ORIGINAL ARTICLE
Long-term Follow-up for Adhesive Small Bowel Obstruction After Open Versus Laparoscopic Surgery for Suspected Appendicitis Karolin Isaksson, MD,∗ Agneta Montgomery, MD, PhD,† Ann-Cathrin Moberg, MD, PhD,† Roland Andersson, MD, PhD,∗ and Bobby Tingstedt, MD, PhD∗
Objective: The aim of the present study was to compare the frequency of readmissions due to small bowel obstruction (SBO) after open versus laparoscopic surgery performed for suspected acute appendicitis. Background: Appendicitis is a common disease, with a lifetime risk of approximately 7%. Appendectomy is the treatment of choice for most patients. Postoperative adhesions are common after abdominal surgery, including appendectomy. Materials and Methods: Consecutive patients, 16 years or older, operated on because of suspected appendicitis at 2 university hospitals between 1992 and 2007 were included. The prime approach was open at one hospital and laparoscopic at the other hospital. Open and laparoscopic procedures were compared retrospectively, reviewing the patients’ charts until the middle of 2012. Hospitalization for SBO after index surgery was registered. Results: A total of 2333 patients in the open group and 2372 patients in the laparoscopic group were included. The frequency of hospitalization for SBO was low in both groups, although a difference between the groups was identified (1.0% in the open group and 0.4% in the laparoscopic group) (P = 0.015). Conclusions: Hospitalization due to SBO, between open and laparoscopic procedures, in patients operated on because of suspected appendicitis demonstrated a significant difference, favoring the laparoscopic approach. The frequency of SBO after the index surgery was, though, low in both groups. Keywords: adhesive, appendicitis, long term follow-up, open versus laparoscopic, small bowel obstruction (Ann Surg 2014;259:1173–1177)
A
ppendicitis is a common condition, with a calculated cumulated lifetime risk of 7% to 8%.1,2 Surgery is the treatment of choice for the majority of patients. The incidence of appendectomy is around 100 of 100,000 inhabitants per year in the Western world.3 Open appendectomy has been the criterion standard until the laparoscopic technique was introduced by Semm4 in early 1980s. Several studies have described advantages of using the laparoscopic technique, including diagnostic possibilities, faster recovery with shortened hospital stay, decreased postoperative pain, and a lower incidence of wound infections.5–7 Others have demonstrated disadvantages such as a possible higher risk of postoperative intraabdominal abscess formation,6,8,9 whereas others have not demonstrated any difference between open and laparoscopic procedures.10 From the ∗ Department of Surgery, Sk˚ane University Hospital, Lund, Sweden; and †Department of Surgery, Sk˚ane University Hospital, Malm¨o, Sweden. Disclosure: This study was partly supported by grants from Eric and Angelica Sparre Foundation, although the funding source had no influence on the study at all. None of the authors have any conflicts of interest. Reprints: Karolin Isaksson, MD, Department of Surgery, Sk˚ane University Hospital, S-221 85 Lund, Sweden. E-mail: [email protected]. C 2013 by Lippincott Williams & Wilkins Copyright ISSN: 0003-4932/13/25906-1173 DOI: 10.1097/SLA.0000000000000322
Annals of Surgery r Volume 259, Number 6, June 2014
A diagnostic laparoscopy is safe and offers the possibility to detect pathological conditions mimicking appendicitis, especially important in fertile women, and also rendering the option to leave a normal appendix in place.11 Postoperative adhesions are quite common, especially not only after surgery of the lower part of the abdomen such as gynecological and colorectal surgery but also after appendectomy. Late complications due to intra-abdominal adhesions include chronic abdominal pain, small bowel obstruction (SBO), and female infertility. These chronic conditions can result in a major impairment for the patient, a challenge to treat, and represent a major cost for society. In Sweden, costs related to admissions due to abdominal adhesions are estimated to about €40 million to €60 million per year.12 Abdominal adhesions are the most common cause of SBO requiring surgical intervention. The lifetime risk of postoperative bowel obstruction after abdominal surgery with a frequency of up to 25% after some procedures has been reported. The incidence of bowel obstruction after appendectomy has historically been reported to be between 0.7% and 10.7%.13–18 Type and grade of surgical trauma seem to play an important role in adhesion formation. There are documented advantages of laparoscopic procedures in general, as compared with open surgery, in reducing postoperative adhesion formation by minimizing the trauma to the peritoneal surface.19 The aim of this study was to determine the incidence of SBO after open and laparoscopic operations in patients with suspected appendicitis in a large cohort of adult patients subjected to a long-term follow-up.
PATIENTS AND MATERIALS Data from patients, 16 years or older, operated on for suspected appendicitis between 1992 until the end of 2007 at the University Hospitals in Lund and Malm¨o (since 2011 merged to form 1 university hospital: Sk˚ane University Hospital) were retrospectively collected. The hospitals are closely localized in the southern region of Sweden. During this time period, the preferred operation technique in Lund was the open approach whereas laparoscopic operation was the procedure of choice in Malm¨o. The open group (OG) consisted of all consecutive patients operated on by open technique in Lund, and the laparoscopic group (LG) consisted of all consecutive patients operated on in Malm¨o. The patients were identified by the ICD (International Classification of Diseases) codes. For open appendectomy, the codes 4510 (ICD-9 until 1996) and JEA 00 (ICD-10 after 1996) were used; for the laparoscopic operations, the codes 4511, 4042 (ICD-9), and JEA 01, JAH 01 (ICD-10) were used. The LG included 3 possible pathways for patients with clinically suspected appendicitis: an appendectomy completed laparoscopically, a conversion to open appendectomy, or a diagnostic/explorative laparoscopy leaving a macroscopically normal appendix in place. The curriculum was to perform an initial laparoscopy for diagnostic purposes. The appendix was left in place when diagnosed as macroscopically normal. When appendicitis was diagnosed at laparoscopy, the surgeons having an accreditation for www.annalsofsurgery.com | 1173
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Annals of Surgery r Volume 259, Number 6, June 2014
Isaksson et al
laparoscopic appendectomy went on with a laparoscopic procedure and converted in case of technical difficulties. The surgeons not having the accreditation for laparoscopic appendectomy converted to open appendectomy after the diagnostic laparoscopy. This strategy resulted in a high conversion rate, although the number of conversions diminished over time as the educational program proceeded. In the OG, an appendectomy was performed for all patients, including when finding macroscopically normal appendices. Patients were analyzed both on the intention-to-treat basis and per protocol. In the per protocol analysis, the converted operations in the LG were excluded to study the laparoscopic versus open technique per se.
Exclusion Criteria
• If the appendectomy was performed as a part in a more extensive surgical procedure (en passant, eg, colorectal resection) or when the operation was extended because of an advanced appendicitis (eg, ileocecal resection). • When the appendectomy was accompanied with another concurrent intra-abdominal surgical procedure (eg, oophorectomy, Meckel diverticulum). • In patients with carcinoma of the appendix (not carcinoids that did not lead to further surgical treatment). • In patients readmitted for SBO having information of conflicting surgery to the lower part of the abdomen, presence of adhesions at the primary operation, or a history of interfering disease (eg, Crohn disease or abdominal cancer). • Patients in the LG who were operated on by open surgery after the diagnostic laparoscopy (n = 42), due to an ongoing randomized study comparing open and laparoscopic surgery performed between March 2001 and July 2003.20 • Patients with incorrect operative code for the appendectomy surgery.
Protocol All individual charts were manually revised in both groups. The charts were reviewed from the date of index surgery for suspected appendicitis until June 30, 2012. An individual protocol was established for patients who were readmitted and hospitalized after the index operation because of symptoms of SBO. Definition of SBO was radiological findings indicating SBO or obvious findings of SBO in the patient on examination (information retrieved from the charts) such as distended abdomen, colicky pain, absence of flatus, and characteristic bowel sounds. Sex, age, previous abdominal surgery, date of readmission, surgical technique at index operation, and macroscopic appearance of the appendix (including the presence of perforation and abscess formation at the time of appendectomy) were registered. In the LG, registration for the performance of a diagnostic laparoscopy (leaving the appendix in place), a complete laparoscopic operation, or a conversion to open appendectomy was performed. The number of readmissions for each patient and whether the condition was handled conservatively or needed surgical intervention were noted.
Power Calculation and Statistical Analyses The hypothesis was that the incidence of patients having symptoms of SBO would be lower in the LG. The incidence of symptoms of SBO was assumed to be 1.2% after open appendectomy, based on previous studies. To prove a 50% reduction in the LG, a total of 1655 patients in each group were needed with a statistical power of 80% and a risk of 5% inaccuracy. To calculate for differences between the groups, the Fisher exact test, the χ 2 test, the independent t test, and the Wilcoxon rank-sum test were used. Pearson bivariate correlation and multivariate logistic regression analysis were used for calculation 1174 | www.annalsofsurgery.com
of risk factors for SBO. Statistical calculations were performed with SPSS version 19.0, IBM Corp., Armonk, NY, USA. A 2-sided P < 0.05 was considered statistically significant.
RESULTS A total of 4705 patients, 2333 in the OG and 2372 in the LG, were included. The excluded patients are shown in Figure 1. There were 994 female patients (43%) and 1339 male patients in the OG (P < 0.001) and 1250 female patients (53%) and 1122 male patients in the LG (P = 0.009). The difference in sex between the groups was statistically significant (P < 0.001). The mean age was 35 (SD = 16) years in the OG and 36 (SD = 16) years in the LG (P = 0.072). The mean follow-up time was 161 (SD = 53) months in the OG and 133 (SD = 49) months in the LG (P < 0.001). In the LG, the distribution of surgical intervention was 1401 laparoscopic appendectomies (59%), 595 converted to open appendectomy (25%), and 376 diagnostic laparoscopies (16%). A total of 34 patients were hospitalized for SBO, most likely related to the index surgery: 24 patients (1.0%) in the OG and 10 patients (0.4%) in the LG (P = 0.015). Readmissions are depicted in Table 1. Outcomes of SBO regarding patient factors are outlined in univariate and multivariate analyses in Table 2. Open appendectomy and older age are independent risk factors for SBO in the multivariate analysis. Altogether 7 patients in the OG and 2 patients in the LG had more than 1 readmission, resulting in a total number of readmissions of 39 in the OG and 14 in the LG. All patients, except one, in both groups had radiological findings and clinical symptoms. In both groups, approximately half of the patients who were readmitted, the SBO was treated surgically (P = 1.000) (Table 3, Fig. 2). The median time to first readmission for SBO was 314 (range, 3–2451) days in the OG and 330 (range, 12–2277) days in the LG (P = 0.691). One of the patients in the LG died postoperatively from respiratory complications after her second surgically treated SBO episode. There were no readmissions due to SBO related to the index operation in the patients being subjected only to a diagnostic laparoscopy. In the per protocol analysis where the converted patients in the LG were excluded, we found a significant difference in the incidence of readmission for SBO, in favor of the laparoscopic (0.3%) compared with the open technique (1.0%) (P = 0.009).
DISCUSSION We found a difference in the incidence of SBO after operation for suspected appendicitis on the intention-to-treat basis in our study favoring the laparoscopic approach. Open appendectomy and older age are independent risk factors for SBO. Results of previous studies comparing open and laparoscopic surgical procedures support the theory of less adhesion formation with the laparoscopic approach.19 To our knowledge, there is only one randomized clinical trial comparing adhesion formation between laparoscopy and laparotomy evaluated at second-look surgery.21 This study, published in 1991 (n = 73), shows significantly fewer adhesions within the operated site in the LG than in the open surgery group, although there was no significant difference for overall adhesion formation even if a trend was observed in favor of the LG. The possible superior role of laparoscopic surgery for acute appendicitis and subsequent SBO has not been clearly demonstrated in a cohort of adult patients. In a fairly recent review by Schn¨uriger et al,22 the laparoscopic technique was found to result in fewer adhesion-related readmissions than the open technique for several abdominal operations, although with the exception of appendectomies. The decreased incidence of SBO after laparoscopic appendectomy has been shown previously in pediatric studies. Tsao et al13 concluded that SBO is less common after laparoscopic appendectomy than after open appendectomy in children. The study C 2013 Lippincott Williams & Wilkins
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Annals of Surgery r Volume 259, Number 6, June 2014
Appendectomy and Small Bowel Obstruction
Study cohort n = 4954
Open group n = 2472
Lap. group n = 2482
Excluded n = 139
Excluded n = 110
Incorrect op code: 92 Incomplete/missing chart: 12 Extended surgery: 25 Cancer in appendix: 4 Other: 6
Incorrect op code: 10 Incomplete/missing chart: 21 Extended surgery: 25 Cancer in appendix: 8 Study: 42 Other: 4
Open group n = 2333
Final cohort n = 4705
FIGURE 1. Flowchart for inclusion. Lap. indicates laparoscopic; op, operative. TABLE 1. Readmitted Patients for SBO
Total No. Only late SBO (>30 d)
TABLE 3. Characteristics for Patients Readmitted for SBO
Open Group, n (%)
Laparoscopic Group, n (%)
P
24 (1.0) 16 (0.7)
10 (0.4) 7 (0.3)
0.016 0.061
TABLE 2. Analysis of Patient Factors on SBO Outcome Univariate Analyses Factors
P
Female sex Age above median Follow-up time above median Laparoscopic appendectomy
Odds Ratio
Multivariate Analyses P
Odds Ratio
0.606 1.25 (0.63–2.48) 0.022 2.31 (1.16–4.63) 0.017 2.33 (1.16–4.67) 0.086 1.87 (0.92–3.79) 0.015 0.46 (0.19–0.85) 0.016 0.41 (0.19–0.85)
SBO outcome based on patient factors and the type of operation. Bold values indicate statistical significance (P = 0.05). The values in parenthesis indicate the 95% confidence interval.
from Tsao et al, however, had a statistically larger proportion of perforated appendicitis in the OG, partly explaining the difference in postoperative SBO. Another pediatric study from Kasela et al23 reported a significantly lower incidence of SBO after laparoscopic appendectomy than after the open approach. In this study, the severity of the appendicitis did not contribute to the incidence of SBO. The corresponding benefit in adult patients has not been clearly demonstrated. Leung et al24 concluded that there was no statistically significant difference in the incidence of SBO in adults when comparing laparoscopic with open appendectomy, a finding supported by Kouhia et al7 and Swank et al.9 These studies are most probably underpowered. However, Angenete et al25 recently demonstrated in C 2013 Lippincott Williams & Wilkins
Lap. group n = 2372
Status of appendix Perforated Nonperforated Normal No. SBO episodes 1 ≥2 Total No. for the group Surgical treatment of SBO, n (%) 1 operation 2 operations
Open Group (n = 24)
Laparoscopic Group (n = 10)
10 11 3
4 6 0
17 7 39 13 (54) 11 2
8 2 14 5 (50) 1 4
a large, population-based register study that open surgery increased the risk of SBO up to 4 times compared with laparoscopic surgery for most abdominal surgical procedures, including appendectomy. The study population was mixed, also including children.25 In our study, the incidence of readmissions for SBO was low in both the OG and the LG, 1.0% and 0.4%, respectively. In a large retrospective cohort study, including almost 250,000 patients with 30 years’ follow-up, Andersson16 showed a cumulative risk of 0.63% for surgical treatment of SBO 1 year after open appendectomy and 1.3% after 30 years. In the study by Tingstedt et al,14 the incidence of assumed SBO of 1.54% after open appendectomy was reported and 0.84% of all patients with appendectomy had to undergo surgical treatment of SBO during a follow-up time period of more than 10 years. The patients in the last 2 referred studies underwent appendectomy between 1964 and 1993, and 1981 and 1996, respectively. In our study, the patients included had their index operation during a later time period (ie, between 1992 and 2007). This could be a part of the explanation to the lower readmission rate for SBO seen after open appendectomy in our study. www.annalsofsurgery.com | 1175
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Annals of Surgery r Volume 259, Number 6, June 2014
Isaksson et al
the symptom diagnose, and the code for the surgical intervention. This could otherwise be a problem when different databases are combined to identify certain surgical procedures with symptom diagnoses. In our study, there were several patients, particularly in the OG, who had incorrect operative code for the index operation. These patients were coded as open appendectomy but had a laparoscopically appendectomy performed. In a previous study by Wilson et al,30 only one third of the patients were correctly coded in a study of the natural history of SBO. The inclusion by “intention to treat,” thus including all the possible surgical outcomes in the LG, has to our knowledge not been demonstrated before and must strengthen the study design.
CONCLUSIONS
FIGURE 2. Strong adhesions between small bowel and abdominal wall in the area of previous open appendectomy, the cause of SBO in this case (Photograph courtesy: Dr Tingstedt). Open appendectomy was identified as an independent risk factor for SBO in our study. With time, surgeons have become more aware of the importance of a more atraumatic surgical approach, including handling of the tissue and the importance of hemostatic control, which are well-known risk factors for adhesion formation. The removal of starch-powdered gloves, known to facilitate adhesions,26 is also a possible factor of contributing to postoperative SBO. Previous studies have declared that the risk of SBO after appendectomy is higher if the appendix is either perforated or normal. Findings of a normal appendix demands a further exploration of the distal part of the small bowel, exploring other possible diagnoses, and this may be associated with increased tissue trauma promoting adhesions in open surgery. The number of macroscopically normal appendices at exploration has gradually decreased over time because of more strict operative indications after repeated bedside assessments in combination with laboratory sampling and more frequent use of preoperative radiological examinations.27 This could, in part, be an explanation for older age as an independent risk factor. Patients operated on early in the study were probably submitted to more extensive exploration as depicted earlier, although subgroup analysis of SBO versus operation date did not reach statistic significance. In our study, the inclusion of the patients in the LG who had only a diagnostic laparoscopy performed partly explains the low readmission rate in the LG. In the present study, there was a statistical difference in sex distribution, with more women in the LG, which is in concordance with other studies.9,28 Limitations of a retrospective study should of course be considered. One is the possibility of missing patients being readmitted for SBO in other hospitals (eg, because of migration). The migration in Sweden is relatively low. However, the migration for the population of the 2 cities enrolled in this study is higher than the average in the country but similar when compared with each other. The potential “loss of patients” would thereby be fairly equal in both groups.29 Another limitation is the fact that we selected laparoscopic approach in one hospital and open in the other. The difference in the followup time between the groups (mean 13.5 years in the OG and 11 in the LG) can be explained by the increasing number of laparoscopic interventions for suspected appendicitis over time during the study period. The strengths of the study are the large and similar numbers of patients in both groups and the fact that all individual charts were reviewed, thereby decreasing the risk of incorrect coding, concerning 1176 | www.annalsofsurgery.com
We have shown a minor yet significant difference in the incidence of SBO after open versus laparoscopic technique for suspected appendicitis favoring the laparoscopic approach. Together with already well-documented benefits such as shorter hospital stay, fewer wound infections, postoperative pain, and the possibility of exploring other possible diagnosis and leaving a nonaffected appendix in place, we recommend the laparoscopic technique to be the preferable approach in adults with suspected appendicitis.
ACKNOWLEDGMENTS The authors thank E. Bergman, L. Hermansson, S. Larsson, and A. Traunsberger for their great help with the chart review process.
REFERENCES 1. Graff L, Russell J, Seashore J, et al. False-negative and false-positive errors in abdominal pain evaluation: failure to diagnose acute appendicitis and unnecessary surgery. Acad Emerg Med. 2000;7:1244–1255. 2. Addiss DG, Shaffer N, Fowler BS, et al. The epidemiology of appendicitis and appendectomy in the United States. Am J Epidemiol. 1990;132:910–925. 3. Flum DR, Morris A, Koepsell T, et al. Has misdiagnosis of appendicitis decreased over time? A population-based analysis. JAMA. 2001;286:1748–1753. 4. Semm K. Endoscopic appendectomy. Endoscopy. 1983;15:59–64. 5. Moberg AC, Montgomery A. Appendicitis: laparoscopic versus conventional operation: a study and review of the literature. Surg Laparosc Endosc. 1997;7:459–463. 6. Golub R, Siddiqui F, Pohl D. Laparoscopic versus open appendectomy: a metaanalysis. J Am Coll Surg. 1998;186:545–553. 7. Kouhia ST, Heiskanen JT, Huttunen R, et al. Long-term follow-up of a randomized clinical trial of open versus laparoscopic appendicectomy. Br J Surg. 2010;97:1395–1400. 8. Sauerland S, Jaschinski T, Neugebauer EA. Laparoscopic versus open surgery for suspected appendicitis. Cochrane Database Syst Rev. 2010:CD001546. 9. Swank HA, Eshuis EJ, van Berge Henegouwen MI, et al. Short- and longterm results of open versus laparoscopic appendectomy. World J Surg. 2011;35:1221–1226; discussion 1227–1228. 10. Wei B, Qi CL, Chen TF, et al. Laparoscopic versus open appendectomy for acute appendicitis: a metaanalysis. Surg Endosc. 2011;25:1199–1208. 11. Moberg AC, Ahlberg G, Leijonmarck CE, et al. Diagnostic laparoscopy in 1043 patients with suspected acute appendicitis. Eur J Surg. 1998;164:833– 840; discussion 841. 12. Tingstedt B, Isaksson J, Andersson R. Long-term follow-up and cost analysis following surgery for small bowel obstruction caused by intra-abdominal adhesions. Br J Surg. 2007;94:743–748. 13. Tsao KJ, St Peter SD, Valusek PA, et al. Adhesive small bowel obstruction after appendectomy in children: comparison between the laparoscopic and open approach. J Pediatr Surg. 2007;42:939–942; discussion 942. 14. Tingstedt B, Johansson J, Nehez L, et al. Late abdominal complaints after appendectomy—readmissions during long-term follow-up. Dig Surg. 2004; 21:23–27. 15. Ahlberg G, Bergdahl S, Rutqvist J, et al. Mechanical small-bowel obstruction after conventional appendectomy in children. Eur J Pediatr Surg. 1997;7: 13–15. 16. Andersson RE. Small bowel obstruction after appendicectomy. Br J Surg. 2001;88:1387–1391. 17. Riber C, Soe K, Jorgensen T, et al. Intestinal obstruction after appendectomy. Scand J Gastroenterol. 1997;32:1125–1128.
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18. Zbar RI, Crede WB, McKhann CF, et al. The postoperative incidence of small bowel obstruction following standard, open appendectomy and cholecystectomy: a six-year retrospective cohort study at Yale-New Haven Hospital. Conn Med. 1993;57:123–127. 19. Gutt CN, Oniu T, Schemmer P, et al. Fewer adhesions induced by laparoscopic surgery? Surg Endosc. 2004;18:898–906. 20. Moberg AC, Berndsen F, Palmquist I, et al. Randomized clinical trial of laparoscopic versus open appendicectomy for confirmed appendicitis. Br J Surg. 2005;92:298–304. 21. Lundorff P, Hahlin M, Kallfelt B, et al. Adhesion formation after laparoscopic surgery in tubal pregnancy: a randomized trial versus laparotomy. Fertil Steril. 1991;55:911–915. 22. Schn¨uriger B, Barmparas G, Branco BC, et al. Prevention of postoperative peritoneal adhesions: a review of the literature. Am J Surg. 2011;201:111– 121. 23. Kaselas C, Molinaro F, Lacreuse I, et al. Postoperative bowel obstruction after laparoscopic and open appendectomy in children: a 15-year experience. J Pediatr Surg. 2009;44:1581–1585.
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Appendectomy and Small Bowel Obstruction
24. Leung TT, Dixon E, Gill M, et al. Bowel obstruction following appendectomy: what is the true incidence? Ann Surg. 2009;250:51–53. 25. Angenete E, Jacobsson A, Gellerstedt M, et al. Effect of laparoscopy on the risk of small-bowel obstruction: a population-based register study. Arch Surg. 2012;147:359–365. 26. Holmdahl L, al-Jabreen M, Xia G, et al. The impact of starch-powdered gloves on the formation of adhesions in rats. Eur J Surg. 1994;160:257–261. 27. Tingstedt B, Andersson R. Improved diagnostic accuracy in patients with suspected appendicitis. Ann Gastroenterol. 2005;18:65–69. 28. Masoomi H, Mills S, Dolich MO, et al. Comparison of outcomes of laparoscopic versus open appendectomy in adults: data from the Nationwide Inpatient Sample (NIS), 2006–2008. J Gastrointest Surg. 2011;15: 2226–2231. 29. Statistiska Centralbyr˚an S. Available at http://www.scb.se. Accessed September 30, 2012. 30. Wilson MS, Hawkswell J, McCloy RF. Natural history of adhesional small bowel obstruction: counting the cost. Br J Surg. 1998;85:1294– 1298.
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Long-term Follow-up for Adhesive Small Bowel Obstruction After Open Versus Laparoscopic Surgery for Suspected Appendicitis Karolin Isaksson, MD,∗ Agneta Montgomery, MD, PhD,† Ann-Cathrin Moberg, MD, PhD,† Roland Andersson, MD, PhD,∗ and Bobby Tingstedt, MD, PhD∗
Objective: The aim of the present study was to compare the frequency of readmissions due to small bowel obstruction (SBO) after open versus laparoscopic surgery performed for suspected acute appendicitis. Background: Appendicitis is a common disease, with a lifetime risk of approximately 7%. Appendectomy is the treatment of choice for most patients. Postoperative adhesions are common after abdominal surgery, including appendectomy. Materials and Methods: Consecutive patients, 16 years or older, operated on because of suspected appendicitis at 2 university hospitals between 1992 and 2007 were included. The prime approach was open at one hospital and laparoscopic at the other hospital. Open and laparoscopic procedures were compared retrospectively, reviewing the patients’ charts until the middle of 2012. Hospitalization for SBO after index surgery was registered. Results: A total of 2333 patients in the open group and 2372 patients in the laparoscopic group were included. The frequency of hospitalization for SBO was low in both groups, although a difference between the groups was identified (1.0% in the open group and 0.4% in the laparoscopic group) (P = 0.015). Conclusions: Hospitalization due to SBO, between open and laparoscopic procedures, in patients operated on because of suspected appendicitis demonstrated a significant difference, favoring the laparoscopic approach. The frequency of SBO after the index surgery was, though, low in both groups. Keywords: adhesive, appendicitis, long term follow-up, open versus laparoscopic, small bowel obstruction (Ann Surg 2014;259:1173–1177)
A
ppendicitis is a common condition, with a calculated cumulated lifetime risk of 7% to 8%.1,2 Surgery is the treatment of choice for the majority of patients. The incidence of appendectomy is around 100 of 100,000 inhabitants per year in the Western world.3 Open appendectomy has been the criterion standard until the laparoscopic technique was introduced by Semm4 in early 1980s. Several studies have described advantages of using the laparoscopic technique, including diagnostic possibilities, faster recovery with shortened hospital stay, decreased postoperative pain, and a lower incidence of wound infections.5–7 Others have demonstrated disadvantages such as a possible higher risk of postoperative intraabdominal abscess formation,6,8,9 whereas others have not demonstrated any difference between open and laparoscopic procedures.10 From the ∗ Department of Surgery, Sk˚ane University Hospital, Lund, Sweden; and †Department of Surgery, Sk˚ane University Hospital, Malm¨o, Sweden. Disclosure: This study was partly supported by grants from Eric and Angelica Sparre Foundation, although the funding source had no influence on the study at all. None of the authors have any conflicts of interest. Reprints: Karolin Isaksson, MD, Department of Surgery, Sk˚ane University Hospital, S-221 85 Lund, Sweden. E-mail: [email protected]. C 2013 by Lippincott Williams & Wilkins Copyright ISSN: 0003-4932/13/25906-1173 DOI: 10.1097/SLA.0000000000000322
Annals of Surgery r Volume 259, Number 6, June 2014
A diagnostic laparoscopy is safe and offers the possibility to detect pathological conditions mimicking appendicitis, especially important in fertile women, and also rendering the option to leave a normal appendix in place.11 Postoperative adhesions are quite common, especially not only after surgery of the lower part of the abdomen such as gynecological and colorectal surgery but also after appendectomy. Late complications due to intra-abdominal adhesions include chronic abdominal pain, small bowel obstruction (SBO), and female infertility. These chronic conditions can result in a major impairment for the patient, a challenge to treat, and represent a major cost for society. In Sweden, costs related to admissions due to abdominal adhesions are estimated to about €40 million to €60 million per year.12 Abdominal adhesions are the most common cause of SBO requiring surgical intervention. The lifetime risk of postoperative bowel obstruction after abdominal surgery with a frequency of up to 25% after some procedures has been reported. The incidence of bowel obstruction after appendectomy has historically been reported to be between 0.7% and 10.7%.13–18 Type and grade of surgical trauma seem to play an important role in adhesion formation. There are documented advantages of laparoscopic procedures in general, as compared with open surgery, in reducing postoperative adhesion formation by minimizing the trauma to the peritoneal surface.19 The aim of this study was to determine the incidence of SBO after open and laparoscopic operations in patients with suspected appendicitis in a large cohort of adult patients subjected to a long-term follow-up.
PATIENTS AND MATERIALS Data from patients, 16 years or older, operated on for suspected appendicitis between 1992 until the end of 2007 at the University Hospitals in Lund and Malm¨o (since 2011 merged to form 1 university hospital: Sk˚ane University Hospital) were retrospectively collected. The hospitals are closely localized in the southern region of Sweden. During this time period, the preferred operation technique in Lund was the open approach whereas laparoscopic operation was the procedure of choice in Malm¨o. The open group (OG) consisted of all consecutive patients operated on by open technique in Lund, and the laparoscopic group (LG) consisted of all consecutive patients operated on in Malm¨o. The patients were identified by the ICD (International Classification of Diseases) codes. For open appendectomy, the codes 4510 (ICD-9 until 1996) and JEA 00 (ICD-10 after 1996) were used; for the laparoscopic operations, the codes 4511, 4042 (ICD-9), and JEA 01, JAH 01 (ICD-10) were used. The LG included 3 possible pathways for patients with clinically suspected appendicitis: an appendectomy completed laparoscopically, a conversion to open appendectomy, or a diagnostic/explorative laparoscopy leaving a macroscopically normal appendix in place. The curriculum was to perform an initial laparoscopy for diagnostic purposes. The appendix was left in place when diagnosed as macroscopically normal. When appendicitis was diagnosed at laparoscopy, the surgeons having an accreditation for www.annalsofsurgery.com | 1173
Copyright © 2013 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Annals of Surgery r Volume 259, Number 6, June 2014
Isaksson et al
laparoscopic appendectomy went on with a laparoscopic procedure and converted in case of technical difficulties. The surgeons not having the accreditation for laparoscopic appendectomy converted to open appendectomy after the diagnostic laparoscopy. This strategy resulted in a high conversion rate, although the number of conversions diminished over time as the educational program proceeded. In the OG, an appendectomy was performed for all patients, including when finding macroscopically normal appendices. Patients were analyzed both on the intention-to-treat basis and per protocol. In the per protocol analysis, the converted operations in the LG were excluded to study the laparoscopic versus open technique per se.
Exclusion Criteria
• If the appendectomy was performed as a part in a more extensive surgical procedure (en passant, eg, colorectal resection) or when the operation was extended because of an advanced appendicitis (eg, ileocecal resection). • When the appendectomy was accompanied with another concurrent intra-abdominal surgical procedure (eg, oophorectomy, Meckel diverticulum). • In patients with carcinoma of the appendix (not carcinoids that did not lead to further surgical treatment). • In patients readmitted for SBO having information of conflicting surgery to the lower part of the abdomen, presence of adhesions at the primary operation, or a history of interfering disease (eg, Crohn disease or abdominal cancer). • Patients in the LG who were operated on by open surgery after the diagnostic laparoscopy (n = 42), due to an ongoing randomized study comparing open and laparoscopic surgery performed between March 2001 and July 2003.20 • Patients with incorrect operative code for the appendectomy surgery.
Protocol All individual charts were manually revised in both groups. The charts were reviewed from the date of index surgery for suspected appendicitis until June 30, 2012. An individual protocol was established for patients who were readmitted and hospitalized after the index operation because of symptoms of SBO. Definition of SBO was radiological findings indicating SBO or obvious findings of SBO in the patient on examination (information retrieved from the charts) such as distended abdomen, colicky pain, absence of flatus, and characteristic bowel sounds. Sex, age, previous abdominal surgery, date of readmission, surgical technique at index operation, and macroscopic appearance of the appendix (including the presence of perforation and abscess formation at the time of appendectomy) were registered. In the LG, registration for the performance of a diagnostic laparoscopy (leaving the appendix in place), a complete laparoscopic operation, or a conversion to open appendectomy was performed. The number of readmissions for each patient and whether the condition was handled conservatively or needed surgical intervention were noted.
Power Calculation and Statistical Analyses The hypothesis was that the incidence of patients having symptoms of SBO would be lower in the LG. The incidence of symptoms of SBO was assumed to be 1.2% after open appendectomy, based on previous studies. To prove a 50% reduction in the LG, a total of 1655 patients in each group were needed with a statistical power of 80% and a risk of 5% inaccuracy. To calculate for differences between the groups, the Fisher exact test, the χ 2 test, the independent t test, and the Wilcoxon rank-sum test were used. Pearson bivariate correlation and multivariate logistic regression analysis were used for calculation 1174 | www.annalsofsurgery.com
of risk factors for SBO. Statistical calculations were performed with SPSS version 19.0, IBM Corp., Armonk, NY, USA. A 2-sided P < 0.05 was considered statistically significant.
RESULTS A total of 4705 patients, 2333 in the OG and 2372 in the LG, were included. The excluded patients are shown in Figure 1. There were 994 female patients (43%) and 1339 male patients in the OG (P < 0.001) and 1250 female patients (53%) and 1122 male patients in the LG (P = 0.009). The difference in sex between the groups was statistically significant (P < 0.001). The mean age was 35 (SD = 16) years in the OG and 36 (SD = 16) years in the LG (P = 0.072). The mean follow-up time was 161 (SD = 53) months in the OG and 133 (SD = 49) months in the LG (P < 0.001). In the LG, the distribution of surgical intervention was 1401 laparoscopic appendectomies (59%), 595 converted to open appendectomy (25%), and 376 diagnostic laparoscopies (16%). A total of 34 patients were hospitalized for SBO, most likely related to the index surgery: 24 patients (1.0%) in the OG and 10 patients (0.4%) in the LG (P = 0.015). Readmissions are depicted in Table 1. Outcomes of SBO regarding patient factors are outlined in univariate and multivariate analyses in Table 2. Open appendectomy and older age are independent risk factors for SBO in the multivariate analysis. Altogether 7 patients in the OG and 2 patients in the LG had more than 1 readmission, resulting in a total number of readmissions of 39 in the OG and 14 in the LG. All patients, except one, in both groups had radiological findings and clinical symptoms. In both groups, approximately half of the patients who were readmitted, the SBO was treated surgically (P = 1.000) (Table 3, Fig. 2). The median time to first readmission for SBO was 314 (range, 3–2451) days in the OG and 330 (range, 12–2277) days in the LG (P = 0.691). One of the patients in the LG died postoperatively from respiratory complications after her second surgically treated SBO episode. There were no readmissions due to SBO related to the index operation in the patients being subjected only to a diagnostic laparoscopy. In the per protocol analysis where the converted patients in the LG were excluded, we found a significant difference in the incidence of readmission for SBO, in favor of the laparoscopic (0.3%) compared with the open technique (1.0%) (P = 0.009).
DISCUSSION We found a difference in the incidence of SBO after operation for suspected appendicitis on the intention-to-treat basis in our study favoring the laparoscopic approach. Open appendectomy and older age are independent risk factors for SBO. Results of previous studies comparing open and laparoscopic surgical procedures support the theory of less adhesion formation with the laparoscopic approach.19 To our knowledge, there is only one randomized clinical trial comparing adhesion formation between laparoscopy and laparotomy evaluated at second-look surgery.21 This study, published in 1991 (n = 73), shows significantly fewer adhesions within the operated site in the LG than in the open surgery group, although there was no significant difference for overall adhesion formation even if a trend was observed in favor of the LG. The possible superior role of laparoscopic surgery for acute appendicitis and subsequent SBO has not been clearly demonstrated in a cohort of adult patients. In a fairly recent review by Schn¨uriger et al,22 the laparoscopic technique was found to result in fewer adhesion-related readmissions than the open technique for several abdominal operations, although with the exception of appendectomies. The decreased incidence of SBO after laparoscopic appendectomy has been shown previously in pediatric studies. Tsao et al13 concluded that SBO is less common after laparoscopic appendectomy than after open appendectomy in children. The study C 2013 Lippincott Williams & Wilkins
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Annals of Surgery r Volume 259, Number 6, June 2014
Appendectomy and Small Bowel Obstruction
Study cohort n = 4954
Open group n = 2472
Lap. group n = 2482
Excluded n = 139
Excluded n = 110
Incorrect op code: 92 Incomplete/missing chart: 12 Extended surgery: 25 Cancer in appendix: 4 Other: 6
Incorrect op code: 10 Incomplete/missing chart: 21 Extended surgery: 25 Cancer in appendix: 8 Study: 42 Other: 4
Open group n = 2333
Final cohort n = 4705
FIGURE 1. Flowchart for inclusion. Lap. indicates laparoscopic; op, operative. TABLE 1. Readmitted Patients for SBO
Total No. Only late SBO (>30 d)
TABLE 3. Characteristics for Patients Readmitted for SBO
Open Group, n (%)
Laparoscopic Group, n (%)
P
24 (1.0) 16 (0.7)
10 (0.4) 7 (0.3)
0.016 0.061
TABLE 2. Analysis of Patient Factors on SBO Outcome Univariate Analyses Factors
P
Female sex Age above median Follow-up time above median Laparoscopic appendectomy
Odds Ratio
Multivariate Analyses P
Odds Ratio
0.606 1.25 (0.63–2.48) 0.022 2.31 (1.16–4.63) 0.017 2.33 (1.16–4.67) 0.086 1.87 (0.92–3.79) 0.015 0.46 (0.19–0.85) 0.016 0.41 (0.19–0.85)
SBO outcome based on patient factors and the type of operation. Bold values indicate statistical significance (P = 0.05). The values in parenthesis indicate the 95% confidence interval.
from Tsao et al, however, had a statistically larger proportion of perforated appendicitis in the OG, partly explaining the difference in postoperative SBO. Another pediatric study from Kasela et al23 reported a significantly lower incidence of SBO after laparoscopic appendectomy than after the open approach. In this study, the severity of the appendicitis did not contribute to the incidence of SBO. The corresponding benefit in adult patients has not been clearly demonstrated. Leung et al24 concluded that there was no statistically significant difference in the incidence of SBO in adults when comparing laparoscopic with open appendectomy, a finding supported by Kouhia et al7 and Swank et al.9 These studies are most probably underpowered. However, Angenete et al25 recently demonstrated in C 2013 Lippincott Williams & Wilkins
Lap. group n = 2372
Status of appendix Perforated Nonperforated Normal No. SBO episodes 1 ≥2 Total No. for the group Surgical treatment of SBO, n (%) 1 operation 2 operations
Open Group (n = 24)
Laparoscopic Group (n = 10)
10 11 3
4 6 0
17 7 39 13 (54) 11 2
8 2 14 5 (50) 1 4
a large, population-based register study that open surgery increased the risk of SBO up to 4 times compared with laparoscopic surgery for most abdominal surgical procedures, including appendectomy. The study population was mixed, also including children.25 In our study, the incidence of readmissions for SBO was low in both the OG and the LG, 1.0% and 0.4%, respectively. In a large retrospective cohort study, including almost 250,000 patients with 30 years’ follow-up, Andersson16 showed a cumulative risk of 0.63% for surgical treatment of SBO 1 year after open appendectomy and 1.3% after 30 years. In the study by Tingstedt et al,14 the incidence of assumed SBO of 1.54% after open appendectomy was reported and 0.84% of all patients with appendectomy had to undergo surgical treatment of SBO during a follow-up time period of more than 10 years. The patients in the last 2 referred studies underwent appendectomy between 1964 and 1993, and 1981 and 1996, respectively. In our study, the patients included had their index operation during a later time period (ie, between 1992 and 2007). This could be a part of the explanation to the lower readmission rate for SBO seen after open appendectomy in our study. www.annalsofsurgery.com | 1175
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Annals of Surgery r Volume 259, Number 6, June 2014
Isaksson et al
the symptom diagnose, and the code for the surgical intervention. This could otherwise be a problem when different databases are combined to identify certain surgical procedures with symptom diagnoses. In our study, there were several patients, particularly in the OG, who had incorrect operative code for the index operation. These patients were coded as open appendectomy but had a laparoscopically appendectomy performed. In a previous study by Wilson et al,30 only one third of the patients were correctly coded in a study of the natural history of SBO. The inclusion by “intention to treat,” thus including all the possible surgical outcomes in the LG, has to our knowledge not been demonstrated before and must strengthen the study design.
CONCLUSIONS
FIGURE 2. Strong adhesions between small bowel and abdominal wall in the area of previous open appendectomy, the cause of SBO in this case (Photograph courtesy: Dr Tingstedt). Open appendectomy was identified as an independent risk factor for SBO in our study. With time, surgeons have become more aware of the importance of a more atraumatic surgical approach, including handling of the tissue and the importance of hemostatic control, which are well-known risk factors for adhesion formation. The removal of starch-powdered gloves, known to facilitate adhesions,26 is also a possible factor of contributing to postoperative SBO. Previous studies have declared that the risk of SBO after appendectomy is higher if the appendix is either perforated or normal. Findings of a normal appendix demands a further exploration of the distal part of the small bowel, exploring other possible diagnoses, and this may be associated with increased tissue trauma promoting adhesions in open surgery. The number of macroscopically normal appendices at exploration has gradually decreased over time because of more strict operative indications after repeated bedside assessments in combination with laboratory sampling and more frequent use of preoperative radiological examinations.27 This could, in part, be an explanation for older age as an independent risk factor. Patients operated on early in the study were probably submitted to more extensive exploration as depicted earlier, although subgroup analysis of SBO versus operation date did not reach statistic significance. In our study, the inclusion of the patients in the LG who had only a diagnostic laparoscopy performed partly explains the low readmission rate in the LG. In the present study, there was a statistical difference in sex distribution, with more women in the LG, which is in concordance with other studies.9,28 Limitations of a retrospective study should of course be considered. One is the possibility of missing patients being readmitted for SBO in other hospitals (eg, because of migration). The migration in Sweden is relatively low. However, the migration for the population of the 2 cities enrolled in this study is higher than the average in the country but similar when compared with each other. The potential “loss of patients” would thereby be fairly equal in both groups.29 Another limitation is the fact that we selected laparoscopic approach in one hospital and open in the other. The difference in the followup time between the groups (mean 13.5 years in the OG and 11 in the LG) can be explained by the increasing number of laparoscopic interventions for suspected appendicitis over time during the study period. The strengths of the study are the large and similar numbers of patients in both groups and the fact that all individual charts were reviewed, thereby decreasing the risk of incorrect coding, concerning 1176 | www.annalsofsurgery.com
We have shown a minor yet significant difference in the incidence of SBO after open versus laparoscopic technique for suspected appendicitis favoring the laparoscopic approach. Together with already well-documented benefits such as shorter hospital stay, fewer wound infections, postoperative pain, and the possibility of exploring other possible diagnosis and leaving a nonaffected appendix in place, we recommend the laparoscopic technique to be the preferable approach in adults with suspected appendicitis.
ACKNOWLEDGMENTS The authors thank E. Bergman, L. Hermansson, S. Larsson, and A. Traunsberger for their great help with the chart review process.
REFERENCES 1. Graff L, Russell J, Seashore J, et al. False-negative and false-positive errors in abdominal pain evaluation: failure to diagnose acute appendicitis and unnecessary surgery. Acad Emerg Med. 2000;7:1244–1255. 2. Addiss DG, Shaffer N, Fowler BS, et al. The epidemiology of appendicitis and appendectomy in the United States. Am J Epidemiol. 1990;132:910–925. 3. Flum DR, Morris A, Koepsell T, et al. Has misdiagnosis of appendicitis decreased over time? A population-based analysis. JAMA. 2001;286:1748–1753. 4. Semm K. Endoscopic appendectomy. Endoscopy. 1983;15:59–64. 5. Moberg AC, Montgomery A. Appendicitis: laparoscopic versus conventional operation: a study and review of the literature. Surg Laparosc Endosc. 1997;7:459–463. 6. Golub R, Siddiqui F, Pohl D. Laparoscopic versus open appendectomy: a metaanalysis. J Am Coll Surg. 1998;186:545–553. 7. Kouhia ST, Heiskanen JT, Huttunen R, et al. Long-term follow-up of a randomized clinical trial of open versus laparoscopic appendicectomy. Br J Surg. 2010;97:1395–1400. 8. Sauerland S, Jaschinski T, Neugebauer EA. Laparoscopic versus open surgery for suspected appendicitis. Cochrane Database Syst Rev. 2010:CD001546. 9. Swank HA, Eshuis EJ, van Berge Henegouwen MI, et al. Short- and longterm results of open versus laparoscopic appendectomy. World J Surg. 2011;35:1221–1226; discussion 1227–1228. 10. Wei B, Qi CL, Chen TF, et al. Laparoscopic versus open appendectomy for acute appendicitis: a metaanalysis. Surg Endosc. 2011;25:1199–1208. 11. Moberg AC, Ahlberg G, Leijonmarck CE, et al. Diagnostic laparoscopy in 1043 patients with suspected acute appendicitis. Eur J Surg. 1998;164:833– 840; discussion 841. 12. Tingstedt B, Isaksson J, Andersson R. Long-term follow-up and cost analysis following surgery for small bowel obstruction caused by intra-abdominal adhesions. Br J Surg. 2007;94:743–748. 13. Tsao KJ, St Peter SD, Valusek PA, et al. Adhesive small bowel obstruction after appendectomy in children: comparison between the laparoscopic and open approach. J Pediatr Surg. 2007;42:939–942; discussion 942. 14. Tingstedt B, Johansson J, Nehez L, et al. Late abdominal complaints after appendectomy—readmissions during long-term follow-up. Dig Surg. 2004; 21:23–27. 15. Ahlberg G, Bergdahl S, Rutqvist J, et al. Mechanical small-bowel obstruction after conventional appendectomy in children. Eur J Pediatr Surg. 1997;7: 13–15. 16. Andersson RE. Small bowel obstruction after appendicectomy. Br J Surg. 2001;88:1387–1391. 17. Riber C, Soe K, Jorgensen T, et al. Intestinal obstruction after appendectomy. Scand J Gastroenterol. 1997;32:1125–1128.
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18. Zbar RI, Crede WB, McKhann CF, et al. The postoperative incidence of small bowel obstruction following standard, open appendectomy and cholecystectomy: a six-year retrospective cohort study at Yale-New Haven Hospital. Conn Med. 1993;57:123–127. 19. Gutt CN, Oniu T, Schemmer P, et al. Fewer adhesions induced by laparoscopic surgery? Surg Endosc. 2004;18:898–906. 20. Moberg AC, Berndsen F, Palmquist I, et al. Randomized clinical trial of laparoscopic versus open appendicectomy for confirmed appendicitis. Br J Surg. 2005;92:298–304. 21. Lundorff P, Hahlin M, Kallfelt B, et al. Adhesion formation after laparoscopic surgery in tubal pregnancy: a randomized trial versus laparotomy. Fertil Steril. 1991;55:911–915. 22. Schn¨uriger B, Barmparas G, Branco BC, et al. Prevention of postoperative peritoneal adhesions: a review of the literature. Am J Surg. 2011;201:111– 121. 23. Kaselas C, Molinaro F, Lacreuse I, et al. Postoperative bowel obstruction after laparoscopic and open appendectomy in children: a 15-year experience. J Pediatr Surg. 2009;44:1581–1585.
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Appendectomy and Small Bowel Obstruction
24. Leung TT, Dixon E, Gill M, et al. Bowel obstruction following appendectomy: what is the true incidence? Ann Surg. 2009;250:51–53. 25. Angenete E, Jacobsson A, Gellerstedt M, et al. Effect of laparoscopy on the risk of small-bowel obstruction: a population-based register study. Arch Surg. 2012;147:359–365. 26. Holmdahl L, al-Jabreen M, Xia G, et al. The impact of starch-powdered gloves on the formation of adhesions in rats. Eur J Surg. 1994;160:257–261. 27. Tingstedt B, Andersson R. Improved diagnostic accuracy in patients with suspected appendicitis. Ann Gastroenterol. 2005;18:65–69. 28. Masoomi H, Mills S, Dolich MO, et al. Comparison of outcomes of laparoscopic versus open appendectomy in adults: data from the Nationwide Inpatient Sample (NIS), 2006–2008. J Gastrointest Surg. 2011;15: 2226–2231. 29. Statistiska Centralbyr˚an S. Available at http://www.scb.se. Accessed September 30, 2012. 30. Wilson MS, Hawkswell J, McCloy RF. Natural history of adhesional small bowel obstruction: counting the cost. Br J Surg. 1998;85:1294– 1298.
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