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Tissue Oxygenation, Anemia, and Perfusion in Relation to Wound Healing in Surgical Patients

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Tissue Oxygenation, Anemia, and Perfusion in Relation to Wound Healing in Surgical Patients Tissue Oxygenation, Anemia, and Perfusion in Relation to Wound Healing in Surgical Patients KENT JONSSON, M.D., PH.D.,* J. ARTHUR JENSEN, M.D., WILLIAM H. GOODSON, III, M.D., F.A.C.S., HEINZ SCHEUENSTUHL, A.B., JUDITH WEST, R.N., M.N., HARRIET WILLIAMS HOPF, M.D., and THOMAS K. HUNT, M.D., F.A.C.S., F.R.C.S. (GLASG) Oxygen tension and collagen deposition were measured in stan- From the Department of Surgery, University of California, dardized, subcutaneous wounds in 33 postoperative surgical pa- San Francisco, California tients. Pertinent clinical and wound parameters were analyzed by Pearson's correlation test and sequential linear regression analysis. Collagen deposition was directly and significantly pro- portional to wound oxygen tension and measures of perfusion. There were no significant correlations with hematocrit, estimated as one of the rationalizations.'0"' Therefore many sur- blood loss, length of operation, smoking, age, weight, sex, or geons find confusing the considerable experimental evi- urine output. This study in humans confirms animal experiments showing that collagen deposition and tensile strength in wounds dence that low hemoglobin levels are compatible with are limited by perfusion and tissue oxygen tension. It appears normal healing, and remain reluctant to tolerate even unnecessary to maintain hemoglobin at normal levels to support moderate anemia in postoperative patients.12-18 repair, provided that peripheral perfusion can be maintained at Unfortunately the anemia question diverts attention a high level in compensation for anemia. These circumstances the greater significance of experimental data that reflect the fact that although oxygen is essential to many aspects from of healing, and must be delivered at adequate partial pressures, link healing closely to arterial and tissue oxygen tension reparative tissue consumes relatively little of it. and far less closely to arterial oxygen content.3 4,6 These data together with a century ofsurgical experience suggest URGEONS HAVE LONG recognized that ischemic that the rate ofperfusion oftissue is particularly important tissues heal poorly and are easily infected. Recently in ensuring repair and furthermore that rapid perfusion that observation has been refined by experiments of hyperoxic blood can not only overcome the effects of in animals showing that arterial hypoxia retards repair significant anemia, but can accelerate healing beyond even when present as an isolated variable. 1-6 Furthermore usual expectations. most components ofhealing exceed normal expectations The present study was designed to measure oxygen ten- during moderate tissue hyperoxia.'-6 Anemia would seem, sion and perfusion in wounds of surgical patients and to therefore, to be inimical to healing, and for many years correlate them to the rate of collagen deposition, which surgeons and anesthesiologists have assumed so, largely is the major determinant of adequacy of repair in closed on the basis of marginal evidence in which nutritional wounds. The goals were (1) to test the validity for humans and blood volume issues were confused with simple, nor- of prior observations in animals in which collagen de- movolemic anemia.79 Some modern textbooks ofsurgery position in wounds was proportional to arterial oxygen still recommend that hemoglobin levels be maintained at tension over a broad range extending above and below or above 10 g/dL, with protection ofwound healing given normal levels, and (2) to determine the degree of anemia that can be tolerated with respect to healing in human patients. Supported by NIH GM 27345. If the relationship between oxygenation and healing * Present address, University of Lund, Department of Surgery, Malmo found in animals can be proved to apply to man, new General Hospital, 21401 Malmo, Sweden. perspectives open on support of wound healing. For in- Address reprint requests to T. K. Hunt, M.D., Department ofSurgery, such as 513 Parnassus Ave., University ofCalifornia, San Francisco, CA 94143- stance vasodilating agents alpha-adrenergic 0522. blockers, nitroprusside, endothelin, etc., could become Accepted for publication February 8, 1991. useful for treatment of endangered wounds. Blood trans- 605 606 JONSSON AND OTHERS Ann. Surg. * November 1991 fusions might be avoided, and a rationale might be con- they were to remain in hospital long enough to complete structed for hyperbaric therapy. the study and were free ofobvious impediments to healing such as diabetes, malnutrition, uremia, and Cushing's Methods syndrome. Pertinent clinical features were recorded (Ta- Wound-tissue oxygen tension (PSCO2) and collagen de- ble 1). position were measured in immediately adjacent, stan- At the end of each operation, a gas-sterilized, Luer- dardized experimental wounds in 33 surgical patients, 23 hubbed Silastic catheter (1 mm outer diameter, 0.8 mm women and 10 men (Table 1). Patients were solicited if inner diameter, 15 cm length) was threaded from caudad TABLE 1. Patients Ranked in Ascending Order ofCollagen Deposition Collagen Ag/cm Operation Length Blood Loss Pre-/Postoperative PscO2 Perfusion Patient Operation (min) (ml) Age HCT (air, max) Score 5 Days 7 Days I Perforated ulcer, 105 50 74 56/57 51, 51 0 0.36 cholecystectomy 2 Modified radical 165 400 57 39/33 48, 53 1 0.40 0.74 mastectomy 3 Repair gastric staple line; 330 300 51 34/29 43, 47 1 0.70 0.53 ventral herniorrhaphy 4 Repair vesicovaginal fistula 480 1050 42 45/30 48, 53 1 0.46 1.45 5 Intestinal fistulectomy 420 1000 56 30/31 41, 53 2 2.47 2.15 6 Breast reconstruction; 230 200 57 40/40 26, 53 1 2.09 3.04 ventral herniorrhaphy 7 Small bowel resection 300 500 39 43/34 44, 53 1 2.26 2.78 (Crohn's disease) 8 Hepatic lobectomy 210 2600 60 44/49 52, 63 2 2.36 9 Femoral herniorrhaphy 110 100 46 43/37 43, 89 3 2.55 2.95 10 Ventral herniorrhaphy 260 300 68 44/37 44, 64 3 2.78 3.55 11 Modified radical 180 300 50 37/37 41, 73 2 2.90 3.54 mastectomy 12 Lyse adhesions, excision of 180 350 60 38/33 52, 88 3 3.00 chylous cyst 13 Angelchik prostesis 215 350 73 35/33 38, 54 3 3.16 3.30 (hiatus hernia) 14 Modified radical 165 800 53 40/27 48, 60 2 1.04 3.53 mastectomy 15 Gastric bypass 255 250 52 43/37 44, 63 3 1.94 4.67 16 Right hemicolectomy 135 100 81 39/34 52, 64 2 2.88 3.73 17 Bowel resection 210 300 75 22/28 47, 52 1 3.17 3.73 (intestinal gangrene) 18 Ventral herniorrhaphy 180 100 34 42/37 34, 68 3 3.55 3.93 19 Ventral herniorrhaphy 70 20 54 45/39 36, 54 3 3.09 4.17 20 Ventral herniorrhaphy 250 500 56 42/31 35, 48 3 3.23 4.25 21 Inguinal herniorrhaphy 110 30 46 40/40 38, 68 2 3.42 4.00 22 Parathyroidectomy 270 100 33 24/25 57, 85 3 3.61 4.31 23 Hemicolectomy 240 650 34 48/43 57, 81 3 4.11 0.82 24 Gastric resection 210 150 69 42/31 47, 73 3 6.51 2.12 25 Soleus flap 170 50 42 18/16 60, 109 3 4.53 4.03 26 Oophorectomy 180 500 38 43/37 50, 98 3 4.74 27 Modified radical 110 50 52 43/33 42, 118 3 4.67 5.18 mastectomy 28 Modified radical 170 200 69 44/36 44, 87 3 3.21 7.63 mastectomy 29 Ileostomy takedown 190 200 64 34/35 28, 44 3 6.33 4.74 30 Gastric resection, 170 150 71 34/34 43, 83 3 5.11 6.66 Roux-en-Y 31 Modified radical 180 200 43 38/40 56, 97 3 7.01 mastectomy 32 Common bile duct 430 1500 25 40/33 47,91 3 5.42 11.55 exploration 33 Modified radical 225 250 53 41/41 51,90 2 7.37 13.65 mastectomy Total Mean ± SD 220 ± 120 414 ± 514 54 ± 14 39 ± 7/35 ± 7 3.3 ± 1.7 4.1 ± 2.8 Range 70-480 50-2600 25-81 18-56/16-57 0.4-7.4 0.4-13.7 Vol. 214 - No. 5 TISSUE OXYGENATION, ANEMIA, PERFUSION, AND WOUND HEALING 607 to cephalad subcutaneously on the lateral aspect of the obtained. Blood was drawn for arterial gas measurement upper arm by means of an 18-gauge, 10-cm needle (Ab- if clinically indicated. bocath T, Abbott Hospital, Inc., North Chicago, IL) so The corresponding values of PwO2 and arterial P02 that 7 cm remained in the subcutaneous position. Two (Pao2) were compared with the curve (Fig. 1) constructed pieces of porous (extruded) polytetrafluoroethylene from data obtained in similar postoperative patients who (ePTFE) tubing (6 cm long, 1 mm OD, pore size 90-120 were considered to be well perfused.20 When tissue hyp- ,Mm) (Gore-Tex, W. L. Gore & Assoc., Flagstaff, AZ) were oxia relative to Pao2 was found, supplemental fluid (250- similarly placed parallel to and approximately two and 500 mL 0.9% saline) above the ongoing rate was given four centimeters laterally from the Silastic tube. A single rapidly and PCO2 was remeasured. IfPsO2 increased dur- piece of 10- X 12-cm adherent plastic film was the only ing the supplemental infusion, more fluid was given until dressing. there was no further increase or until PwO2 rose into the Wound-tissue oxygen tension was measured 2 to 6 normal range. All patients breathed supplemental oxygen hours after the operation and daily thereafter. A reference by nasal prongs at 4 L/min for approximately 12 hours (silver/silver chloride) electrode was inserted through a per day during the first 3 postoperative days.
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