Original paper Videosurgery Laparoscopic Nissen fundoplication in the treatment of Barrett’s esophagus – 10 years of experience MMaarrcciinn MMiiggaacczzeewwsskkii,, MMiicchhaałł PPęęddzziiwwiiaattrr,, MMaacciieejj MMaattłłookk,, AAnnddrrzzeejj BBuuddzzyyńńsskkii Second Department of General Surgery, Jagiellonian University Medical College, Krakow, Poland Videosurgery Miniinv 2013; 8 (2): 139-145 DOI: 10.5114/wiitm.2011.32941 Abstract IInnttrroodduuccttiioonn:: Barrett’s esophagus (BE) is astate in which the distal portion of esophageal mucosa becomes lined with cylindrical epithelium as aresult of adaptive remodeling. It is widely accepted that the metaplastic lesions result from chronic irritation with gastric and/or duodenal contents in the course of reflux disease. For many years, research cen- tered on the risk factors of BE and resulting adenocarcinoma. Anti-reflux operations are the only procedures which offer the possibility of treating the cause by restoring the anatomic barrier responsible for guarding against irritating effects of gastroduodenal content on the distal esophagus. Total (i.e. 360°) laparoscopic Nissen fundoplication (LNF) is considered the most effective amongst these procedures. Still, controversies related to the indications for anti-reflux surgery are frequently encountered. AAiimm:: Retrospective analysis of long-term treatment outcomes in patients with BE subjected to laparoscopic Nissen fundoplication. MMaatteerriiaall aanndd mmeetthhooddss:: The group included 42 BE patients, amongst them 30 men and 12 women. Initially, all the patients were treated conservatively for at least 1 year. The subgroup with dysplasia was subjected to preoperative argon plasma coagulation (APC). From 1 year after surgery (laparoscopic Nissen fundoplication), control biopsy spec- imens were obtained from the gastroesophageal junction of all the patients. RReessuullttss:: None of the patients showed the development of esophageal adenocarcinoma during the follow-up period. Furthermore, no cases of dysplasia progression or de novo development of dysplasia were observed in the analyzed group. In the initial 12-24 months after surgery, complete regression of metaplasia was documented in 7 (31.8%) patients from group A, and areduction in the area of Barrett’s metaplasia was observed in another 7 patients (31.8%). Throughout the period of this study, persistent planoepithelial re-epithelialization was observed in 14 (70%) group B patients, i.e. in individuals with baseline dysplasia subjected to preoperative argon plasma ablation. In the remaining patients of this group, the developed changes of BE character were less advanced than at baseline. CCoonncclluussiioonnss:: Our opinion is that laparoscopic Nissen fundoplication, as aresult of high effectiveness, represents the method of choice in the treatment of BE in the case of patients who were qualified for surgery. KKeeyy wwoorrddss:: laparoscopy, Nissen fundoplication, Barrett’s esophagus. with cylindrical epithelium as a result of adaptive Introduction re modeling. The replacement of normal squamous Barrett’s esophagus (BE) is astate in which the dis- epithelium with glandular epithelium can be observed tal portion of the esophageal mucosa becomes lined on microscopic examination (Photo 1). It is widely ac - Address for correspondence Marcin Migaczewski MD, PhD, Second Department of General Surgery, Jagiellonian University Medical College, 21 Kopernika St, 31-234 Krakow, Poland, phone: +48 12 424 82 01, 502 714 639, fax: +48 12 421 34 56, e-mail: [email protected] VideosurgeryandOtherMiniinvasiveTechniques2,June/2013 139 Marcin Migaczewski, Michał Pędziwiatr, Maciej Matłok, Andrzej Budzyński some malignancies, should not be underestimated. Even assuming that PPIs effectively reduce gastric secretion of acids, decidedly, they do not play an important role in the case of non-acidic reflux. More- over, it should be emphasized that bile acid salts, the principal components of alkaline refluxate, play a particularly important role in the promotion of esophageal adenocarcinoma development [3-5]. For many years, research centered on the risk fac- tors of BE and resulting adenocarcinoma. Although the role of chronic irritation of the distal esophageal mucosa with refluxate is unquestionable, still it re- mains unexplained why some patients develop solely mucosal inflammation, while Barrett’s metaplasia is observed in others. According to the literature, the PPhhoottoo 11.. Barrett's metaplasia – the glandular risk factors of BE include duration of exposure and epithelium, intestinalisation without dysplasia. the composition of the refluxate. Furthermore, Histochemical staining Alcian blue + PAS (pH anumber of authors point out that the effective sup- 2.5) – acidic mucus tinged with blue, neutral red, pink, 20× lens (courtesy of Dr. K. Urbańczyk – pression of gastric secretion not only leads to pla- Department of Pathology, Jagiellonian Universi- noepithelial re-epithelialization, but is also reflected ty Medical College) by reduced expression of certain proliferation-specif- ic biomarkers [6]. cepted that the metaplastic lesions result from chron- Anti-reflux operations are the only procedures ic irritation with gastric and/or duodenal contents in which offer the possibility of treating the cause by re - the course of reflux disease. Also, as aresult of adap- storing the anatomic barrier responsible for guarding tive remodeling of the esophagus, the Zline does not against irritating effects of gastroduodenal content correspond to the upper threshold of gastric folds. on the distal esophagus [7]. Total (i.e. 360°) Nissen Many authors consider BE as the most advanced fundoplication (NF) is considered the most effective stage of gastroesophageal reflux disease (GERD). Al - amongst these procedures [8]. According to many though the hypothesis on the close association be - authors, the laparoscopic version of this procedure tween glandular metaplasia of the gastroeso phageal (LNF) represents agold standard in patients qualified junction and the risk of esophageal adenocarcinoma is for surgical treatment due to both uncomplicated widely accepted, the exact mechanisms behind this GERD and GERD associated with Barrett’s metaplasia relationship are not fully understood. In view of the [9, 10]. discrepancies with regards to the possible clinical pic- Still, controversies related to the indications for ture, frequent modifications of disease definition, and anti-reflux surgery are frequently encountered. Most poorly understood pathogenic mechanisms of BE, BE patients are qualified for LNF on the basis of the aunified diagnostic and therapeutic algorithm has not same criteria as subjects with uncomplicated GERD. been developed thus far for this group of patients [1]. These indications seem particularly justified in the Control of duodenogastroesophageal reflux con- case of younger patients, potentially exposed to stitutes the principal therapeutic objective in BE pa- a chronic injury of the esophageal mucosa. Perhaps tients [2]. Anti-secretive pharmacotherapy, mostly the fact that more than one-third of BE patients do with proton pump inhibitors (PPIs), is of vital impor- not experience reflux symptoms requiring chronic tance. However, according to numerous authorities, pharmacotherapy makes them one of the groups commonly used PPIs only attenuate the symptoms of which can benefit from LNF. Due to the lack of phar- reflux, but do not completely normalize pH of the dis- macological agents efficient against this condition, tal esophagus [2]. Additionally, such negative conse- confirmed non-acidic reflux is deemed to constitute quences of chronic PPI administration as hypergas- another important indication for surgical treatment. trinemia, and disturbances of the bacterial gastric The techniques of endoscopic ablation are used as microflora, potentially promoting the development of an adjunct to surgical procedures in patients with dys- 140 Videosurgery and Other Miniinvasive Techniques 2, June/2013 Laparoscopic Nissen fundoplication in the treatment of Barrett’s esophagus – 10 years of experience plasia of metaplastic epithelium. Such techniques, A complete circular metaplastic segment was including argon plasma ablation, enable the re-epithe- revealed in 27 (64.3%) patients, while 15 (35.7%) pa - lialization of the gastroesophageal junction [11]. tients presented with incomplete circular metaplasia. The classic (> 3 cm) BE was observed in 25 (59.5%) Aim patients. Maximal extent of metaplasia in this group of patients was 5 cm. The “short segment” type of BE The aim of this study was to perform aretrospec- was documented in 17 (40.5%) individuals. On preop- tive analysis of long-term treatment outcomes in pa - erative endoscopy, 38 (90.5%) patients showed slid- tients with BE subjected to laparoscopic Nissen fun- ing hiatal hernia; 4 subjects (9.5%) had mixed type of doplication. hiatal hernia. One year after surgery, control biopsy specimens Material and methods were obtained from the gastroesophageal junction of Atotal of 168 laparoscopic Nissen fundoplications all the patients. were performed in reflux disease patients of the Sec- For the purpose of further analysis, the patients ond Department of Surgery, Jagiellonian University Me - were divided into two groups based on the lack dical College, between January 1st, 2001 and April 30th, (group A) or presence of dysplasia (group B). 2012. This group included 42 BE patients, amongst them 30 men and 12 women. Mean age of enrolled Results patients was 49 years, and mean duration of follow- None of the patients showed the development of up amounted to 62 months (range: 3-94 months). esophageal adenocarcinoma during the follow-up pe - Endoscopic examination of the upper gastroin- riod. Furthermore, no cases of dysplasia progression testinal tract was conducted in all patients during the or de novo development of dysplasia were ob served preparatory period before surgery, and biopsy speci- in the analyzed group. In 36 (85.7%) subjects, laparo- mens were obtained from four esophageal quadrants scopic Nissen fundoplication was reflected by the to confirm the diagnosis. The biopsies were taken at attenuation of reflux disease symptoms during the 1 cm intervals at the level of the metaplastic seg- observation period. Thirty-three (78.6%) patients ment, in accordance with the recommendations of reported transient swallowing disorders during the the Montreal consensus (2006). Control endoscopy first 2 months after surgery. These complaints did not was performed 12 months after surgery. If persistent require hospitalization and resolved spontaneously in metaplastic lesions were observed, further control most cases. Nine (21.4%) patients were treated suc- endoscopies were performed on an annual basis. cessfully with oral hydroxyzine (2 × 25 mg). Initially, all the patients were treated conserva- In the first 12-24 months after surgery, complete tively (life style modification, dietary changes, PPIs) regression of metaplasia was documented in 7 (31.8%) for at least one year. Mean duration of therapy was patients from group A, and areduction in the area of 2.5 years (range: 1-4 years). Barrett’s metaplasia was observed in another 7 pa - Signs of dysplasia in the baseline specimens of tients (31.8%). The remaining 8 (36.4%) patients did gastroesophageal junction mucosa were observed in 20 (47.6%) of the patients. This subgroup was sub- not show any endoscopically or histopathologically jected to preoperative argon plasma coagulation evident changes. The effects of anti-reflux therapy (APC) in order to eliminate dysplasia, since the lack of were observed in patients with no baseline signs of the latter was required to perform LNF. Endoscopic dysplasia, with gastric metaplasia (n = 3), and with ablation was not performed in the remaining complete intestinal metaplasia (n= 4); the so-called 22 (52.4%) patients with no signs of dysplasia within “short segment” type lesions were observed in all the metaplastic epithelium. these patients. Throughout the period of this study, During the surgery, diaphragmatic crura were persistent planoepithelial re-epithelialization was sewn together in all the patients irrespective of the observed in 14 (70%) group B patients, i.e. in individ- size of the hiatal hernia. The thoracic esophagus was uals with baseline dysplasia subjected to preopera- mobilized up to 7 cm above the hiatal line. Both the tive argon plasma ablation. In the remaining patients diaphragmatic crura and the fundoplication wrap of this group, the developed changes of BE character were sutured using non-absorbable stitches. were less advanced than at baseline. Videosurgery and Other Miniinvasive Techniques 2, June/2013 141 Marcin Migaczewski, Michał Pędziwiatr, Maciej Matłok, Andrzej Budzyński Discussion All the above-mentioned facts unambiguously substantiate administration of chronic anti-secretory Barrett’s esophagus represents the most seri- therapy in the majority of BE patients. Currently, ous complication of gastroesophageal reflux disease, most authors recommend basing the therapy on being an established precancerous lesion. While PPIs, although aunified therapeutic protocol has not one can easily find the therapeutic recommenda- been developed thus far. The most frequently postu- tions regarding uncomplicated GERD in the avail- lated protocol is based on over-the-standard dosage able literature, the management of patients with of PPIs; however, this approach is associated with glandular esophageal metaplasia still raises many established, more severe, and prolonged course of questions. reflux disease in BE patients as compared to the Progression of Barrett’s metaplasia towards eso - group with uncomplicated GERD. The available litera- phageal adenocarcinoma results from chronic reflux- ture contains reports suggesting the possibility of ate-induced injury of the esophageal mucosa. While complete remission of glandular metaplasia in pa - BE is areversible state, persistent chronic inflamma- tients treated solely with PPIs; nevertheless, authors tion promotes carcinogenesis [12]. Chemical compo- assign varying significance to these findings. In sition of the refluxate seems to play an exceptionally adouble-blinded randomized study, Peters observed important role in BE pathogenesis; specifically, the acomplete remission of Barrett’s metaplasia in 8% of concentration of bile acids in reflux content is partic- patients subjected to 24 months of continuous ther- ularly correlated with the degree of esophageal mu - apy with 80 mg of omeprazole [15]. Simultaneously, cosal injury [13]. there were no cases of complete regression of meta- It is widely accepted that controlling the signs plastic lesions documented in a ranitidine-treated of gastroesophageal reflux disease constitutes the group. In the opinion of the majority of authors, principal therapeutic objective [2]. Achieving this chronic administration of proton pump inhibitors can therapeutic effect requires normalization of pH at lead only to reduction of the metaplastic area with the esophageal-gastric junction; this goal is mostly potential development of islets lined with normal achieved with proton pump inhibitors (PPI). This ap - squamous epithelium [16, 17]. However, according to proach attenuates the signs of reflux disease by some opinions, the residual foci of metaplastic epithe- reducing the intensity of inflammatory lesions in the lium can be localized deeper than the newly formed distal esophagus. However, a number of authors point to the limited value of such an approach in islets, raising the question about the effectiveness of some patients. Mikes and Gerson observed persist- the aforementioned therapeutic approach. ent acidic reflux on pH-metric examination in 50% of The above-mentioned data suggest that pharma- asymptomatic patients treated with PPIs [14]. Also, cotherapy alone is not reflected by regression of glan- the evidence of negative consequences associated dular metaplasia in the majority of BE patients and with persistent hypergastrinemia should not be under- does not enable planoepithelial re-epithelialization. estimated. There is increasing evidence of the necessity of Anti-reflux surgery, optimally performed laparo- implementing one of the ablation techniques at the scopically, remains an alternative therapeutic ap - early stage of treatment in order to remove the meta- proach as the only modality of treating the cause in plastic foci frequently associated with dysplasia. patients with dysfunction of the lower esophageal Combining endoscopic techniques with anti-secreto- sphincter. Such treatment enables restoration of the ry therapy is also reflected by persistent planoepithe- physiological barrier reducing exposure of the esoph- lial re-epithelialization [18]. In our study, the combi- agus to reflux content. nation of argon plasma ablation with laparoscopic Reduction of the area of glandular metaplasia Nissen fundoplication enabled persistent elimination constitutes the principal component of adjunctive of Barrett’s metaplasia in approximately 70% of the treatment in BE patients. Most commonly, ablation patients. However, the available literature lacks un - techniques are recommended in patients with asso- ambiguous confirmation of the protective effect of ciated dysplasia. The most popular methods include such an approach with regards to the risk of eso - photodynamic technique, ablation with radiofrequen- phageal adenocarcinoma; this necessitates further cy waves, and argon plasma ablation. research on the problem in question [19, 20]. 142 Videosurgery and Other Miniinvasive Techniques 2, June/2013 Laparoscopic Nissen fundoplication in the treatment of Barrett’s esophagus – 10 years of experience Anti-reflux surgery has become acommon com- Current research suggests the possibility of com- ponent of treatment, particularly due to the popular- plete regression of metaplasia after surgical correc- ization of the laparoscopic approach. Pharmacother- tion of an inefficient anti-reflux barrier. This phenom- apy enables a transient normalization of pH at the enon was observed in 4 out of 10 surgically treated esophageal-gastric junction, but does not modulate patients included in Brand’s study, the findings of the efficiency of the physiological anti-reflux barrier. which were published in 1980 [26]. In Oelschlager’s Patients subjected to argon plasma ablation of meta- report, during the mean 40-month follow-up period, plastic mucosa require long-term elimination of the the complete remission of metaplasia was revealed harmful effect of stomach-regurgitated content in in 33% of 106 cases of laparoscopically operated order to establish the therapeutic outcome. Nissen patients with short BE. The results of previous analy- fundoplication is currently postulated as the most ses suggest that such an approach can be effective in no more than 20% of patients with classic BE. Also, efficient modality of reflux treatment. Many authors reports suggesting the possibility of regression of BE- consider the laparoscopic form of this procedure as related dysplasia can be found in the available litera- agold standard of GERD therapy. Surgical treatment ture [27-29]. The results of these studies suggest that seems particularly substantiated in BE patients, par- complete regression of mild dysplasia can be ob - ticularly in those lacking reflux symptoms. According tained in even up to 70% of the patients. Complete to Sharma, surgical treatment plays avital role in the regression of glandular metaplasia was documented management of BE patients, as well as in the preven- in seven of the analyzed patients with short BE. tion of BE-induced esophageal adenocarcinoma [21]. The prevailing opinion indicates that Nissen fun- The outcomes of laparoscopic anti-reflux surgery doplication, as a result of high effectiveness, repre- proved excellent with regards to the attenuation of sents the method of choice in the treatment of BE in reflux symptoms. In Parill’s study, the control of GERD the case of patients who were qualified for surgery. symptoms was achieved in 91% of operated patients However, such a consistent attitude is lacking with [22]. In Eubanks’ analysis, mean 43-month postsurgi- regards to the details of its modifications. Early expe- cal follow-up revealed a95% reduction of reflux dis- riences with LNF were limited to mobilization of the orders [23]. In our study, the typical GERD-related esophagus solely at the level of the esophageal hia- complaints resolved in 86% of patients analyzed dur- tus. Currently, according to the recommendations of ing the period of the experiment. acknowledged authorities, the threshold of mobiliza- According to numerous authors, there is a pre- tion should be placed much higher (Photo 2). Howev- dominance of alkaline component of the reflux in er, there are some discrepancies with regards to the patients with BE [24, 25]. The authors of previous re - level of esophageal mobilization in the mediastinum. ports emphasize that the degree of esophageal According to Dallemagne, the esophagus should be mucosal exposure to bile content in BE patients is similar to that observed in individuals subjected to partial gastric resection. These facts point to limited effectiveness of pharmacotherapy in this group of patients. Consequently, surgical restoration of the Right crus of anti-reflux barrier should be markedly more effective diaphragm Esophagus in the normalization of this type of reflux. In Parilla’s study, limited exposure to bile content was observed in 92% of the patients subjected to the anti-reflux Left crus of procedure and in only 25% of individuals treated with diaphragm Left lobe of PPI [22]. Consequently, it could be expected that the the liver outcomes regarding reduction of the metaplastic Cardia area and the prevention of dysplasia and develop- Fundus of ment of malignancy would be markedly better in sur- stomach gically treated patients than in those in whom abla- PPhhoottoo 22.. Laparoscopic Nissen fundoplication – tion techniques were combined with anti-secretory intraoperative view during preparation of the pharmacotherapy. esophagus within the mediastinum Videosurgery and Other Miniinvasive Techniques 2, June/2013 143 Marcin Migaczewski, Michał Pędziwiatr, Maciej Matłok, Andrzej Budzyński mobilized up to 5-7 cm above the esophageal hiatus 7. Tarnowski W, Kiciak A, Borycka-Kiciak K, et al. Laparoscopic fun- [30]. In contrast, Swanstrom defines this threshold doplication improves oesophageal motility – aprospective study. Videosurgery Miniinv 2011; 6: 73-83. at the level of inferior pulmonary veins [31]. Such 8. Szyca R, Leksowski K, Cornelia de Lange syndrome – character- amaneuver enables the restoration of asufficiently istics and laparoscopic treatment modalities of reflux based on long abdominal section of the esophagus, which own material. Videosurgery Miniinv 2011; 6: 173-7. seems to be one of the most important components 9. Wróblewski T, Skalski M, Ziarkiewicz-Wróblewska B, et al. New of the anti-reflux barrier. Furthermore, high mobiliza- antireflux surgical technique in GERD treatment. Videosurgery tion of the esophagus along with tighter than previ- Miniinv 2007; 2: 139-44. ously postulated suturing of the diaphragmatic crura 10. 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