Long-Term Follow-Up for Adhesive Small Bowel Obstruction After Open

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∗

A diagnostic laparoscopy is safe and offers the possibility to detect Objective: The aim of the present study was to compare the frequency of read- pathological conditions mimicking appendicitis, especially important missions due to small bowel obstruction (SBO) after open versus laparoscopic in fertile women, and also rendering the option to leave a normal ap- surgery performed for suspected acute appendicitis. pendix in place.11 Background: Appendicitis is a common disease, with a lifetime risk of ap- Postoperative adhesions are quite common, especially not only proximately 7%. Appendectomy is the treatment of choice for most patients. after surgery of the lower part of the abdomen such as gynecological Postoperative adhesions are common after abdominal surgery, including ap- and colorectal surgery but also after appendectomy. Late complica- pendectomy. tions due to intra-abdominal adhesions include chronic abdominal Materials and Methods: Consecutive patients, 16 years or older, operated pain, small bowel obstruction (SBO), and female infertility. These on because of suspected appendicitis at 2 university hospitals between 1992 chronic conditions can result in a major impairment for the patient, a and 2007 were included. The prime approach was open at one hospital and challenge to treat, and represent a major cost for society. In Sweden, laparoscopic at the other hospital. Open and laparoscopic procedures were costs related to admissions due to abdominal adhesions are estimated compared retrospectively, reviewing the patients’ charts until the middle of to about €40 million to €60 million per year.12 Abdominal adhesions 2012. Hospitalization for SBO after index surgery was registered. are the most common cause of SBO requiring surgical intervention. Results: A total of 2333 patients in the open group and 2372 patients in The lifetime risk of postoperative bowel obstruction after abdominal the laparoscopic group were included. The frequency of hospitalization for surgery with a frequency of up to 25% after some procedures has been SBO was low in both groups, although a difference between the groups was reported. The incidence of bowel obstruction after appendectomy has identiﬁed (1.0% in the open group and 0.4% in the laparoscopic group) (P = historically been reported to be between 0.7% and 10.7%.13–18 0.015). Type and grade of surgical trauma seem to play an important Conclusions: Hospitalization due to SBO, between open and laparoscopic role in adhesion formation. There are documented advantages of la- procedures, in patients operated on because of suspected appendicitis demon- paroscopic procedures in general, as compared with open surgery, in strated a signiﬁcant difference, favoring the laparoscopic approach. The fre- reducing postoperative adhesion formation by minimizing the trauma quency of SBO after the index surgery was, though, low in both groups. to the peritoneal surface.19 The aim of this study was to determine Keywords: adhesive, appendicitis, long term follow-up, open versus laparo- the incidence of SBO after open and laparoscopic operations in pa- scopic, small bowel obstruction tients with suspected appendicitis in a large cohort of adult patients subjected to a long-term follow-up. (Ann Surg 2014;259:1173–1177)

PATIENTS AND MATERIALS ppendicitis is a common condition, with a calculated cumu- Data from patients, 16 years or older, operated on for suspected 1,2 A lated lifetime risk of 7% to 8%. Surgery is the treatment appendicitis between 1992 until the end of 2007 at the University of choice for the majority of patients. The incidence of appendec- Hospitals in Lund and Malmo¨ (since 2011 merged to form 1 university tomy is around 100 of 100,000 inhabitants per year in the Western hospital: Skane˚ University Hospital) were retrospectively collected. 3 world. Open appendectomy has been the criterion standard until the The hospitals are closely localized in the southern region of Sweden. 4 laparoscopic technique was introduced by Semm in early 1980s. During this time period, the preferred operation technique in Lund was Several studies have described advantages of using the laparoscopic the open approach whereas laparoscopic operation was the procedure technique, including diagnostic possibilities, faster recovery with of choice in Malmo.¨ shortened hospital stay, decreased postoperative pain, and a lower The open group (OG) consisted of all consecutive patients op- 5–7 incidence of wound infections. Others have demonstrated dis- erated on by open technique in Lund, and the laparoscopic group advantages such as a possible higher risk of postoperative intra- (LG) consisted of all consecutive patients operated on in Malmo.¨ 6,8,9 abdominal abscess formation, whereas others have not demon- The patients were identified by the ICD (International Classification 10 strated any difference between open and laparoscopic procedures. 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, ∗ From the Department of Surgery, Skane˚ University Hospital, Lund, Sweden; and JAH 01 (ICD-10) were used. The LG included 3 possible pathways †Department of Surgery, Skane˚ University Hospital, Malmo,¨ Sweden. Disclosure: This study was partly supported by grants from Eric and Angelica for patients with clinically suspected appendicitis: an appendectomy Sparre Foundation, although the funding source had no influence on the study completed laparoscopically, a conversion to open appendectomy, or at all. None of the authors have any conflicts of interest. a diagnostic/explorative laparoscopy leaving a macroscopically nor- Reprints: Karolin Isaksson, MD, Department of Surgery, Skane˚ University Hospital, mal appendix in place. The curriculum was to perform an initial S-221 85 Lund, Sweden. E-mail: [email protected]. laparoscopy for diagnostic purposes. The appendix was left in place Copyright C 2013 by Lippincott Williams & Wilkins ISSN: 0003-4932/13/25906-1173 when diagnosed as macroscopically normal. When appendicitis was DOI: 10.1097/SLA.0000000000000322 diagnosed at laparoscopy, the surgeons having an accreditation for r Annals of Surgery Volume 259, Number 6, June 2014 www.annalsofsurgery.com | 1173

laparoscopic appendectomy went on with a laparoscopic procedure of risk factors for SBO. Statistical calculations were performed with and converted in case of technical difficulties. The surgeons not hav- SPSS version 19.0, IBM Corp., Armonk, NY, USA. A 2-sided P < ing the accreditation for laparoscopic appendectomy converted to 0.05 was considered statistically significant. open appendectomy after the diagnostic laparoscopy. This strategy resulted in a high conversion rate, although the number of conver- RESULTS sions diminished over time as the educational program proceeded. In A total of 4705 patients, 2333 in the OG and 2372 in the LG, the OG, an appendectomy was performed for all patients, including were included. The excluded patients are shown in Figure 1. There when finding macroscopically normal appendices. were 994 female patients (43%) and 1339 male patients in the OG Patients were analyzed both on the intention-to-treat basis and (P < 0.001) and 1250 female patients (53%) and 1122 male patients per protocol. In the per protocol analysis, the converted operations in in the LG (P = 0.009). The difference in sex between the groups was the LG were excluded to study the laparoscopic versus open technique statistically significant (P < 0.001). The mean age was 35 (SD = 16) per se. 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 Exclusion Criteria (SD = 49) months in the LG (P < 0.001). • If the appendectomy was performed as a part in a more extensive In the LG, the distribution of surgical intervention was 1401 surgical procedure (en passant, eg, colorectal resection) or when laparoscopic appendectomies (59%), 595 converted to open appen- the operation was extended because of an advanced appendicitis dectomy (25%), and 376 diagnostic laparoscopies (16%). A total of (eg, ileocecal resection). 34 patients were hospitalized for SBO, most likely related to the index • When the appendectomy was accompanied with another concurrent surgery: 24 patients (1.0%) in the OG and 10 patients (0.4%) in the LG intra-abdominal surgical procedure (eg, oophorectomy, Meckel di- (P = 0.015). Readmissions are depicted in Table 1. Outcomes of SBO verticulum). regarding patient factors are outlined in univariate and multivariate • In patients with carcinoma of the appendix (not carcinoids that did analyses in Table 2. Open appendectomy and older age are indepen- not lead to further surgical treatment). dent risk factors for SBO in the multivariate analysis. Altogether 7 • In patients readmitted for SBO having information of conflicting patients in the OG and 2 patients in the LG had more than 1 readmis- surgery to the lower part of the abdomen, presence of adhesions at sion, resulting in a total number of readmissions of 39 in the OG and the primary operation, or a history of interfering disease (eg, Crohn 14 in the LG. All patients, except one, in both groups had radiological disease or abdominal cancer). findings and clinical symptoms. In both groups, approximately half • Patients in the LG who were operated on by open surgery after of the patients who were readmitted, the SBO was treated surgically the diagnostic laparoscopy (n = 42), due to an ongoing random- (P = 1.000) (Table 3, Fig. 2). The median time to first readmission ized study comparing open and laparoscopic surgery performed for SBO was 314 (range, 3–2451) days in the OG and 330 (range, between March 2001 and July 2003.20 12–2277) days in the LG (P = 0.691). One of the patients in the LG • Patients with incorrect operative code for the appendectomy died postoperatively from respiratory complications after her second surgery. surgically treated SBO episode. There were no readmissions due to SBO related to the index operation in the patients being subjected Protocol only to a diagnostic laparoscopy. In the per protocol analysis where All individual charts were manually revised in both groups. the converted patients in the LG were excluded, we found a signifi- The charts were reviewed from the date of index surgery for suspected cant difference in the incidence of readmission for SBO, in favor of appendicitis until June 30, 2012. the laparoscopic (0.3%) compared with the open technique (1.0%) An individual protocol was established for patients who were (P = 0.009). readmitted and hospitalized after the index operation because of symptoms of SBO. Definition of SBO was radiological findings indi- DISCUSSION cating SBO or obvious findings of SBO in the patient on examination We found a difference in the incidence of SBO after operation (information retrieved from the charts) such as distended abdomen, for suspected appendicitis on the intention-to-treat basis in our study colicky pain, absence of flatus, and characteristic bowel sounds. favoring the laparoscopic approach. Open appendectomy and older Sex, age, previous abdominal surgery, date of readmission, age are independent risk factors for SBO. surgical technique at index operation, and macroscopic appearance Results of previous studies comparing open and laparoscopic of the appendix (including the presence of perforation and abscess surgical procedures support the theory of less adhesion formation formation at the time of appendectomy) were registered. In the LG, with the laparoscopic approach.19 To our knowledge, there is only registration for the performance of a diagnostic laparoscopy (leav- one randomized clinical trial comparing adhesion formation between ing the appendix in place), a complete laparoscopic operation, or a laparoscopy and laparotomy evaluated at second-look surgery.21 This conversion to open appendectomy was performed. The number of study, published in 1991 (n = 73), shows significantly fewer adhe- readmissions for each patient and whether the condition was handled sions within the operated site in the LG than in the open surgery conservatively or needed surgical intervention were noted. group, although there was no significant difference for overall adhesion formation even if a trend was observed in favor of the LG. Power Calculation and Statistical Analyses The possible superior role of laparoscopic surgery for acute The hypothesis was that the incidence of patients having symp- appendicitis and subsequent SBO has not been clearly demon- toms of SBO would be lower in the LG. The incidence of symptoms strated in a cohort of adult patients. In a fairly recent review by of SBO was assumed to be 1.2% after open appendectomy, based on Schnuriger¨ et al,22 the laparoscopic technique was found to result previous studies. To prove a 50% reduction in the LG, a total of 1655 in fewer adhesion-related readmissions than the open technique patients in each group were needed with a statistical power of 80% for several abdominal operations, although with the exception of and a risk of 5% inaccuracy. To calculate for differences between the appendectomies. The decreased incidence of SBO after laparoscopic groups, the Fisher exact test, the χ 2 test, the independent t test, and appendectomy has been shown previously in pediatric studies. the Wilcoxon rank-sum test were used. Pearson bivariate correlation Tsao et al13 concluded that SBO is less common after laparoscopic and multivariate logistic regression analysis were used for calculation appendectomy than after open appendectomy in children. The study

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Study cohort n = 4954

Open group Lap. group n = 2472 n = 2482

Excluded n = 139 Excluded n = 110 Incorrect op code: 92 Incorrect op code: 10 Incomplete/missing chart: 12 Incomplete/missing chart: 21 Extended surgery: 25 Extended surgery: 25 Cancer in appendix: 4 Cancer in appendix: 8 Other: 6 Study: 42 Other: 4

Open group Lap. group n = 2333 n = 2372

FIGURE 1. Flowchart for inclusion. Final cohort Lap. indicates laparoscopic; op, n = 4705 operative.

TABLE 1. Readmitted Patients for SBO TABLE 3. Characteristics for Patients Readmitted for SBO Open Group, Laparoscopic Open Group Laparoscopic n(%) Group, n (%) P (n = 24) Group (n = 10) Total No. 24 (1.0) 10 (0.4) 0.016 Status of appendix Only late SBO (>30 d) 16 (0.7) 7 (0.3) 0.061 Perforated 10 4 Nonperforated 11 6 Normal 3 0 No. SBO episodes TABLE 2. Analysis of Patient Factors on SBO Outcome 1178 ≥272 Univariate Analyses Multivariate Analyses Total No. for the group 39 14 Surgical treatment of SBO, n (%) 13 (54) 5 (50) Factors P Odds Ratio P Odds Ratio 1 operation 11 1 Female sex 0.606 1.25 (0.63–2.48) 2 operations 2 4 Age above median 0.022 2.31 (1.16–4.63) 0.017 2.33 (1.16–4.67) Follow-up time 0.086 1.87 (0.92–3.79) above median Laparoscopic 0.015 0.46 (0.19–0.85) 0.016 0.41 (0.19–0.85) a large, population-based register study that open surgery increased appendectomy the risk of SBO up to 4 times compared with laparoscopic surgery for SBO outcome based on patient factors and the type of operation. Bold values most abdominal surgical procedures, including appendectomy. The 25 indicate statistical significance (P = 0.05). The values in parenthesis indicate the study population was mixed, also including children. 95% confidence interval. 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 from Tsao et al, however, had a statistically larger proportion of years’ follow-up, Andersson16 showed a cumulative risk of 0.63% perforated appendicitis in the OG, partly explaining the difference for surgical treatment of SBO 1 year after open appendectomy and in postoperative SBO. Another pediatric study from Kasela et al23 1.3% after 30 years. In the study by Tingstedt et al,14 the incidence reported a significantly lower incidence of SBO after laparoscopic of assumed SBO of 1.54% after open appendectomy was reported appendectomy than after the open approach. In this study, the severity and 0.84% of all patients with appendectomy had to undergo surgical of the appendicitis did not contribute to the incidence of SBO. treatment of SBO during a follow-up time period of more than 10 The corresponding benefit in adult patients has not been clearly years. The patients in the last 2 referred studies underwent appen- demonstrated. Leung et al24 concluded that there was no statistically dectomy between 1964 and 1993, and 1981 and 1996, respectively. significant difference in the incidence of SBO in adults when com- In our study, the patients included had their index operation during a paring laparoscopic with open appendectomy, a finding supported later time period (ie, between 1992 and 2007). This could be a part by Kouhia et al7 and Swank et al.9 These studies are most probably of the explanation to the lower readmission rate for SBO seen after underpowered. However, Angenete et al25 recently demonstrated in open appendectomy in our study.

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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 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 al- ready well-documented beneﬁts such as shorter hospital stay, fewer FIGURE 2. Strong adhesions between small bowel and abdom- wound infections, postoperative pain, and the possibility of explor- inal wall in the area of previous open appendectomy, the cause ing other possible diagnosis and leaving a nonaffected appendix in of SBO in this case (Photograph courtesy: Dr Tingstedt). place, we recommend the laparoscopic technique to be the preferable approach in adults with suspected appendicitis.

Open appendectomy was identiﬁed as an independent risk fac- ACKNOWLEDGMENTS tor for SBO in our study. With time, surgeons have become more The authors thank E. Bergman, L. Hermansson, S. Larsson, aware of the importance of a more atraumatic surgical approach, in- and A. Traunsberger for their great help with the chart review process. cluding handling of the tissue and the importance of hemostatic con- trol, which are well-known risk factors for adhesion formation. The REFERENCES removal of starch-powdered gloves, known to facilitate adhesions,26 1. Graff L, Russell J, Seashore J, et al. False-negative and false-positive errors in is also a possible factor of contributing to postoperative SBO. Previ- abdominal pain evaluation: failure to diagnose acute appendicitis and unnec- ous studies have declared that the risk of SBO after appendectomy essary surgery. Acad Emerg Med. 2000;7:1244–1255. 2. Addiss DG, Shaffer N, Fowler BS, et al. The epidemiology of appendicitis and is higher if the appendix is either perforated or normal. Findings of appendectomy in the United States. Am J Epidemiol. 1990;132:910–925. a normal appendix demands a further exploration of the distal part 3. Flum DR, Morris A, Koepsell T, et al. Has misdiagnosis of appendicitis de- of the small bowel, exploring other possible diagnoses, and this may creased over time? A population-based analysis. JAMA. 2001;286:1748–1753. be associated with increased tissue trauma promoting adhesions in 4. Semm K. Endoscopic appendectomy. Endoscopy. 1983;15:59–64. open surgery. The number of macroscopically normal appendices at 5. Moberg AC, Montgomery A. Appendicitis: laparoscopic versus conventional exploration has gradually decreased over time because of more strict operation: a study and review of the literature. Surg Laparosc Endosc. operative indications after repeated bedside assessments in combina- 1997;7:459–463. tion with laboratory sampling and more frequent use of preoperative 6. Golub R, Siddiqui F, Pohl D. Laparoscopic versus open appendectomy: a radiological examinations.27 This could, in part, be an explanation for metaanalysis. J Am Coll Surg. 1998;186:545–553. 7. Kouhia ST, Heiskanen JT, Huttunen R, et al. Long-term follow-up of a ran- older age as an independent risk factor. Patients operated on early in domized clinical trial of open versus laparoscopic appendicectomy. Br J Surg. the study were probably submitted to more extensive exploration as 2010;97:1395–1400. depicted earlier, although subgroup analysis of SBO versus operation 8. Sauerland S, Jaschinski T, Neugebauer EA. Laparoscopic versus open surgery date did not reach statistic signiﬁcance. In our study, the inclusion of for suspected appendicitis. Cochrane Database Syst Rev. 2010:CD001546. the patients in the LG who had only a diagnostic laparoscopy per- 9. Swank HA, Eshuis EJ, van Berge Henegouwen MI, et al. Short- and long- formed partly explains the low readmission rate in the LG. In the term results of open versus laparoscopic appendectomy. World J Surg. present study, there was a statistical difference in sex distribution, 2011;35:1221–1226; discussion 1227–1228. with more women in the LG, which is in concordance with other 10. Wei B, Qi CL, Chen TF, et al. Laparoscopic versus open appendectomy for 9,28 acute appendicitis: a metaanalysis. Surg Endosc. 2011;25:1199–1208. studies. 11. Moberg AC, Ahlberg G, Leijonmarck CE, et al. Diagnostic laparoscopy in Limitations of a retrospective study should of course be con- 1043 patients with suspected acute appendicitis. Eur J Surg. 1998;164:833– sidered. One is the possibility of missing patients being readmitted 840; discussion 841. for SBO in other hospitals (eg, because of migration). The migration 12. Tingstedt B, Isaksson J, Andersson R. Long-term follow-up and cost analy- in Sweden is relatively low. However, the migration for the population sis following surgery for small bowel obstruction caused by intra-abdominal of the 2 cities enrolled in this study is higher than the average in the adhesions. Br J Surg. 2007;94:743–748. country but similar when compared with each other. The potential 13. Tsao KJ, St Peter SD, Valusek PA, et al. Adhesive small bowel obstruction 29 after appendectomy in children: comparison between the laparoscopic and “loss of patients” would thereby be fairly equal in both groups. open approach. J Pediatr Surg. 2007;42:939–942; discussion 942. Another limitation is the fact that we selected laparoscopic approach 14. Tingstedt B, Johansson J, Nehez L, et al. Late abdominal complaints after in one hospital and open in the other. The difference in the follow- appendectomy—readmissions during long-term follow-up. Dig Surg. 2004; up time between the groups (mean 13.5 years in the OG and 11 in 21:23–27. the LG) can be explained by the increasing number of laparoscopic 15. Ahlberg G, Bergdahl S, Rutqvist J, et al. Mechanical small-bowel obstruction after conventional appendectomy in children. Eur J Pediatr Surg. 1997;7: interventions for suspected appendicitis over time during the study 13–15. period. 16. Andersson RE. Small bowel obstruction after appendicectomy. Br J Surg. The strengths of the study are the large and similar numbers 2001;88:1387–1391. of patients in both groups and the fact that all individual charts were 17. Riber C, Soe K, Jorgensen T, et al. Intestinal obstruction after appendectomy. reviewed, thereby decreasing the risk of incorrect coding, concerning 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 24. Leung TT, Dixon E, Gill M, et al. Bowel obstruction following appendectomy: bowel obstruction following standard, open appendectomy and cholecystec- what is the true incidence? Ann Surg. 2009;250:51–53. tomy: a six-year retrospective cohort study at Yale-New Haven Hospital. Conn 25. Angenete E, Jacobsson A, Gellerstedt M, et al. Effect of laparoscopy on the Med. 1993;57:123–127. risk of small-bowel obstruction: a population-based register study. Arch Surg. 19. Gutt CN, Oniu T, Schemmer P, et al. Fewer adhesions induced by laparoscopic 2012;147:359–365. surgery? Surg Endosc. 2004;18:898–906. 26. Holmdahl L, al-Jabreen M, Xia G, et al. The impact of starch-powdered gloves 20. Moberg AC, Berndsen F, Palmquist I, et al. Randomized clinical trial of la- on the formation of adhesions in rats. Eur J Surg. 1994;160:257–261. paroscopic versus open appendicectomy for conﬁrmed appendicitis. Br J Surg. 27. Tingstedt B, Andersson R. Improved diagnostic accuracy in patients with sus- 2005;92:298–304. pected appendicitis. Ann Gastroenterol. 2005;18:65–69. 21. Lundorff P, Hahlin M, Kallfelt B, et al. Adhesion formation after laparoscopic 28. Masoomi H, Mills S, Dolich MO, et al. Comparison of outcomes of la- surgery in tubal pregnancy: a randomized trial versus laparotomy. Fertil Steril. paroscopic versus open appendectomy in adults: data from the Nation- 1991;55:911–915. wide Inpatient Sample (NIS), 2006–2008. J Gastrointest Surg. 2011;15: 22. Schnuriger¨ B, Barmparas G, Branco BC, et al. Prevention of postoperative 2226–2231. peritoneal adhesions: a review of the literature. Am J Surg. 2011;201:111– 29. Statistiska Centralbyran˚ S. Available at http://www.scb.se. Accessed September 121. 30, 2012. 23. Kaselas C, Molinaro F, Lacreuse I, et al. Postoperative bowel obstruction 30. Wilson MS, Hawkswell J, McCloy RF. Natural history of adhesional after laparoscopic and open appendectomy in children: a 15-year experience. small bowel obstruction: counting the cost. Br J Surg. 1998;85:1294– J Pediatr Surg. 2009;44:1581–1585. 1298.

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