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Eur J Cardiothorac Surg 2004;25:1079-1088
© 2004 Elsevier Science NL
a Department of Surgery, Intensive Care, and Organ Transplantation: Center for the Study and Therapy of Diseases of the Oesophagus (Surgical Section), University of Bologna, Bologna, Italy
b Department of Radiological and Histopathological Sciences, University of Bologna, Bologna, Italy
Received 10 October 2003; received in revised form 27 January 2004; accepted 9 February 2004.
* Corresponding author. Address: Dipartimento di Discipline Chirurgiche, Rianimatorie e dei Trapianti, Università di Bologna, Via Massarenti 9, 40138 Bologna, Italy. Tel.: +39-51-636-4870; fax: +39-51-397-661
e-mail: sandro.mattioli{at}unibo.it
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Abstract |
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 Top Abstract 1. Introduction2. Methods3. Results4. DiscussionAppendix A. Conference...References |
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Key Words: Gastro-oesophageal reflux disease • Hiatus hernia • Short oesophagus • Antireflux surgery
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1. Introduction |
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TopAbstract1. Introduction2. Methods3. Results4. DiscussionAppendix A. Conference...References |
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During the era of ‘open’ antireflux surgery, in order to treat patients with oesophageal shortening secondary to gastro-oesophageal reflux disease (GORD), surgeons experimented and applied new surgical procedures, to adequately mobilize the thoracic oesophagus or to elongate it in large patient case series. The aim of these procedures was to create an intraabdominal antireflux fundoplication, without tension, which was known to predispose to disruption of the sutures and failure of most of the standard full or partial fundoplication techniques [1,2]. In general, discussion was focused on the diagnosis and, consequently, on the frequency of short oesophagus in patients undergoing antireflux surgery, on the indications and on the results of the different surgical techniques developed over the years in order to treat this condition.
In the present era of ‘mini-invasive’ antireflux surgery, after an initiation period for the new surgery during which the problem of the possible non-reducibility of the gastro-oesophageal (g–o) junction in the abdomen was apparently ignored [3–5], new articles dedicated to short oesophagus have recently been appearing more and more frequently in the surgical literature. Not surprisingly the same topics as in the recent past are today again debated upon: the prevalence of short oesophagus in GORD and in patients undergoing antireflux surgery; preoperative diagnosis and predictability; intraoperative evaluation; and surgical management of shortened oesophagus [4–10].
The aim of the present study was to propose preoperative, reproducible diagnostic and classification methods to guide the surgeon in indicating antireflux surgical therapy. In particular, to predict cases of fore-shortened oesophagus requiring dedicated surgical approaches and to select updated procedures with which to safely and efficiently manage these conditions.
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2. Methods |
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TopAbstract1. Introduction2. Methods3. Results4. DiscussionAppendix A. Conference...References |
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In the period considered, important modifications occurred with regard to medical (H2 blockers and PPI antisecretors) and surgical (open and mini-invasive techniques) therapy. We, therefore, split the case series into two parts, doing a comparative analysis of the data collected in the periods 1980–1991 and 1992–2003 with 149 and 170 patients, respectively.
2.1. Preoperative study
Since the late 1970s, observed at the Center for GORD, clinical and instrumental data have been collected for each patient according to a protocol aimed at prospectively investigating diagnostic, pathophysiological, evolutive and therapeutical aspects of the disease.
Candidates for antireflux surgery preoperatively underwent a clinical assessment based on a questionnaire, barium swallow, upper GI endoscopy and manometry. Oesophageal or oesophagogastric ambulatory 24 h pH recording were routine until the mid-1990s. Later, in the presence of typical GOR symptoms, endoscopic evidence of reflux oesophagitis and/or clear positive response to PPI therapy, pH recording was not routinely performed. In general, patients affected by massive incarcerated hiatus hernia did not undergo pH recording.
The typical and atypical GOR symptoms and the dysphagia related symptoms were collected in a questionnaire and graded according to semiquantitative scales (Table 1a). We recorded the symptoms described by the patients while not on medical therapy. Duration of reflux and dysphagia symptoms were calculated in the months from their appearance to the preoperative work up.
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Table 1b shows the endoscopic and histological reflux oesophagitis grading scale that we adopted according to the modified Savary and Miller and Ismail–Beigi criteria [12]. Barret's microscopic diagnosis was always made according to Paull [13].
Diagnosis of Barret's oesophagus was macroscopic and microscopic. Until 1995 we macroscopically classified the columnar lined oesophagus in three stages (stage I, creeping substitution; stage II, columnar segment under 3 cm; stage III, segment more than 3 cm in length) according to Bremner's criteria [14]. Successively Barret's oesophagus was classified as short segment (<3 cm) and long segment (>3 cm) [15]. As the creeping substitution definition corresponds in morphology and length to the ectopic mucosa of the short segment Barret's oesophagus, the creeping substitution was called short segment Barret's oesophagus in the results to improve comprehension of the data.
Oesophageal manometry was performed according to our standard [11,16]. Since 1990 after performing the standard recording in the supine position according to the slow pull-through technique, a second recording was performed in the sitting position, in order to favour the descent of the g–o junction with gravity). The relationship between the LES (intrinsic component) and the diaphragmatic pinchcock (extrinsic components of the high pressure zone of the distal oesophagus) was assessed in both positions. Oesophageal or oesophago-gastric pH recording was performed according to techniques previously described [16].
2.2. Surgical techniques
In the first period, only open surgery was performed. When the barium swallow showed an intraabdominal or well reducible g–o junction, the laparotomic approach was electively chosen and the Nissen fundoplication performed. When X-ray showed that the g–o junction was located at or above the hiatus in association with a straightened oesophagus, a left 6th space posterolateral thoracotomy was preferred, the thoracic oesophagus was mobilized up to the aortic arch. If the g–o junction was reduced easily below the hiatus, the Belsey MKIV was adopted. If the surgeon felt tension in reducing the g–o junction, he freely proceeded to elongate the oesophagus according to the Pearson technique [1] (called Collis–Belsey here for symmetry). In the event of contraindications to thoracotomy or in the presence of gallstones, patients were treated via laparotomy according to the same principles adopted in the thoracic approach: in the event of a non-reducible g–o junction, the Collis–Nissen operation according to the Steichen technique [17] was performed. The preferred approach for obese patients and massive incarcerated hiatus hernia (MIHH) was thoracotomy.
In the second period, we progressively and carefully switched to laparoscopy. We soon realized that the intraoperative endoscopic assessment of the relationship between the g–o junction and the hiatus was crucial during laparoscopy, when it is possible to miss the passage from the tubular oesophagus into the stomach. After a 7–8 cm mobilization of the lower oesophagus, a fiberscope was perorally introduced as far as the level of the proximal margin of the gastric mucosal folds. The surgeon relieved any tension applied to the stomach and determined by transillumination the position of the g–o junction marked, with respect to the apex of the hiatus [6,8,18]. If the light and the tip of the endoscope were positioned roughly 2.5 cm below the apex of the hiatus in open surgery and 3 cm in laparoscopy, a floppy Nissen fundoplication was the procedure of choice. Contrarily, if the g–o junction was at the level or above the hiatus, the Collis procedure was added to the fundoplication. In borderline cases we privileged the lack of tension at the price of a more complex operation. Recently, we switched from the open Collis–Nissen to a mini-invasive left thoracoscopic–laparoscopic Collis–Nissen [6,8].
The crural repair, if necessary associated with an alloplastic reinforcement, completed the antireflux procedures in all cases in both periods.
2.3. Postoperative follow up
After surgery, patients were routinely seen at the outpatient clinic twice in the first year, once a year for 4 more years and successively every 3 years. At 12 months we repeated the barium swallow, endoscopy and oesophageal manometry. pH recording was indicated in the presence of reflux symptoms (RS) without macroscopic oesophagitis to assess the nature of the symptoms. Afterwards we ordered endoscopy, radiology and functional tests according to symptoms; at the 5th and the 10th postoperative year we routinely repeated the barium swallow and endoscopy. Clinical interview and tests were performed as preoperatively, by the different specialists of the Center. The questionnaires were always compiled by one of the surgeons.
The result of surgical therapy was graded from excellent to poor according to the semiquantitative scale reported in Table 1c. The result was poor even when only one of the considered parameters was graded 2 or 3. If patients were clinically well but under medical therapy or asymptomatic in the presence of hiatus hernia recurrence or slipping of the fundoplication, the result was also downgraded to poor.
The preoperative study, surgical therapy and follow up of the patients were carried out according to the principles of current clinical practice.
2.4. Statistical analysis
Univariate analysis was carried out by means of the Mann–Whitney and 
2 tests as appropriate.
Multivariate analysis was performed using the logistics regression method in order to identify the preoperative factors predicting the need to carry out the elongation procedure according to Collis. A P value <0.05 was considered statistically significant.
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3. Results |
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TopAbstract1. Introduction2. Methods3. Results4. DiscussionAppendix A. Conference...References |
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Oesophageal manometry was performed in the supine position in 140 patients, and in the supine and sitting position in 179. Abnormalities of the oesophageal peristalsis secondary to GOR were recorded in 38% of 319 patients. In 30/179 (16.7%) patients the LES remained above the diaphragm in the sitting position.
pH recording was performed in 173 patients and it was positive for abnormal acid reflux in 154 (89%).
In the two periods, some of the clinical and instrumental parameters that were measured were different in terms of severity or frequency (Table 2).
Table 3 shows the distribution of the patients subgrouped for the two periods with regard to the radiological classification of hiatus hernias and the type of surgery. All mini-invasive procedures belong to the second period: 62 floppy Nissen and 12 Collis–Nissen, 10 of which were performed by laparo-thoracoscopy according to Awad's technique [6,8]. The percentage of open thoracic procedures decreased considerably in the second period. The Collis procedure was added to the Nissen or the Belsey fundoplication in 29.5% of cases in the first period and in 23.5% in the second period.
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The multivariate analysis showed the following preoperative factors as predicting the need for a Collis procedure: radiological classification (P=0.005) (odds ratio 20.53) (95% CI 2.47–170.15), manometry in the upright position (P=0.038) (odds ratio 5.26) (95% CI 1.09–25.41) and the presence of peptic stenosis (P=0.015) (odds ratio 5.18) (95% CI 1.38–19.44).
Causes of postoperative mortality and morbidity and of poor long-term outcome of surgery are reported in Table 4. Complications were more frequent in the second than in the first period (P=0.0015).
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The postoperative results and long term follow up time (in months), obtained in the two periods, considered globally and for each surgical technique, are reported in Table 5.
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According to preoperative radiological classification, hernia recurrence or slipping of the fundoplication occurred in five sliding hiatus hernias, in two concentric hiatus hernias, in one short oesophagus and in three out of 56 (5.3%) massive incarcerated hiatus hernias operated upon. The three MIHH had a standard Nissen procedure.
Preoperative determinants such as age, type of hernia, grade of oesophagitis, oesophageal motility or duration of symptoms were not predictive factors of poor postoperative results at multivariate analysis (P>0.05 logistic regression analysis)
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4. Discussion |
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TopAbstract1. Introduction2. Methods3. Results4. DiscussionAppendix A. Conference...References |
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After the rush to utilize laparoscopic techniques, the analysis of complications, in short and long term results indicates that some of the basic principles of ‘open’ antireflux surgery can no longer be ignored [4,10]. One of the most common and severe complications with laparoscopic antireflux surgery is para-oesophageal hiatus herniation [7], which has been related to oesophageal shortening [4,7,19].
The rediscovery of short oesophagus has inevitably renewed the discussion on the same topics from the past, which were debated but then not definitely clarified. Mini-invasive surgery is less flexible than ‘open’ surgery when it becomes necessary to change the surgical action. Experience, planning and skill are required to successfully carry out mini-invasive operations, particularly if they are complex and not frequently performed [10]. With regard to antireflux surgery, so popular today, it must be kept in mind that at laparoscopy it is possible to miss the exact position of the g–o junction because the proximal stomach, attracted upward, acquires a funnel like form after years of herniation, the serosa loses brightness and the wall thickens. The tubularized proximal stomach is hardly distinguishable from the distal oesophagus [10,18]. Moreover, the pneumoperitoneum forces the diaphragm upwards, thus artificially increasing the length of the intraabdominal oesophagus [20].
The pending questions on short oesophagus require a quick answer. The primary cause of confusion is the misunderstanding of the significance and the interdependence between the axial migration of the g–o junction into the chest, and the ‘true’ short oesophagus. The first is a preoperative diagnosis obtained with non-invasive methods such as barium swallow and oesophageal manometry, both performed in the upright position. In contrast, the second diagnosis at the present time can only be recognized intraoperatively. Although, the first diagnosis includes the second one, in fact cases of elastic retraction of the oesophageal muscular wall secondary to the loss of anchorage of the g–o junction in the abdomen and cases of fibrotic retraction of the oesophagus from panmural oesophagitis secondary to GORD may have the same radiological presentation. The present data demonstrate the presence of the same radiological characteristics for elastic or fibrotic oesophageal retraction in the various grades of orad axial migration of the g–o junction, particularly in the concentric hiatus hernia and short oesophagus phases. An elastically retracted g–o junction is usually repositioned in the abdomen without any particular difficulty, thus the oesophagus is not irreversibly shortened, while the fibrotic, ‘truly short’ oesophagus requires extensive mobilization and possibly an elongation procedure to achieve a correct intraabdominal fundoplication. Data on the prevalence of both pathological conditions in the open antireflux surgery case series range from 0 [21] to 60% [1]. The lack of agreement on definition and classification (whether based on preoperative or intraoperative, morphological or pathophysiological criteria), on diagnostic methods, on the indications for surgical therapy and consequently on the types of patients included in the case series was and is responsible for the extreme difficulty in comparing data in the literature regarding the conditions of axial migration of the g–o junction and short oesophagus.
In the past 23 years we have progressively refined our approach to surgical therapy for GORD and specifically for the cases of shortened oesophagus. Intraoperative oesophagoscopy after mobilization of the lower oesophagus gives the surgeon objective information on the position of the g–o junction with respect to the diaphragmatic hiatus and consequently ensures that the decision whether to elongate the oesophagus or not is based on a precise process and not on a subjective evaluation. With this test we reduced the number of Collis procedures performed from 29% in the first period to 23% in the second period. In the same period, the Collis procedure was applied in none of the sliding hiatus hernias, in 2% (one patient) of hiatal insufficiencies, in 23% of concentric hiatus hernias and in 76% of the short oesophagus groups. The severity of oesophagitis, the duration of symptoms and the presence of an oesophageal stenosis also correlated with the cases that underwent a Collis gastroplasty in the second period. According to our experience, the preoperative barium swallow interpreted with the radiological classification we adopted offers enough elements on the basis of which the patient can be informed of the possibility of undergoing a more complex procedure; all steps of the surgery can be planned, including the choice of the first surgeon who should preferably have experience in complex antireflux surgical techniques. In other reports, the radiological diagnosis of a large size hiatus hernia (5 cm or more), irreducible in the upright position, was considered an indicator for short oesophagus [3,22]. Our radiological classification seems to be a more detailed and reliable predictor of the need for a dedicated procedure to manage oesophageal shortening. We did elongate several cases radiologically diagnosed as short oesophagus in which the distance between the g–o junction and the diaphragmatic hiatus was shorter than 50 mm. The 50 mm distance between the g–o junction and the hiatus adopted to indicate a high probability of a truly shortened oesophagus underestimates the phenomenon. Moreover, the present radiological classification, covering three steps of shortening, may also indicate cases of moderate oesophageal shortening (MOS) as advocated in the past by Collis [23] and more recently by others [23], that may be properly treated with the extensive mobilization of the thoracic oesophagus alone [5,10,22,23]. Today, in the presence of a radiological diagnosis of concentric hiatus hernia or short oesophagus, we place the patient in the left lateral position on the operating table, following the same principle we adopted for surgery for cancer of the thoracic oesophagus. In this position, while rotating the bed on the left or on the right, the surgeon can comfortably operate in laparoscopy and in laparoscopy-left thoracoscopy; the 10 mm optic port is placed at least 5 cm above the standard umbilicus position to allow a standard Nissen or a Collis–Nissen (Fig. 1) to be comfortably performed.
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Early intra and postoperative complications of antireflux surgery were more frequent in the second period than in the first one. The increase of complications noted in the second period was influenced by the introduction of mini-invasive Nissen and Collis–Nissen procedures; complications generally occurred during the early phases for both techniques. It is worth pointing out that the intraoperative split of the endosuture during mini-invasive Collis–Nissen procedures was due to the inappropriate size of the Maloney bougie.While for the ‘open’ Collis–Nissen we used a no. 52–54, for the mini-invasive procedure we currently use a bougie no bigger than no. 46.
Long term results of surgery were evaluated according to rigorous clinical-instrumental parameters: the systematic need for antisecretory drugs or the presence of a recurrent hiatus hernia or a slipped fundoplication downgraded the result to poor even in the absence of RS or oesophagitis.
Overall results were satisfactory in 81.6% in the first period and in 92.6% in the second period. Results of standard antireflux procedures were satisfactory in 84.8% in the first period and in 96.9% in the second period. Results of Collis–Nissen and Collis–Belsey seem to be improved in the second period. The follow up time of the second period was significantly shorter than for the first period and further evaluation of the results obtained mainly with mini-invasive procedures is required. Furthermore, it cannot be theoretically excluded that reflux oesophagitis recurs in the patients actually free of RS and oesophagitis who consequently were not controlled with pH recording. However, the long follow-up of patients of the first period excludes evolution in GORD.
The results of Collis gastroplasty plus fundoplication were still poor in 20% of the patients operated upon in the second period. We did not obtain any significant relationship between preoperative patterns and postoperative unsatisfactory results. Patients with shortened oesophagus undoubtedly present with complex functional and organic patterns. Nevertheless we feel that recurrence of reflux, particularly after Collis–Nissen, is prevalently secondary to the surgical technique. It was speculated that the combination of acid secretion produced by the portion of secreting gastric mucosa of the neo-oesophagus remaining above the fundoplication associated with dismotility of the gastric tube may be the cause of recurrent reflux and oesophagitis after Collis–Nissen [24].
After gastroplasty, the gastric fundus may assume a conical shape with a considerable loss of the fundal area. This neo-fundus may not be large enough to cover the whole length of the neo-oesophagus. To prevent the formation of a gastric pouch above the wrapped fundus, we actually fix the wrap laterally to the native cardia with two stitches placed at the apex of the gastroplasty suture. To prevent postoperative dysphagia due to lack of motility of the gastric tube, we usually calibrated the gastroplasty over a 52–54 Maloney bougie. Later on we downsized the tube to a 50 gauge. In the nine patients in whom we used a 46 Maloney bougie to perform the laparoscopic-left thoracoscopic Collis–Nissen we did not have significant dysphagia either at postoperative or short term follow up. We are aiming at routinely using a 46 Maloney bougie to do the Collis gastroplasty. Long term follow up will tell us whether the surgical technique we have recently adopted will improve functional results.
It has been suggested that PPI based therapy could more substantially reduce GOR damage and consequently the risk of fibrotic oesophageal shortening; these effects of medical therapy associated with earlier surgery, promoted by the introduction of laparoscopy, could have reduced the prevalence of short oesophagus in patients operated upon in the last decade [3,5,19]. In fact within the second period of the present review we operated upon more patients with radiologically diagnosed short oesophagus and we performed less Collis gastroplasties than in the first period. The 6% decrease of elongation procedures of the oesophagus is more probably due to a better intraoperative assessment of the position of the g–o junction, than to a bias against the procedure during the learning curve of the minimally invasive technique. We always paid maximal attention to the ‘short oesophagus’ problem and we did not hesitate to elongate the oesophagus when needed. In contrast to the first period, prior to surgery the majority of patients within the second period had undergone several courses of medical therapy prevalently based on PPI. Other than a reduced number of elongation procedures performed, preoperative findings were also different in the two periods for the presence of peptic stenosis (more frequent in the first period) and for the orad migration of the g–o junction (more frequent in the second period). No conclusive data are available to date on the effects of the current medical therapy on the evolution of severe GORD with respect to the intrathoracic axial migration of the g–o junction [25]. However, as the number of oesophageal stenosis was significantly reduced in contrast, the cases of orad migration of the g–o junction increased in the second period with respect to the first one. Thus a logical and attractive speculation would suggest that PPI therapy does not interfere with the elastic retraction of the oesophagus although it reduces the parietal inflammation and fibrosis induced by GOR, at least in the hiatal insufficiency and concentric hiatus hernia phases.
In summary, the condition of axial orad migration of the g–o junction has two important implications for the surgeon: the first affects the indications for surgical therapy of patients affected by GORD [11,12]; the second affects the management in the operating room of patients with axial migration, whether it is secondary to an elastic or fibrotic retraction [4,5,9]. The role of hiatus hernia in GORD has been revaluated with the demonstration that the intrathoracic migration of the g–o junction is the anatomical cause of severe permanent cardial incontinence in 50% of patients affected by severe GORD, suggesting a possible change in the indications for antireflux surgery [11,12,25]. Given that only surgery can definitively correct an anatomical defect, thus patients affected by severe GORD in the presence of hiatal insufficiency, concentric hiatus hernia and short oesophagus should be elective candidates for surgical therapy [25]. Early surgical therapy in the first two phases could prevent the development of severe pan-mural oesophagitis that requires more complex and less effective surgical techniques to treat it.
Preoperative barium swallow may offer the surgeon the opportunity to correctly inform the patient of the pros and cons of antireflux surgery and plan the technical details of the operation. Intraoperative oesophagoscopy provides fairly objective elements in order to decide whether to perform a standard or a more complex operation. With a tailored approach to antireflux surgery, the medium term results we achieved with standard antireflux procedures in the last 10 years seem to be very promising. However, the definitive evaluation of the results shall withstand the effects of further follow up. It is not the same for complex procedures in cases of true short oesophagus for which we still had 20% unsatisfactory results. This suggests that the optimal surgical technique has not yet been developed and the Collis–Nissen technique should probably be improved and better defined. In borderline cases, when the options could be a standard fundoplication, an antireflux procedure with a strong anchorage of the gastroplasty below the diaphragm may be a better option [4].
Today surgeons are once again discussing oesophageal shortening in GORD surgery. Hopefully the remaining controversies on this much debated topic will soon be clarified.
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Footnotes |
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Appendix A. Conference discussion |
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TopAbstract1. Introduction2. Methods3. Results4. DiscussionAppendix A. Conference...References |
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Dr Mattioli: The preoperative barium swallow may indicate a condition of intrathoracic migration of the gastro-esophageal junction. However, only intraoperatively, after adequate mobilization of the lower esophagus, it is possible to decide if an elongation procedure of the esophagus is necessary to place the fundoplication below the diaphragm without tension. With this regard, intraoperative esophagoscopy is very useful in order to asses the position of the GE junction with respect to the diaphragmatic hiatus.
Dr M. Migliore (Catania, Italy): It is clear that using this new technique to treat short esophagus you are performing a minimally invasive thoraco-abdominal approach to construct a lenghthening procedure such as Collis–Nissen fundoplication. I tried to perform the Belsey Mark IV fundoplication through thoracoscopy, and it is quite difficult. So my question is, are you going to perform more Collis–Nissen than Collis–Belsey in the following years to treat short esophagus?
Dr Mattioli: Unfortunately, yes. I still believe that the Collis–Belsey operation is the best operation we can do, but it's hard to propose today a sixth space posterolateral thoracotomy, so I switched it to the Collis–Nissen.
Dr G. Friedel (Gerlingen, Germany): Why do you prefer the left thoracoscopic approach?
Dr Mattioli: Well, we have three options. One is that proposed by Swanstrom, the right thoracoscopic approach. The second one is the laparoscopic Steichen procedure. You make a hole, and after, you elongate. And the third one is that one proposed by Awad. I did change a bit the technique. I do believe honestly that this is the right way to do things, because it's very easy and it's safe, because you know where the aorta is, where the heart is, and you pass through, and you walk over the diaphragm, and all the time you see where your tip of the endoGIA is. So it's not stupid, believe me. And you do exactly the elongation how we did with the Collis–Belsey, because you do the elongation from above, and this makes the big difference.
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References |
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TopAbstract1. Introduction2. Methods3. Results4. DiscussionAppendix A. Conference...References |
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  S. Mattioli, M. L. Lugaresi, M. Costantini, A. Del Genio, N. Di Martino, L. Fei, U. Fumagalli, V. Maffettone, L. Monaco, M. Morino, et al. The short esophagus: intraoperative assessment of esophageal length. J. Thorac. Cardiovasc. Surg., October 1, 2008; 136(4): 834 - 841. [Abstract] [Full Text] [PDF]
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