4
AJOG REVIEWS Nonclosure of peritoneum: A reappraisal Togas Tulandi, MD, and Dania Al-Jaroudi, MD Montreal, Quebec, Canada In our specialty, the practice of closing or not closing the peritoneum is still being debated. Our purpose was to review the literature on the subject, to evaluate the advantages and disadvantages of the procedure, and to provide clinical opinions. Closure of the peritoneum either parietal or visceral peritoneum is unnecessary, it is associated with a slightly longer operating time and more postoperative pain, and there are some suggestions that it might cause more adhesion formation. There are more advantages than disadvantages to not closing the peritoneum. We encourage clinicians not to close both parietal and visceral peritoneum. (Am J Obstet Gynecol 2003;189:609-12.) Key words: Peritoneal closure, peritoneal nonclosure, adhesion, bowel obstruction In a recent international meeting in the United States, we were surprised to learn that some gynecologists still consider closing the peritoneum to be a necessity and to fail to do so is a poor surgical technique. They stated that younger gynecologists do not respect the traditional technique of abdominal closure, which includes closure of both visceral and parietal peritoneum. These gy- necologists argued that peritoneal closure restores the normal anatomy, closes the peritoneal defect, reduces the risks of infection and herniation, and decreases adhesion formation. We hereby re-examine the current evidence whether visceral or parietal peritoneum should or should not be closed. Peritoneal healing in an animal model The peritoneum is the serous membrane that covers the abdominal wall (parietal peritoneum) and the viscera (visceral peritoneum). As early as 1919, it was noted that, unlike the healing of a skin defect that gradually heals from the wound edges, the peritoneal defect restores simultaneously by regeneration. 1 It heals rapidly, and the duration of repair is independent on the size of the peritoneal defect. 2 Most animal studies compared closure and non- closure of the parietal peritoneum. 3-5 In a rabbit model, peritoneal healing occurred in 5 days; however, when the peritoneum was sutured, it occurred in 2 to 3 weeks. The presence of sutures promotes intense inflammatory foreign body reaction and tissue necrosis that might predispose to adhesion formation. 6 Indeed, several animal studies have demonstrated that the closure of the parietal peritoneum, either by sutures or staples, is associated with more adhesion formation than leaving it open to heal by secondary intention. 3-6 For example, in a horse model, the closure of the parietal peritoneum is associated with a 50% adhesion rate. This was higher than the rate without peritoneal closure (27%). 3 Other investigators reported similar findings. 7 It appears that leaving the peritoneum to heal by secondary intention does not predispose to wound dehiscence or incisional hernia and is associated with less adhesion formation. 8,9 What we can learn from general surgery Our colleagues in general surgery have long realized that the closure of parietal peritoneum is unnecessary and that they have abandoned this practice. 8,10-12 Parietal peritoneum. In 1977, Ellis and Heddle 8 first reported the results of a randomized study that compared closure and nonclosure of parietal peritoneum with a vertical laparotomy incision. They found no difference in the incidence of wound dehiscence or hernia between the closure (2.5% and 4.3%, respectively) and the nonclosure group (3.0% and 4.3%, respectively). They concluded that peritoneal closure plays no role in the healing of the laparotomy wound. Two decades later, Dorfman et al 13 randomly assigned 129 patients who underwent cholecystectomy with Kocher From the Department of Obstetrics and Gynecology, McGill University. Received for publication November 19, 2002; revised January 31, 2003; accepted February 24, 2003. Reprint requests: Togas Tulandi, MD, Department of Obstetrics and Gynecology, McGill University, 687 Pine Ave W, Montreal, Quebec, Canada, H3A 1A1. E-mail: [email protected] Ó 2003, Mosby, Inc. All rights reserved. 0002-9378/2003 $30.00 + 0 doi:10.1067/S0002-9378(03)00299-0 609

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AJOG REVIEWS

Nonclosure of peritoneum: A reappraisal

Togas Tulandi, MD, and Dania Al-Jaroudi, MD

Montreal, Quebec, Canada

In our specialty, the practice of closing or not closing the peritoneum is still being debated. Our purpose was to

review the literature on the subject, to evaluate the advantages and disadvantages of the procedure, and to

provide clinical opinions. Closure of the peritoneum either parietal or visceral peritoneum is unnecessary, it is

associated with a slightly longer operating time and more postoperative pain, and there are some suggestions

that it might cause more adhesion formation. There are more advantages than disadvantages to not closing

the peritoneum. We encourage clinicians not to close both parietal and visceral peritoneum. (Am J Obstet

Gynecol 2003;189:609-12.)

Key words: Peritoneal closure, peritoneal nonclosure, adhesion, bowel obstruction

In a recent international meeting in the United States,

we were surprised to learn that some gynecologists still

consider closing the peritoneum to be a necessity and to

fail to do so is a poor surgical technique. They stated that

younger gynecologists do not respect the traditional

technique of abdominal closure, which includes closure

of both visceral and parietal peritoneum. These gy-

necologists argued that peritoneal closure restores the

normal anatomy, closes the peritoneal defect, reduces the

risks of infection and herniation, and decreases adhesion

formation. We hereby re-examine the current evidence

whether visceral or parietal peritoneum should or should

not be closed.

Peritoneal healing in an animal model

The peritoneum is the serous membrane that covers

the abdominal wall (parietal peritoneum) and the viscera

(visceral peritoneum). As early as 1919, it was noted that,

unlike the healing of a skin defect that gradually heals

from the wound edges, the peritoneal defect restores

simultaneously by regeneration.1 It heals rapidly, and the

duration of repair is independent on the size of the

peritoneal defect.2

Most animal studies compared closure and non-

closure of the parietal peritoneum.3-5 In a rabbit model,

From the Department of Obstetrics and Gynecology, McGill University.Received for publication November 19, 2002; revised January 31, 2003;accepted February 24, 2003.Reprint requests: Togas Tulandi, MD, Department of Obstetrics andGynecology, McGill University, 687 Pine Ave W, Montreal, Quebec,Canada, H3A 1A1. E-mail: [email protected]� 2003, Mosby, Inc. All rights reserved.0002-9378/2003 $30.00 + 0doi:10.1067/S0002-9378(03)00299-0

peritoneal healing occurred in 5 days; however, when

the peritoneum was sutured, it occurred in 2 to 3 weeks.

The presence of sutures promotes intense inflammatory

foreign body reaction and tissue necrosis that might

predispose to adhesion formation.6 Indeed, several

animal studies have demonstrated that the closure of

the parietal peritoneum, either by sutures or staples, is

associated with more adhesion formation than leaving it

open to heal by secondary intention.3-6 For example, in

a horse model, the closure of the parietal peritoneum is

associated with a 50% adhesion rate. This was higher

than the rate without peritoneal closure (27%).3

Other investigators reported similar findings.7 It

appears that leaving the peritoneum to heal by secondary

intention does not predispose to wound dehiscence or

incisional hernia and is associated with less adhesion

formation.8,9

What we can learn from general surgery

Our colleagues in general surgery have long realized

that the closure of parietal peritoneum is unnecessary and

that they have abandoned this practice.8,10-12

Parietal peritoneum. In 1977, Ellis and Heddle8 first

reported the results of a randomized study that compared

closure and nonclosure of parietal peritoneum with

a vertical laparotomy incision. They found no difference

in the incidence of wound dehiscence or hernia between

the closure (2.5% and 4.3%, respectively) and the

nonclosure group (3.0% and 4.3%, respectively). They

concluded that peritoneal closure plays no role in the

healing of the laparotomy wound.

Two decades later, Dorfman et al13 randomly assigned

129 patients who underwent cholecystectomy with Kocher

609

Page 2: peritoneium

August 2003Am J Obstet Gynecol

610 Tulandi and Al-Jaroudi

incision into closure and nonclosure of parietal perito-

neum. They also found that there were no differences in

the overall wound complications, wound dehiscence, and

incisional hernia in the two groups of patients. Similar

findings were reported in another randomized trial after

a laparotomy with lateral paramedian incision12 and with

vertical incision.11

Visceral peritoneum. An observational study in 1952

revealed that, of 18 patients who had undergone

reperitonealization after abdominoperineal resection, 4

patients had intestinal obstruction.14 No bowel obstruc-

tion was found in those patients with no closure of the

visceral peritoneum. It seems that the bowel obstruction

was due to incarceration of the intestine in the newly

reconstructed pelvic floor.15

Gynecologic operations

Parietal peritoneum. In 1988, by means of a second-

look laparoscopy, we first reported that there was no

difference in the adhesion formation after laparotomy

with peritoneal closure (22.2%) and without peritoneal

closure (16%).16 We did not encounter wound de-

hiscence or hernia in either closure or nonclosure groups.

The incidence of wound infection was 3.6% and 2.4%,

respectively. In a nonrandomized study, Palazzetti et al17

reported that the incidence of ileus after abdominal

hysterectomy was significantly higher in women with

peritoneal closure (40%) than in women without perito-

neal closure (21%, P = .003).

Visceral peritoneum. Lipscomb et al18 compared the

clinical outcome of 106 women who underwent vaginal

hysterectomy with or without peritoneal closure. There

was no difference in postoperative complications between

the two groups of patients. However, the authors

acknowledged that the power of their study was only 20%.

In women with ovarian cancer, the closure of pelvic

and periaortic peritoneum is associated with more

adhesion formation than in women with no closure.19,20

There was also no difference in the duration of

postoperative ileus and in the hospital stay between the

closure group (3.6 and 8.6 days, respectively) and the

nonclosure group (3.8 and 9.3 days, respectively).19 In

1999, we evaluated 262 women who were admitted to the

hospital for small bowel obstruction.21 We found that

the most common cause of small bowel obstruction was

intra-abdominal adhesions. Furthermore, adhesions that

involved the site of closure of the pelvic peritoneum

were responsible for bowel obstruction in 85% of cases,

with adhesions to the anterior abdominal wall occurring

in another 15% of cases. This is in agreement with the

findings after closure of visceral peritoneum during

abdominoperineal resection.15

Parietal and visceral peritoneum. Franchi et al22

randomly assigned 120 patients who underwent radical

hysterectomy and node dissection to closure and non-

closure of both parietal and visceral peritoneum. They

found that the amount of drainage in the nonclosure

group was less than in the closure group (340 mL and 740

mL, respectively; P < .005). They attributed it to the

escape of lymph fluid into the abdominal cavity in the

nonclosure group; the fluid was then absorbed. No

difference was found in the operating time and in the

incidence of lymphocyst formation, infection, and bowel

obstruction between the two groups.

In another randomized trial, Gupta et al23 studied 144

patients who underwent a hysterectomy with and without

peritoneal closure. The postoperative pain between the

two groups was similar. The mean estimated blood loss in

the closure group was more than in the nonclosure group

(258 and 213 mL, P = .03), and the mean operating time

in the closure group was 10minutes longer (49.1 and 39.1

minutes, respectively, P < .001).

These findings suggest that, even among oncologic

patients, the closing of the peritoneum is unnecessary and

might increase adhesion formation. The results of

randomized trials on peritoneal closure versus nonclosure

among women who underwent gynecologic operations

and cesarean deliveries are depicted in Table I.*

Cesarean delivery

There have been many studies that compare the effects

of nonclosing the peritoneum at the time of cesarean

delivery. Most investigators compared the closing and

nonclosing of both parietal and visceral peritoneum; the

peritoneal suturing was done with polyglactin.

Parietal peritoneum. Closure of the parietal perito-

neum was compared with peritoneal nonclosure at the

time of cesarean delivery through a Pfannenstiel incision

in 248 women.24 The mean duration of surgery in the

nonclosure group (48.1 ± 1.2 minutes) was shorter than

in the closuregroup(53.2 ± 1.4minutes,P < .005).There

was no difference in the amount of blood loss, ileus, and

dehiscence between the two groups. The mean hospital

stay was 4.5 days in the closure group and 4.8 days in the

nonclosure group; the incidence of wound infection was

1.0% and 0.9%, respectively. In a small series, Hojberg

et al25 reported that the use of postoperative analgesics

was lower if the parietal peritoneum was left open. The

duration of hospital stay was 7.1 ± 0.4 days in the closure

group and 6.3 ± 0.3 days in the nonclosure group. Febrile

morbidity was encountered only in two patients in the

closure group.

Visceral peritoneum. Nagele et al26 conducted the

largest randomized trial that compared closure and

nonclosure of visceral peritoneum among 549 women.

The operating time was significantly longer in the

closure group (56.9 ± 17.9 minutes) than in the non-

*References 8,11,12,18,19,22,23.

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Volume 189, Number 2Am J Obstet Gynecol

Tulandi and Al-Jaroudi 611

Table II. Randomized trials of closure or nonclosure of parietal and visceral peritoneum at the time of cesarean delivery

ParameterHull andVarner27

Irionet al28

Ohelet al29

Grundsellet al30

Rafiqueet al31

Hoet al32

C NC C NC C NC C NC C NC C NCPatients (No.) 59 54 143 137 100 100 182 179 50 50 94 96Mean operating time (min) 57.9 50.0 53.2 47.3 44 32 41.3 33.4 38.8 32.8 40.4 38.8Mean hospital stay (d) 4.2 4.0 6.8 6.5 NA NA 6.4 5.3 NA NA 4.4 4.6Febrile morbidity (%) 13.5 16.6 8 8 10 10 19.2 7.8 NA NA NA NAWound infection (%) 8.5 5.6 NA NA 3.0 4.0 3.2 2.2 2.0 2.0 NA NA

C, Closure; NC, nonclosure; NA, not applicable.

Table I. Randomized trials of peritoneal closure or nonclosure in general surgery and gynecology

AuthorsEllis andHeddle8 Gilbert et al12 Hugh et al11 Kadanah et al19 Lipscomb et al18 Franchi et al22 Gupta e et al23

Procedure/incision

Vertical,median, orparamedianincision forgeneral surgicalcases

Lateralparamedianincision forgeneralsurgicalcases

Midlineincision forgeneralsurgicalcases

Pelvic andparaaorticlymphad-enectomy forovariancancer

Vaginalhysterectomy

Radicalhysterectomyand nodedissection

Hysterectomy,transverse,or leftparamedianincisions

Peritoneum Parietal Parietal Parietal Visceral Visceral Parietal andvisceral

Parietal andvisceral

C vs NC C NC C NC C NC C NC C NC C NC C NCPatients 162 164 77 75 87 92 50 52 49 57 59 61 76 68Febrile (%)morbidity

8.0 12.2 NA NA NA NA 28.0 26.9 NA NA 3.4 1.6 16.2 15.2

Woundinfection (%)

NA NA 9.1 12.0 2.3 3.3 8.0 5.8 2.0 1.8 10.2 18.0 6.8 0

C, Closure; NC, nonclosure.

closure group (50.6 ± 16.8 minutes). The incidence of

febrile morbidity was significantly higher when the

peritoneum was closed (15.7% vs 8.4% in the non-

closure group, P = .009). The incidence of cystitis was

also higher in the closure group (7.7% vs 3.1% in the

nonclosure group, P = .01). The incidence of wound

infection and endometritis was 4.9% and 5.1% in the

closure group and 1.9% and 3.9% in the nonclosure

group. Patients in the closure group also required more

postoperative narcotics (P < .001). Hospital stay was

significantly longer in the closure group (7.9 ± 1.8 days

vs 7.2 ± 1.6 days, P < .001). The authors concluded that

the routine closure of the visceral peritoneum should be

abandoned in women who undergo cesarean delivery.

Parietal and visceral peritoneum. Table II shows the

results of randomized trials that compared closure and

nonclosure of peritoneum at the time of cesarean delivery

that involved 1284 women.27-32 The results show that

there are no disadvantages of not closing the peritoneum.

Hull and Varner27 found that there was no difference in

the postoperative morbidity between the two groups of

patients. The number of oral analgesics and the operating

time, however, were significantly higher in the closure

group. Among 361 patients, Grundsell et al30 found that

the incidence of febrile morbidity and wound infection

was lower among the women with closure of visceral and

parietal peritoneum. The operating time in the non-

closure group was shorter (P < .01) and the average

hospital stay was 1 day less (P < .01).

In another study, postoperative pain was found to be

less if the visceral and parietal peritoneum were not

sutured.31 Irion et al28 found that the return of bowel

function occurred faster in patients whose peritoneum

was left open. Adhesion formation at repeat cesarean

delivery has been evaluated also.33,34 Confirming previous

clinical and animal studies, the results suggest that

peritoneal nonclosure does not promote, and might even

decrease, adhesion formation.

Clearly, these studies demonstrate that closing the

peritoneum is not only unnecessary but also associated

with a longer operating time and more postoperative

pain. In a systematic review, Wilkinson and Enkin35

concluded that there is a consistent trend for improved

immediate postoperative outcome if the peritoneum is

not closed.

Comment

Evidence of the safety of not closing the peritoneum is

overwhelming. Most studies show that this practice not

only reduces the operating time but also that the

postoperative recovery is similar or even better than in

those with peritoneal closure. This is applicable to both

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August 2003Am J Obstet Gynecol

612 Tulandi and Al-Jaroudi

parietal and visceral peritoneumand to both cesarean and

gynecological operations. The fewer requirements of

analgesics and the shorter hospital stay are economical.

We may ask why nonclosure of the peritoneum has not

gainedmuch general acceptance among the obstetricians

and gynecologists.36 The answers might be that it is

difficult to change the traditional dogma of peritoneal

closure or that this topic has not received sufficient

attention from our colleagues.

In our specialty, there have been more randomized

trials on peritoneal nonclosure than in general surgery.

The results show that closing either the parietal or visceral

peritoneum is unnecessary and is associated with a slightly

longer operating time andmore postoperative pain; there

is a suggestion that it might cause more adhesion

formation. In a recent article, Ellis37 acknowledged that

there have been increasing medicolegal claims that arise

from adhesion-related complications. He stated that

‘‘peritoneal defects and the pelvic floor should be left

open since they rapidly reperitonealized.’’

We encourage obstetricians and gynecologists to omit

peritoneal closure. As shown in the randomized trials,

there are more advantages than disadvantages of not

closing the peritoneum.

REFERENCES

1. Hertzler AR. The peritoneum. Vol 1. St. Louis: Mosby; 1919.2. Ellis H, Harrison W, Hugh TB. The healing of peritoneum under

normal and pathological conditions. Br J Surg 1965;52:471-6.3. Swanwick RA, Stockdale PH, Milne FJ. Healing of parietal perito-

neum in the horse. Br Vet J 1963;129:29-35.4. McDonald MN, Elkins TE, Wortham GF, Stovall TG, Ling FW,

McNeeley SG, Jr. Adhesion formation and prevention after perito-neal injury and repair in the rabbit. J Reprod Med 1988;33:436-9.

5. Ling FW, Stovall TG, Meyer NL, Elkins TE, Muram D. Adhesion for-mation associated with the use of absorbable staples in comparison toother types of peritoneal injury. Int J Gynaecol Obstet 1989;30:361-6.

6. Elkins TE, Stovall TG, Warren J, Ling FW, Meyer NL. A histologicalevaluation of peritoneal injury and repair: implications for adhesionformation. Obstet Gynecol 1987;70:225-8.

7. Kyzer S, Bayer I, Turani H, Chaimoff C. The influence of peritonealclosure on formation of intraperitoneal adhesions: an experimentalstudy. Int J Tissue React 1986;8:355-9.

8. Ellis H, Heddle R. Does the peritoneum need to be closed atlaparotomy? Br J Surg 1977;64:733-7.

9. Kapur B, Danewar A, Chopra P. Evaluation of peritoneal closure atlaparotomy. Am J Surg 1979;137:650-2.

10. McFadden PM, Peacock EE. Preperitoneal abdominal wound repair:incidence of dehiscence. Am J Surg 1983;145:213-4.

11. Hugh TB, Nankivell C, Meagher AP. Is closure of the peritoneal layernecessary in the repair of midline surgical abdominal wounds? WorldJ Surg 1990;14:231-3.

12. Gilbert JM, Ellis H, Foweraker S. Peritoneal closure after lateralparamedian incision. Br J Surg 1987;74:113-5.

13. Dorfman S, Rincon A, Short H. Cholecystectomy via Kocher incisionwithout peritoneal closure. Invest Clin 1997;38:3-7.

14. Trimpi HD, Bacon HE. Clinical and experimental study of denudedsurfaces in extensive surgery of the colon and rectum. Am J Surg1952;34:596-602.

15. Ulfelder H, Quinby WC Jr. Small bowel obstruction following com-bined abdominoperineal resection of the rectum. Surg 1951;30:174-7.

16. Tulandi T, Hum HS, Gelfand MM. Closure of laparotomy incisionswith or without peritoneal suturing and second-look laparoscopy. AmJ Obstet Gynecol 1988;158:536-7.

17. Palazzetti PL, Cipriano L, Pachi A. Is peritoneal closure necessaryafter abdominal hysterectomy? Int J Gynecol Obstet 2000;71:255-6.

18. Lipscomb GH, Ling FW, Stovall TG, Summitt RL Jr. Peritonealclosure at vaginal hysterectomy: a reassessment. Obstet Gynecol1996;87:40-3.

19. Kadanah S, Erten O, Kucukozkan T. Pelvic and periaortic peritonealclosure or non-closure at lymphadenectomy in ovarian cancer: effectson morbidity and adhesion formation. Eur J Surg Oncol 1996;22:282-5.

20. Than GN, Arany AA, Schunk E, Vizer M, Krommer KF. Closure ornon-closure of visceral peritoneums after abdominal hysterectomiesand Wertheim-Meigs radical abdominal hysterectomies. Acta ChirHung 1994;34:79-86.

21. Al-Took S, Platt R, Tulandi T. Adhesion-related small bowel obstruc-tion after gynecologic operations. Am J Obstet Gynecol 1999;180:313-5.

22. Franchi M, Ghezzi F, Zanaboni F, Scarabelli C, Beretta P, DonadelloN. Nonclosure of peritoneum at radical abdominal hysterectomy andpelvic node dissection: a randomized study. Obstet Gynecol1997;90:622-7.

23. Gupta JK, Dinas K, Khan KS. To peritonealize or not to peritonealize?A randomized trial at abdominal hysterectomy. Am J Obstet Gynecol1998;178:796-800.

24. Pietrantoni M, Parsons MT, O’Brien WF, Collins E, Knuppel RA,Spellacy WN. Peritoneal closure or non-closure at cesarean. ObstetGynecol 1991;77:293-6.

25. Hojberg KE, Aagard J, Laursen H, Diab L, Secher NJ. Closure versusnon-closure of peritoneum at cesarean section: evaluation of pain.Acta Obstet Gynecol Scand 1998;77:741-5.

26. Nagele F, Karas H, Spitzer D, Staudach A, Karasegh S, Beck A, et al.Closure or nonclosure of the visceral peritoneum at cesareandelivery. Am J Obstet Gynecol 1996;174:1366-70.

27. Hull DB, Varner MW. A randomized study of closure of theperitoneum at cesarean delivery. Obstet Gynecol 1991;77:818-21.

28. Irion O, Luzuy F, Beguin F. Nonclosure of the visceral and parietalperitoneum at cesarean section: a randomized controlled trial. Br JObstet Gynaecol 1996;103:690-4.

29. Ohel G, Younis JS, Lang N, Levit A. Double-layer closure of uterineincision with visceral and parietal peritoneal closure: are theyobligatory steps of routine cesarean sections? J Matern Fetal Med1996;5:366-9.

30. Grundsell HS, Rizk DE, Kumar RM. Randomized study of non-closure of peritoneum in lower segment cesarean section. ActaObstet Gynecol Scand 1998;77:110-5.

31. Rafique Z, Shibli KU, Russell IF, Lindow SW. A randomisedcontrolled trial of the closure or non-closure of peritoneum atcaesarean section: effect on postoperative pain. Br J Obstet Gynaecol2002;109:694-8.

32. Ho WP, NorAzlin MI, Patrick CFW, Nasri NM, Adeeb N. Peritonealclosure at caesarean section. Acta Obstet Gynecol Scand 1997;76:30-4.

33. Stark M, Chavkin Y, Kupfersztain C, Guedj P, Finkel AR. Evaluation ofcombinations of procedures in cesarean section. Int J Obstet Gynecol1995;48:273-6.

34. Joura EA, Nather A, Hohlagschwandtner M, Husslein P. Peritonealclosure and adhesions. Hum Reprod 2002;17:249-50.

35. Wilkinson CS, Enkin MW. Peritoneal non-closure at caesareansection (Cochrane Review). In: Cochrane Library, issue 3. Oxford:Update Software; 2002.

36. Duffy DM, diZerega GS. Is peritoneal closure necessary? ObstetGynecol Surv 1994;49:817-22.

37. Ellis H. Medicolegal consequences of postoperative intra-abdominaladhesions. J R Soc Med 2001;94:331-2.