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5 May 1999
Approaches to
FOCAL POINT Esophageal Sutures
★One-layer closure of esophageal The Hebrew University of Jerusalem San Juan, Puerto Rico
incisions using the submucosa
as the holding layer, avoiding
Rehovot, Israel Carlos M. Mongil, DVM
penetration of the mucosa, and Merav H. Shamir, DVM
using absorbable suture material Ron Shahar, DVM, MSc
in an interrupted pattern permits Dudley E. Johnston, MVSc
normal esophageal healing
following surgery. ABSTRACT: Suturing the esophagus after esophagotomy or esophageal resection and anasto-
mosis can be problematic, and complications such as suture line breakdown, leakage, and
stenosis are reported. This article discusses esophageal anatomy and physiology and compli-
KEY FACTS cations associated with esophageal surgery; a history of suture methods used in esophageal
surgery is also provided. A new suture technique is described and evaluated based on a retro-
■ The surface epithelium of the spective study.
mucosa is stratified squamous
with varying degrees of
F
oreign bodies, tumors, and diverticula are some of the common reasons
keratinization in different
for performing an esophagotomy or esophageal resection and anastomosis.
species.
The method of closing esophageal incisions is controversial. Esophageal
incisions have traditionally been closed in two layers using different suture pat-
■ The collateral vascular pathways
terns and materials, and the mucosa has historically been considered the strength
in the wall of the esophagus are
layer of the esophageal wall. In 1988, Dallman1 revealed that the submucosa is
sufficient to maintain its viability
the functional holding layer of the esophagus and that including the mucosa in
and to ensure healing of an
the closure did not increase the strength of repair. This article presents a retro-
anastomosis when the entire
spective report of 21 clinical cases in which esophageal closure was performed
thoracic blood supply to the
using the submucosa as the holding layer, avoiding penetration of the mucosa,
esophagus is cut off.
and using absorbable suture material in an interrupted pattern.
■ One reason for the high rate
ESOPHAGEAL ANATOMY AND PHYSIOLOGY
of complications following
The esophagus is a simple muscular tube that has peristaltic activity and
esophageal surgery is that the
sphincters at both ends. The upper esophageal sphincter is a distinct anatomic
esophagus is in constant motion
structure comprised of muscle fibers of the cricopharyngeus muscle and circular
from respiration and swallowing.
muscle fibers of the proximal wall of the esophagus. The lower esophageal
sphincter performs a physiologic function (i.e., it prevents food from indiscrimi-
■ The submucosa is the functional
nately entering the esophagus from the stomach, thus keeping the esophagus
holding layer of the esophageal
empty), but no distinct muscular structures have been identified.2,3 The lower
wall.
sphincter also has a valvelike action to prevent acidic gastric reflux into the
esophagus during inspiration when the intraluminal pressure of the esophagus is
low.
In dogs, the esophagus narrows at four places: near its origin, near its termina-
tion, at the thoracic inlet, and over the base of the heart. This explains why most
obstructing foreign bodies are found at these sites. Also, the esophagus is fixed to
Compendium May 1999 20TH ANNIVERSARY Small Animal/Exotics
surrounding structures at these four sites, and the short Necrosis and perforation can occur (always at the level
distances between these sites prevents mobilization of of the second thoracic vertebra) when both the cervical
the esophagus. This must be taken into consideration and thoracic segmental blood supplies to the esophagus
when resection and anastomosis is planned.4 are ligated. This study suggests that the transition zone
between the cervical and thoracic esophagus has the
Layers in the Esophageal Wall poorest blood supply of any part of the structure.6
The esophageal wall has four layers: mucosa, submu-
cosa, inner circular and outer longitudinal muscularis, COMPLICATIONS OF ESOPHAGEAL SURGERY
and adventitia.2 The serosa in the rest of the gastroin- Complications reported after esophageal surgery in-
testinal (GI) tract (except the caudal half of the rectum) clude suture line breakdown, leakage, and stenosis.7,8
represents the visceral layer of the peritoneum that re- Several explanations for the high complication rate
flects on and around the abdominal viscera. It is com- have been suggested.
posed mainly of mesothelial cells in a loose connective The absence of the serosal layer that exists in most of
tissue. The esophagus is surrounded by adventitia only, the GI tract is one potential reason for postoperative
except in the thorax where it is partially covered ven- complications. The serosa is believed to exude a fibrin
trally by mediastinal pleura. Although this attachment clot that creates an early seal of the incision and to pro-
is loose, the pleura can be a source of mesothelial cells vide alignment of apposed tissue layers after suturing. It
and fibrin to help seal the esophageal incision after su- is now known that the former role is performed by the
turing.4 mediastinal pleura; to replace the missing latter role, a
The surface epithelium of the mucosa is stratified more accurate apposition of layers after esophageal
squamous with varying degrees of keratinization in dif- surgery is required.9,10
ferent species. The lamina propria of the mucosa is Tissue rest is one of the basic requirements of wound
strong and thick and is comprised of loose connective healing; however, the esophagus is in constant motion
tissue of collagenous, elastic, and reticular fibers.5 The because of swallowing and diaphragmatic movement.
mucosal layer is thicker in the esophagus than in other Diaphragmatic contractions cause the line of an anasto-
parts of the tubular digestive tract, primarily because it mosis to move up and down as much as 3 cm. Such
has a thicker lamina propria. However, most of the movements would obviously interfere with the impor-
connective tissue in the wall of the esophagus is in the tant sealing process that is desirable in the early postop-
submucosa.1 erative period.11,12
The esophageal wall poorly tolerates longitudinal
Segmental Blood Supply stretching and tension. When a portion of the esopha-
The esophageal blood supply has traditionally been gus is resected, tension is created in the suture line be-
described as segmental. The bronchoesophageal artery cause of lack of mobility in the esophagus. This tension
supplies blood to the cervical and cranial portions of increases considerably during diaphragmatic contrac-
the thoracic esophagus. The caudal part of the thoracic tions.3,12 A mortality rate of 33% was reported in dogs
esophagus is supplied by the left gastric artery that with esophageal anastomosis after resection of a third of
crosses the diaphragm. Other segments of the thoracic the thoracic esophagus.13 In another experiment, a posi-
esophagus are supplied by direct segmental branches tive correlation was found between the extent of resec-
from the thoracic aorta.2 tion and the mortality rate from anastomotic break-
In addition, a collateral blood supply in the wall of down.14
the esophagus has been shown to exist. In a classic ex- The segmental blood supply was thought to influ-
periment, Macmanus and colleagues6 devascularized ence esophageal healing after suturing. However, as dis-
large portions of the canine esophagus (thoracic esoph- cussed, a rich plexus of intramural vessels exists in the
agus, cervical esophagus, or both) by ligating the seg- submucosa. These vessels can support segments of the
mental blood supply. The esophagus was then divided, esophagus that have had their segmental blood supply
and a reanastomosis was performed immediately. On compromised. This suggests that a successful anasto-
postmortem examinations, no necrosis of the esopha- mosis can be expected in cases of considerable segmen-
gus was observed. These results confirmed that the col- tal vascular compromise as long as there is no disrup-
lateral vascular pathways in the wall of the esophagus tion of the intramural blood supply.4,6,11,14
are sufficient to maintain its viability and to ensure Another important reason for the greater vulnerabili-
healing of an anastomosis when the entire thoracic ty of the esophagus is the lack of omentum. The omen-
blood supply to the esophagus is cut off. The capacity tum serves an important role in supporting GI anasto-
of this intrinsic blood vessel network does have a limit. moses, and omental wrapping is the most valuable
adjunct procedure for protecting such anastomoses. ence to meticulous technique in suturing the esophagus
The omentum adds a supplementary layer that pro- is more important than is the type of suture used.3 He
vides a seal after adhering to the outer layer of an anas- suggested that preference should be given to one of two
tomosis, and new blood vessels arising from the omen- techniques: (1) an inner mucosal–submucosal layer of
tal vessels may provide additional blood supply. In continuous absorbable suture and an outer muscular
addition, phagocytic and other immune functions of layer of interrupted nonabsorbable suture, or (2) an in-
the omentum may allow local containment of anasto- ner layer of interrupted nonabsorbable sutures with the
motic leakage.15 knots tied in the lumen and an outer layer of interrupt-
Lack of serosa, movement associated with respiration ed nonabsorbable sutures. Sutures should be placed ap-
and swallowing, and a meager blood supply compared proximately 2 to 3 mm apart and 2 mm from the cut
with the remainder of the alimentary tract all contri- edge and should be tied with sufficient tension so that a
bute to potential problems that may be encountered dur- tight seal forms without interfering with the blood sup-
ing and after surgery of the esophagus.3 Thus esoph- ply.3
ageal surgery requires even more exacting techniques To enhance esophageal dilation during bolus passage,
than does surgery on other portions of the alimentary some authors do not recommend a continuous pattern
tract. when suturing anastomoses.4 In an experimental study
in 1993, three suture methods (i.e., double-layer apposi-
SUTURE METHODS tional closure, single-layer simple interrupted closure,
The classic two-layer inverting esophageal suture de- and single-layer continuous closure) were compared, all
veloped for humans in the 1920s was first described in of which used absorbable sutures of polydioxanone sul-
the veterinary literature in 1965.16 At that time, the fate through all layers of the esophageal wall.19 All meth-
mucosa was considered to have the greatest suture- ods were basically successful; however, based on mea-
holding capabilities of all the esophageal layers and the surement of bursting strength and operating time, the
submucosa was not mentioned. Mucosa was sutured in authors recommended either the double-layer apposi-
one layer, and the muscularis (with serosa if possible) tional closure or the single-layer interrupted closure.
was sutured in the other.16 It was also believed that the
closure must be leak-proof because rapid sealing with REINFORCING THE SUTURE LINE
fibrin does not occur in the esophagus as it does in the Circumferential myotomy and omental flap are two
rest of the intestinal tract.10 of the most commonly used techniques for reinforcing
The method of using an inverting suture pattern to cre- esophageal anastomoses. They are especially indicated
ate serosal apposition is no longer considered necessary in when tension is anticipated.
surgery of the intestine or esophagus.9 Some authors still A circumferential myotomy is recommended to re-
recommend everting the muscular layer, especially if ten- duce tension from the anastomosis site.4 Complete cir-
sion at the suture line is anticipated, whereas others claim cular myotomy was found to interrupt the deep longi-
that one layer of everting suture pattern is sufficient.4,16 tudinal vessels in the submucosal vascular plexus, which
In 1949, Swenson described a method in which one tends to adhere to the circular muscle layer and is de-
row of 4-0 braided silk interrupted sutures was placed stroyed or damaged by complete myotomy. Partial cir-
in the mucosa and the knots were tied within the lu- cular myotomy, in which only the longitudinal muscle
men. The second layer of interrupted 4-0 silk included layer is transected, preserves this submucosal vascular
the full thickness of the muscular coat and some of the network and yet is as effective as complete myotomy in
submucosa. Sutures were placed 2 to 3 mm apart.12 reducing tension.14
The practice of using nonabsorbable suture material The omental flap is used successfully to reinforce
in the mucosa and keeping the knots within the lumen esophageal anastomoses. In a controlled study of anasto-
is very much accepted today, except that polypropylene moses of the thoracic esophagus, a 25% defect was left in
is used more commonly than is silk.4,7,17 There appears the suture line and then wrapped with omentum. Only
to be some movement away from the use of traditional 1 of 12 dogs died following leakage from the suture
nonabsorbable suture material for esophageal suturing; line.20 Omental grafts are used in humans to support
however, the literature continues to stress the necessity esophageal perforation repairs and to provide blood sup-
of suturing the mucosa. ply to the mediastinal area when infection is present.15
The most widely recommended suture pattern today
is a two-layer closure in which the first layer incorpo- SUBMUCOSA IN THE GASTROINTESTINAL TRACT
rates the mucosa and submucosa and the second layer The submucosa in the GI tract (other than the
apposes the muscularis.3–5,7,18 Rosin stated that adher- esophagus) is the strong, fibroelastic connective tissue
20th
CO
geal disease. Esophago- from a foreign body (right), and resected segment of the
ANNIVERSARY
grams were performed 30 esophagus showing several areas of necrosis (left). Some
esophageal wall damage can be seen at the line of resection,
A LookBack and 35 days after surgery
in cases 17 and 19. Esoph-
which was left untouched to avoid resection of an excessive
length of esophagus.
ageal diameter and motili-
Almost any textbook discussion ty were normal.
of esophageal surgery comments Resection and anastomo- tween sutures; furthermore, all methods were found to
on the difficulty of and sis was performed in one be adequate for proper healing of a healthy esophagus.19
complications associated with dog to remove a large di- It was also reported that closing the incision with one
the procedure. Various theories verticulum (case 21). Eigh- layer of sutures took half the time required for closing
have been purported to explain teen months after surgery, it in two layers.19
these phenomena. We believe the patient was eating a The surface epithelium of the esophagus is generally
that the basic principles of commercial diet and was stratified squamous with varying degrees of keratiniza-
esophageal suturing that have clinically normal. Seven tion.2 This epithelium and the strong, thick lamina
months after surgery, an propria produce a mucosa that resembles skin. It is well
evolved over the past 70 years
esophagogram revealed known that suppuration occurs around nonabsorbable
should change based on
persistence of a small di- sutures left in the skin and that scar tissue forms until
Dallman’s finding in 1988 verticulum. the sutures are removed. It is likely that the same thing
(i.e., that the mucosa is the happens in the esophagus and that nonabsorbable su-
strength layer in the wall of the Discussion tures left in place indefinitely can be a factor in exces-
esophagus, as it is elsewhere in The use of absorbable sive scar tissue formation and stenosis. The report of a
the gastrointestinal tract). suture material and one 50% mortality rate in a study in which a double layer
The single-layer closure layer of sutures, utilization of nonabsorbable sutures (with the knots tied within
recommended in this article of the submucosa as the the lumen) was used13 supports this hypothesis.
brings esophageal surgery into holding layer of the esoph- In 1965, it was reported that peritoneal and serosal
the same realm as surgery of the agus, and avoidance of the defects sutured with fine silk in rats and rabbits yielded
small and large intestine and mucosa represent a new a higher percentage of adhesions than occurred when
approach to esophageal such defects were left unsutured.9 It can be assumed
the urinary bladder, in which
closure. Based on a con- that a two-layer closure is stronger and provides a
single-layer appositional closures
trolled study conducted to tighter seal than does a one-layer closure; however, a
are commonly accepted as the compare three esophageal two-layer closure can interfere with the blood supply to
preferred technique today. suture patterns in which the healing edges, and the large volume of suture mate-
the sutures penetrated all rial can cause irritation.22
layers of the esophagus, it Procedures such as pericardial and transdiaphrag-
was concluded that the matic omental patching have been used to decrease the
esophageal closure was chance of leakage from an esophageal incision. It has
more likely to fail at suture been reported that contiguous mediastinal structures
holes than at the space be- become adherent to the area of anastomosis, which is as
effective a sealing barrier as the omentum in the ab- 10. Gideon L: Esophageal anastomosis in two foals. JAVMA
domen.4 184:1146–1148, 1984.
In our study of esophageal surgery in 21 animals, 11. Pavletic MM: Reconstractive esophageal surgery in the dog:
A literature review and case report. JAAHA 17:435–442,
only one dog died as a result of leakage from the suture
1981.
site after resection of a large portion of the thoracic 12. Swenson O, Clatworthy HW: Partial esophagectomy with
esophagus. In many cases, the sutured edges of the end-to-end anastomosis in the posterior mediastinum.
esophagotomy or anastomosis were compromised by Surgery 25:839–848, 1949.
pressure from the foreign body (Figure 2). Long-term 13. Parker NR, Walter PA, Gay J: Diagnosis and surgical man-
clinical evaluation and esophagograms showed no prob- agement of esophageal perforation. JAAHA 25:587–594,
lems. 1989.
14. Muangsombut J, Hankins JR, Mason GR: The use of circu-
lar myotomy to facilitate resection and end–to-end anasto-
CONCLUSION
mosis of the esophagus. J Thorac Cardiovasc Surg 68:522–
The analysis of clinical cases in this report is suffi- 529, 1974.
cient and accurate to demonstrate the efficacy and safe- 15. Hosgood G: The Omentum—The forgotten organ: Physiol-
ty of the new suture method. No animals were exclud- ogy and potential surgical applications in dogs and cats.
ed from this study because of complications related to Compend Contin Educ Pract Vet 12(1):45–51, 1990.
the suture method. 16. Pass MA: Surgical repair of esophageal defects. JAVMA
We conclude that the technique of a one-layer clo- 59:1453–1456, 1971.
sure of esophageal incisions using the submucosa as the 17. Waldron DR: Cervical and thoracic esophageal resection
strength layer, not penetrating into the lumen, and us- and anastomosis, in Bojrab MJ (ed): Current Techniques in
Small Animal Surgery, ed 2. Philadelphia, Lea & Febiger,
ing absorbable suture material is adequate for proper 1983, pp 133–142.
esophageal healing. This technique is safe and does not 18. Lipowitz AJ, Caywood DD: Atlas of General Small Animal
appear to predispose animals to postoperative compli- Surgery. St. Louis, Mosby, 1989, pp 46–50.
cations such as leakage or stenosis. Although both PDS 19. Oakes MG, Hosgood G, Snider TG, et al: Esophagotomy
and chromic surgical gut suture material were used in closure in the dog. A comparison of a double-layer apposi-
this study, we strongly recommend the use of a synthet- tional and two single-layer appositional techniques. Vet Surg
ic absorbable monofilament material such as PDS. 22:451–456, 1993.
20. Goldsmith HS, Kiely AA, Randall HT: Protection of in-
trathoracic esophageal anastomoses by omentum. Surgery
REFERENCES 63:464–466, 1968.
1. Dallman MJ: Functional suture-holding layer of the esopha-
21. Johnston DE: Reflections on suturing. Compend Contin
gus in the dog. JAVMA 192:638, 1988.
Educ Pract Vet 11(1):56, 1989.
2. Dyce KM, Sack WO, Wensing CJG: Textbook of Veterinary
22. Hermreck AS, Crawford DG: The esophageal anastomotic
Anatomy. Philadelphia, WB Saunders Co, 1987, pp 116–
leak. Am J Surg 132:794–798, 1976.
117.
3. Rosin E: Surgery of the esophagus. Vet Clin North Am 5:
557–564, 1975.
4. Fingeroth JM: Surgical techniques for esophageal disease, in About the Authors
Slatter D (ed): Textbook of Small Animal Surgery. Philadel- Drs. Shamir, Shahar, and Johnston are affiliated with the
phia, WB Saunders Co, 1993, pp 549–561. Department of Surgery, Veterinary Teaching Hospital, Ko-
5. Gourley IM, Vasseur PB: General Small Animal Surgery. ret School of Veterinary Medicine, The Hebrew University
Philadelphia, JB Lippincott Co, 1985, pp 233–299. of Jerusalem, Rehovot, Israel. Dr. Mongil operates a
6. Macmanus JE, Dameron JT, Paine JR: The extent to which surgery referral practice out of the Dr. Diaz Umpierre Vet-
one may interfere with the blood supply of the esophagus erinary Hospital in San Juan, Puerto Rico. Dr. Shahar is a
and obtain healing on anastomosis. Surgery 28:11–23, 1950.
Diplomate of the European College of Veterinary Sur-
7. Schunk CM: Removal of esophageal foreign bodies, in Bo-
jrab MJ (ed):Current Techniques in Small Animal Surgery, ed geons and the American Board of Veterinary Practitio-
3. Philadelphia, Lea & Febiger, 1990, pp 201–207. ners, Dr. Johnston is a Diplomate of the American Col-
8. Knight GC: Transthoracic esophagotomy in dogs: A survey lege of Veterinary Surgeons and the European College of
of 75 operations. Vet Rec 75:264–266, 1963. Veterinary Surgeons, and Dr. Mongil is a Diplomate of the
9. Glucksman DL: Serosal integrity and intestinal adhesions. American College of Veterinary Surgeons.
Surgery 60:1009–1011, 1966.