian J Pathol Microbiol 1999;42(3):317–20. [14] Ozumba UC, Jibrum BC. Bacteriology of burn wounds in Enugu, Nigeria. Burns 2000;26(2):178–80. [15] Karyoute SM. Burn wound infection in 100 patients treated in a burn unit at Jordan University Hospital. Burns 1989;15(1):117–9. [16] Mabogunje OA, Khwaja MS, Lawrie JH. Childhood burns in Zaria, Nigeria. Burns 1978;13(4):198–204. [17] Nakhla LS, Sanden R. Microbiological aspects of burns at Mount Verman Hospital, UK. Burns 1991;17(4):309–12. [18] Pruitt BA, Colonel Mc, Mc Manvs AD. Opportunistic infections in severely burnt patients. Am J Med 1984;76(1):146–54. [19] Singh NP, Goyal R, Manchanda V, Das S, Kaur I, Talwar V. Changing trends in bact. of burns in the burns unit, Delhi, India. Burns 2003;29(2):129–32. [20] Ananthnarayan R, Panikar CKJ. Staphylococcus, chapter 22. In: Ananthnarayan, Panikar CKJ, editors. Text book of microbiology. 5th ed., Orient Longman Ltd.; 1998. p. 177–86. [21] Baurchard KW, Minor LB, Slotman GJ, Gann DS. Staphylococcus epidermidis sepsis in surgical patients. Arch Surg 1984;119:96–100. [22] Eade Gilbert G. The relationship between granulation tissue, bacteria and skin grafts in burned patients. Plastic Reconstructive Surg 1958;22(1):42–55.
available at www.sciencedirect.com
journal homepage: www.elsevier.com/locate/burns
Comparative study of skin grafting with and without surgical removal of granulation tissue in chronic burn wounds Sanjay Dhar *, Rakesh Saraf, Anand K. Gupta, Bhavani Raina Department of Surgery, Govt. Medical College, Jammu, India
article info
abstract
Article history:
A prospective comparative study of skin grafting of chronic wounds with and without
Accepted 21 November 2006
surgical removal of granulation tissue was done on 51 patients with an objective of finding a better method of skin grafting objectively in the chronic burns wounds. Comparative study
Keywords:
was done on those patients who had wounds on both the sides of their body. Wounds
Chronic burn wound
present on the right side of the body labeled as Group A were skin grafted after removal of
Skin grafting
granulation tissue and wounds present on left side of the body labeled as Group B were skin
Graft uptake
grafted without removal of granulation tissue.
Cosmetic appearance
There was no significant difference in the comparative bacteriology, graft uptake and cosmetic appearance of the grafts. We found no effect of bacteriology and chronicity of the wounds on the uptake of grafts in the two groups. Serum albumin levels <4 g% was found to be associated with statistically significant decreased graft uptake only in Group A wounds. It was further observed that Group A wounds were associated with more blood loss, less secure haemostasis, prolonged surgical duration and thus more cost of surgery as compared to Group B wounds. # 2006 Elsevier Ltd and ISBI. All rights reserved.
1.
Introduction
The primary objective of any wound treatment is to achieve secure primary epithelial coverage of the defect rapidly and completely either by suturing or by application of graft or a flap. However, due to increased number of admissions in government hospitals as well as due to paucity of operative time, all these patients with tissue loss cannot be taken up for early wound closure. Moreover, in our center, many patients belonging to low socio economic status present quite late for treatment when their wounds are grossly infected, financial resources exhausted and morale down. Such patients are built up physiologically and psychologically and wound closure delayed till the dead tissue separates and granulation tissue is developed when the wound becomes ready for skin grafting.
The problem which now arises is, how to go about applying skin grafts on these chronic granulating wounds; whether to apply it on the granulation tissue per se; or to apply it after removal of granulation tissue. Opinions are divided on this issue. Some surgeons favour application of grafts after removal of granulation tissue in such wounds [1–4], while others favour application of grafts directly on the granulation tissue [5–8]. So far no controlled study has been reported in the literature, comparing the success of skin grafting by these two methods, that is, skin grafting with removal of granulation tissue and without removal of granulation tissue. Which of the two methods offered a better take of skin grafts was the object of our study so that these physically and psychologically scarred people could get a better treatment approach.
* Corresponding author at: 309-B, Sector-1, Durga Nagar, Jammu Tawi 180013, India. Tel.: +91 1912592156/9419194131. E-mail address: [email protected] (S. Dhar). 0305-4179/$32.00 # 2006 Elsevier Ltd and ISBI. All rights reserved. doi:10.1016/j.burns.2006.11.012
873
burns 33 (2007) 872–878
Fig. 1 – Granulation tissue on the wound sustained due to flame burns.
2.
Materials and methods
A prospective comparative study was carried out in the Department of Surgery on 51 patients in Government Medical College, Jammu, India. This study was done after being approved by the ethical committee of our institution and after taking written consent of the patients and their guardians. ‘Chronic burn wound’ for the purpose of this study meant a wound with skin loss which failed to heal or epithelise on its own within 3 weeks of the date of injury (Figs. 1 and 5). This study was done by dividing the wounds into Group A and Group B (Fig. 2). Group A included wounds on right side of the body in which granulation tissue was removed before skin grafting (right side remove granulations). Group B included wounds on left side of the body in which granulation tissue was not removed before grafting (left side leave granulations), instead it was cleansed with Ether (Rankem (diethyl ether 99%), manufactured by Fine Chemicals Ltd. an ISO 9001:2000 certified company of Ranbaxy) and Povidone iodine 5% (Betadine 5% w/v, manufactured by G.S. Pharmbutor Pvt. Ltd., Rajasthan, India and marketed by Win Medicare Pvt. Ltd.) followed by saline wash. Swabs for culture and sensitivity were taken using standard methods before removal of granulation tissue in Group A and after cleansing of granulation tissue with Ether and Betadine in Group B. Keeping in mind that removal of granulation tissue in Group A wounds might decrease skin graft uptake because of improper haemostasis and clot formation underneath the grafts, skin graft application was delayed for 24 h in both the groups for uniformity of comparison during which period partial thickness skin grafts were preserved in sterile saline gauze with dermal surfaces in apposition and refrigerated (not frozen). The skin grafts were meshed manually and placed on the wounds in the burn ward using sterile methods after giving injectible analgesics like diclofenac sodium or tramadol (Fig. 3). The grafted areas were dressed with tulle grass, adequately padded and splinted for immobility whenever necessary. The first post-graft dressing was done after 72 h which was followed by alternate day dressings (Fig. 6). Graft uptake was assessed on 16th post-grafting day (Fig. 7) and uptake was correlated with parameters like bacteriology,
Fig. 2 – Appearance of wound bed after excision of granulation on right side (black arrow) and after cleansing of granulation tissue on left side (white arrow).
chronicity and serum proteins. Cosmetic appearance of these grafted areas was assessed using Modified Scar Assessment Scale [9] after a minimum period of 3 months post-grafting (Fig. 4). This scar rating scale has three major categories of Colour, Texture and Symmetry.
Fig. 3 – Application of skin grafts.
874
burns 33 (2007) 872–878
Fig. 4 – Cosmetic appearance of the skin grafts 3 months after skin graft application (black arrow indicates right side and white arrow indicates left side).
Colour was further divided into (a) Pigmentation and (b) Vascularity. In Pigmentation a score of 1 and 2 was given to the graft for hypo or hyper pigmentation, respectively, in comparison to normal skin. Vascularity of the grafts was
Fig. 6 – Skin grafting after removal of granulation tissue on right leg and without removing granulation tissue on left leg. Bandage area shows the donor area.
Fig. 5 – Granulating wounds involving both legs following flame burns ready for grafting.
divided into three grades, i.e. Pink, Red and Purple which were given a score of 1, 2 and 3, respectively. Texture of the grafted area was divided into (a) Pliability and (b) Height above the normal surrounding skin. Pliability was further divided into Supple, Yields to pressure, Firm and flexible and Banding with a score of 1, 2, 3 and 4, respectively. Height of the grafted areas above normal skin was given a score of 1, 2, 3 depending on whether the graft was <2, <5, and >5 mm, respectively. Symmetry of the affected portion was judged comparing it to the normal skin and also with respect to the other affected side. Score of 1–3 depending on the asymmetry, i.e. mild, moderate or severe asymmetry, respectively, was given to the wounds. The design of the study was such as to enable us to achieve two important objectives. One was to control the variables like age, gender, duration of wounds, nutrition, etc. that may affect graft uptake, by doing both the types of grafting on the same patient. The other was to remove any bias in the selection of the patients by taking consecutive patients in the study and by randomizing wounds into right and left groups.
875
burns 33 (2007) 872–878
Table 2 – Comparative uptake of graft on 16th postgrafting day % uptake
Group A (n = 38)
91–100 81–90 71–80 <70
16 10 5 7
Group B (n = 38)
(42.09) (26.31) (13.15) (18.42)
12 16 5 5
(31.57) (42.10) (13.15) (13.15)
Figures in parenthesis indicate percentages ( p = 0.51).
Table 3 – Comparative distribution of isolates Organisms
Group A (n = 38)
Solitary isolates Twin isolates Nil
18 (47.36) 1 (7.89) 19 (50)
Group B (n = 38) 19 (50) 0 19 (50)
Figures in parenthesis indicate percentages.
Fig. 7 – Skin grafts on 16th post-grafting day.
Results were analysed statistically using Chi-square test.
3.
Observations
Fifty-one consecutive subjects were studied. These 38 subjects had wounds present on both sides of the body and presented a milieu for an ideal comparative study. Of the remaining 13 subjects, 5 had wounds only on right side and 8 had wounds only on left side of the body. The data obtained from these 13 provided additional information which helped in the formulation of the conclusion of the study. There was no statistically significant difference in the % body surface area of the wounds in the two groups (Table 1). Mean %BSA of wounds grafted in Group A was 4.65 2.35
Table 1 – Comparative distribution of %age of wounds grafted %BSA of wounds 1–5 6–10
(mean S.D.) and in Group B was 3.71 1.79 which again showed no significant difference. Only 68.40% of Group A against 73.67% of Group B wounds showed an uptake of 81–100% (Table 2). Mean graft uptake % in Group A was 83.74 16.74 (mean S.D.) and in Group B was 84.23 18.90. These differences were not statistically significant. Both the groups of wounds showed an almost similar bacteriological profile (Tables 3 and 4). Staph. epidermidis as a solitary isolate was the most common organism in both the groups followed by Pseudomonas, Staph. aureus, Escherchia coli and Klebsiella. There was further no statistically significant difference between the two groups of wounds when graft uptake was compared with the type of organisms cultured (Table 5). It was further observed that Gram negative organisms decreased the graft uptake against Gram positive organisms in either study groups. However, the total number of Gram negative organisms cultured was too small to assess
Group A (n = 38) 27 (71.05) 11 (28.94)
Figures in parenthesis indicate percentages.
Table 4 – Comparative distribution of organisms cultured Organisms cultured Staph. epidermidis Staph. aureus Pseudomonas E. coli Klebsiella
12 4 3 1 0
(60) (20) (15) (5)
Group B (n = 19) 11 3 3 1 1
(57.8) (15.7) (15.7) (5.2) (5.2)
Figures in parenthesis indicate percentages.
Table 5 – Comparative distribution of graft uptake in relation to organisms cultured Organisms cultured
Wounds
Gram+ve
Group A (n = 16) Group B (n = 14)
Gram ve
Group A (n = 4) Group B (n = 5)
Group B (n = 38) 32 (84.21) 6 (15.78)
Group A (n = 20)
Graft uptake Graft uptake (81–100%) (<81%) 10 (62.5) 11 (78.57) 2 (50) 3 (60)
Figures in parenthesis indicate percentages.
6 (37.5) 3 (21.42) 2 (50) 2 (40)
876
burns 33 (2007) 872–878
Table 6 – Comparative distribution of graft uptake in relation to the chronicity of wounds Chronicity (days)
% uptake
Group A
Table 9 – Comparative observations Factors
Group B
21–40 (n = 10)
81–100 <81
6 (60) 4 (40)
6 (60) 4 (40)
41–60 (n = 5)
81–100 <81
4 (80) 1 (20)
5 (100) 0
>60 (n = 23)
81–100 <81
15 (65.25) 8 (34.78)
15 (65.25) 8 (34.78)
Figures in parenthesis indicate percentages.
Graft uptake Cosmesis Blood loss Physiological insult Haemostasis Blood transfusions Operative time Cost of surgery Nutritional status (proteins)
Group A (excision) Same Same More More Less secure (takes more time) Required More More Affects uptake
Group B (non-excision) Same Same Minimal Minimal More secure (takes less time) Not required Less Less Does not affect
Table 7 – Comparative uptake of the graft in comparison to serum albumin concentration Serum albumin (g%)
Groups
% uptake of grafts 81–100
<81
4
A* (n = 20) B** (n = 20)
11 (55) 12 (60)
9 (45) 8 (40)
>4
A* (n = 23) B** (n = 26)
19 (82.60) 21 (80.76)
4 (17.39) 5 (19.23)
Figures in parenthesis indicate percentages. x2 = 3.87, d.f. = 1, p = 0.04 (significant). ** x2 = 2.41, d.f. = 1, p = 0.12 (not significant). *
its statistical significance. No statistically significant difference in graft uptake between two groups was noted when chronicity of the wounds was considered (Table 6). Table 7 reveals a comparison between two groups when 13 (5 + 8) subjects with unilateral wounds were added to 38 subjects. Thus, we had 43 wounds (38 + 5) in Group A and 46 wounds (38 + 8) in Group B for comparison. Our study revealed that when granulation tissue was removed (Group A) serum albumin conc. did affect the graft uptake significantly ( p = 0.04), meaning that when serum albumin levels were >4 g%, graft uptake was more than when serum albumin levels were 4 g%. Similar comparison in Group B wounds did not reveal any statistically significant results ( p = 0.12) meaning that graft uptake was better even when serum albumin levels were <4 g%. Cosmetic appearance using Modified Scar Assessment Scale revealed mean scar rating score of 4.93 1.43 (mean S.D.) in Group A wounds which was marginally better than Group B wounds which had a mean score of
Table 8 – Comparative cosmetic appearance score using Modified Scar Assessment Scale at 3 months postgrafting Score 3 4 5 6 7 8
Group A (n = 30) 5 7 10 3 3 2
(16.66) (23.33) (33.33) (10) (10) (6.66)
Figures in parenthesis indicate percentages.
Group B (n = 30) 4 10 3 6 6 1
(13.33) (33.33) (10) (20) (20) (3.33)
5.1 1.49 (Table 8). However, the difference was not statistically significant. In a subgroup of 13 subjects with unilateral wounds, all 5 in Group A were transfused blood because of blood loss during surgery as against no transfusions required in 8 of Group B, even though there was no statistically significant difference in the mean % of wounds grafted in two groups (Group A 4% and Group B 3.12%) (Table 9). Besides, operative time was also increased in Group A wounds because of the need to secure haemostasis before grafting.
4.
Discussion
After reviewing the literature we came across various studies either favouring excision of granulation tissue before application of grafts [1–4] or application of grafts directly on the granulation tissue without removal [5–8]. Some surgeons are of the view that if the granulations are fresh they can be grafted upon directly, but if granulations are long standing and fibrous they should be removed [3]. Some authors favouring excision of granulation tissue, however, state that if excision causes too much of bleeding the procedure can be omitted and grafts applied directly. All these views are very conflicting and present a very controversial picture of the status of granulation tissue. In all the studies mentioned the decision whether to or not to remove granulation tissue has been subjective based on surgeon’s experience and expertise. However, after searching the literature and Internet extensively we could not come across any controlled study comparing skin grafting with and without removal of granulation tissue. Our study was an attempt to objectively study the effect of granulation tissue on skin grafting. In our study a period of 3 weeks was kept as the criterion for labeling the wound as chronic because during this period the superficial wounds and small second degree burn wounds heal on their own [10]. Moreover during this period the slough and dead tissues in deep wounds get separated and granulation tissue is formed and wounds are considered fit for grafting [1–3].
4.1.
Bacteriology
We took 38 swabs from each group of wounds before grafting (Table 3). In Group A, we cultured solitary isolates from 18
burns 33 (2007) 872–878
swabs, twin isolates of Staph. aureus and Pseudomonas from 1 surface swab. From 19 swabs no organism could be cultured. In Group B wounds, only solitary isolates were cultured from 19 swabs and 19 swabs revealed no growth. There was comparable distribution of organisms cultured from both the groups (Table 4). Because of 1 twin culture in Group A total organisms present were 20 as against only 19 in Group B. There was predominance of Staph. epidermidis followed by Pseudomonas, Staph. aureus, E. coli and Klebsiella in both the groups. This is similar to observations from other studies [11–13]. However, in a few other studies Gram negative organisms have been found to be most prevalent with Klebsiella in some [14–16] and Pseudomonas in others [17–19]. Despite the fact that Staph. epidermidis was cultured from most of the wounds it was not found to affect graft uptake in our study [22]. Staph. epidermidis is considered to be a surface contaminant and non-pathogenic ordinarily but can cause disease when host defenses are breached and should be considered a significant pathogen in both burn patients and critically ill patients [20,21]. The decreased uptake of the grafts when Gram negative organisms were cultured in both the groups even though not significant (Table 5), could be attributed to Pseudomonas in our study. However, it requires further studies to uphold this view, since the total number of Gram negative organisms cultured in our study was less. Pseudomonas is a highly evolved nosocomial pathogen which is highly pathogenic in burn patients contributing considerably to morbidity and mortality and reduces the graft uptake by 5–10% [8] which may be the case in our study.
4.2.
Nutrition
Serum albumin can be considered an indicator of the nutritional state of the person as proteins are required by the body for wound healing and repair. Surgical removal of granulation tissue results in significant blood loss and adds physiological and operative insult to already compromised and catabolic patient. There is also more oozing of tissue fluids after surgical debridement (Group A) which also leads to protein loss. Proteins in such patient are needed for building up body reserves in the form of haemoglobin and tissue proteins in addition to skin graft uptake. When the granulation tissue is not removed (Group B) there is minimal blood loss and minimal physiological insult and more secure haemostasis and proteins are thus conserved for graft uptake only.
4.3.
877
thus causing stasis of the venous blood and more extraction of oxygen from the blood and hence the colour. As the graft matures, colour changes towards red and finally pink indicating that vascular network in the laid graft has achieved its peak. Usually after 6 months to 1 year, wound and scar maturation starts occurring resulting in decreased vascularity, and graft also becomes softer and flatter and colour of the graft may approach that of the normal skin. In our study at 3 months after skin grafting vascularity noted was usually pink which is consistent with colour changes of the scar at this time after injury. Most of the wounds had a pliability rating score of 1 or 2 with few showing a score of 3, i.e. firm and inflexible. Height of the graft was either the same as surrounding skin or in few cases <2 mm. In our study most of the cases showed mild asymmetry and few had moderate asymmetry.
5.
Conclusion
It is immaterial whether grafts are placed on granulation tissue or after scraping, however, it is better to graft the wounds without removing the granulation tissue for the reasons enumerated in Table 9. Graft uptake and cosmesis are the same in both the groups but other listed factors in the table tilt the balance strongly in favour of application of grafts without removal of granulation tissue. Scraping off of the granulation tissue entails loss of much blood and requires alertness on the part of attending doctors to detect hypotension which usually occurs suddenly. This causes more physiological instability in an already chronically ill patient if replacement by fluids and blood is not swift and adequate. The arrangement of blood preoperatively requires significant efforts and consumes much time and energy. This difficulty in arranging blood preoperatively is a great deterrent towards taking up the patients for surgery in our setup. Blood requirement for surgery can be virtually dispensed with in these patients if granulation tissue is not removed because minimal blood loss occurs. The base of the wound continues to ooze for a considerable period of time after removal of granulation tissue in Group A wounds, requiring much time and patience to achieve haemostasis. This increases time spent in surgery and also subjects the patient to potentially harmful anaesthetic drugs for more period of time. All these things also add to the increased cost of surgery.
Cosmesis
6. Out of the 38 subjects, 8 patients were lost to the follow up and only 30 patients were considered for comparative cosmetic appearance results which was found to be statistically similar (Table 8). In majority of cases in our study skin grafts observed were found to be hyperpigmented irrespective of the groups they belonged to. Purple colour is usually seen in the initial few weeks of the graft application because of immaturity of vascular system,
Suggestion
We strongly recommend grafting of chronic burn wounds without removing the granulation tissue and, thus, curtailing if not mitigating the misery of the patients.
Conflict of interest No conflicts of interests are involved in this study.
878
burns 33 (2007) 872–878
references
[1] Blair VP, Brown JB. The use and uses of large split skin grafts of intermediate thickness.. Surg Gynecol Obstretics 1929;49(1):82–97. [2] Brown JB, Byars Louis T, Blair VP. A study of ulcerations of lower extremity and their repair with thick split skin grafts. Surg Gynecol Obestretics 1936;63(3):331–40. [3] Brown JB, Mcdowell F. Massive repair of burns with thick split skin grafts. Ann Surg 1942;115(4):658–74. [4] Ackman D, Gerrie JW, Pritchard JE, Mills ES. A report on the management of burns using the occlusive compression with sulphathiazide emulsion. Ann Surg 1944;119(2):167–77. [5] Pollock William J, Parkes James C. Open skin grafting of war wounds. J Bone Joint Surg 1969;51-A(5):926–34. [6] Harlanstone H, Fabian Timothy C, Turklson Margaret L, et al. Management of acute full thickness losses of the abdominal wall. Ann Surg 1981;193(5):612–8. [7] Rudolph R, Ballantyne DL. Skin grafts. In: McCarthy Joseph G, editor. Plastic surgery, vol. 1. Philadephia: WB Saunders Company; 1990. p. 221–74. [8] McGregor Alan D. Free skin Grafts, chapter 3. In: McGregor Alan D, editor. Fundamental techniques of plastic surgery. 10th ed., Churchill Livingstone: Harcourt Publishers Ltd.; 2000. p. 35–59. [9] Fraulin Frankie OG, Illmayer SJ, Tredget EE. Assessment of cosmetic and functional results of conservative versus surgical management of facial burns. J Burn Care Rehabil 1996;17(1):19–29. [10] Larson DL. Closure of burn wound. J Trauma 1965;5(2): 254–66.
[11] Winkler M, Erbs G, Muller FE, Konig W. Epidemiology studies of microbial colonization of severely burned patients. Zentralbl Bakteriol Mikrobiol Hyg (B) 1987;184(3– 4):304–20. [12] Vindeness H, Bjerknes R. Microbial colonization of large wounds. Burns 1995;21(8):575–9. [13] Choudhary A, Rao TV. Bacteraemia in a tertiary care urban hospital in South India. Indian J Pathol Microbiol 1999;42(3):317–20. [14] Ozumba UC, Jibrum BC. Bacteriology of burn wounds in Enugu, Nigeria. Burns 2000;26(2):178–80. [15] Karyoute SM. Burn wound infection in 100 patients treated in a burn unit at Jordan University Hospital. Burns 1989;15(1):117–9. [16] Mabogunje OA, Khwaja MS, Lawrie JH. Childhood burns in Zaria, Nigeria. Burns 1978;13(4):198–204. [17] Nakhla LS, Sanden R. Microbiological aspects of burns at Mount Verman Hospital, UK. Burns 1991;17(4):309–12. [18] Pruitt BA, Colonel Mc, Mc Manvs AD. Opportunistic infections in severely burnt patients. Am J Med 1984;76(1):146–54. [19] Singh NP, Goyal R, Manchanda V, Das S, Kaur I, Talwar V. Changing trends in bact. of burns in the burns unit, Delhi, India. Burns 2003;29(2):129–32. [20] Ananthnarayan R, Panikar CKJ. Staphylococcus, chapter 22. In: Ananthnarayan, Panikar CKJ, editors. Text book of microbiology. 5th ed., Orient Longman Ltd.; 1998. p. 177–86. [21] Baurchard KW, Minor LB, Slotman GJ, Gann DS. Staphylococcus epidermidis sepsis in surgical patients. Arch Surg 1984;119:96–100. [22] Eade Gilbert G. The relationship between granulation tissue, bacteria and skin grafts in burned patients. Plastic Reconstructive Surg 1958;22(1):42–55.