Effects of circular myotomy on the healing of esophageal suture anastomosis: an experimental study

Efeitos da miotomia circular na cicatrização das anastomoses esofágicas: estudo experimental

EFFECTS OF CIRCULAR MYOTOMY ON THE HEALING OF ESOPHAGEAL SUTURE ANASTOMOSIS: AN EXPERIMENTAL STUDY

Uenis Tannuri, Ana Cristina Aoun Tannuri, Marina Fussae Fukutaki, Maura Salaroli de Oliveira, Valéria Marques Figueira Muoio and Alfonso Araujo Massaguer

RHCFAP/2953

TANNURI, U. et al. - Effects of circular myotomy on the healing of esophageal suture anastomosis: An experimental study. Rev. Hosp. Clín. Fac. Med. S. Paulo 54 (1): 9 - 16, 1999.

SUMMARY: For esophageal reconstruction in newborns with esophageal atresia, esophageal reunion with an end-to-end anastomosis is the ideal procedure, although it may result in leaks and strictures due to tension on the suture line, mainly in cases with a wide gap between the ends. Circular myotomy (Livaditis' procedure) is the best method to elongate the proximal esophageal pouch and reduce anastomotic tension. This experimental investigation in dogs was undertaken to attempt to verify that circular myotomy decreases the anastomotic leak rate in newborns with wide gap esophageal atresia, and to analyze whether the technique promotes morphologic changes in the anastomotic scar. A pilot study demonstrated that it is necessary to resect more than 8 cm (40% of the total esophageal length) in order to obtain high leak rates. In the experimental project, such resection was performed in dogs divided into two groups (control group, anastomosis only, and experimental group, anastomosis plus circular myotomy in the proximal esophageal segment). The animals were killed in the 14th postoperative day, submitted to autopsy, and were evaluated as to the presence of leaks and strictures, as well as to the features (macroscopic and microscopic aspects) of the anastomosis. Leak rates were the same in both groups. Morphometric analysis revealed that in animals in the experimental group, the anastomotic scar was thinner than the control animals, and the isolated muscular manchette distal to the site of myotomy was replaced by fibrous tissue. Correspondingly, a decreased number of newly formed small vessels were noted in the experimental animals, compared to control animals.

We concluded that circular myotomy does not decrease the incidence of anastomotic leaks, and it also promotes deleterious changes in anastomotic healing.

DESCRIPTORS: Esophagus. Circular esophageal myotomy. Esophageal atresia. Long gap.

Despite medical progress, surgical procedures for establishment of esophageal continuity are a challenge for the surgeon because of the anatomical and topographical peculiarities of the esophagus. Among the diseases in which a primary esophageal anastomosis is indicated, one of the most important is atresia of the esophagus, a congenital disorder of the digestive apparatus in the newborn^{5,16,31,38,59}.

End-to-end anastomosis between the esophageal segments is the treatment of choice in neonates with esophageal atresia. However, this procedure may result in leaks and strictures in the suture line, which occur more frequently here than in other viscera of gastrointestinal tract. These complications are related to the tension on the anastomosis, and the tension is larger in the wide gap cases. Additionally, the natural contraction of longitudinal muscular layer causes retraction of the esophageal ends, separating the anastomotic edges. Finally, in contrast to the bowel submitted to a surgical trauma, the esophagus does not decrease its peristalsis during the early postoperative period.

Esophageal anastomotic leaks are the most serious complication in the first postoperative days, particularly when the suture is placed in the posterior mediastinum. Leakage of saliva and secretions causes acute mediastinitis and sepsis, which, if not corrected by surgery, may result in the patient's death. Thus, recent data from our Pediatric Surgery Division demonstrated that among 41 newborns with esophageal atresia, three of them died because of dehiscence of anastomosis.⁵⁸ Similarly, several authors have emphasized the morbidity and mortality of esophageal leaks in the newborn^{7,10,13,52,54,64}.

We have observed that esophageal leaks are more frequent in cases with long distances between the esophageal ends, because of the severe anastomotic tension. It has been demonstrated in piglets that when approximation force between the esophageal ends was greater than 75 g, leaks occurred, and increased fibrosis was noted at the anastomosis.⁵⁷ As a result, techniques have been proposed for mechanical reinforcement of esophageal anastomosis or elongating the esophageal pouches, primarily the proximal one. In the newborn with esophageal atresia, the proximal end is dilated and the wall is thicker because of fetal swallowing movements during intrauterine life.^10,15,18,20

Delayed surgical reconstruction and circular myotomy of the proximal esophageal pouch are two approaches that have been used to establish esophageal continuity. The first consists of performing esophageal anastomosis after 3 to 6 months and/or after baby's weight doubles, thus permitting the spontaneous growth of esophageal segments.^{6,8,11,14,39,45,48} During this waiting period, the child is fed by gastrostomy. The other method is to section the circular muscular layer of esophagus in order to elongate the proximal esophageal pouch and reduce anastomotic tension.^25,28

Delayed primary anastomosis was performed in 12 newborns with wide gap esophageal atresia treated in the Pediatric Surgery Division of University of São Paulo School of Medicine (Child Institute Prof. Pedro de Alcantara). After an average waiting period of 4 months, the growth of the esophageal ends was observed in 4 cases, although primary anastomosis could be done in only 2 of them.³² Thus, this procedure is limited by the risks and costs of a prolonged hospital stay.

In 1973, Livaditis and colleagues first demonstrated the utility of circular myotomy in the reconstruction of long-gap esophageal atresia. According to these authors, circular myotomy permits a technically easier accomplisshment of the anastomosis by reducing anastomotic tension. It also obviates the need for esophageal mobilization and minor upward traction of the anastomosed proximal segment postoperatively.^25-29 Since the myotomy reduces the tension, the sutures can be easily tied, and they do not cut through the esophageal wall even in wide gap cases. Finally, circular myotomy prevents the transmission of contractions to the suture line induced by straining or efforts at swallowing.

Subsequently, several authors have emphasized the utility of circular myotomy in the proximal esophageal pouch, alone or together with the distal one, for relief of anastomotic tension.^{12,19,21,23,30,40,46,47,50,51} However, in our personal experience with operating on more than 150 newborns with esophageal atresia (Tannuri, U.), we have not observed the utility of Livaditis' circular myotomy. We have used this technique in five newborns in which the distance between the ends was greater than 3 cm, and although a relief of anastomotic tension could be obtained, leaks occurred in all cases. Furthermore, we noted an intensive bleeding due to the sectioning of small arterial branches of muscular layer that would certainly decrease the blood supply to the suture line.

Although anastomotic leaks are related to the tension on the suture line, there is no controlled experimental or clinical work demonstrating that Livaditis' myotomy decreases the rates of breakdown of esophageal anastomosis. Moreover, the utility of circular myotomy was recently contested by Boyle and colleagnes³, who treated eight newborns with long-gap esophageal atresia (3.5 to 6.0 cm) and showed that, despite severe anastomotic tension, in all cases, without any lengthening procedure, there were no anastomotic leaks. These authors were concerned about the probable complications at the myotomy site, such as diverticular formation and ballooning of the mucosa.

Taking into consideration the high incidence of newborns with esophageal atresia treated in the Pediatric Surgery Division of University of São Paulo School of Medicine, and since circular myotomy proposed by Livaditis is the most widely used method of lengthening the esophagus to allow primary repair, we decided to conduct the present study in order to verify that circular myotomy decreases the incidence of leaks in anastomosis performed under severe tension. In addition, we wanted to determine whether circular myotomy causes any morphologic change in the scar tissue of the anastomosis.

MATERIAL AND METHODS

Experimental Animal - Forty-eight small dogs (weighing 5 to 10 kg) of both sexes were used. We opted for little animals for better comparison of this model with human newborns.

Pilot Study - The objective of this initial phase was to establish the length of esophagus that could be resected and still allow an anastomosis between the ends under severe tension and result in a high rate of leakage at the anastomosis.

Ten dogs that were submitted to cervical esophagectomy were divided into two groups, with 5 animals each (Table 1).

After anesthesia with thionembutal 4.0% (0.6-0.7 ml/kg) and endotracheal intubation, the dogs were placed in dorsal recumbent position. To better expose the left cervical region, the neck was extended, with the head and neck turned to the right side.

A left longitudinal lateral incision of 6.0 to 8.0 cm was made. By blunt dissection between the fascial planes of the cervical muscles, the esophagus was exposed and dissected from the laryngeal and vagus nerves and carotid artery. The esophagus was mobilized over a length similar to the proposed resection. The esophagus was divided 3 cm below the level of cricoid cartilage, and 0 to 8.0 cm segments of the esophagus distal to this point were resected.

After esophageal resection, fine suturing of the segments was performed using one layer of continuous 4-0 nylon suture and an atraumatic needle, with care being taken to include mucosa in the sutures. The incision was closed in layers.

Fourteen days after the surgery, the dogs were sacrificed by intravenous injection of thionembutal 4.0% and submitted to autopsy. Similarly, the non-surviving animals were submitted to autopsy. The anastomotic sites were carefully examined. Longitudinal sections of the anastomotic area were obtained and stained with hematoxylin (H) and eosin (E) for microscopic evaluation.

Results of Pilot Study

The incidences of leaks in both groups of pilot study were low (20% in each group). In all the animals in which the anastomoses were intact, the histologic study demonstrated that there was a normal healing of all layers, with contact between the edges of the mucosa. We concluded that these anastomoses were performed without tension, in contrast to anastomoses performed in newborns with wide gap esophageal atresia. Thus, the efficacy of the myotomy and its effect on anastomotic tension could not be evaluated if 0 to 8 cm resections were performed.

Taking into consideration the results of pilot study, we decided to perform a wide mobilization of cervical and thoracic esophagus by blunt digital dissection, and resect the maximum length of esophagus (more than 8 cm, which comprised approximately 40% of the esophagus) that would still allow successful anastomosis.

Experimental Design - Thirty-eight small dogs (weighing 5 to 10 kg) of both sexes were divided in two groups (Table 2).

As in the pilot study, the dogs were anesthetized and placed in dorsal position with the neck in extension and the head turned to the right side. Through a 6 to 8 cm left cervicotomy, the esophagus was approached and extensively mobilized from the pharynx down to the thoracic inlet and up to level of the left lung hilus. This dissection was performed close to esophagus, and care was taken to avoid the injury to the mediastinal pleura. Usually a few bleeding vessels resulting from the esophageal dissection required ligation with a fine cotton thread. After completion of this dissection, the surgeon could palpate with his finger the left bronchus and the pulsating left lung hilus.

Four nylon sutures (two proximal and two distal sutures) were placed through the esophagus at known distance apart, to serve for traction and to verify the maximum length of esophageal segment that was allowed to be resected, resulting in an anastomosis under severe tension. The segment of esophagus was resected, leaving an extension of 3 cm of proximal esophagus.

In the myotomy group, a complete circumferential division of both muscle layers was performed in the proximal esophageal segment 1.5 cm from the resected end, according to the original description of Livaditis. This procedure was accomplished using curve scissors, taking care to avoid injury to the mucosa or to the vessels of the submucosa (Fig. 1).

As in the pilot study, suturing of the ends of the divided esophagus was performed using one layer of continuous 4-0 nylon suture, with care being taken to include mucosa in the sutures. While performing the anastomosis, both esophageal ends were approximated by the traction sutures previously placed. Using this technique, the sutures could be easily tied, and they did not cut through the esophageal wall despite the severe tension. After the completion of the anastomosis, it was noted in the myotomy group that the musculature of the esophagus retracted markedly, exposing at least 2 to 3 cm of the underlying submucosa. The cervical incision was closed in layers without drainage. In the postoperative period, the dogs were allowed to drink water and to eat a soft diet.

Autopsy - Macroscopy - All surviving dogs were observed for 14 days, and after this period of time they were sacrificed with an overdose of thionembutal 4.0% given intravenously and autopsied. The esophagus was dissected out and examined thoroughly. The dogs that failed to survive were also subjected to a complete autopsy. The esophagus was evaluated for the presence of leaks or strictures at the site of anastomosis, was cut longitudinally, and the mucosal surface was examined.

Microscopy - After macroscopic evaluation, the anastomotic areas were fixed in 10% formalin, paraffin embedded, sectioned longitudinally, and stained with hematoxylin (H) and eosin (E) for microscopic examination.

The histologic examination was accomplished using a Nikon microscope equipped with a 20X magnification eyepiece, with 5X and 10X magnification objectives. For morphometric studies of esophageal scar the same microscope was used with a 5X magnification objective and a 20X magnification eyepiece that contained a test scale of 1 mm. The scars were studied in 20 random microscopic fields per histological section.

Statistical Analysis - Results were reported as mean ± standard deviation, and they were compared using the Student's t test. The chi-square test was used to compare the leak rates of the experimental groups. The level of significance was P < 0.05.

RESULTS

Autopsy - Macroscopy - All non-surviving animals died of complete anastomotic breakdown, with pus and saliva deep in the neck and mediastinum. The surviving dogs were sacrificed 14 days after the surgery, and the autopsy revealed that the anastomoses were intact with some degree of stricture. The mucosal surface of the esophagus showed that the inner surface of the anastomoses was not epithelialized, but was completely healed with fibrous tissue. In the dogs of myotomy group, the gap between the edges of the divided musculature was bridged by a thin layer of fibrous tissue, and the muscular manchette distal to the site of myotomy could not be identified; there was evidence of fibrosis at this site. In these animals, the macroscopic examination showed that the thickness of the scar at the anastomosis was reduced in comparison with control animals. The anastomotic leak rate in the experimental group is shown in table 3.

Microscopy - Histologic examination showed that the scar at the anastomosis was formed by fibrous tissue, without mucosa or muscular tissue, with a lymphoplasmacytic infiltrate. In animals in the experimental group, this scar was considerably thinner than that of the control animals, and the isolated muscular manchette was replaced by fibrous tissue. Correspondingly, a decreased number of newly formed small vessels was noted in the experimental, compared to the control animals (Fig. 2 and 3).

The results of morphometric analyses of the scar at the anastomosis and the statistical calculations are listed in table 4.

DISCUSSION

The first step of the present experiment was to choose an adequate animal model, with a small size and esophageal morphology comparable to the human newborn. We initially chose the adult rabbit, whose weight is similar to the human newborn. However, after operating on 40 rabbits, we concluded that the rabbit was not appropriate for this investigation because of the high mortality rate in the postoperative period from causes not related to the surgery, mainly sepsis. Thus, we decided to use small dogs, provided by the Central Vivarium of University of São Paulo School of Medicine. When we operated on the first dog, we verified that the cervical and thoracic esophagus could be approached by a small cervicotomy and blunt dissection. Additionally, we noted that the muscular layer of the esophagus could be easily divided circumferentially and separated from the underlying mucosa by dissection.

The experimental model utilized in this study was designed to simulate the difficulties encountered by the pediatric surgeon in the correction of a wide gap esophageal atresia and in the performance of an anastomosis under severe tension.

Besides the undue tension, the other problem of esophageal anastomosis is the poor blood supply of the atretic esophagus. Extensive mobilization sometimes is necessary to approximate the esophageal segments, but the dissection of the distal portion is highly undesirable, since it may seriously impair the esophageal blood supply and lead to a non-viable anastomosis.³⁷ Thus, when the distance between the upper and lower esophageal pouches precludes primary anastomosis, an esophageal substitution procedure using colon conduit, gastric tube, or total gastric transposition is required.^{1,2,16,33,35,36,43,44,52,53,55-57,60,61,63,65}

Although esophageal substitution techniques are well described, every attempt should be made to use the patient's own esophagus. Thus, in cases of long gap esophageal atresia, primary anastomosis of widely separated esophageal pouches may be achieved after a period of growth and stretching of the esophagus.^9,18,39 However, Livaditis' circular myotomy of the proximal esophageal pouch has been the most utilized procedure to elongate the proximal segment and to reduce the tension in the anastomosis.

In newborns we have noted that when the distance between the esophageal segments is less than 2.5 cm, the techniques for esophageal elongation are unnecessary, since the anastomosis can be successfully accomplished even under high tension on the suture line. Additionally, Boyle et al³ carried out successful primary repair of ultra-long gap esophageal atresia without myotomies. We suspected that myotomies have been used without any advantage.

In the present experiment, the comparison of the experimental and control groups showed that the circular myotomy did not prevent postoperative anastomotic leaks, although this procedure could elongate the proximal esophageal segment. The circular myotomy neutralizes the tonus of the esophageal musculature, but cannot exert any effect on the submucosa, which is predominantly made up of elastic connective tissue with a loose attachment to the overlying musculature. Since the healing phenomena are predominant in the submucosa²⁶, we may conclude that circular myotomy is ineffective in preventing anastomotic leaks. These conclusions are in agreement with the results of other experimental works performed in dogs.^34,42

The morphometric analysis of the scar demonstrated a decreased thickness in the myotomized animals. This result has an important implication if we consider the increased risks of esophageal rupture at this site, particularly by endoscopic maneuvers.

Studies on the intrinsic blood supply of the esophagus in dogs and human beings demonstrated the submucosa to be by far the most vascular layer⁴¹. In addition, its vascular architecture exhibits a strictly longitudinal pattern as contrasted with the predominantly segmental arrangement encountered in the muscular layers. These findings suggest that the submucosa is to a large extent nutritionally independent of the surrounding musculature, and as a consequence, it is believed that myotomies or myectomies can be performed without compromising the blood supply to the demuscularized area⁴. Our results, demonstrating a decreased thickness of the scar at the anastomosis in the myotomized animals, do not agree with these statements, probably because the submucosal vascular plexus was partially damaged by the myotomy.

The destruction of the structural integrity of the esophagus musculature in consequence of circular myotomy deserves consideration. Motility disturbances²² and the late diverticular formation with ballooning of the mucosa at the myotomy site are the most serious consequences of circular myotomy. The latter complication has been associated with dysphagia resulting in malnutrition and ventilatory respiratory compromise and tracheomalacia when they reach large size.^49,62 Thus, modifications of Livaditis' myotomy to bridge a long gap esophageal atresia, like spiral myotomy^22,48 or several small horizontal incisions through the muscle layer²⁴, have been proposed.

In conclusion, we demonstrated in an animal model that the circular myotomy of the proximal end of the esophagus did not decrease the incidence of anastomosis breakdown and promotes deleterious changes in the healing of the suture line. Thus, in cases of long gap esophageal atresia, new techniques for esophageal elongating need to be researched in order to reduce the incidence of esophageal anastomosis complications.

ACKNOWLEDGMENTS: The authors are very grateful to Mrs. Maria Cecília Mendonça Coelho and Neide Aparecida da Silva Rosendo dos Santos for their excellent technical assistance. The authors thank the grants from B Braun Laboratories.

RESUMO

RHCFAP/2953

TANNURI, U. e col. - Efeitos da miotomia circular na cicatrização das anastomoses esofágicas: Estudo experimental. Rev. Hosp. Clín. Fac. Med. S. Paulo 54 (1): 9 - 16, 1999.

A anastomose término-terminal entre os segmentos esofágicos, embora constitua a melhor solução para a atresia do esôfago do recém-nascido, pode resultar em fístulas, deiscências ou estenoses devidas à tensão na linha de sutura, principalmente nos casos de grande distância entre os cotos. A miotomia circular do segmento proximal (manobra de Livaditis) é a técnica de alongamento esofágico mais utilizada. No presente trabalho experimental, realizado em cães, procurou-se verificar se esta técnica diminui o índice de deiscência de anastomose entre cotos sob grande tensão e estudar se ela promove alterações morfológicas na cicatriz da anastomose. O projeto piloto demonstrou que seria necessário ressecar 40% do esôfago para se obterem índices elevados de deiscência. No projeto experimental, realizou-se tal ressecção, e os cães foram divididos em dois grupos (grupo controle, apenas anastomose, e grupo experimental, anastomose com miotomia circular). Os animais foram mortos no 14º dia de pós-operatório e a seguir submetidos a necropsia, avaliando-se a presença de deiscência e estenose da anastomose. A avaliação microscópica constou de análise histológica qualitativa e histomorfometria da cicatriz da anastomose. Os índices de deiscência foram iguais nos dois grupos. Nos animais do grupo controle a espessura da fibrose e o número de vasos neoformados foram maiores que no grupo experimental. A avaliação morfométrica revelou que a miotomia promoveu diminuição na espessura da fibrose cicatricial. Concluiu-se que a miotomia circular não diminui a possibilidade de deiscência, além de promover alterações deletérias na cicatrização da anastomose.

DESCRITORES: Esôfago. Miotomia circular. Atresia de esôfago.

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Received for publication on the 04/11/98

From the Pediatric Surgery Laboratory (LIM-30) and Surgical Technique Divisions, University of São Paulo Medical School, São Paulo, Brazil. Address: Faculdade de Medicina da Universidade de São Paulo, Av. Dr. Arnaldo, 455, 4º andar, Sala 4106. Fone 30667479, Fax [phone] São Paulo - SP. CEP: 01246-000, Brazil.

Publication Dates

• Publication in this collection
  12 Sept 2000
• Date of issue
  Feb 1999

History

• Received
  04 Nov 1998