Transverse uterine incision non-closure versus closure: an experimental study in sheep

Copyright C Acta Obstet Gynecol Scand 2000

Acta Obstet Gynecol Scand 2000; 79: 813–817 Printed in Denmark ¡ All rights reserved

Acta Obstetricia et Gynecologica Scandinavica ISSN 0001-6349

ORIGINAL ARTICLE

Transverse uterine incision non-closure versus closure: an experimental study in sheep ABDU¨LAZIZ GU¨L1, YALC¸IN S¸˙IMS¸EK1, SERDAR UGˇRAS¸2 AND TALIP GU¨L3 From the Departments of 1Obstetrics and Gynecology and 2Pathology, Yüzüncü Yıl University School of Medicine, Van, and the 3Department of Obstetrics and Gynecology, Dicle University School of Medicine, Diyarbakir, Turkey

Acta Obstet Gynecol Scand 2000; 79: 813–817. C Acta Obstet Gynecol Scand 2000 Subject. This study was designed to investigate whether the non-closure of the layers of the uterus during low transverse cesarean section would result in healing and have advantage on closure. Material and method. Thirty pregnant ewes randomly divided into two groups. Each group included 15 ewes. Each ewe was anesthetized at para-vertebral region with the injection of 20 ml Prilocine 2%. Following left transverse abdominal incision, a transverse incision was made on the uterus and lambs were delivered. In the first group, uterine incision line was left open. In the second group, uterine incision line was sutured with no. 1 Chromic catgut by Schimiden technique. In both groups, all layers of abdominal wall except skin were sutured as en-bloc with VicrylA no. 2, by continuous suture technique. Skin was sutured with no. 00 silk interrupted sutures. The ewes were slaughtered four months after cesarean section. A coworker was asked to open the abdominal cavities, and score the intra-abdominal adhesions. Tissues taken from incision line of each uterus were fixed in 10% neutral buffered-formalin and were embedded in paraffin-block. Sections were cut and stained with hematoxylin-eosin. A pathologist, who knew nothing about the study, evaluated all sections, and reported the findings. Student’s t test was used for comparison of mean ewe age, gestational age, and mean operation time of the two groups. Z test was used for comparing the ratio of the two groups by means of histopathological findings. Results. No cervical dilatation and delivery of the placenta were seen during the four week follow up period. The average operating time was significantly less for the non-closure group (48.07∫3.83 minutes) than for the closure group (62.53∫6.57 minutes; pΩ0.001). The ranges of myometrial necrosis (100% versus 13.3%; pΩ0.001) and endometriosis (53.3% versus 00.0%; pΩ0.001) were significantly higher for closure group than for non-closure group. Conclusion. It was found that non-closure layers of the uterus along low transverse cesarean incision proves to have no adverse effect on immediate and late postoperative period in ewes. Our data showed that non-closure of all layers of the uterus results in significantly less muscular necrosis and endometriosis than closure group. We suggest that lower uterine incision can be left unclosed or, at least, simple closure can be preferable instead of vigorous locking technique. Key words: cesarean incision; closure; non-closure; sheep Submitted 18 March, 1999 Accepted 20 January, 2000

Cesarean section is defined as delivery of the fetus through incision in the abdominal wall (laparotomy) and the uterine wall (hysterotomy) (1, 2). Cesarean section is the most widespread surgical procedure in the United States (3, 4). Many reports have been written about its increasing use and the

reasons for cesarean delivery. However, there is little information relating to optimum operative technique for this method of delivery (5). Theoretically, in one-layer closure, tissue damage and introduction of foreign materials are less, required operation time is shorter, and achievement of C Acta Obstet Gynecol Scand 79 (2000)

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homostasis is more effective than two layer closure. Hauth et al. (5) recommended a one-layer closure when its use is anatomically feasible. Adhesion formation is related to suture reactivity, tissue devascularization, ischemia, and infection (6–9), and it has been proposed that routine closure of the peritoneum should be reexamined (7). Fibrinolytic and microscopic cellular studies in animals have demonstrated that the broad peritoneal reparative process is different from that of the edge-to-edge skin scatrization (10, 11). After 48– 72 hours, the entire surface is re-mesothelialized without re-approximation with suture material (12, 13). The aim of this experimental study was designed to investigate whether the non-closure of all layers of the uterus during low transverse cesarean section would result in healing and have advantage on closure. For this purpose ewes with gestational age of 150 (144–157) days, two horns and one cervix type uterus, and Syndesmochorial type placenta (14), were used.

For cervical dilatation or delivery of the placenta the animals were followed up during next four weeks. The ewes were slaughtered four months after cesarean section. A coworker who had no information about detail of the study was asked to open the abdominal cavities, and score the intra-abdominal adhesions according to the guidelines shown in Table I. Tissues taken from incision line of each uterus by our assistant were fixed in 10% neutral bufferedformalin prior to routine processing and were embedded in paraffin-block. Sections were cut and stained with hematoxylin-eosin. A pathologist, who knew nothing about of the study, evaluated all sections, and reported the findings. Student’s t test was used for comparison of mean ewe age, gestational age and mean operation time of the two groups. A confidence interval (95%) was constructed for differences between two means for mentioned groups. Z test was used to compare the ratio of two groups by means of histopathological findings.

Material and methods

Results

This prospective experimental study received institutional ethic committee approval. Thirty pregnant ewes were randomly divided into two groups (First group: non-closure, second group: closure). Each group included 15 ewes. Left side abdomen of each ewe was shaved and prepared with povidone iodine. The drapes, instruments and operating staff were all sterile. Each ewe was anesthetized at paravertebral region with the injection of 20 ml Prilocine 2% (CitanestA/Eczacıbas¸ı, Turkey). Following left transverse abdominal incision, a 7–8 cm transverse incision was performed on the uterus at 2–3 cm distance from cervix and lambs were delivered. In the first group, uterine incision line was left open. Because there was no significant bleeding on incision line, nothing was done for hemostasis. In the second group, the uterine incision line was sutured with no. 1 Chromic catgut by Schimiden technique. Removal of placentas failed in both groups due to Sydesmochorial type of placenta. Soon after the delivery of lambs, one dose of Oxytocin 5 IU (Synpitan forteA/Deva, Turkey) was administered intramuscularly in both groups. For prophylaxy a combination of 232 mg Streptomycin and 226.000 IU Penicillin G (VetimisinA/Vetas¸, Turkey) was administered to the ewes. In both groups, all layers of abdominal wall except skin were sutured as en-bloc with VicrylA no. 2, Ethicon, Nordersdet by continuous suture technique. Skin was sutured with no. 00 silk interrupted sutures. Administration of prophylactic antibiotic continued for ten days in both groups.

No cervical dilatation and delivery of the placenta were seen during the four week follow up period. In the early and late postoperative time, there was no mortality or morbidity. The mean ewe age, the mean gestational age, and the mean operative time of each two groups are shown in Table II. While the comparison of the two groups according to the mean age and the mean gestational age was not statistically significant (p⬎0.05), the difference be-

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Table I. Adhesion scores Score

Criterion

0 1 2 3

No macroscopic adhesions observed One filmy macroscopic fibrin adhesion Multiple macroscopic filmy fibrous adhesions One dense macroscopic fibrous adhesion with or without additional macroscopic filmy adhesion Multiple dense macroscopic fibrous adhesions with or without additional filmy adhesion

No adhesion Mild Moderate Severe

4 More severe

Table II. The age, gestational age and operation time of the two groups Closure group (nΩ15)

Age (years) Gestational age (days) Operation time (min.)

Non-closure group (nΩ15)

Mean

∫s.d.

Mean

∫s.d.

p

4.27 123.70 62.53

1.39 16.80 6.57

5.20 116.07 48.07

1.52 7.47 3.83

0.09 0.12 0.001

Non-closure uterine incision

Fig. 1. Adhesion in one ewe of the uterine closure group. Arrow heads: Dense adhesion between uterine horns. Thin arrows: Fibrous adhesions between the uterus and abdominal wall.

tween the two groups by means of operating time was statistically significant (pΩ0.001). Spontaneous healing of the uterine incision sites both in closure and non-closure groups was observed. In the non-closure group, no adhesion formation in the abdominal cavity and uterine incision line was observed. However, in the closure group, one ewe had stage 2 adhesion between uterine incision line and right abdominal wall (Fig. 1). The rate of incidence of myometrial necrosis stained as homogenous eosinophylic, and endometriosis in the presence of endometrial glands, which have single layers of cubic epithelial cells in the depth of the myometrium, far from endometrium along the incision line, were significantly higher in the closure group than the non-closure group (Table III), (p⬍0.05). The histopathological findings of incision line of one animal in the non-closure group and one animal in the closure group were shown in Fig. 2A and 2B, 2C, respectively. Discussion

Cesarean section is the most widespread surgical procedure in the United States (3, 4). Many reports

Table III. The comparison of histopathologic findings of incision line in closure and non-closure groups

Muscular necrosis Endometriosis Fibrosis

Closure group (nΩ15)

Non-closure group (nΩ15)

n (%)

n (%)

p

15 (100) 8 (53.3) 3 (20.0)

2 (13.3) 0 (0.0) 0 (0.0)

0.001 0.001 0.20

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have been addressed to its increasing incidence and indication for cesarean delivery. However, there is little information relating to the optimum operative technique for this method of delivery (5). In 1926 Kerr (15) described the transverse lower uterine segment incision and recommended a two-layer closure. In the fifteenth edition of Williams Obstetrics Pritchard and MacDonald (16) recommended that the first layer be running and locked and that ‘when the lower segment is thin, satisfactory approximation of the cut edge can usually be obtained with one layer of suture. If approximation is not satisfactory after a single-layer continuous closure then another layer may be placed’ (16). We recommend that non-closure of all the layers of uterus can be resorted if lower uterine segment is sufficiently thinned and widened. The amount of adhesion formation has been correlated with the presence and quantity of suture material (17). Suture of low caliber, as is commonly used in conservative or re-constructive surgery, should be less frequently associated with adhesion induction by reducing the development of tension and, therefore, ischemia along the lines of incision (7, 8). We assumed that there should be no reason not to apply the same principles for muscular layer suture. Pritchard and MacDonald (16) suggested a one-layer closure could be easily accomplished. Our experimental study has proved the benefits of this non-closure technique including less required operation time, less occurrence of myometrial necrosis and endometriosis, compared to a one-layer closure. The parietal and visceral peritoneal defects made by abdominal operations healed spontaneously when left un-sutured (18, 19). We suggest that muscular non-closure can be healed spontaneously by the above mentioned spontaneous healing mechanism, together with the closure of the wound edges in incision line during uterine involution. Ellis (19) considered that adhesions were formed at ischemic areas. Boys (20) and many surgeons believe that, by minimizing mechanical damage to intra-abdominal tissues during the course of operations, the incidence of development of adhesion is reduced (18). Re-approximation of peritoneal edges, even with suture considered to be minimally reactive, resulted in increased tissue necrosis and foreign body tissue reactions that may slow the healing (6, 8, 19). In our study, muscular necrosis seen in closure group might be caused by ischemia. It should be noted that placenta was left inside due to its Syndesmochorial type and the uterus line was faced down when the ewe got up on its feet. Non-removal of the placentas was accepted as a disadvantage, leading to high morbidity and mortality. We obtained similar results in another study, performed in dogs C Acta Obstet Gynecol Scand 79 (2000)

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Fig. 2. A. From above to below; Endometrium, endo-myometrial junction and myometrium at the healed incision line of uterus were normally seen in one ewe of non-closure group (hematoxylin-eosin stain, original magnification, ¿10). B. Endometrial gland and hemosiderin-laden macrophages in connective tissue between disrupted muscular fibers near the serous vessels were seen in the uterus of one ewe in closure group (hematoxylin-eosin stain, original magnification, ¿50). C. The fibrosis (F) (fibroblast proliferation together with hyaline and connective tissue), and necrosis (N) of the healed incision line were seen underlining the endometrial gland and hemosiderine laden-macrophages in the uterus of one ewe in the closure group (hematoxylin-eosin stain, original magnification ¿50).

with an endotheliochorial type of placenta that could be removed (21). In spite of all these disadvantages compared to women, the applied method proved to be successful for the ewes. C Acta Obstet Gynecol Scand 79 (2000)

As a result, uterus is not similar to intestine, stomach or bladder. Its content does not cause peritonitis. Postpartum bleeding is physiologically controlled by constriction of interlacing myo-

Non-closure uterine incision metrial fibers that surround the blood vessels supplying the placental implantation site. Within 48– 72 hours after injury, the entire surface of visceral and parietal peritoneum is re-mesothelialized without re-approximation with suture material (18, 19). In our opinion lower transverse uterine incision can be left unclosed, or at least, simple closure can be prefer instead of conventional vigorous locking suture technique. References 1. Cunningham FG, MacDonald PC, Gant NF. Cesarean section and cesarean hysterectomy. In: Cunningham FG, MacDonald PC, Gant NF, eds. Williams Obstetrics. 19th ed. Norwalk, Connecticut: Appleton & Lange, 1993; 591–613. 2. Cunningham FG, MacDonald PC, Gant NF. Cesarean section and cesarean hysterectomy. In: Cunningham FG, MacDonald PC, Gant NF, eds. Williams Obstetrics. 18th ed. Norwalk, Connecticut: Appleton & Lange, 1989; 451–72. 3. Hibbard LT. Cesarean section and other surgical procedures. In: Gabbe SG, Niebyl JR, Simpson JL, eds. Obstetrics: Normal and problem pregnancies. New York: Churchill Livingstone, 1986: 522–3. 4. Taffel SM, Placek PJ, Moien M, Kosary CL. 1989 U.S. cesarean section rate steadies: Vaginal birth after cesarean rate rises to nearly one in five. Birth 1991; 18: 73–7. 5. Hauth JC, Owen J, Davis RO. Transverse uterine incision closure: one versus two layers. Am J Obstet Gynecol 1992; 167: 1108–11. 6. Elkins TE, Stovall TG, Warren J, Ling FW, Meyer NL. A histologic evaluation of peritoneal injury and repair: Implication for adhesion formation. Obstet Gynecol 1987; 70: 225–8. 7. Holtz G. Adhesion induction by suture of varying tissue reactivity and caliber. Int J Fertil 1982; 27: 134–5. 8. Neff MR, Holtz GL, Betsill WL. Adhesion formation and histologic reaction with polydiaxnone and polyglactin suture. Am J Obstet Gynecol 1985; 151: 20–1. 9. O’Brien WF, Collins E, Knuppel RA, Spellacy WA. Peritoneal closure or non-closure at cesarean. Obstet Gynecol 1991; 77: 293–7.

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10. Porter JM, McGregor FH, Mullen DC, Silver D. Fibrinolytic activity of mesothelial surfaces. Surg Forum 1969; 20: 80–2. 11. Raftery AT. Effect of peritoneal trauma on peritoneal fibrinolytic activity and intraperitoneal adhesion formation. Eur Surg Res 1981; 13: 397–401. 12. Hubbard TB, Khan MZ, Carag VR, Abbites VE, Hricko GM. The pathology of peritoneal repair: Its relation to the formation of adhesions. Ann Surg 1967; 165: 908–16. 13. Robbins GF, Brunchwig A, Foote FW. Deperitonealization: Clinical and experimental observations. Ann Surg 1949; 130: 466–72. 14. Küplülü T¸. Placentation and pregnancy process. In: Alac¸am E, ed. Theriogenologi Nural matbaacılık, A.S¸: Ankara, 1990: 97–107. 15. Kerr JMM. The techniques of cesarean section, with special reference to the lower uterine segment incision. Am J Obstet Gynecol 1926; 12: 729–34. 16. Pritchard JA, MacDonald PC. Cesarean section and cesarean hysterectomy. In: Pritchard JA, MacDonald PC, eds. Williams Obstetrics. 15th ed. New York: Appleton-Century-Crofts, 1976: 903–23. 17. Luciano AA, Hauser KS, Benda J. Evaluation of commonly used adjuvants in the prevention of postoperative adhesions. Am J Obstet Gynecol 1983; 146: 88–92. 18. Conolly WB, Stephens FO. Factors influencing the incidence of intraperitoneal adhesion: An experimental study. Surgery 1968; 63: 976–9. 19. Ellis H. The etiology of postoperative abdominal adhesion: An experimental study. Br J Surg 1962; 10: 50–7. 20. Boys F. Prophylaxis of peritoneal adhesion: Review of literature. Surgery 1942; 11: 118–21. 21. Gül A, Kotan C ¸ , Ugˇras¸ S, Alan M, Gül T. Transverse uterine incision non-closure versus closure: an experimental study in dogs. Eur J Obstet Gynecol Reprod Biol 1999; 88(1): 95–9.

Address for correspondence: Assistant Professor Abdülaziz Gu¨l, M.D. Department of Obstetrics and Gynecology Faculty of Medicine Yüzüncü Yıl University 65200, Van, Turkey

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