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Incidental appendectomy? Microscopy tells another story: A retrospective cohort study in patients presenting acute right lower quadrant abdominal pain
International Journal of Surgery 28 (2016) 149e152
Contents lists available at ScienceDirect
International Journal of Surgery journal homepage: www.journal-surgery.net
Original research
Incidental appendectomy? Microscopy tells another story: A retrospective cohort study in patients presenting acute right lower quadrant abdominal pain Dario Tartaglia, Andrea Bertolucci*, Christian Galatioto, Matteo Palmeri, Furbetta, Massimo Chiarugi Gregorio Di franco, Rita Fantacci, Niccolo Emergency Surgery Unit, University of Pisa, Pisa, Italy
h i g h l i g h t s Only 24% of macroscopically normal appendices during laparoscopy for acute lower abdominal pain are histologically normal. The majority of normal-looking appendices showed a catarrhal inflammation without serosa involvement at histology. A 2% of the innocent appendices showed a neuroendocrine tumor leading the patients to receive further treatments. Appendectomy should be performed in all diagnostic laparoscopies for acute lower abdominal pain showing a normal appendix.
a r t i c l e i n f o
a b s t r a c t
Article history: Received 15 December 2015 Received in revised form 17 February 2016 Accepted 22 February 2016 Available online 27 February 2016
Background: Optimal management of macroscopically normal appendix encountered during laparoscopy for acute abdominal pain is still unclear. Methods: 164 acute abdominal pain cases in which laparoscopy showed a normal appendix were reviewed. No other intra-peritoneal acute disease was present in 50 patients (Group 1) whereas a miscellanea of intra-peritoneal conditions was identified in the other 114 (Group 2). All the patients underwent appendectomy with specimen examination. Results: Following incidental appendectomy significant microscopical changes were seen in 125 specimens (76%). Among these, inflammation was found in 122 and neuroendocrine tumors in 3. Appendices harbored pathological changes in n ¼ 45 patients (90%) of Group 1 and in n ¼ 34 patients (70%) of Group 2 patients (p < 0.05). Morbidity for incidental appendectomy was 2%. Conclusion: This study supports an appendectomy in patients who are undergoing laparoscopy for acute right lower quadrant abdominal pain even when the appendix appears normal on visual inspection. © 2016 IJS Publishing Group Limited. Published by Elsevier Ltd. All rights reserved.
Keywords: Abdominal pain Normal appendix Appendicitis Laparoscopic appendectomy
1. Introduction Laparoscopic appendectomy (LA) is one of the most commonly performed acute abdominal surgical operations [1]. Up to 40% of appendices identified during surgery, however, appear macroscopically normal [2,3]. To date, no agreement has been reached as to whether a macroscopically normal appendix found at laparoscopy for acute right lower quadrant abdominal (RLQA) pain should be removed or left in situ.
* Corresponding author. Emergency Surgery Unit, University of Pisa, New Santa Chiara Hospital, Via Paradisa 2, 56124 Pisa, Italy. E-mail address: [email protected] (A. Bertolucci).
A negative appendectomy is not completely risk-free as significant morbidity rates and extended hospital stays have been reported [4,5]. On the other hand, according to the Society of American Gastrointestinal and Endoscopic Surgeons (SAGES), the removal of a normal appendix, after exclusion of other significant diseases, should be considered although in individual clinical scenarios. This choice is based on the observation that a macroscopically normal appendix may harbor abnormal histopathology [6]. Thus, surgery in these cases is addressed against endo-appendicitis rather than appendicitis and it may prevent recurrence of symptoms once the appendix has been left in situ [7e9]. The aim of this study was to analyze the microscopical changes observed in a series of apparently normal appendices removed
http://dx.doi.org/10.1016/j.ijsu.2016.02.085 1743-9191/© 2016 IJS Publishing Group Limited. Published by Elsevier Ltd. All rights reserved.
150
D. Tartaglia et al. / International Journal of Surgery 28 (2016) 149e152
during laparoscopic surgery for acute RLQA pain. 2. Patients and methods A database containing the charts of 1388 patients who underwent laparoscopic appendectomy for acute RLQA pain during the period 2004e2014 was searched. One-hundred-sixty-four patients (20 males and 144 females; median age of 23.4 yrs, range: 4e52) with a macroscopically normal appendix at surgery were identified (Table 1). The appendix was defined as macroscopically normal in absence of hyperemia/necrosis, wall thickness, parietal fibrin deposit and/or peri-appendicular peritoneal fluid effusion. We divided these patients into two groups: Group 1 included 50 patients (30%) who did not present any simultaneous intra-peritoneal disease at laparoscopy; Group 2 comprised 114 patients (70%), in whom digestive tract or gynecological (55%) conditions that could have explained the acute symptoms were identified. As the policy of our institution was to remove a normal-looking appendix whether or not any other abdominal pathology was present, incidental appendectomy was always performed. Senior surgeons assisted surgery and evaluated the recorded procedures on the screen in order to confirm the “normality” of the appendix. Laparoscopic surgery was performed with patient supine in the Trendelenburg position and 10 e15 left rotation of the table. After induction of the pneumoperitoneum with an intra-abdominal pressure ranging from 10 to 14 mmHg 3 trocars were inserted. Following laparoscopic exploration of the cavity, the mesoappendix was dissected and blood vessels were secured and divided between clips, bipolar coagulation or staplers. The appendix stump was either stapled or closed with a loop. The specimen was placed in a plastic bag and removed via the umbilical port. The abdominal cavity was then irrigated with saline solution. Appendectomy specimens were prepared and immediately fixed in formalin before transport to the pathology laboratory. Here specimens were sectioned at the tip, the body, and the base and examined by a senior pathologist. Four classes of appendicitis were identified: 1) catarrhal, with the presence of focal mucosa inflammation, 2) phlegmonous, with polymorphonuclear infiltration of the entire appendicular wall without evidence of necrosis, 3) gangrenous with the same characteristics as the former but with necrosis, 4) scleroatrophic with occasional findings of granulation tissue and fibrosis associated with acute and chronic inflammation. The appendix was defined normal when no evidence of phlogosis was found. The main outcome measure of the study was the prevalence of pathological changes in normal-looking appendices. Secondary outcome measures included length of the procedure, postoperative hospital stay and morbidity. This latter parameter was classified according to the Clavien-Dindo Classification [10]. The paper has been worded in line with the STROBE Statement [11]. Data collection and analysis were performed according to the institutional guidelines and to the ethical standards of the Helsinki Declaration.
Table 1 Patients' general and operative data. Total patients F:M (N, %) Median age (range) Etiopathology (N, %)
Operative time (min) Average length stay (days) Morbidity (N, %) Mortality
164 144 (88%): 20 (12%) 23.8 (4e52) No pathologies Digestive causes Gynecological causese 49.24 (20e140) 1.76 (1e5) 3 (2%) 0
Statistical analysis was performed with SPSS software vers. 17 (SPSS, Chicago, Illinois, USA). Comparisons between groups were made using Student's t-test and Fisher's exact test accordingly. Differences were defined statistically significant when p value was <0.05. 3. Results Only 24% (n ¼ 39) of the normal-appearing removed appendices were confirmed to be normal after microscope examination. In the other 125 specimens the pathologist reported catarrhal appendicitis in 109 (66%), phlegmonous appendicitis in 8 (5%), scleroatrophic changes in 5 (3%) and neuroendocrine tumors in 3 (2%) (Table 2). The majority of the catarrhal appendices were characterized by mild or intermediate focal serositis. All the phlegmonous appendices presented intra-parietal phlogosis with leukocyte infiltration of the mucosa and submucosa but not extending to the serosa. In group 2 patients, the appendix appeared normal but other conditions affecting the digestive tract (n ¼ 24, 15%) or the female reproductive system (n ¼ 90, 55%) were detected and managed. Comparison between group 1 and group 2 showed significant differences in the number of normal appendices (5 in Group 1 vs 34 in Group 2, p < 0.05) and the number of those with of catarrhal appendicitis (40 of Group 1 vs 69 of Group 2, p < 0.05). No significant differences were found for the other histological items. (Table 3). The mean operative time was 49 min (range 20e140) with no need to convert to open surgery. There were 3 recorded postoperative complications (2%): two patients presented hyperpyrexia resolved with antibiotic therapy (Grade I Clavien-Dindo Classification) and the last had a transient cutaneous rash due to adverse drug reaction (Grade II Clavien-Dindo Classification). The average hospital stay was 1.76 days (range 1e5 days) (Table 1). 4. Discussion Thanks to the image clarity and magnification provided by laparoscopy, there is an increasing trend, in patients with RLQA pain, to identify a normal looking appendix. In the open appendectomy era, a normal-looking appendix was almost always removed, even if the cause of the pain was located elsewhere in the abdominal cavity. In a recent international survey by Jaunoo et al. among members of the Society of American Gastrointestinal and Endoscopic Surgeons (SAGES), the French Society for Endoscopic Surgery (SFCE), and the Italian Society for Endoscopic Surgery (SICE), 64% to 73% of surgeons affirmed that they would remove a macroscopically normal appendix in patients with right iliac fossa pain. It is believed that the advantages include early diagnosis of neoplasms, removal of endoluminal appendicitis, avoidance of misdiagnosis in acute abdomen patients, and the prevention of acute appendicitis in later life [12]. Phillips et al. argue that the removal of macroscopically normal appendices in patients undergoing laparoscopy for right iliac fossa
Table 2 Histopathology results. 50 (30%) 24 (15%) 90 (55%)
Histological diagnosis
Number (%)
Catarrhal appendix Phlegmonous appendix Scleroatrofic appendix Neuroendocrine tumor Normal appendix
109 8 5 3 39
(66%) (5%) (3%) (2%) (24%)
D. Tartaglia et al. / International Journal of Surgery 28 (2016) 149e152 Table 3 Histopathological differences between Group 1 and Group 2.
Catarrhal appendix Phlegmonous appendix Scleroatrofic appendix Neuroendocrine tumor Normal appendix TOTAL
Group 1 No other disease (%)
Group 2 Other diseases (n %)
p value
40 3 1 1 5 50
69 (61%) 5 (4%) 4 (3%) 2 (2%) 34 (30%) 114
0.0243 0.9617 0.9808 0.9140 0.0109
(80%) (6%) (2%) (2%) (10%)
pain is to be advocated, also in the absence of other explanatory pathologies, considering that the operative time and the incidence of port-site infections do not significantly increase [13]. Some authors suggest the presence of microscopic inflammation in a macroscopically normal appendix so therefore recommend routine appendectomy [14,15]. On the other hand, Champault et al. recommend not removing a macroscopically normal appendix discovered during diagnostic laparoscopy for abdominal pain, considering that only 1.3% of patients with normal appendix found during laparoscopy, underwent surgery for chronic appendicitis within 3 years after the first admission [16]. A low grade histological inflammation of the appendix could be the consequence of intra-operative manipulation of the appendix before appendectomy [3]. In this study, 164 of 1388 patients (12%) who underwent LA for acute RLQA pain presented a macroscopically normal appendix. This rate is comparable with data from other studies [16,17]. However only 24% of macroscopically normal appendices were confirmed to be truly normal after histological examination. Most negative appendectomies were performed in young women (88%); this is related to a diagnostic difficulty in the fertile female with abdominal right pain, which often requires further diagnosis with CT abdomen [18]. Compared to data from studies focusing on patients undergoing only diagnostic laparoscopy without appendectomy for acute RLQA pain, we recorded a lower morbidity rate (1.8% vs. 4.5%) and a shorter hospital stay (1.8 vs. 3 days) [17,19] for appendectomized patients. In our study the majority of normal-looking appendices was shown to be affected by catarrhal inflammation (66%) or by phlegmonous inflammation (5%) on histopathological examination. The serosa was not involved in any of these cases. In other studies the prevalence of endo-appendicitis ranges from 29 to 58% [8,13]. The percentage of appendices with microscopic alterations was significantly higher in Group 1 than in Group 2 (90% vs. 70% respectively), and this may explain acute symptoms in those patients in whom the laparoscopic exploration was negative. However, some pathological changes to the appendix were also found in those patients in whom laparoscopy detected a simultaneous acute abdominal disease. We cannot give any valuable explanation of this observation but in our opinion it represents an indication to perform incidental appendectomy even in these cases. In 3 patients (2%) microscope examination of the innocent appendix showed a neuroendocrine tumor and led to the patients receiving further treatment: these data are comparable with the results reported by Bucher et al. [20]. These appendicular neoplasms are rarely associated with clinical manifestations and are frequently recognized during pathological examination of appendices resected mainly for acute RLQA pain (up to 55%). Despite the fact that laparoscopy is becoming a widely used diagnostic tool in many acute abdominal conditions, the management of a normal appendix found at laparoscopy for right iliac fossa pain remains controversial. Clear guidelines on this issue from
151
international surgical societies are still lacking, so the decision between performing appendectomy or not is mostly left to individual choice. Large multi-center studies focusing on the long-term follow-up of patients who had a normal appendix left in situ after diagnostic laparoscopy may help to build a shared consensus on this topic and are strongly needed. In the meantime, considering the low morbidity, the short hospital stay, and most of all, the by no means negligible rate of appendicular abnormalities found at histological examination, we encourage prophylactic appendectomy in all patients undergoing diagnostic laparoscopy for acute RLQA pain and showing a macroscopically “normal” appendix. Ethical approval Considering that this is a descriptive and retrospective study, no Ethical Approval has been requested. Funding sources No sources of funding to state. Author contribution Dario Tartaglia performed the conception and design of the study. Andrea Bertoucci performed the analysis of the data. Matteo Palmeri performed the analysis of the data. Gregorio Di Franco performed the acquisition of the data. Rita Fantacci performed the acquisition of the data. Furbetta performed the acquisition of the data. Niccolo Christian Galatioto revised the article critically for important intellectual content. Massimo Chiarugi revised the article critically for important intellectual content. Conflicts of interest No conflicts of interest to state. Guarantor Dario Tartaglia, MD, University of Pisa, Italy. Research registration unique identifying number (UIN) Researchregistry781. References [1] D.G. Addis, N. Shaffer, B.S. Fowler, The epidemiology of appendicitis and appendectomy in the United States, Am. J. Epidemiol. 132 (1990) 910e925. [2] R. Marudanayagam, G.T. Williams, B.I. Rees, Review of the pathological results of 2660 appendicectomy specimens, J. Gastroenterol. 41 (2006) 745e749. [3] T. Slotboom, J.T. Hamminga, H.S. Hofker, et al., Intraoperative motive for performing a laparoscopic appendectomy on a postoperative histological proven normal appendix, Scand. J. Surg. 103 (4) (2014) 245e248. [4] O.J. Bakker, P.M. Go, J.B. Puylaert, WerkgroeprichtlijnDiagnostiek en behandeling van acute appendicitis [Guideline on diagnosis and treatment of acute appendicitis: imaging prior to appendectomy is recommended], Ned. Tijdschr. Geneeskd. 154 (2010) A303. [5] C.L. Bijnen, W.T. Van Den Broek, A.B. Bijnen, Implications of removing a normal appendix, Dig. Surg. 20 (2003) 115e121. [6] SAGES guidelines committee, Guidelines for Laparoscopic Appendectomy [SAGES web site], October, 1992. Available at: http://www.sages.org/ publications/guidelines/guidelines-for-laparoscopic-appendectomy/ (accessed April 2009). [7] B. Navez, A. Therasse, Should every patient undergoing laparoscopy for clinical diagnosis of appendicitis have an appendicectomy? Acta Chir. Belg. 103 (2003) 87e89. [8] M. Chiarugi, P. Buccianti, L. Decanini, et al., ‘What you see is not what you get’
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[9]
[10]
[11]
[12]
[13]
D. Tartaglia et al. / International Journal of Surgery 28 (2016) 149e152 a plea to remove a ‘normal’ appendix during diagnostic laparoscopy, Acta Chir. Belg. 101 (2001) 243e245. N. Vettoretto, S. Gobbi, A. Corradi, et al., Italian Association of Hospital Surgeons Consensus conference on laparoscopic appendectomy: development of guidelines, Colorectal Dis. 13 (7) (2011) 748e754. D. Dindo, N. Demartines, P.A. Clavien, Classification of surgical complications, a new proposal with evaluation in a cohort of 6336 patients and results of a survey, Ann. Surg. 240 (2) (2004) 205e213. E.G. Von Elmg, D. Altmanb, M. Eggera, et al., The strengthening the reporting of observational studies in epidemiology (STROBE) statement: guidelines for reporting observational studies, Int. J. Surg. 12 (2014) 1495e1499. S.S. Jaunoo, A.L. Hale, J.P. Masters, et al., An international survey of opinion regarding investigation of possible appendicitis and laparoscopic management of a macroscopically normal appendix, Ann. R. Coll. Surg. Engl. 94 (7) (2012) 476e480. A.W. Phillips, A.E. Jones, K. Sargen, Should the macroscopically normal appendix be removed during laparoscopy for acute right iliac fossa pain when no other explanatory pathology is found? Surg. Laparosc. Endosc. Percutan. Tech. 19 (5) (2009) 392e394.
[14] C.L. Bijnen, W.T. Van Den Broek, A.B. Bijnen, et al., Implications of removing a normal appendix, Dig. Surg. 20 (2) (2003) 115e121. [15] E. Sadot, A. Keidar, R. Shapiro, et al., Laparoscopic accuracy in prediction of appendiceal pathology: oncologic and inflammatory aspects, Am. J. Surg. 206 (5) (2013) 805e809. [16] A. Champault, C. Polliand, P. Mendes da Costa, et al., Laparoscopic appendectomies: retrospective study of 2074 cases, Surg. Laparosc. Endosc. Percutan. Tech. 18 (2) (2008) 168e172. [17] Garlipp B1, G. Arlt, Laparoscopy for suspected appendicitis. Should an appendix that appears normal be removed? Chirurg 80 (7) (2009) 615e621. [18] P.M. Rao, J.T. Rhea, R.A. Novelline, et al., Effect of computed tomography of the appendix on treatment of patients and use of hospital resources, N. Engl. J. Med. 38 (1998) 141e146. [19] W.T. Van den Broek, A.B. Bijnen, P. De Ruiter, et al., A normal appendix found during diagnostic laparoscopy should not be removed, Br. J. Surg. 88 (2) (2001) 251e254. [20] P. Bucher, Z. Mathe, A. Demirag, et al., Appendix tumors in the era of laparoscopic appendectomy, Surg. Endosc. 18 (7) (2004) 1063e1066.
Contents lists available at ScienceDirect
International Journal of Surgery journal homepage: www.journal-surgery.net
Original research
Incidental appendectomy? Microscopy tells another story: A retrospective cohort study in patients presenting acute right lower quadrant abdominal pain Dario Tartaglia, Andrea Bertolucci*, Christian Galatioto, Matteo Palmeri, Furbetta, Massimo Chiarugi Gregorio Di franco, Rita Fantacci, Niccolo Emergency Surgery Unit, University of Pisa, Pisa, Italy
h i g h l i g h t s Only 24% of macroscopically normal appendices during laparoscopy for acute lower abdominal pain are histologically normal. The majority of normal-looking appendices showed a catarrhal inflammation without serosa involvement at histology. A 2% of the innocent appendices showed a neuroendocrine tumor leading the patients to receive further treatments. Appendectomy should be performed in all diagnostic laparoscopies for acute lower abdominal pain showing a normal appendix.
a r t i c l e i n f o
a b s t r a c t
Article history: Received 15 December 2015 Received in revised form 17 February 2016 Accepted 22 February 2016 Available online 27 February 2016
Background: Optimal management of macroscopically normal appendix encountered during laparoscopy for acute abdominal pain is still unclear. Methods: 164 acute abdominal pain cases in which laparoscopy showed a normal appendix were reviewed. No other intra-peritoneal acute disease was present in 50 patients (Group 1) whereas a miscellanea of intra-peritoneal conditions was identified in the other 114 (Group 2). All the patients underwent appendectomy with specimen examination. Results: Following incidental appendectomy significant microscopical changes were seen in 125 specimens (76%). Among these, inflammation was found in 122 and neuroendocrine tumors in 3. Appendices harbored pathological changes in n ¼ 45 patients (90%) of Group 1 and in n ¼ 34 patients (70%) of Group 2 patients (p < 0.05). Morbidity for incidental appendectomy was 2%. Conclusion: This study supports an appendectomy in patients who are undergoing laparoscopy for acute right lower quadrant abdominal pain even when the appendix appears normal on visual inspection. © 2016 IJS Publishing Group Limited. Published by Elsevier Ltd. All rights reserved.
Keywords: Abdominal pain Normal appendix Appendicitis Laparoscopic appendectomy
1. Introduction Laparoscopic appendectomy (LA) is one of the most commonly performed acute abdominal surgical operations [1]. Up to 40% of appendices identified during surgery, however, appear macroscopically normal [2,3]. To date, no agreement has been reached as to whether a macroscopically normal appendix found at laparoscopy for acute right lower quadrant abdominal (RLQA) pain should be removed or left in situ.
* Corresponding author. Emergency Surgery Unit, University of Pisa, New Santa Chiara Hospital, Via Paradisa 2, 56124 Pisa, Italy. E-mail address: [email protected] (A. Bertolucci).
A negative appendectomy is not completely risk-free as significant morbidity rates and extended hospital stays have been reported [4,5]. On the other hand, according to the Society of American Gastrointestinal and Endoscopic Surgeons (SAGES), the removal of a normal appendix, after exclusion of other significant diseases, should be considered although in individual clinical scenarios. This choice is based on the observation that a macroscopically normal appendix may harbor abnormal histopathology [6]. Thus, surgery in these cases is addressed against endo-appendicitis rather than appendicitis and it may prevent recurrence of symptoms once the appendix has been left in situ [7e9]. The aim of this study was to analyze the microscopical changes observed in a series of apparently normal appendices removed
http://dx.doi.org/10.1016/j.ijsu.2016.02.085 1743-9191/© 2016 IJS Publishing Group Limited. Published by Elsevier Ltd. All rights reserved.
150
D. Tartaglia et al. / International Journal of Surgery 28 (2016) 149e152
during laparoscopic surgery for acute RLQA pain. 2. Patients and methods A database containing the charts of 1388 patients who underwent laparoscopic appendectomy for acute RLQA pain during the period 2004e2014 was searched. One-hundred-sixty-four patients (20 males and 144 females; median age of 23.4 yrs, range: 4e52) with a macroscopically normal appendix at surgery were identified (Table 1). The appendix was defined as macroscopically normal in absence of hyperemia/necrosis, wall thickness, parietal fibrin deposit and/or peri-appendicular peritoneal fluid effusion. We divided these patients into two groups: Group 1 included 50 patients (30%) who did not present any simultaneous intra-peritoneal disease at laparoscopy; Group 2 comprised 114 patients (70%), in whom digestive tract or gynecological (55%) conditions that could have explained the acute symptoms were identified. As the policy of our institution was to remove a normal-looking appendix whether or not any other abdominal pathology was present, incidental appendectomy was always performed. Senior surgeons assisted surgery and evaluated the recorded procedures on the screen in order to confirm the “normality” of the appendix. Laparoscopic surgery was performed with patient supine in the Trendelenburg position and 10 e15 left rotation of the table. After induction of the pneumoperitoneum with an intra-abdominal pressure ranging from 10 to 14 mmHg 3 trocars were inserted. Following laparoscopic exploration of the cavity, the mesoappendix was dissected and blood vessels were secured and divided between clips, bipolar coagulation or staplers. The appendix stump was either stapled or closed with a loop. The specimen was placed in a plastic bag and removed via the umbilical port. The abdominal cavity was then irrigated with saline solution. Appendectomy specimens were prepared and immediately fixed in formalin before transport to the pathology laboratory. Here specimens were sectioned at the tip, the body, and the base and examined by a senior pathologist. Four classes of appendicitis were identified: 1) catarrhal, with the presence of focal mucosa inflammation, 2) phlegmonous, with polymorphonuclear infiltration of the entire appendicular wall without evidence of necrosis, 3) gangrenous with the same characteristics as the former but with necrosis, 4) scleroatrophic with occasional findings of granulation tissue and fibrosis associated with acute and chronic inflammation. The appendix was defined normal when no evidence of phlogosis was found. The main outcome measure of the study was the prevalence of pathological changes in normal-looking appendices. Secondary outcome measures included length of the procedure, postoperative hospital stay and morbidity. This latter parameter was classified according to the Clavien-Dindo Classification [10]. The paper has been worded in line with the STROBE Statement [11]. Data collection and analysis were performed according to the institutional guidelines and to the ethical standards of the Helsinki Declaration.
Table 1 Patients' general and operative data. Total patients F:M (N, %) Median age (range) Etiopathology (N, %)
Operative time (min) Average length stay (days) Morbidity (N, %) Mortality
164 144 (88%): 20 (12%) 23.8 (4e52) No pathologies Digestive causes Gynecological causese 49.24 (20e140) 1.76 (1e5) 3 (2%) 0
Statistical analysis was performed with SPSS software vers. 17 (SPSS, Chicago, Illinois, USA). Comparisons between groups were made using Student's t-test and Fisher's exact test accordingly. Differences were defined statistically significant when p value was <0.05. 3. Results Only 24% (n ¼ 39) of the normal-appearing removed appendices were confirmed to be normal after microscope examination. In the other 125 specimens the pathologist reported catarrhal appendicitis in 109 (66%), phlegmonous appendicitis in 8 (5%), scleroatrophic changes in 5 (3%) and neuroendocrine tumors in 3 (2%) (Table 2). The majority of the catarrhal appendices were characterized by mild or intermediate focal serositis. All the phlegmonous appendices presented intra-parietal phlogosis with leukocyte infiltration of the mucosa and submucosa but not extending to the serosa. In group 2 patients, the appendix appeared normal but other conditions affecting the digestive tract (n ¼ 24, 15%) or the female reproductive system (n ¼ 90, 55%) were detected and managed. Comparison between group 1 and group 2 showed significant differences in the number of normal appendices (5 in Group 1 vs 34 in Group 2, p < 0.05) and the number of those with of catarrhal appendicitis (40 of Group 1 vs 69 of Group 2, p < 0.05). No significant differences were found for the other histological items. (Table 3). The mean operative time was 49 min (range 20e140) with no need to convert to open surgery. There were 3 recorded postoperative complications (2%): two patients presented hyperpyrexia resolved with antibiotic therapy (Grade I Clavien-Dindo Classification) and the last had a transient cutaneous rash due to adverse drug reaction (Grade II Clavien-Dindo Classification). The average hospital stay was 1.76 days (range 1e5 days) (Table 1). 4. Discussion Thanks to the image clarity and magnification provided by laparoscopy, there is an increasing trend, in patients with RLQA pain, to identify a normal looking appendix. In the open appendectomy era, a normal-looking appendix was almost always removed, even if the cause of the pain was located elsewhere in the abdominal cavity. In a recent international survey by Jaunoo et al. among members of the Society of American Gastrointestinal and Endoscopic Surgeons (SAGES), the French Society for Endoscopic Surgery (SFCE), and the Italian Society for Endoscopic Surgery (SICE), 64% to 73% of surgeons affirmed that they would remove a macroscopically normal appendix in patients with right iliac fossa pain. It is believed that the advantages include early diagnosis of neoplasms, removal of endoluminal appendicitis, avoidance of misdiagnosis in acute abdomen patients, and the prevention of acute appendicitis in later life [12]. Phillips et al. argue that the removal of macroscopically normal appendices in patients undergoing laparoscopy for right iliac fossa
Table 2 Histopathology results. 50 (30%) 24 (15%) 90 (55%)
Histological diagnosis
Number (%)
Catarrhal appendix Phlegmonous appendix Scleroatrofic appendix Neuroendocrine tumor Normal appendix
109 8 5 3 39
(66%) (5%) (3%) (2%) (24%)
D. Tartaglia et al. / International Journal of Surgery 28 (2016) 149e152 Table 3 Histopathological differences between Group 1 and Group 2.
Catarrhal appendix Phlegmonous appendix Scleroatrofic appendix Neuroendocrine tumor Normal appendix TOTAL
Group 1 No other disease (%)
Group 2 Other diseases (n %)
p value
40 3 1 1 5 50
69 (61%) 5 (4%) 4 (3%) 2 (2%) 34 (30%) 114
0.0243 0.9617 0.9808 0.9140 0.0109
(80%) (6%) (2%) (2%) (10%)
pain is to be advocated, also in the absence of other explanatory pathologies, considering that the operative time and the incidence of port-site infections do not significantly increase [13]. Some authors suggest the presence of microscopic inflammation in a macroscopically normal appendix so therefore recommend routine appendectomy [14,15]. On the other hand, Champault et al. recommend not removing a macroscopically normal appendix discovered during diagnostic laparoscopy for abdominal pain, considering that only 1.3% of patients with normal appendix found during laparoscopy, underwent surgery for chronic appendicitis within 3 years after the first admission [16]. A low grade histological inflammation of the appendix could be the consequence of intra-operative manipulation of the appendix before appendectomy [3]. In this study, 164 of 1388 patients (12%) who underwent LA for acute RLQA pain presented a macroscopically normal appendix. This rate is comparable with data from other studies [16,17]. However only 24% of macroscopically normal appendices were confirmed to be truly normal after histological examination. Most negative appendectomies were performed in young women (88%); this is related to a diagnostic difficulty in the fertile female with abdominal right pain, which often requires further diagnosis with CT abdomen [18]. Compared to data from studies focusing on patients undergoing only diagnostic laparoscopy without appendectomy for acute RLQA pain, we recorded a lower morbidity rate (1.8% vs. 4.5%) and a shorter hospital stay (1.8 vs. 3 days) [17,19] for appendectomized patients. In our study the majority of normal-looking appendices was shown to be affected by catarrhal inflammation (66%) or by phlegmonous inflammation (5%) on histopathological examination. The serosa was not involved in any of these cases. In other studies the prevalence of endo-appendicitis ranges from 29 to 58% [8,13]. The percentage of appendices with microscopic alterations was significantly higher in Group 1 than in Group 2 (90% vs. 70% respectively), and this may explain acute symptoms in those patients in whom the laparoscopic exploration was negative. However, some pathological changes to the appendix were also found in those patients in whom laparoscopy detected a simultaneous acute abdominal disease. We cannot give any valuable explanation of this observation but in our opinion it represents an indication to perform incidental appendectomy even in these cases. In 3 patients (2%) microscope examination of the innocent appendix showed a neuroendocrine tumor and led to the patients receiving further treatment: these data are comparable with the results reported by Bucher et al. [20]. These appendicular neoplasms are rarely associated with clinical manifestations and are frequently recognized during pathological examination of appendices resected mainly for acute RLQA pain (up to 55%). Despite the fact that laparoscopy is becoming a widely used diagnostic tool in many acute abdominal conditions, the management of a normal appendix found at laparoscopy for right iliac fossa pain remains controversial. Clear guidelines on this issue from
151
international surgical societies are still lacking, so the decision between performing appendectomy or not is mostly left to individual choice. Large multi-center studies focusing on the long-term follow-up of patients who had a normal appendix left in situ after diagnostic laparoscopy may help to build a shared consensus on this topic and are strongly needed. In the meantime, considering the low morbidity, the short hospital stay, and most of all, the by no means negligible rate of appendicular abnormalities found at histological examination, we encourage prophylactic appendectomy in all patients undergoing diagnostic laparoscopy for acute RLQA pain and showing a macroscopically “normal” appendix. Ethical approval Considering that this is a descriptive and retrospective study, no Ethical Approval has been requested. Funding sources No sources of funding to state. Author contribution Dario Tartaglia performed the conception and design of the study. Andrea Bertoucci performed the analysis of the data. Matteo Palmeri performed the analysis of the data. Gregorio Di Franco performed the acquisition of the data. Rita Fantacci performed the acquisition of the data. Furbetta performed the acquisition of the data. Niccolo Christian Galatioto revised the article critically for important intellectual content. Massimo Chiarugi revised the article critically for important intellectual content. Conflicts of interest No conflicts of interest to state. Guarantor Dario Tartaglia, MD, University of Pisa, Italy. Research registration unique identifying number (UIN) Researchregistry781. References [1] D.G. Addis, N. Shaffer, B.S. Fowler, The epidemiology of appendicitis and appendectomy in the United States, Am. J. Epidemiol. 132 (1990) 910e925. [2] R. Marudanayagam, G.T. Williams, B.I. Rees, Review of the pathological results of 2660 appendicectomy specimens, J. Gastroenterol. 41 (2006) 745e749. [3] T. Slotboom, J.T. Hamminga, H.S. Hofker, et al., Intraoperative motive for performing a laparoscopic appendectomy on a postoperative histological proven normal appendix, Scand. J. Surg. 103 (4) (2014) 245e248. [4] O.J. Bakker, P.M. Go, J.B. Puylaert, WerkgroeprichtlijnDiagnostiek en behandeling van acute appendicitis [Guideline on diagnosis and treatment of acute appendicitis: imaging prior to appendectomy is recommended], Ned. Tijdschr. Geneeskd. 154 (2010) A303. [5] C.L. Bijnen, W.T. Van Den Broek, A.B. Bijnen, Implications of removing a normal appendix, Dig. Surg. 20 (2003) 115e121. [6] SAGES guidelines committee, Guidelines for Laparoscopic Appendectomy [SAGES web site], October, 1992. Available at: http://www.sages.org/ publications/guidelines/guidelines-for-laparoscopic-appendectomy/ (accessed April 2009). [7] B. Navez, A. Therasse, Should every patient undergoing laparoscopy for clinical diagnosis of appendicitis have an appendicectomy? Acta Chir. Belg. 103 (2003) 87e89. [8] M. Chiarugi, P. Buccianti, L. Decanini, et al., ‘What you see is not what you get’
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D. Tartaglia et al. / International Journal of Surgery 28 (2016) 149e152 a plea to remove a ‘normal’ appendix during diagnostic laparoscopy, Acta Chir. Belg. 101 (2001) 243e245. N. Vettoretto, S. Gobbi, A. Corradi, et al., Italian Association of Hospital Surgeons Consensus conference on laparoscopic appendectomy: development of guidelines, Colorectal Dis. 13 (7) (2011) 748e754. D. Dindo, N. Demartines, P.A. Clavien, Classification of surgical complications, a new proposal with evaluation in a cohort of 6336 patients and results of a survey, Ann. Surg. 240 (2) (2004) 205e213. E.G. Von Elmg, D. Altmanb, M. Eggera, et al., The strengthening the reporting of observational studies in epidemiology (STROBE) statement: guidelines for reporting observational studies, Int. J. Surg. 12 (2014) 1495e1499. S.S. Jaunoo, A.L. Hale, J.P. Masters, et al., An international survey of opinion regarding investigation of possible appendicitis and laparoscopic management of a macroscopically normal appendix, Ann. R. Coll. Surg. Engl. 94 (7) (2012) 476e480. A.W. Phillips, A.E. Jones, K. Sargen, Should the macroscopically normal appendix be removed during laparoscopy for acute right iliac fossa pain when no other explanatory pathology is found? Surg. Laparosc. Endosc. Percutan. Tech. 19 (5) (2009) 392e394.
[14] C.L. Bijnen, W.T. Van Den Broek, A.B. Bijnen, et al., Implications of removing a normal appendix, Dig. Surg. 20 (2) (2003) 115e121. [15] E. Sadot, A. Keidar, R. Shapiro, et al., Laparoscopic accuracy in prediction of appendiceal pathology: oncologic and inflammatory aspects, Am. J. Surg. 206 (5) (2013) 805e809. [16] A. Champault, C. Polliand, P. Mendes da Costa, et al., Laparoscopic appendectomies: retrospective study of 2074 cases, Surg. Laparosc. Endosc. Percutan. Tech. 18 (2) (2008) 168e172. [17] Garlipp B1, G. Arlt, Laparoscopy for suspected appendicitis. Should an appendix that appears normal be removed? Chirurg 80 (7) (2009) 615e621. [18] P.M. Rao, J.T. Rhea, R.A. Novelline, et al., Effect of computed tomography of the appendix on treatment of patients and use of hospital resources, N. Engl. J. Med. 38 (1998) 141e146. [19] W.T. Van den Broek, A.B. Bijnen, P. De Ruiter, et al., A normal appendix found during diagnostic laparoscopy should not be removed, Br. J. Surg. 88 (2) (2001) 251e254. [20] P. Bucher, Z. Mathe, A. Demirag, et al., Appendix tumors in the era of laparoscopic appendectomy, Surg. Endosc. 18 (7) (2004) 1063e1066.