Are There Specific Indications for Laparoscopic Appendectomy? A Review and Critical Appraisal of the Literature

Abstract

Introduction:

Laparoscopic appendectomy (LA) has proven to be a feasible alternative to open appendectomy (OA). However, as some of the purported advantages of LA (versus OA) are marginal, evidence is accumulating that appendectomy may not be necessary for uncomplicated appendicitis and there is concern about using laparoscopy for all patients with suspected acute appendicitis. In spite of widespread popularity and use, the literature reporting the indications is sparse and sometimes misleading (i.e., containing distorted deductions or conclusions, also called “spin”). This study aimed to determine subsets of patients for whom LA may present real advantages over OA and to analyze the validity of specific indications for LA (instead of OA).

Materials and Methods:

A systematic review and critical analysis of the literature were conducted.

Results:

We analyzed 90 retrospective reviews, prospective studies, meta-analyses, and cohort and prospective randomized studies, presenting a total of approximately 390,000 patients, concerning potentially specific advantages of LA in the elderly, the obese, during pregnancy, and complicated appendicitis, including diffuse peritonitis and ectopic appendices. Overall, LA was associated with (1) lower overall complication rates (and notably less decompensated comorbidities), mortality, and costs, as well as shorter duration of hospital stay, in the elderly, (2) decreased morbidity (notably parietal) in the obese, and (3) potential (diagnostic) advantages in pregnancy (even though LA is associated with a higher rate of fetal loss than in OA). In complicated or ectopic appendicitis, LA is feasible and safe and, if performed without conversion, should lead to less short- and long-term parietal morbidity. However, published data are very heterogeneous, there are few sound controlled trials, and conclusions found in the literature are often based on misleading deductions or a very low level of evidence.

Conclusions:

LA is a safe and effective method to treat acute appendicitis in specific settings such as the elderly and the obese, as well as in ectopic appendices, with potentially specific parietal advantages in these subsets of patients. Further randomized studies and robust meta-analyses are necessary before recommending LA for complicated appendicitis and peritonitis, as well as in pregnancy.

Introduction

Acute appendicitis is the most frequent surgical abdominal emergency. Laparoscopic appendectomy (LA) has been shown to be a feasible alternative to open appendectomy (OA)^1–4 and is widely practiced and touted as a teaching tool.^5–7

The established advantages of laparoscopy over open surgery (less postoperative pain, faster recovery, fewer surgical-site infections [SSIs]) seem marginal as concerns LA^1,2 and contrast with often neglected disadvantages, both general (higher learning curve, more expensive equipment) and specific (potentially higher incidence of intraperitoneal postoperative abscess in complicated appendicitis,^8,9 higher direct costs^10,11), which are reasons why LA is not yet considered the gold standard by all and for all cases of appendicitis.^5,12 Indeed, although good practice teaching states that the indications for LA should be the same as for OA,¹³ several authors have questioned the use of laparoscopy for every patient presenting with a picture of acute appendicitis.^2,14,15 There is accumulating evidence that appendectomy might not be necessary for all patients with suspected appendicitis,¹⁶ and at least two controlled randomized trials have shown that LA offered no advantages over OA in men.^17,18 Moreover, LA for uncomplicated appendicitis, as a teaching tool, is fraught with increased operative times and therefore, again, increased costs,¹⁰ as well as more postoperative complications,¹⁹ and certainly should be examined more scientifically. Last, published data are very heterogeneous, with few sound controlled trials on the precise indications for LA,^4,5 and conclusions often based on misleading inferences or deductions (“spin”) or very low level of evidence.

This article aims to determine the patients and/or situations in which LA might well have specific advantages, potentially suggesting the minimal access route as the true gold standard in these specific settings, as based on a critical analysis of the existing literature. We specifically investigated the indications for LA in the elderly, in the obese, during pregnancy, in the immunocompromised patient, in patients with complicated appendicitis including diffuse peritonitis, or in those with ectopic appendices, as opposed to routine use of LA for all patients with acute appendicitis.^15,16

Materials and Methods

A systematic search of the scientific literature was performed using the Medline, Thompson, and Scopus listings for the years 1994–2015 to obtain access to all publications, focusing on randomized controlled trials, systematic reviews, and meta-analyses involving the advantages of LA over OA. The search strategy was that described by Dickersin et al.²⁰ and Tumber and Dickersin.²¹ Terms used in this study included “laparoscopic appendectomy,” “appendicectomy,” “elderly,” “obese,” “pregnancy,” “immunocompromised,” “peritonitis,” “diagnosis,” “costs,” “surgical site infections (SSI),” “intra-abdominal infections,” “organ space infections (OSI),” “controlled trials,” and “reviews.”

Definitions

The elderly were defined as patients 65 years of age or older. The obese were patients with a body mass index of ≥30 kg/m². “Spin” was defined as “inappropriate interpretation (of the writer) and/or discussion in reporting that could distort the interpretation of results (by the reader) and mislead readers, or concluding equivalence between surgical techniques based on nonsignificant differences or claiming improved benefits, despite nonsignificance.”²²

Results

We analyzed 90 publications: 12 retrospective reviews, 28 retrospective studies, 3 case series, 1 population study, 1 editorial, 18 prospective studies, 1 cohort study, 3 prospective double-blind randomized trials, 4 meta-analyses, and 2 guidelines, which included a total of approximately 390,000 patients. Seventeen articles specifically concerned the elderly, 13 the obese, 2 the immunocompromised, 7 complicated appendicitis, 17 pregnancy, and 13 costs.

Analysis of the literature

The elderly

Studies on the elderly included administrative databases,^23–25 a prospective study,²⁶ a literature review,¹⁵ and a meta-analysis.²⁷ There were no randomized studies.

At least four studies concluded that LA yielded lower overall morbidity, shorter duration of hospital stay, less in-hospital mortality, and fewer superficial SSIs,^23–26 leading to lower mean hospital charges ($43,339 versus $57,943; P < .01).^23,24 Of note, LA did not increase any of the comorbidity risks associated with surgery.^15,23,24

According to the meta-analysis²⁷ analyzing six (five retrospective and one prospective) studies (15,852 appendectomies: 4398 laparoscopic and 11,454 open), LA was associated with statistically significant decreased postoperative mortality (pooled odds ratio [OR] = 0.24; 95% confidence interval [CI], 0.15–0.37), postoperative complications (pooled OR = 0.61; 95% CI, 0.50–0.73), and length of hospital stay (weighted mean difference, −0.51 days; 95% CI, −0.64 to −0.37 days) (P < .05 for all). No significant group differences were found in operative time, postoperative wound infection, or intraabdominal collections, leading the authors to recommend LA for the elderly.

The obese

Studies included prospective randomized studies,^28,29 a retrospective study,³⁰ administrative databases,^31,32 and a meta-analysis.⁹

Mason et al.,³¹ analyzing the American College of Surgeons National Surgical Quality Improvement Program (NSQIP) database (2005–2009), identified 13,330 obese patients who underwent an appendectomy (78% LA, 22% OA). Multivariable risk-adjusted analysis showed that LA was associated with a 57% reduction in overall morbidity (OR = 0.43; 95% CI, 0.36–0.52; P < .0001) and a 53% reduction in risk in the matched cohort analysis (2228 patients matched for their baseline characteristics and 41 preoperative covariates; OR = 0.47; 95% CI, 0.32–0.65; P < .0001). Mortality rates did not differ significantly. The authors concluded that in obese patients, LA had superior clinical outcomes versus OA after accounting for preoperative risk factors.³¹ Senekjian and Nirul,³² in a population-based study from the same database, found that obesity had an adverse effect on the rate of SSI, in both OA and LA. Although LA was associated with a lower probability of SSI overall, the risk of OSI was greater for LA.

A 2012 meta-analysis identified seven (four retrospective and three prospective) randomized studies that concluded there was a 50% reduction in morbidity and 66% reduction in SSI in favor of LA, without increasing the intraabdominal abscess (OSI) rate.⁹

Shorter duration of hospital stay has been reported in most of the studies.^30,31

Pregnancy

The Society of American Gastrointestinal and Endoscopic Surgeons (SAGES) guideline states that LA can be safely performed in any trimester of the pregnancy.³³ Four other small series have shown that LA is feasible and safe (with a low rate of complications).^34–37 A recent meta-analysis including 11 studies (from 1990 to 2011) with a total of 3415 women undergoing appendectomy (599 LA and 2816 OA) found that LA had almost a twofold increased relative risk of fetal loss compared with OA. Conversely, there were no significant differences found for preterm labor, SSI, or duration of operation.³⁸ However, there were no randomized trials included in this meta-analysis.

Immunocompromised patients

Only one publication was found lauding LA for the immunocompromised patient (those receiving immunosuppressive therapy for autoimmune diseases, cancer, and/or AIDS).³⁹ Masoomi et al.³⁹ analyzed 800 patients with AIDS, having both noncomplicated and complicated appendicitis, operated on by the open or the laparoscopic approach. LA was associated with lower morbidity, lower mortality, and shorter length of stay compared with OA, in both complicated and noncomplicated appendicitis. The authors concluded that LA should be the operation of choice in human immunodeficiency virus–positive patients.³⁹

Complicated appendicitis including diffuse peritonitis

At least six nonrandomized studies comparing LA with OA for complicated appendicitis were found and analyzed: data were very heterogeneous in terms of type of study, number of patients, and surgical team experience.^40–46 The meta-analysis of these nonrandomized studies⁴⁶ was in favor of LA because of fewer SSIs, backed by a Level of Evidence of 3a. The only randomized trial on this topic was published recently.⁴⁷ Although the authors published the outcome before the number of patients was attained, they concluded that LA for complicated appendicitis (defined as localized right iliac fossa peritonitis or diffuse abdominal peritonitis) was at least as safe as OA, with statistically significantly fewer SSIs. Of note is that there was no statistically significant difference found in the OSI rate (P = .08) or duration of operation. The degree of infection did not affect the duration of operation.

Senekjian and Nirula³² (in a population-based study from the NSQIP database, of which 9998 of 61,830 LA procedures performed were for complicated [generalized peritonitis or intraperitoneal abscess]) appendicitis, found that LA was associated with a lower probability of SSI but that the risk of OSI was greater for LA in both noncomplicated (notably when the body mass index is >37.5 kg/m²) and complicated (when the white blood cell count is <12,000/mL) appendicitis.²³

Discussion

Of note is that most uncomplicated cases of acute appendicitis can be treated through a single (open) 15–20-mm incision in the right iliac fossa.^14,16,48 Specific elective indications in the literature for the laparoscopic approach being better than the open counterpart are lacking or not based on sound studies. LA seems to be better for the elderly and the obese. As concerns complicated appendicitis, laparoscopy seems safe; trends can be found as to advantages, but the level of evidence is low. More studies are necessary before conclusion can be made in pregnancy and the immunocompromised patient.

Specific indications

The elderly

As the lifespan increases worldwide, the proportion of patients over 65 years of age undergoing surgery rises as well; it has been projected that this will represent 20% of the U.S. population in 2030.⁴⁹ The rates of perforated appendicitis have been reported to be twice as high in the elderly (50 versus 25%; P < .01).²³ Yet, some surgeons still prefer OA over LA for the elderly compared with patients younger than 65 years old.²³ Of note, however, according to Masoomi et al.,²³ is that the use of LA increased from 46.5% in 2006 to 57.8% in 2008 in the elderly (P < .01) and represented 72% in the American College of Surgeons NSQIP study.²⁵ The three administrative database studies all seemed to favor LA.^23–25 Creditor⁵⁰ has outlined that less postoperative pain and earlier mobilization, obtained more easily with LA, are especially important in the elderly, limiting falls, nosocomial infections, and decompensation of comorbidity. A cross-sectional analysis of patients undergoing OA or LA in the U.S. Nationwide Inpatient Sample including 257,484 patients concluded that LA was associated with shorter length of stay (4.44 days versus 7.86 days; P < .01), fewer total patient safety indicator events (1.8% versus 3.5%; P < .001), and a decreased mortality rate (0.9% versus 2.8%; P < 0.001; on multivariate analysis, the authors observed a 32% decreased probability of safety events in favor of LA.⁵¹

The obese

Although reputed by some early reports to be more difficult, the laparoscopic approach has obvious advantages in obese patients as concerns the parietal insult,^{28,30,52–54} and the overall analysis points to the laparoscopic approach as the preferred route of access for appendectomy in the obese, especially in complicated cases.^30–32

As access to the abdominal cavity can be limited through a classical gridiron (McBurney) incision, especially in the patient with complicated or ectopic appendicitis, laparoscopy can be an interesting alternative to extending the McBurney incision or resorting to a midline laparotomy in this setting.⁴⁸

Delaney et al.⁵³ have shown that obese patients undergoing traditional open surgical procedures incur larger wounds, more postoperative pain, and more pulmonary morbidity and did not regain mobility as easy as nonobese patients.

Although the study by Clarke et al.²⁸ concluded “laparoscopic appendectomy did not show a benefit over the open approach for obese patients with appendicitis,” this conclusion, however, was based on subgroup analysis and therefore constitutes another example of “spin.”^22,54

Pregnancy

Basing surgical decisions on the meta-analysis by Wilasrusmee et al.³⁸ raises concerns as to the feasibility and safety of LA on one hand, and the increased risk of fetal loss, on the other, because one study⁵⁵ enrolled 3133 pregnant women (87% of the total population in the meta-analysis), strongly affecting the overall results. There were no randomized studies included. Therefore, we need more homogeneous studies, better descriptions of the disease, and results from experienced teams; for the time being, the decision in favor of LA versus OA should be made according to surgeons' laparoscopic expertise and the complexity of the case.

Special details of LA during pregnancy have been described and include taking into account the expected date of delivery, uterine height, and comorbidities.^34,35

Complicated appendicitis

The laparoscopic approach in complicated appendicitis is still a subject of discussion. In order to avoid postoperative complications, special attention should be paid to the complexity of adhesiolysis and peritoneal lavage in the Douglas pouch, pericecal space, hepatophrenic space, and infrahepatic space.^33,56,57 One potential advantage of laparoscopy is that it should allow a better view of the entire peritoneal cavity and of all the spaces without the necessity of extending the incision, or opting for a midline incision if a complication is found or an anatomic variation (ectopic appendix) is discovered.^41,48 In cases with difficult access to an ectopic appendix (retrocecal, subhepatic, or mesoceliac) or limited mobility of the cecum or discovery of peritonitis, conversion from a small right iliac fossa incision⁴⁸ to laparoscopy (coined “reversed conversion” by Schrenk et al.⁴⁶ and developed by Navez et al.⁴³ is an alternative that is in line with authors who state that not every patient with appendicitis should undergo LA.^2,14,48

One of the most reported downsides of LA has been the seemingly higher rate of deep OSIs, especially in complicated cases.^1,14,32 Several recent articles have tried to shed light on this matter.^44,56,57 Thereaux et al.⁵⁶ published a series of 141 patients operated on for diffuse appendicular peritonitis via laparoscopy; the conversion rate was 3.5% (5 patients), whereas 7.1% (10 patients) sustained postoperative deep OSI, 7 of whom were treated percutaneously. Fukami et al.⁵⁷ reported that of 39 patients undergoing LA for perforated appendicitis, none required conversion, and there were no postoperative deep OSIs. In the only randomized controlled trial on complicated appendicitis, Thomson et al.⁵⁸ asserted that LA was at least as safe as OA in complicated appendicitis, with no difference in the rate of OSI, as underlined in the meta-analysis by Markides et al.⁴⁷

All in all, although the conclusions are controversial, the more recent studies with experienced laparoscopic surgeons have not been able to find any statistically significant differences in terms of postoperative deep OSI.^44–47

Critical analysis

There are several general criticisms of the literature on which indications for LA are based, criticisms that should be disclosed in order to understand that LA is not indicated for all.

First, many of the recommendations and indications in the literature stem from databases, rather than from randomized trials.^{23–25,31,32} Databases have some inherent biases: (1) there is no way of knowing how patients were selected for one or the other approach as the relative decisions for LA versus OA were made by individual surgeons before being captured by the administrative data. It is therefore possible that sicker patients or those with previous operations were selected for the open approach.³² (2) The postoperative follow-up in databases usually does not cover more than in-hospital stay. (3) Databases do not evaluate postoperative features such as pain or cosmesis.^32,59 (4) Indications coming from databases derive from analysis and comparison of various subgroups in the specific setting of the database and therefore may not reflect the overall population.^28,59

Second, other recommendations and indications are based on inappropriate methodology or misleading⁶⁰ or incomplete information, categorized as “spin,”^22,54 and often based on subgroup analysis,^28,29 retrospective studies,⁵² or even personal beliefs, camouflaged as “evidence.”⁵⁴

Third, many indications in the current literature are based on meta-analyses of nonrandomized trials. Meta-analyses were originally meant to quantify effects found in the literature using only randomized trials, but this is no longer necessarily true.⁶¹ The quality of meta-analyses depends on the quality of the associated systematic review.⁶² Moreover, meta-analyses should comply with the PRISMA guidelines and be planned according to a strict protocol.⁶³ Although the methodology for meta-analysis of nonrandomized epidemiology studies has been described,⁶⁴ these meta-analyses lack robustness and, in the absence of associated multivariate analysis, lack causality. Several meta-analyses^9,38,47 included studies with different levels of evidence, mixing nonrandomized, retrospective and prospective studies, making it difficult to eliminate biases^9,27 and limiting any inference of causality.²⁷

Fourth, many publications have cited duration of hospital stay as an argument in favor of LA.^25,30,52 Duration of hospital stay is known to be dependent on local settings, traditions, and also the underlying pathology.⁵²

Last, another weakness of many of the studies discussed above is that LAs converted to open procedures are not always correctly included in the analysis of indications and therefore may include patients with complex abdomens, a midline incision as opposed to a McBurney incision, or longer operative times.⁵²

In conclusion, as the benefits of LA appear to be marginal for uncomplicated appendicitis (in the nonobese, nonpregnant woman), the advantages of the minimal access obtained by laparoscopy could potentially be proposed to the obese, appendicitis complicated by abscess or peritonitis, or when a small right iliac fossa incision is insufficient to treat an ectopic and/or complicated appendicitis, especially in the obese, and the elderly, where the advantages of the laparoscopic approach seem most positive and in whom long incisions are not well tolerated and/or desirable and the short- and long-term parietal benefits seem promising. It is therefore capital that conversion be kept to a minimum, which implies that these patients should be under the care of surgeons with the necessary experience and expertise.

However, these recommendations warrant caution. The literature abounds with heterogeneity of patients with acute appendicitis (with an apparent selection bias to the experience of the operating team) and the variability of laparoscopic experience of the operating teams. Surgeons who have better and extensive experience in laparoscopic surgery can obtain better results with LA than with OA. Many studies exhibit “spin.”

Further randomized studies and meta-analyses according to each of these specific settings are necessary before recommending LA in these subgroups.

Another issue for the future would be to determine whether LA should play a role in day surgery care. Preferring laparoscopic surgery over traditional surgery in the daycare setting remains to be shown to be more cost-effective in a robust comparative study.

Footnotes

Disclosure Statement

No competing financial interests exist.

References

Sauerland

, Agresta

, Bergamaschi

, Borzellino

, Budzynski

, Champault

, et al. Laparoscopy for abdominal emergencies: Evidence-based guidelines of the European Association for Endoscopic Surgery. Surg Endosc, 2006; 20:14–29.

Sauerland

, Neugebauer

. Laparoscopy for every acute appendicitis? The authors reply. Surg Endosc, 2007; 21:342.

Ingraham

, Cohen

, Bilimoria

, Pritts

, Ko

, Esposito

. Comparison of outcomes after laparoscopic versus open appendectomy for acute appendicitis at 222 ACS NSQIP 502 hospitals. Surgery, 2010; 148:625–635.

Jaschinski

, Mosch

, Eikermann

, Neugebauer

EAM

. Laparoscopic versus open appendectomy in patients with suspected appendicitis: A systematic review of meta-analyses of randomised controlled trials. BMC Gastroenterol, 2015; 15:48.

Vettoretto

, Gobbi

, Belli

, Corradi

, Mannino

, Ricciardelli

, Vinciguerra

, Piccolo

; Young Surgeons' Committee, Italian Association of Hospital Surgeons. Diffusion of laparoscopic appendectomies in Italy: A national audit. Minim Invasive Ther Allied Technol, 2012; 21:101–107.

Van Hove

, Hardiman

, Diggs

, Deveney

, Sheppard

. Demographic and socioeconomic trends in the use of laparoscopic appendectomy from 1997 to 2003. Am J Surg, 2008; 195:580–584.

Nguyen

, Zainabadi

, Mayandadi

, Paya

, Stevens

, Root

, Wilson

. Trends in utilization and outcomes of laparoscopic versus open appendectomy. Am J Surg, 2004; 188:813–820.

Lim

, Ahn

, Kim

, Chung

, Park

, Choi

. A clinical comparison of laparoscopic versus open appendectomy for complicated appendicitis. J Korean Soc Coloproctol, 2011; 27:293–297.

Woodham

, Cox

, Eslick

. Evidence to support the use of laparoscopic over open appendicectomy for obese individuals: A meta-analysis. Surg Endosc, 2012; 26:2566–2570.

10.

Cothren

, Moore

, Johnson

, Moore

, Ciesla

, Burch

. Can we afford to do laparoscopic appendectomy in an academic hospital?. Am J Surg, 2005; 190:950–954.

11.

McGrath

, Buckius

, Grim

, Bell

, Ahuja

. Economics of appendicitis: Cost trend analysis of laparoscopic versus open appendectomy from 1998 to 2008. J Surg Res, 2011; 171:161–168.

12.

Kocherling

, Schug-Pass

, Grund

. Laparoscopic appendectomy. The new standard?. Chirurg, 2009; 80:594–601.

13.

Loury

, Hong

. Appendicitis and appendiceal abscess. In: Fischer

, et al. (eds). Mastery of Surgery, 5th ed. Philadelphia: Lippincott Williams & Wilkins, 2007, p. 1436.

14.

Slim

, Chipponi

. Laparoscopy for every acute appendicitis?. Surg Endosc, 2006; 20:1785–1786.

15.

Gorter

, Heij

, Eker

, Kazemier

. Laparoscopic appendectomy: State of the art. Tailored approach to the application of laparoscopic appendectomy?. Best Pract Res Clin Gastroenterol, 2014; 28:211–224.

16.

Livingston

, Vons

. Treating appendicitis without surgery. JAMA, 2015; 313:2327–2328.

17.

Mutter

, Vix

, Bui

, Evrard

, Tassetti

, Breton

, Marescaux

. Laparoscopy not recommended for routine appendectomy in men: Results of a prospective randomized study. Surgery, 1996; 120:71–74.

18.

Tzivaras

, Baloyiannis

, Kouritas

, Symeonidis

, Spyridakis

, Tepetes

, Zacharoulis

. Laparoscopic versus open appendectomy in men: A prospective randomized trial. Surg Endosc, 2010; 24:2987–2992.

19.

Advani

, Ahad

, Gonczy

, Markwell

, Hassan

. Does resident involvement effect surgical times and complication rates during laparoscopic appendectomy for uncomplicated appendicitis? An analysis of 16,849 cases from the ACS-NSQIP. Am J Surg, 2012; 203:347–352.

20.

Dickersin

, Scherer

, Lefebvre

. Identifying relevant studies for systematic reviews. BMJ, 1994; 309:1286–1291.

21.

Tumber

, Dickersin

. Publication of clinical trials: Accountability and accessibility. J Int Med, 2004; 256:271–283.

22.

Boutron

, Dutton

, Ravaud

, Altman

. Reporting and interpretation of randomized controlled trials with statistically nonsignificant results for primary outcomes. JAMA, 2010; 303:2058–2064.

23.

Masoomi

, Mills

, Dolich

, Ketana

, Carmichael

, Nguyen

, Stamos

. Does laparoscopic appendectomy impart an advantage over open appendectomy in elderly patients?. World J Surg, 2012; 36:1534–1539.

24.

Wang

, Yang

, Chung

, Jeng

, Chen

. Laparoscopic appendectomy in the elderly. Surg Endosc, 2006; 20:887–889.

25.

Moazzes

, Mason

, Katkouda

. Thirty-day outcomes of laparoscopic versus open appendectomy in elderly using ACS/NSQIP database. Surg Endosc, 2013; 27:1061–1071.

26.

Kim

, Fleming

, Gunzler

, Messing

, Salloum

, Monson

JRT

. Laparoscopic appendectomy is safe and efficacious for the elderly: An analysis using the National Surgical Quality Improvement Project database. Surg Endosc, 2011; 25:1802–1807.

27.

Southgate

, Vousden

, Karthikesalingam

, Markar

, Black

, Zaidi

. Laparoscopic vs open appendectomy in older patients. Arch Surg, 2012; 147:557–562.

28.

Clarke

, Katkhouda

, Mason

, Cheng

, Olasky

, Sohn

, Moazzez

, Algra

, Chaghouri

, Berne

. Laparoscopic versus open appendectomy for the obese patient: A subset analysis from a prospective, randomized, double-blind study. Surg Endosc, 2011; 25:1276–1280.

29.

Enochsson

, Hellberg

, Rudberg

, et al. Laparoscopic vs open appendectomy in overweight patients. Surg Endosc, 2001; 15:387–392.

30.

Tam-Tam

, Yorke

, Wasdell

, Barcan

, Konkin

, Blair

. The benefits of laparoscopic appendectomies in obese patients. Am J Surg, 2012; 203:609–612.

31.

Mason

, Moazzez

, Moroney

, Katkhouda

. Laparoscopic vs open appendectomy in obese patients: Outcomes using the American College of Surgeons National Surgical Quality Improvement Program database. J Am Coll Surg, 2012; 215:88–100.

32.

Senekjian

, Nirula

. Tailoring the operative approach for appendicitis to the patient: A prediction model from National Surgical Quality Improvement Program data. J Am Coll Surg, 2013; 216:34–40.

33.

Korndorffer

Jr , Fellinger

, Reed

. SAGES guideline for laparoscopic appendectomy. Surg Endosc, 2010; 24:757–761.

34.

Lemieux

, Rheaume

, Levesque

, Bujold

, Brochu

. Laparoscopic appendectomy in pregnant patients: A review of 45 cases. Surg Endosc, 2009; 23:1701–1705.

35.

Park

, Park

, Choi

, Lee

, Kim

. Laparoscopic appendectomy performed during pregnancy by gynecological laparoscopists. Eur J Obstet Gynecol Reprod Biol, 2010; 148:44–48.

36.

Chung

, Shin

, Kim

, Song

. Clinical outcomes compared between laparoscopic and open appendectomy in pregnant women. Can J Surg, 2013; 56:341–346.

37.

Kirshtein

, Perry

, Avinoach

, Mizrahi

, Lantsberg

. Safety of laparoscopic appendectomy during pregnancy. World J Surg, 2009; 33:475–480.

38.

Wilasrusmee

, Sukrat

, McEvoy

, Attia

, Thakkinstian

. Systematic review and meta-analysis of safety of laparoscopic versus open appendicectomy for suspected appendicitis in pregnancy. Br J Surg, 2012; 99:1470–1478.

39.

Masoomi

, Mills

, Dolich

, Dang

, Carmichael

, Nguyen

, Stamos

. Outcomes of laparoscopic and open appendectomy for acute appendicitis in patients with acquired immunodeficiency syndrome. Am Surg, 2011; 77:1372–1376.

40.

Ball

, Kortbeek

, Kirkpatrick

, Mitchell

. Laparoscopic appendectomy for complicated appendicitis: An evaluation of postoperative factors. Surg Endosc, 2004; 18:969–973.

41.

Wullstein

, Barkhausen

, Gross

. Results of laparoscopic vs. conventional appendectomy in complicated appendicitis. Dis Colon Rectum, 2001; 44:1700–1705.

42.

Pokala

, Sadhasivam

, Kiran

, Parithivel

. Complicated appendicitis—Is the laparoscopic approach appropriate? A comparative study with the open approach: Outcome in a community hospital setting. Am Surg, 2007; 73:737–741.

43.

Navez

, Delgadillo

, Cambier

, Richir

, Guiot

. Laparoscopic approach for acute appendicular peritonitis: Efficacy and safety. A report of 96 consecutive cases. Surg Laparosc Endosc Percutan Tech, 2001; 11:313–316.

44.

Mancini

, Mancini

, Nelson

Jr , Crass

, Namias

, Haller

Jr , Ballinger

. Efficacy of laparoscopic appendectomy in appendicitis with peritonitis. Am Surg, 2005; 71:1–5.

45.

Stöltzing

, Thon

. Perforated appendicitis: Is laparoscopic operation advisable?. Dig Surg, 2000; 17:610–616.

46.

Schrenk

, Rieger

, Shamiyeh

, Wayand

. Diagnostic laparoscopy through the right lower abdominal incision following open appendectomy. Surg Endosc, 1999; 13:133–135.

47.

Markides

, Subar

, Riyad

. Laparoscopic versus open appendectomy in adults with complicated appendicitis: Systematic review and meta-analysis. World J Surg, 2010; 34:2026–2040.

48.

Fingerhut

. Conversion from open to laparoscopic treatment of peritonitis: “Reversed conversion” revisited. Surg Innov, 2011; 18:5–7.

49.

Vincent

, Velkoff

. The Next Four Decades. The Older Population in the United States: 2010 to 2050. Current Population Reports, Number P25-1138. Washington, DC: U.S. Census Bureau, 2010.

50.

Creditor

. Hazards of hospitalization of the elderly. Ann Intern Med, 1993; 118:219–223.

51.

Ward

, Ramamoorthy

, Chang

, Parsons

. Laparoscopic appendectomy is safer than open appendectomy in an elderly population. JSLS, 2014; 18:e2014.00322.

52.

Corneille

, Steigelman

, Myers

, Jundt

, Dent

, Lopez

, Cohn

, Stewart

. Laparoscopic appendectomy is superior to open appendectomy in obese patients. Am J Surg, 2007; 194:877–881.

53.

Delaney

, Pokala

, Senagore

, et al. Is laparoscopic colectomy applicable to patients with body mass index >30? A case-matched comparative study with open colectomy. Dis Colon Rectum, 2005; 48:975–981.

54.

Fingerhut

, Lacaine

, Cuschieri

. Medical SPIN: Misinformation by another name. Surg Endosc, 2015; 29:1257–1258.

55.

McGory

, Zingmond

, Tillou

, Hiatt

, Ko

, Cryer

. Negative appendectomy in pregnant women is associated with a substantial risk of fetal loss. J Am Coll Surg, 2007; 205:534–540.

56.

Thereaux

, Veyrie

, Corigliano

, Servajean

, Czernichow

, Bouillot

. Is laparoscopy a safe approach for diffuse appendicular peritonitis? Feasibility and determination of risk factors for post-operative intra-abdominal abscess. Surg Endosc, 2014; 28:1908–1913.

57.

Fukami

, Hasegawa

, Sakamoto

, Komatsu

, Hiromatsu

. Value of laparoscopic appendectomy in perforated appendicitis. World J Surg, 2007; 31:93–97.

58.

Thomson

J-E

, Kruger

, Jann-Kruger

, Kiss

, Omoshoro-Jones

JAO

, Luvhengo

, Brand

. Laparoscopic versus open surgery for complicated appendicitis: A randomized controlled trial to prove safety. Surg Endosc, 2015; 29:2027–2032.

59.

Varela

, Hinojosa

, Nguyen

. Laparoscopy should be the approach of choice for acute appendicitis in the morbidly obese. Am J Surg, 2008; 196:218–222.

60.

Clavien

, Puhan

. Biased reporting in surgery. Br J Surg, 2014; 101:591–592.

61.

Haidich

. Meta-analysis in medical research. Hippokratia, 2010; 14(Suppl 1):29–37.

62.

Bailar

. The promise and problems of meta-analysis. N Engl J Med, 1997; 337:559–561.

63.

Moher

, Shamseer

, Clarke

, Ghersi

, Liberati

, Petticrew

, Shekelle

, Stewart

; PRISMA-P Group. Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015 statement. Syst Rev, 2015; 4:1.

64.

Stoup

, Berlin

, Morton

, Olkin

, Williamson

, Rennie

, Moher

, Becker

, Sipe

, Thacker

. Meta-analysis of observational studies in epidemiology. A proposal for reporting. JAMA, 2000; 283:2008–2012.