Study of the Effectiveness
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1 An Experimental Study of the Effectiveness of Various Antireflux Operations Howard K. Leonardi, M.D., Myles E. Lee, M.D., M. Fathi El-Kurd, M.B., Ch.B., and F. Henry Ellis, Jr., M.D., Ph.D. ABSTRACT After a hypotensive lower esophageal sphincter was created in cats by circular myectomy of the distal esophagus, a comparative study was performed of the sphincter-enhancing operations currently in use: the Nissen fundoplication, the Belsey Mark IV, and the Hill posterior gastropexy. Subdiaphragmatic transposition of the myectomized segment was included to assess the effectiveness of intraabdominal positioning on lower esophageal sphincter competence. The mean lower esophageal sphincter pressure after Nissen fundoplication (21.7 f 1.5 cm Ha) did not differ significantly from control values (24.3 f 1.8 cm H,O), whereas significantly lower pressures were recorded after the Belsey Mark IV (11.7 k 1.5 cm H@), Hill posterior gastropexy (9.0 f 1.5 cm HP), and subdiaphragmatic transposition (4.0 k 1.5 cm Ha) procedures. The adaptive response of the lower esophageal sphincter to increased intragastric pressure was restored to near normal levels by both the Nissen and Belsey procedures, whereas the Hill posterior gastropexy and subdiaphragmatic transposition were less effective. In addition, ph reflux testing clearly indicated that the Nissen fundoplication afforded maximum protection against acid reflux. The experimental evidence suggests that optimum results in the surgical treatment of gastroesophageal reflux are achieved when the resting lower esophageal sphincter pressure and the adaptive response are restored to normal levels. The Nissen fun- From the Department of Thoracic and Cardiovascular Surgery and Sias Research Laboratory, Lahey Clinic Foundation, Boston, MA. Supported in part by Grant AM from the National Institutes of Health. We gratefully acknowledge the assistance of Ms. Anne D. Sevin for the statistical analysis of the experimental data, and John Cormack, Research Assistant in Surgery, and Margaret Gorrilla, R.N., for their technical assistance. Presented at the Thirteenth Annual Meeting of The Society of Thoracic Surgeons, Jan 24-26, 1977, San Francisco, CA. Address reprint requests to Dr. Ellis, Department of Surgery, Lahey Clinic Foundation, 605 Commonwealth Ave, Boston, MA doplication accomplishes these objectives more effectively than the alternative antireflux procedures. Recognition that gastroesophageal reflux is primarily the result of a physiological rather than an anatomical abnormality [51 has led to the development of a variety of surgical procedures designed to restore normal lower esophageal sphincter function. These procedures include the Nissen fundoplication, the Belsey Mark IV, and the Hill posterior gastropexy. Each method involves techniques of encircling the distal esophagus to varying degrees with adjacent gastric fundus. To date, none of these procedures has been shown conclusively to be superior to the others. This study was undertaken to clarify the issue. The cat was selected as the experimental animal because of anatomical similarities between the feline and human esophagus [31. Materials and Methods Operative Procedures The lower esophageal sphincter of 40 laboratory cats was rendered hypotensive by means of the technique originally described by Vandertoll and associates [18] (Fig 1). Circular myectomy of the distal 2 cm of esophagus was performed with careful preservation of vagal innervation to the stomach. Operative procedures designed to restore lower esophageal sphincter function included the Nissen fundoplication (10 cats), the Belsey Mark IV (10 cats), the Hill posterior gastropexy (10 cats), and subdiaphragmatic transposition of the myectomized segment (10 cats). The last procedure was included to assess the effect of intraabdominal positioning alone on the hypotensive lower esophageal sphincter. The Nissen, Belsey, and Hill procedures were performed in the standard fashion [l, 10, 161. Subdiaphragmatic transposition was accomplished by securing the myectomized segment below the dia- 215
2 216 The Annals of Thoracic Surgery Vol 24 No 3 September 1977 Subdiaphragmatic 1 transposition Fig 1. Technique ofmyectomy and the various sphincter-enhancingprocedures used in this study. phragm with six mattress sutures, incorporating diaphragm and esophageal musculature just proximal to the myectomy. All procedures were performed under intravenously induced sodium pentobarbital anesthesia in a dose of 20 mg per kilogram of body weight. Endotracheal intubation was carried out and respirations were maintained with a Bennett PR-1A respirator. Manometric Techniques Esophageal manometry was performed using a continuously perfused dual catheter system.* Each catheter had two laterally positioned pressure-sensing orifices spaced 3 cm apart. A *Intramedic PE 205 tubing. Harvard infusion pumpt delivered ml of distilled water per minute through each catheter. The catheters were connected to external transducers,$ and pressures were recorded graphically on a multichannel recorder, calibrated to create a 1 cm deflection for each 10 cm of water pressure. The catheters were withdrawn at the rate of 0.5 cm per second, and lower esophageal sphincter pressure was determined in reference to gastric pressure recorded in the fundus, which was arbitrarily considered as zero. Maximal end-inspiratory and endexpiratory pressures were averaged to obtain the mean maximal sphincter pressure. A pneumograph recorded the respirations. The adaptive response of the lower tmodel 941, Harvard Apparatus Co, Millis, MA. *Statham P23Db Transducer, Gould-Statham Instruments, Hato Rey, Puerto Rico. 5DR8, Electronics for Medicine, White Plains, NY.
3 217 Leonardi et al: Antireflux Operations esophageal sphincter was measured by manometrically positioning the catheters so that the distal orifice was within the stomach and the proximal orifice within the lower esophageal sphincter. Abdominal compression was applied manually while pressures were recorded. A ratio of the increment in sphincteric pressure to the increment in intragastric pressure of 1.4 or more was accepted as a normal response. The hormonal response of the lower esophageal sphincter was assessed using pentagastrin. A 10 pglkg dose was administered intravenously, and resting pressures and lengths of the lower esophageal sphincter were measured 30 minutes later. ph Reflux Testing Studies of ph were performed with a Beckman ph mete? utilizing an exploring electrodet for ph measurements and a reference electrode.$ A length of polyethylene tubing was introduced into the stomach, and 15 ml of 0.1 N hydrochloric acid was instilled. The tubing was flushed with distilled water during rapid withdrawal. The exploring electrode was passed into the esophagus until it met the resistance of the lower esophageal sphincter and was then withdrawn 3 cm, and a ph reading was taken to preclude the presence of residual acid. If the ph was 5 or higher, abdominal compression was applied manually and the ph noted. Reflux was considered present if a ph of 4.5 or less was recorded. Methods of Evaluation Esophageal manometry and ph reflux testing, as described, were performed preoperatively on unanesthetized animals. All operative survivors were studied approximately three weeks postoperatively in a similar fashion. Intraoperative testing was performed after myectomy to confirm lower esophageal sphincter incompetence before each sphincter-enhancing procedure was performed. An additional subgroup of myectomized control animals was studied in an *Zeromatic SS-3, Beckman Instruments, Wakefield, MA. tmodel39042, Beckman Instruments, Wakefield, MA. $Model 40242, Beckman Instruments, Wakefield, MA. unanesthetized state approximately three weeks after myectomy to verify the permanence of sphincter removal. Analysis of variance was used to compare the four late postoperative groups to each other and to the preoperative controls. In all instances when the results of this analysis revealed a significant difference in the mean values of the groups, the Scheffe method of multiple comparisons was used to determine which group means were significantly different from each other. Results Of the 40 cats, 27 were available for postoperative studies distributed as follows: Nissen fundoplication (7), Belsey Mark IV (7), Hill posterior gastropexy (7), and subdiaphragmatic transposition (6). The results are summarized in the Table and are expressed as mean values k SEM. Resting lower esophageal sphincter pressures in the various experimental groups are presented in Figures 2 to 4. The Nissen fundoplication was most effective in restoring lower esophageal sphincter pressures to control levels. In contrast, the Belsey, Hill, and subdiaphragmatic transposition procedures produced lower esophageal sphincter pressures significantly lower than the controls when analyzed statistically. Lower esophageal sphincter length was restored equally well by the Nissen, Belsey, and Hill procedures. Subdiaphragmatic transposition was less effective in this respect. Abdominal compression in normal controls produced a ratio of increment in sphincteric pressure to increment in intragastric pressure of 1.6 k 0.2. Both the Nissen and the Belsey procedures restored the adaptive response to near normal levels that did not differ significantly from control values. Following the Hill posterior gastropexy and subdiaphragmatic transposition, the adaptive response was strikingly diminished. The results of the ph reflux test are presented in Figure 5. A mean distal esophageal ph of 5.9 k 0.13 was obtained in control animals. Reflux could not be induced after the Nissen fundoplication, while the Belsey, Hill, and subdiaphragmatic transposition procedures provided inferior protection against acid reflux.
4 218 The Annals of Thoracic Surgery Vol 24 No 3 September 1977 Lower Esophageal Sphincter Evaluations following Myectomy and Repair Compared to Normal and Myectomized Cats LES Pressure LES Length LES LES Adaptive ph Reflux after Penta- after Penta- No. of Pressure Length Response Test gastrin gastrin Group Animals (cm HzO) (cm) (ASP/AGP) (ph) (cmhzo) (cm) Normal control f f f f k f 0.2 Myectomized f LOa 0.5 f 0.2a 0.9 f 0.02b 4.2 f 0.3a control Nissen fundo f f f f f * 0.3 plication Belsey Mark TV f 1.5b 1.8 f _t f 0.4b 8.3 f f 0.4 Hill posterior f 1.5a 1.4 f f 0.02b 2.5 f O.la 9.0 f f 0.2 gas tropexy Subdiaphragmatic 6 4.0? l.sa 1.0 f 0.3b 1.1 f 0.04b " 5.5 f f 0.7 transposition ap < compared to control values. bp < 0.05 compared to control values. Results expressed as mean values f SEM. LES = lower esophageal sphincter; SP = sphincter pressure; GP = gastric pressurr. NORMAL POSTMY ECTOMY POST NISSEN FUNDOPLICATION H PZ MYECTOMIZED SEGMENT Esoph IOsec HPZ neumogmph HPZn Fig2. Resting lower esophageal sphincter pressures after Nissen fundoplication compared with a normal control and a rnyectomized animal. (Baseline markings = 1 cm withdrawals. HPZ = high-pressure zone.) While parenterally administered pentagastrin produced a marked increase in the amplitude and length of the lower esophageal sphincter in normal controls, go response could be demonstrated in any of the postoperative groups. Comment A few experimental studies have compared the Nissen, Belsey, and Hill procedures using objec- tive measurements of lower esophageal sphincter function in a controlled fashion. Bombeck and associates [21 studied a variety of sphincter-enhancing procedures in dogs whose lower esophageal sphincter was rendered incompetent by myectomy. Only the Nissen fundoplication was uniformly successful in preventing reflux as assessed by cinefluorography and esophageal biopsy. Unfortunately, manometric studies were not performed. In addition, inherent differences in the muscular anatomy of the canine and human esophagus make extrapolation of results uncertain [8, 91. Butterfields postmortem studies E41 used
5 219 Leonardi et al: Antireflux Operations POSTNISSEN fs POST BELSEY POST H ILL POST SUBDIAPHRAGMATIC TRANSPOSITION HPZ H PZ Esoph w,* Stom Esoph b d HPZA H PZ Fig 3. Resting lower esophageal sphincter pressures after each of the four experimentalprocedures. (Baseline markings = 1 cm withdrawals. HPZ = high-pressure zone.) PRESSURE (cm HZO) r PCO 6 CONTROL MYECTOMV NISSEN BELSEY HILL SUBDIAPH. TRANSPOSITION Fig4. Mean amplitude of lower esophageal sphincter pressure in the postoperativegroups compared with controls. (*p values obtained by comparison with controls.) human cadaver stomachs filled with water to compare the effectiveness of the Nissen, Belsey, and Hill repairs. Although the Nissen and Hill repairs were satisfactory, the circumstances were hardly physiological. The majority of clinical studies reported suffer from a lack of objective preoperative and postoperative documentation of lower esophageal sphincter function. Many series also include cases complicated by stricture, bleeding, and previously unsuccessful repairs. Such circumstances make valid comparisons extremely difficult. Perhaps the most comprehensive comparative clinical study was that of DeMeester and associates [6] in which the Nissen, Belsey, and Hill procedures were evaluated. Esophagitis was present in 38 of 45 patients. Preoperative and postoperative studies included historical, radiographic, and manometric assessments as well as ph reflux testing. The Nissen fundoplication was most effective in restoring lower esophageal sphincter function and preventing reflux. Recently, Nicholson and Nohl-Oser [151 have confirmed the superiority of the Nissen procedure as compared to the Belsey Mark IV in preventing gastroesophageal reflux in man. The experimental study compared the effectiveness of the Nissen, Belsey, and Hill procedures in restoring function to the lower esophageal sphincter rendered incompetent by myectomy. Subdiaphragmatic transposition of the myectomized segment was included to assess the effect of intraabdominal positioning on lower esophageal sphincter function, for some have suggested that establishment of an infradiaphragmatic segment of esophagus exposed to high intraabdominal pressure is critical to the surgical control of reflux [ll, 141. Our data indicate that fundoplication is significantly more effective than either the Belsey or Hill procedure in restoring resting lower esophageal sphincter pressure to normal levels. Positioning the myectomized distal esophagus intraabdominally was ineffective in restoring a high-pressure zone and in preventing reflux. Restoration of lower esophageal sphincter pressure correlated positively with protection
6 220 The Annals of Thoracic Surgery Vol 24 No 3 September 1977 PC.05 T ISEM PC CONTROL MYECTOMY NISSEN EELSEY HILL SUEOIAPH. TRANSPOSITION Fig 5. Mean distal esophageal ph after reflux testing in the postoperativegroups compared with controls. (*p values obtained by comparison with controls.) against reflux as shown in the ph reflux test and thus lends support to the concept that fundoplication succeeds at least in part by mechanical strengthening of the lower esophageal sphincter. Restoration of lower esophageal sphincter length seemed relatively less important since reflux occurred after the Belsey and Hill procedures, which restored sphincter lengths to normal. Both the Nissen and Belsey procedures restored the adaptive response of the lower esophageal sphincter to normal levels, whereas the Hill posterior gastropexy and the subdiaphragmatic transposition procedure were less effective. The clinical studies of DeMeester and colleagues [61 and DiMarino and co-workers [7] revealed a similar deficiency in the gastropexy. The explanation, although uncertain, may relate to the lesser degree of fundic wrapping used in this operation. Whatever the explanation, this aspect of lower esophageal sphincter function, which is believed to be neural in origin, was restored by two of the experimental procedures, suggesting that their effect on sphincter function is more than merely mechanical. The absence of a sphincteric response to parenteralpentagastrin in ourpostoperative groups is perplexing. Evidence of a gastrin response after Belsey and Hill repairs has been presented in the clinical study of Lipshutz and associates [131. Siewart and colleagues [171 presented ex- perimental evidence of a comparable gastrin response after fundoplication in myectomized dogs. Additional in vitro studies by this group disclosed that canine fundic muscle responded to gastrin in a way very similar to the lower esophageal sphincter. In contrast, in vitro studies by Lipshutz and associates [12] comparing the gastrin dose response curves of fundic, lower esophageal sphincter, and proximal esophageal muscle strips in the opossum suggested the presence of gastrin receptors in the lower esophageal sphincter but not in adjacent gastric musculature. In short, it seems plausible that a species-dependent difference may exist with regard to the gastrin sensitivity of fundic muscle, which could explain the absence of a gastrin response in our experimental animals. References 1. Baue AE, Belsey RH: The treatment of sliding hiatus hernia and reflux esophagitis by the Mark IV technique. Surgery 62:396, Bombeck CT, Coelho RG, Castro VA, et al: An experimental comparison of procedures for the operative correction of gastroesophageal reflux. Bull SOC Int Chir 30:435, Bremner CG, Shorter RG, Ellis FH Jr: Anatomy of feline esophagus with special reference to its muscular wall and phrenoesophageal membrane. J Surg Res 10:327, Butterfield WC: Current hiatal hernia repairs: similarities, mechanisms, and extended indications-an autopsy study. Surgery 69:910, Cohen S, Harris LD: Does hiatus hernia affect competence of the gastroesophageal sphincter? N Engl J Med 284:1053, DeMeester TR, Johnson LF, Kent AH: Evaluation of current operations for the prevention of gastroesophageal reflux. Ann Surg 180:511, DiMarino AJ, Rosato E, Rosato F, et al: Improvement in lower esophageal sphincter pressure following surgery for complicated gastroesophageal reflux. Ann Surg 181:239, Earlam RJ, Ellis FH Jr: Repair of experimental hiatal hernia in dogs. Arch Surg 95:585, Higgs B, Shorter RG, Ellis FH Jr: A study of the anatomy of the human esophagus with special reference to the gastroesophageal sphincter. J Surg Res 5:503, Hill LD: An effective operation for hiatal hernia: an eight year appraisal. Ann Surg 166:681, Kaunitz VH, Maas LC, Vastola DL, et al: A simple physiological repair of diaphragmatic hernia: re-
7 221 Leonardi et al: Antireflux Operations positioning of the lower esophageal sphincter. J Thorac Cardiovasc Surg 68:513, Lipshutz W, Cohen S: Physiological determinants of lower esophageal sphincter function. Gastroenterology 61:16, Lipshutz WH, Eckert RJ, Gaskins RD, et al: Normal lower-esophageal-sphincter function after surgical treatment of gastroesophageal reflux. N Engl J Med 291:1107, Mustard RA: A survey of techniques and results of hiatus hernia repair. Surg Gynecol Obstet 130:131, Nicholson DA, Nohl-Oser HC: Hiatus hernia: a comparison between two methods of fundoplication by evaluation of the long-term results. J Thorac Cardiovasc Surg 72:938, Nissen, R: The treatment of hiatal hernia and esophageal reflw by fundoplication, in Hernia. Edited by LM Nyhus, H Harkins. Philadelphia, Lippincott, 1964, pp Siewart R, Koch A, Kirtch H, et al: The mechanism of action of fundoplication. Bull SOC Int Chir 34:284, Vandertoll DJ, Ellis FH Jr, Schlegel JF, et al: An experimental study of the role of gastric and esophageal muscle in gastroesophageal competence. Surg Gynecol Obstet 122:579, 1966 Discussion DR. DAVID B. SKINNER (Chicago, IL): This study demonstrates that a cat having the misfortune of losing its distal esophageal muscle is better off being reconstructed by a full rather than a partial fundoplication. I have no disagreement with this conclusion, nor with the experimental methods. The study does confirm previously reported observations and concepts, but it does not advance our understanding of the antireflux mechanisms. Two factors contribute to the success of antireflux operations for restoration of the high-pressure zone. One is the creation of an intraabdominal segment of the small-diameter swallowing tube entering the large-diameter gastric pouch in a common pressure chamber. The laws of physics indicate that the smaller-diameter tube should have a greater wall tension. Dr. Leonardi has shown that this is true even if the esophageal muscle is excised and the wall is sutured to the rim of the hiatus to hold the tube in an open position. This law of Laplace is the basis for stressing the importance of an intraabdominal segment of esophagus in these repairs. The second factor in the antireflux operation is mechanical compression of the swallowing tube by the partial or full fundoplication. This wrap contributes to the amplitude of the high-pressure zone. Of the several repairs, the full Nissen fundoplication causes the greatest increase in pressure and will make a competent antireflux valve, even if left in the chest (as Dr. Ellis Jones reported to this society in 1970) or even when done as an in vitro cadaver repair, as Butterfield has reported. Our own previously published patient data show that pressure is raised more by the Nissen fundoplication than by the partial fundoplication described by Belsey and Hill. DeMeester s randomized patient study also showed this, and Dr. Leonardi has reconfirmed this in a different animal species. The real unsettled clinical controversy is not whether the full fundoplication is a tighter antireflux valve-which it is in both human and animal studie-but whether a less tight partial fundoplication coupled with placement of an intact esophageal wall in an intraabdominal position, which is also known to control reflux, will do so with less gas-bloat syndrome and inability to belch or vomit. A study in cats with a circular myectomy, which shows that full fundoplication is better than partial, is not applicable to this current clinical debate. It is applicable, however, to a patient I treated recently for a circumferential leiomyoma of the distal esophagus. The tumor was resected, leaving the mucosal tube intact. Reconstruction using the full fundoplication worked very well, and the high-pressure zone and reflux control were maintained. DR. JOEL COOPER (Toronto, Ont, Canada): We have evaluated lower esophageal pressure of the Collis- Belsey repair by measuring intraesophageal pressures in 9 patients during the various phases of the operation itself. We were aided in this by using the new MP-3 transducer. This miniature transducer contains three small transducers spaced 5 cm apart. Because it can be felt in the esophagus at the time of operation, the surgeon can be very precise as to the exact location of the individual transducers. Postoperative manometric studies were done using a fluoroscope to locate the transducers with the aid of metallic clips left at the upper and lower ends of the gastroplasty during the procedure. At operation a gastroplasty tube 5 cm long was created from the lesser curvature of the stomach. The transducers were then advanced into the stomach and slowly withdrawn into the esophagus. In each instance, as soon as the transducer reached the lowest limit of the gastroplasty tube, there was a sharp increase in pressure. When the transducer was withdrawn past the upper end of the gastroplasty, there was a sharp fall in pressure. Thus the entire gastroplasty tube functions as a new high-pressure zone. It is honnonally sensitive, relaxes on swallowing, responds dramatically to injection of pentagastrin by increasing its tone, and relaxes when buscopan is given intravenously. After the Belsey fundoplication has been added, the pressures are rerecorded, and an even higher pressure is recorded in the gastroplasty tube. In an intraoperative study we showed that pressure rose in one lead as the transducer was withdrawn
8 222 The Annals of Thoracic Surgery Vol 24 No 3 September 1977 from the stomach into the gastroplasty, and then fell sharply as soon as the transducer left the gastroplasty. The pressure reached about 55 to 60 cm H20. Preliminary data on 9 patients studied showed the average preoperative pressure to be 15 cm H20. After anesthesia, with the chest closed or open, the pressure was about the same, 13 to 15 cm H20. After operation the pressure in the gastroplasty averaged 30 cm HZO, which rose to 57 upon completion of the Belsey fundoplication and repair. One week postoperatively the pressure in the gastroplasty was 36 cm H20; at three months it still seemed to be holding; and we have some six-month data suggesting it is staying at about the same level. It is really too soon to say how these data relate to the quality of the clinical results obtained. DR. LEONARDI: I wish to thank the discussants, Drs. Skinner and Cooper, for their comments. Dr. Skinner raised a point about the importance of the intraabdominal position of the lower esophagus as part of the antireflux mechanism and interpreted our experimental data as supporting this concept. While it is true that the myectomized segment showed a slight pressure increase when advanced into an intraabdominal position, its level of pressure (4.0 * 1.5 cm HzO) was insignificant compared with the normal cat s lower sphincter pressure and was well below that achieved by all the antireflux techniques studied. While we generally reestablish an intraabdominal esophagus when treating patients with a sliding hernia and hypotension of the lower sphincter, we are not reluctant to leave the esophagus wrapped by gastric fundus within the chest, providing that the stomach cannot be obstructed by the diaphragmatic hiatus. This is accomplished by widening the hiatus somewhat and is most applicable in instances of a short esophagus. This experimental study sheds no light on the risk of the gas-bloat syndrome following the Nissen procedure. However, in our clinical experience the gasbloat syndrome following a Nissen procedure is exceedingly rare. We believe this is explained by the placement of a 36F mercury-filled dilator or Ewald tube within the esophagus during performance of the plication. This precaution ensures that the wrap is not too tight. Notice from the American Board of Thoracic Surgery The 1977 annual certifying examination of the Please address all communications to the American Board of Thoracic Surgery (written American Board of Thoracic Surgery, E and oral) will be held in Chicago in March, Seven Mile Rd, Detroit, MI Final date for filing application was August 1, 1977.
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