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Upper Esophageal Sphincter in Health and Disease
Symposium on Gastrointestinal Surgery
Upper Esophageal Sphincter in Health and Disease F. Henry Ellis, Jr., M.D., Ph.D.
The upper sphincter of the esophagus or the pharyngo-esophageal sphincter has received surprisingly little attention in the surgical literature. Only recently have detailed studies of its physiology been made. Before the introduction of manometric techniques, observations of this portion of the alimentary tract depended entirely on contrast radiography, which did not permit the precise measurement and timing of events that is possible with current methods. Now that other techniques are available it has become increasingly clear that disorders of upper sphincteric function may occur under a variety of circumstances and can lead to disabling symptoms. Before discussing some of these abnormalities, their recognition, and treatment, it is necessary to reexamine the normal anatomy and physiology of the area in question.
ANATOMY AND PHYSIOLOGY The anatomy of the pharynx and upper esophagus should no longer be a subject of controversy. Recently an excellent and detailed study has been reported. 33 The cricopharyngeus muscle runs transversely across the posterior wall of the esophagus, connecting the two lateral borders of the cricoid cartilage (Fig. 1). This muscle is bordered superiorly by the oblique fibers of the inferior pharyngeal constrictor muscle that pass upward and backward from their origin on the thyroid cartilage to insert into a median raphe. Inferiorly the cricopharyngeus muscle blends into the circular and longitudinal muscle fibers of the upper esophagus. It is sometimes difficult at the operating table to define precisely the limits of these various muscle groups, although it is usually easier to separate the cricopharyngeus muscle from the oblique constrictor fibers of the pharynx than from the circular muscle of the esophagus. Some anatomists consider the cricopharyngeus muscle as part of the inferior constrictor of the pharynx, although it possesses no median raphe. The transverse fibers of the cricopharyngeus muscle have shown sufficient anatomic differentiation to justify their being called a true sphincter. The nervous innervation. of this sphincter remains a subject of controversy. While the motor supply of the cricopharyngeus muscle in Surgical Clinics of North America- Vol. 51, No.3, June 1971
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INF. CONSTR M.
THYROID CART.
Figure 1. Anatomy of pharynx and upper esophagus. Posterolateral view.
CRICOID CART.
M.
VAGUS N.
ESOPH.
the dog is from a single nerve derived from the vagus by its pharyngeal branch, no such nerve has been identified in man. 19 There is no evidence that the recurrent laryngeal nerve is concerned with cricopharyngeal function since this muscle functions normally in patients with bilateral vocal cord palsy. On the other hand, some patients with pharyngeal palsy show abnormal function of the upper esophageal sphincter, leading to the supposition that the nerve of the sphincter may be derived from pharyngeal branches of the vagus through the pharyngeal plexus (Fig. 1). Whatever its innervation may be, its normal function has repeatedly been studied. 5 A zone of elevated pressure is regularly detected in man between the upper esophagus and the pharynx, varying from 2.5 to 6.5 cm. in length, with an average of 3.0 cm. (Fig. 2). Since the width of the band of maximum pressure is about 1.0 cm. and corresponds to the location of the cricopharyngeus muscle, the adjacent pharyngeal and esophageal muscles must contribute to the total width of the zone of elevated pressure as defined manometrically. The maximum resting pressure ranges from 18 to 60 cm. above atmospheric pressure, and consecutive determinations in anyone individual over a period of time often register widely differing sphincteric pressures. The sphincter relaxes with swallowing and then contracts. Relaxation occurs early in the deglutitive sequence simultaneously with or just after the contractions of the tongue and upper part of the pharynx (Fig. 3). The sphincter always opens before pharyngeal contraction, and the period of sphincteric relaxation is brief -less than 1 second in duration. After pharyngeal contraction, the sphincter contracts, producing pressures of 70 to 100 cm. of water, lasting 2 to 4 seconds. As the contraction subsides, sphincteric pressure returns to resting levels.
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30 seconds
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Figure 2. Resting pressure profile of pharyngo-esophageal sphincter in two healthy individuals (A and B) during successive withdrawals of two open-tipped recording tubes (O.T.) spaced 5.0 cm. apart. (From Code, C. F., and Schlegel, J. F.: Motor action of the esophagus and its sphincters. In Handbook of Physiology-Alimentary Canal. Section 6, Chapter 90. Bethesda, Maryland, American Physiological Society, 1967, p. 1826.)
The act of swallowing is a complex phenomenon in which the muscles of the tongue, larynx, pharynx, and upper esophagus are precisely coordinated. There is an initial oral phase that is voluntary and a second pharyngo-esophageal phase that is almost entirely involuntary. The tongue initiates the swallowing act by propelling the food bolus into the posterior oral pharynx. The tongue then acts to close the oral cavity, while the palate closes the nasopharynx and the larynx elevates and moves forward to close the supraglottis, creating a negative pressure by widening the hypopharynx. The pharyngeal constrictors contract to propel the food bolus into the esophagus as the cricopharyngeal muscle relaxes. Contraction of the cricopharyngeus then occurs, initiating the primary peristaltic wave of the esophagus. It is clear from this summary that if anything disturbs this coordinated sequence of events, the ingested bolus may have difficulty in reaching the esophagus. Such a disturbance could result either from ineffective contractions of the pharyngeal muscles or from some abnormality of function of the cricopharyngeus muscle, such as premature contraction or incomplete relaxation. Any of these disturbances could lead to symptoms of dysphagia. Unfortunately, surprisingly little objective data are present to explain the precise mechanisms responsible for upper esophageal dysphagia. The next section will detail briefly some of the proposals that have been made and will emphasize the physiologic data that are available concerning abnormalities of pharyngo-esophageal function.
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I·
50 cm.
em. from INCISORS:
7
/I
MOUTH\
H2 0 Pressure
PHARYNX
I
I second
23
Figure 3. Pressures in the mouth, pharynx, pharyngo-esophageal sphincter, and upper esophagus recorded simultaneously during a swallow. Note the peristaltic sequence to the muscular contractions. Sphincteric relaxation anticipates pharyngeal contraction. (From Code, C. F., and Schlegel, J. F.: Motor action of the esophagus and its sphincters. In Handbook of Physiology-Alimentary Canal. Section 6, Chapter 90. Bethesda, Maryland, American Physiological Society, 1967, p. 1827.
ABNORMALITIES OF PHARYNGO-ESOPHAGEAL FUNCTION The lack of objective data makes the subject of functional derangements of pharyngo-esophageal function a confused one. The literature is full of varying concepts regarding the nature of physiologic disturbances in this region. Ever since the suggestion by Kelly 14 in 1919 that there was "spasm" at the entrance to the esophagus in patients with the disease that later became known in Great Britain as the Paterson-Kelly syndrome and in this country as the Plummer-Vinson syndrome, a variety of proposals has been offered by the medical profession to explain abnormalities of function of this portion of the gullet. In addition to Kelly, a number of others have emphasized the role of cricopharyngeal spasm in certain swallowing disorders. In 1946, Lahey 17 directed attention to the cricopharyngeal muscle, implicating it in the etiology of esophageal diverticula and advised forceful dilation of the muscle as well as surgical excision. Negus 21 • 22 also advised dilation in patients with pharyngo-esophageal diverticula, although cricopharyngeal incoordination rather than spasm was considered as the cause of the pouch. Delayed relaxation of the sphincter was considered an important mechanism by Cross and associates. 6
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A related concept is that of cricopharyngeal achalasia in which, theoretically, the sphincter fails to relax. As early as 1926, Jackson and Shallow 12 postulated such a mechanism as being the cause of pharyngoesophageal diverticula. Asherson 2 is usually given credit for introducing the term achalasia in 1950 as applied to various neuromuscular disorders affecting the cricopharyngeus muscle. Sutherland30 revived the term in 1962 and implicated this mechanism in the development of pharyngo-esophageal diverticula. Belsey3 also used the term in explaining the development of diverticula in a paper written in 1966, although he seems to use the terms achalasia and spasm synonymously. Another form of incoordination of the sphincter is that of a "second swallow" against a closed sphincter. This concept stemmed from radiographic studies of the upper gullet and was invoked to explain the development of pharyngo-esophageal diverticula. 32 Another possible mechanism for which there is recent physiologic support is that of premature contraction of the sphincter. In 1961 Ardran and Kemp,! basing their findings on radiography of the upper food passages, described partial or complete closure of the cricopharyngeus sphincter before all of the ingested bolus had been displaced from the pharynx into the esophagus. Lund19 has also described similar findings in instances of pharyngo-esophageal diverticulum. Esophageal manometric studies carried out on patients with pharyngo-esophageal diverticula, to be described in detail later, have supported this concept of premature contraction of the sphincter in such individuals.9 In addition to these various concepts regarding disordered function of the cricopharyngeus muscle in patients with diverticula, it has from time to time been postulated that abnormal pharyngeal function may be secondary to a variety of neuromuscular disorders. The following section represents an attempt to classify these various conditions. Classification of Disorders Table 1 represents a tentative classification of abnormalities of pharyngo-esophageal function based on personal and published inforTable 1. Classification of Abnormalities of Pharyngo-Esophageal Function Central nervous system disease Bulbar poliomyelitis Cerebrovascular accident Diseases affecting muscular activity Muscular dystrophy Myasthenia gravis Thyrotoxic myopathy Postsurgical dysphagia Radical oropharyngeal surgery Idiopathic incoordination Pharyngo·esophageal diverticulum
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mation. It is not intended to be all inclusive but rather is limited to the conditions that are most likely to be encountered clinically. With the exception of pharyngo-esophageal diverticulum, objective physiologic data relative to the mechanisms responsible for upper esophageal dysphagia are notably lacking. Abundant evidence exists, however, that some individuals, after injury to the brain stem, such as occurs with bulbar poliomyelitis or after a cerebrovascular accident, have difficulties in swallowing. 4, 13, 19,31 Diseases that directly affect muscular activity also may result in swallowing difficulties. Most common among these diseases are muscular dystrophy, myasthenia gravis, and the myopathy of thyrotoxicosis.4, 18, 24, 25 Of 34 patients with local lesions of the brain examined radiographically by Silbiger and associates,27 27 had motility disturbances of pharyngo-esophageal function while one third of those with primary muscle disease were so affected. Abnormalities of sphincteric relaxation are said to characterize central nervous system lesions, while the muscle diseases result in failure to develop effective pharyngeal peristalsis. Cricopharyngeal myotomy has been employed in scattered instances of this sort with inconclusive results. Difficulty in swallowing has been reported after extensive operations on the oropharyngeal region. Spasm of the cricopharyngeus muscle was considered by Schobinger26 to be the cause of dysphagia after total laryngectomy. Ogura et al. 23 subsequently advocated routine cricopharyngeal myotomy in patients undergoing supraglottic laryngectomy. More recently Mladick and associates20 have emphasized the role of the cricopharyngeus muscle in the pathophysiology of dysphagia after certain major oropharyngeal resections and described the use of cricopharyngeal myotomy in 21 patients. Their indications included a variety of operative procedures, such as resection of half or more of the oral pharynx or hypopharynx, total glossectomy, epiglottectomy, supraglottic laryngectomy, and resection of half or more of the base of the tongue. Finally, my associates and J9 have recently described a type of incoordination in patients with pharyngo-esophageal diverticulum that may be significant etiologically and supports the earlier radiographic findings mentioned previously. Using esophageal motility studies, we carried out 21 observations of pressures in the pharynx and esophagus on 11 patients with pharyngo-esophageal diverticula and compared them with 21 patients who had a normal pharynx and upper esophagus. A zone of elevated pressure was detected at the pharyngo-esophageal sphincter in all patients with pharyngo-esophageal diverticula. The elevated pressure zone was slightly longer and the maximal pressures within it were slightly lower than those reported from normal individuals. With deglutition all of the patients studied had immediate sphincteric relaxation followed by contraction, although the magnitude of relaxation and its duration were slightly longer than normal and the amplitude of contraction was slightly less. These findings clearly exclude the possibility of cricopharyngeal achalasia being present in patients with this disease. However, all of the
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Health
PE Diverticulum
PE Diverticulum
I
H2
Swallow
1"5 em J" Pressure
t
Figure 4. Deglutition pressures at pharyngo-esophageal junction in a normal person and in two patients with pharyngo-esophageal diverticula. Note that in health (left panel) the pharyngo-esophageal sphincter (PES) is open during the entire period of pharyngeal contraction. In the two patients with diverticula, part or all of the period of pharyngeal contraction occurs after closure of the sphincter (middle and right panels). (From Ellis, F. H., Jr., et aI., Ann. Surg. 170:342, Sept., 1969.)
patients were noted to have an abnormal temporal relationship between pharyngeal contraction and pharyngo-esophageal sphincteric relaxation and contraction. In these patients, sphincteric contraction occurred before completion of the contraction of the pharynx (Fig. 4). No such abnormality was observed in any of the normal patients studied. In other words, clear evidence for incoordination of the pharyngo-esophageal junction was identified in all of the patients with the abnormality under discussion, suggesting that this incoordination, whatever its cause, might be responsible for the development of the lesion. These findings have not been confirmed by other workers, however. Kodicek and Creamer 16 carried out successful studies on 5 patients with pharyngo-esophageal diverticula without evidence of any abnormality of function. Of considerable interest is the recent report of Hunt and associates l l showing that sphincteric resting pressures were elevated in most patients with a pharyngeal pouch, in contrast to our findings, which showed the pressures to be slightly lower than normal. This difference may be explained partially by the fact that in our series of cases only 1 patient had a hiatal hernia, while 28 of their 30 patients with pharyngeal pouches had a hernia. Smiley and associates 28 postulated that since cricopharyngeal resting pressures were found to be high in the presence of gastroesophageal reflux, pharyngeal pouches result from cricopharyngeal dysfunction secondary to reflux.
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CRICOPHARYNGEAL MYOTOMY The concept of purposely weakening the pharyngo-esophageal sphincter is not a new one. Reference has already been made to the use of forceful dilation in the management of patients with pharyngoesophageal diverticula. Endoscopic diathermy division of the septum or common wall between the esophagus and the diverticulum has been used by Dohlman and Mattsson 8 among others. The procedure of cricopharyngeal myotomy was a natural consequence of the introduction by Asherson 2 of the term "achalasia" as applied to various neuromuscular disorders affecting the cricopharyngeal muscle and, as indicated before, a number of reports have appeared in the literature describing the successful use of this operative procedure in such conditions. While Harrison 10 employed cricopharyngeal myotomy combined with inversion of the diverticulum in 3 patients who had pharyngeal pouches, Sutherland 30 was perhaps the first to use the technique alone in patients with this condition. Subsequently, Davis and associates 7 and Blakely and associates 4 each reported the cases of 2 patients with pharyngeal pouches successfully treated by cricopharyngeal myotomy. The most extensive experience with this technique is that of Belsey 3 who in 1966 reported its use in 32 patients with pharyngo-esophageal diverticula, most of whom had diverticulopexy performed at the same time. Of the 18 pa-
Figure 5. Technique of esophagomyotomy. A, Site of skin incision. B, Exposure of diverticulum. Dotted line indicates proposed myotomy site. C, Completed operation. (From Ellis, F. H., Jr., et ai., Ann. Surg. 170:343, Sept., 1969.)
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tients we reported in 1969,9 all had cricopharyngeal myotomy, 4 had diverticulopexy in addition, and 4 had diverticulectomy. All but one were improved by the operation. Others have advocated the use of cricopharyngeal myotomy whenever diverticulectomy is performed, as recurrences have been reported with diverticulectomy alone. 15 • 29 It has been my experience that cricopharyngeal myotomy is a successful procedure for patients with smallsize to medium-size pouches. Those with pouches larger than 5.0 to 6.0 cm. in diameter should have diverticulectomy performed.
Surgical Technique The technique of esophagomyotomy is illustrated in Figure 5. Access to the diseased area is obtained through a left oblique cervical incision bordering the anterior edge of the sternocleidomastoid muscle. The
Figure 6. Esophageal roentgenograms in patient with pharyngo-esophageal diverticulum. A and B, Before operation. C and D, Four days after esophagomyotomy. E and F, Ten months later. (From Ellis, F. H., Jr., et al., Ann. Surg. 170:346, Sept., 1969.)
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pharyngo-esophageal region is exposed by retraction of the carotid sheath laterally and the trachea and larynx anteriorly and to the right. After the diverticulum is freed to its neck, the transverse fibers of the cricopharyngeus muscle bordering the inferior margin of the neck of the diverticulum are easily identified and incised. The incision is carried down to the mucosa and is extended caudally onto the esophagus, the length of the incision averaging about 3.0 cm. After the myotomy, the esophageal and cricopharyngeal muscles are dissected from the underlying mucosa for about half the circumference of the mucosal tube to allow the mucosa to protrude freely through the incision. The cervical wound is then closed with interrupted sutures, with or without drainage. The patient is allowed free oral feedings and is discharged from the hospital in a few days. At the time of dismissal from the hospital, roentgenograms of the esophagus reveal that the diverticulum either is no longer identifiable or is considerably smaller than before surgery (Fig. 6). Postoperative motility studies disclose a reduction by 50 per cent in the resting pressures at the pharyngo-esophageal sphincter accompanied by a decrease in length (Fig. 7). While with deglutition, relaxation and contraction persist, the magnitude of each component is reduced. The abnormal temporal relationships existing between the pharynx and sphincter before operation are also present after operation (Fig. 8). Preoperative
I
25 em H20 Pressure
5
Days
After
Cricopharyngeal
Myotomy
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Figure 7. Resting pressures at the pharyngo-esophageal junction in patient with pharyngo-esophageal diverticulum before esophagomyotomy (upper panel) and five days after surgery (lower panel). Note decrease in sphincteric pressure and shortening of sphincter after operation. (From Ellis, F. H., Jr., Ann. Surg. 170:347, Sept., 1969.)
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Preoperative 25cm
Pressure
cm from Incisors:
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Post Myotomy
I sec
1-1
" +-
Atmospheric- Pressure Swallow
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Figure 8. Deglutition pressures at pharyngo-esophageal junction in patient with pharyngo-esophageal diverticulum before surgery (upper panel) and five days after esophagomyotomy (lower panel). Some patient as in Figure 7. Note occurrence of pharyngeal contraction after closure of pharyngo-esophageal sphincter (PES). This abnormal sequence is not altered by myotomy, but the amplitude of sphincteric contraction is markedly reduced, as is the amplitude of relaxation. (From Ellis, F. H., Jr., et ai., Ann. Surg.170:347, Sept., 1969.)
SUMMARY The act of swallowing involves a complex mechanism reqUITIng precise coordination of the tongue, larynx, pharynx, and upper esophagus. Esophageal manometry has identified as part of this mechanism a high pressure zone corresponding to the cricopharyngeus muscle and adjacent pharyngeal and esophageal musculatures. This zone has the characteristics of a sphincter. It relaxes with swallowing just before and including the period of pharyngeal contraction and subsequently contracts to initiate the primary peristaltic wave of the esophagus. Many conditions may disturb the coordinated events that characterize normal pharyngo-esophageal function. These include central nervous system lesions, conditions affecting muscle function directly, major oropharyngeal surgery, and the idiopathic sphincteric incoordination characteristic of pharyngoesophageal diverticulum. Much needs to be learned about the exact nature of the physiologic disturbance that exists in these various disease states before cricopharyngeal myotomy can freely be recommended. If sphincteric pressures are high or if relaxation is incomplete, the operation should be
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beneficial. It is particularly useful in the treatment of small-size to moderate-size pharyngeal pouches, conditions characterized by closure of the cricopharyngeal sphincter before completion of pharyngeal contraction. Cricopharyngeal myotomy alone is accompanied by a high rate of symptomatic improvement coupled with radiographic evidence of regression in size or disappearance of the diverticulum in almost all cases.
REFERENCES 1. Ardran, G. M., and Kemp, F. H.: The radiography of the lower lateral food channels. J. Laryng. 75:358-370 (April) 1961. 2. Asherson, N.: Achalasia of cricopharyngeal sphincter: record of cases, with profile pharyngograms. J. Laryng. & Otol. 64:747-758 (Dec.) 1950. 3. Belsey, R: Functional disease of the esophagus. J. Thorac. Cardiov. Surg. 52:164-188 (Aug.) 1966. 4. Blakely, W. R, Garety, E. J., and Smith, D. E.: Section of the cricopharyngeus muscle for dysphagia. Arch. Surg. 96:745-762 (May) 1968. 5. Code, C. F., and Schlegel, J. F.: Motor action of the esophagus and its sphincters. In Handbook of Physiology-Alimentary Canal. Section 6, Chapter 90. Bethesda, Maryland, American PhysiolOgiC Society, 1967, pp. 1821-1839. 6. Cross, F. S., Johnson, G. F., and Gerein, A. N.: Esophageal diverticula. Associated neuromuscular changes in the esophagus. Arch. Surg. 83:525-533 (Oct.) 1961. 7. Davis, M. V., Mitchel, B. F., and Adam, M.: Cricopharyngeal achalasia: variant of hypopharyngeal diverticulum syndrome. Texas J. Med. 62:47-49 (Feb.) 1966. 8. Dohlman, G., and Mattsson, 0.: The endoscopic operation for hypopharyngeal diverticula; a roentgencinematographic study. Arch. Otolaryng; 71 :744-752 (May) 1960. 9. Ellis, F. H., Jr., Schlegel, J. F., Lynch, V. P., et al.: Cricopharyngeal myotomyforpharyngoesophageal diverticulum. Ann. Surg. 170:340-349 (Sept.) 1969. 10. Harrison, M. S.: The aetiology, diagnosis and surgical treatment of pharyngeal diverticula. J. Lar. Otol. 72:523 -534 (July) 1958. 11. Hunt, P. S., Connell, A. M., and Smiley, T. B.: The cricopharyngeal sphincter in gastric reflux. Gut 11 :303-306 (April) 1970. 12. Jackson, C., and Shallow, T. A.: Diverticula of oesophagus, pulsion, traction, malignant and congenital. Ann. Surg. 83:1-19 (Jan.) 1926. 13. Kaplan, S.: Paralysis of deglutition, post-poliomyelitis complication treated by section of cricopharyngeus muscle. Ann. Surg. 133:572-573 (April) 1951. 14. Kelly, A. B.: Spasm at entrance to oesophagus. J. Lar. Otol. 34:285-289 (Aug.) 1919. 15. Kinley, C. E.: The management of hypo pharyngeal diverticulum. Canad. J. Surg. 9:27-32 (Jan.) 1966. 16. Kodicek, J., and Creamer, B.: A study of pharyngeal pouches. J. Laryng. 75:406-411 (April) 1961. 17. Lahey, F. H.: Pharyngo-esophageal diverticulum; its management and complications. Ann. Surg. 124:617-636 (Oct.) 1946. 18. Leach, W.: Generalized muscular diseases presenting as pharyngeal dysphagia. J. Laryng. 76:237-240 (March) 1962. 19. Lund, W. S.: A study of the cricopharyngeal sphincter in man and in the dog. Ann. Roy. ColI. Surg. Eng. 37:225-246 (Oct.) 1965. 20. Mladick, R A., Horton, C. E., and Adamson, J. E.: Cricopharyngeal myotomy: Application and technique in major oral-pharyngeal resections. Arch. Surg. 102:1-5 (Jan.) 1971. 21. Negus, V. E.: Pharyngeal diverticula; observations on their evolution and treatment. Brit. J. Surg. 38:129-146 (Oct.) 1950. 22. Negus, V. E.: The etiology of pharyngeal diverticula. Bull. Johns Hopkins Hosp. 101: 209-223 (Oct.) 1957. 23. Ogura, J. H., Saltzstein, S. L., and Spjut, H. J.: Experiences with conservation surgery in laryngeal and pharyngeal carcinoma. Laryngoscope 71 :258-276 (March) 1961. 24. Peterman, A. F., Lillington, G. A., and Jamplis, R W.: Progressive muscular dystrophy with ptosis and dysphagia. Arch. Neurol. 10:38-41 (Jan.) 1964. 25. Pierce, J. W., Creamer, B., and MacDermot, V.: Pharynx and esophagus in dystrophia myotonica. Gut 6:392-395 (Aug.) 1965. 26. Schobinger, R: Spasm of the cricopharyngeal muscle as cause of dysphagia after total laryngectomy. Arch. Otolaryng. 67:271-275 (March) 1958.
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27. Silbiger, M. L., Pikielney, R., and Donner, M. W.: Neuromuscular disorders affecting the pharynx. Cineradiographic analysis. Invest. Radiol. 2:442-448 (Nov.-Dec.) 1967. 28. Smiley, T. B., Carer, T. B., and Porter, D. C.: Relationship between posterior pharyngeal pouch and hiatus hernia. Thorax 25:725-731 (Nov.) 1970. 29. Smith, S., and Buchtel, B. C.: Pharyngo-esophageal diverticula and dysfunction of the cricopharyngeus muscle. Southern Med. J. 61 :826-828 (Aug.) 1968. 30. Sutherland, H. D.: Cricopharyngeal achalasia. J. Thorac. Cardiov. Surg. 43:114-126 (Jan.) 1962. 31. Wilkins, S. A., Jr.: Indications for section of the cricopharyngeus muscle. Amer. J. Surg. 108 :533-538 (Oct.) 1964. 32. Wilson, C. P.: Pharyngeal diverticula, their cause and treatment. J. Laryng. 76:151-180 (March) 1962. 33. Zaino, C., Jacobson, H. G., Lepow, H., and Ozturk, C. H.: Pharyngoesophageal Sphincter. Springfield, Ill., Charles C Thomas, 1970,209 pp.
Upper Esophageal Sphincter in Health and Disease F. Henry Ellis, Jr., M.D., Ph.D.
The upper sphincter of the esophagus or the pharyngo-esophageal sphincter has received surprisingly little attention in the surgical literature. Only recently have detailed studies of its physiology been made. Before the introduction of manometric techniques, observations of this portion of the alimentary tract depended entirely on contrast radiography, which did not permit the precise measurement and timing of events that is possible with current methods. Now that other techniques are available it has become increasingly clear that disorders of upper sphincteric function may occur under a variety of circumstances and can lead to disabling symptoms. Before discussing some of these abnormalities, their recognition, and treatment, it is necessary to reexamine the normal anatomy and physiology of the area in question.
ANATOMY AND PHYSIOLOGY The anatomy of the pharynx and upper esophagus should no longer be a subject of controversy. Recently an excellent and detailed study has been reported. 33 The cricopharyngeus muscle runs transversely across the posterior wall of the esophagus, connecting the two lateral borders of the cricoid cartilage (Fig. 1). This muscle is bordered superiorly by the oblique fibers of the inferior pharyngeal constrictor muscle that pass upward and backward from their origin on the thyroid cartilage to insert into a median raphe. Inferiorly the cricopharyngeus muscle blends into the circular and longitudinal muscle fibers of the upper esophagus. It is sometimes difficult at the operating table to define precisely the limits of these various muscle groups, although it is usually easier to separate the cricopharyngeus muscle from the oblique constrictor fibers of the pharynx than from the circular muscle of the esophagus. Some anatomists consider the cricopharyngeus muscle as part of the inferior constrictor of the pharynx, although it possesses no median raphe. The transverse fibers of the cricopharyngeus muscle have shown sufficient anatomic differentiation to justify their being called a true sphincter. The nervous innervation. of this sphincter remains a subject of controversy. While the motor supply of the cricopharyngeus muscle in Surgical Clinics of North America- Vol. 51, No.3, June 1971
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Figure 1. Anatomy of pharynx and upper esophagus. Posterolateral view.
CRICOID CART.
M.
VAGUS N.
ESOPH.
the dog is from a single nerve derived from the vagus by its pharyngeal branch, no such nerve has been identified in man. 19 There is no evidence that the recurrent laryngeal nerve is concerned with cricopharyngeal function since this muscle functions normally in patients with bilateral vocal cord palsy. On the other hand, some patients with pharyngeal palsy show abnormal function of the upper esophageal sphincter, leading to the supposition that the nerve of the sphincter may be derived from pharyngeal branches of the vagus through the pharyngeal plexus (Fig. 1). Whatever its innervation may be, its normal function has repeatedly been studied. 5 A zone of elevated pressure is regularly detected in man between the upper esophagus and the pharynx, varying from 2.5 to 6.5 cm. in length, with an average of 3.0 cm. (Fig. 2). Since the width of the band of maximum pressure is about 1.0 cm. and corresponds to the location of the cricopharyngeus muscle, the adjacent pharyngeal and esophageal muscles must contribute to the total width of the zone of elevated pressure as defined manometrically. The maximum resting pressure ranges from 18 to 60 cm. above atmospheric pressure, and consecutive determinations in anyone individual over a period of time often register widely differing sphincteric pressures. The sphincter relaxes with swallowing and then contracts. Relaxation occurs early in the deglutitive sequence simultaneously with or just after the contractions of the tongue and upper part of the pharynx (Fig. 3). The sphincter always opens before pharyngeal contraction, and the period of sphincteric relaxation is brief -less than 1 second in duration. After pharyngeal contraction, the sphincter contracts, producing pressures of 70 to 100 cm. of water, lasting 2 to 4 seconds. As the contraction subsides, sphincteric pressure returns to resting levels.
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B
'{}'I\~ O. T. Pneumogroph
Figure 2. Resting pressure profile of pharyngo-esophageal sphincter in two healthy individuals (A and B) during successive withdrawals of two open-tipped recording tubes (O.T.) spaced 5.0 cm. apart. (From Code, C. F., and Schlegel, J. F.: Motor action of the esophagus and its sphincters. In Handbook of Physiology-Alimentary Canal. Section 6, Chapter 90. Bethesda, Maryland, American Physiological Society, 1967, p. 1826.)
The act of swallowing is a complex phenomenon in which the muscles of the tongue, larynx, pharynx, and upper esophagus are precisely coordinated. There is an initial oral phase that is voluntary and a second pharyngo-esophageal phase that is almost entirely involuntary. The tongue initiates the swallowing act by propelling the food bolus into the posterior oral pharynx. The tongue then acts to close the oral cavity, while the palate closes the nasopharynx and the larynx elevates and moves forward to close the supraglottis, creating a negative pressure by widening the hypopharynx. The pharyngeal constrictors contract to propel the food bolus into the esophagus as the cricopharyngeal muscle relaxes. Contraction of the cricopharyngeus then occurs, initiating the primary peristaltic wave of the esophagus. It is clear from this summary that if anything disturbs this coordinated sequence of events, the ingested bolus may have difficulty in reaching the esophagus. Such a disturbance could result either from ineffective contractions of the pharyngeal muscles or from some abnormality of function of the cricopharyngeus muscle, such as premature contraction or incomplete relaxation. Any of these disturbances could lead to symptoms of dysphagia. Unfortunately, surprisingly little objective data are present to explain the precise mechanisms responsible for upper esophageal dysphagia. The next section will detail briefly some of the proposals that have been made and will emphasize the physiologic data that are available concerning abnormalities of pharyngo-esophageal function.
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I·
50 cm.
em. from INCISORS:
7
/I
MOUTH\
H2 0 Pressure
PHARYNX
I
I second
23
Figure 3. Pressures in the mouth, pharynx, pharyngo-esophageal sphincter, and upper esophagus recorded simultaneously during a swallow. Note the peristaltic sequence to the muscular contractions. Sphincteric relaxation anticipates pharyngeal contraction. (From Code, C. F., and Schlegel, J. F.: Motor action of the esophagus and its sphincters. In Handbook of Physiology-Alimentary Canal. Section 6, Chapter 90. Bethesda, Maryland, American Physiological Society, 1967, p. 1827.
ABNORMALITIES OF PHARYNGO-ESOPHAGEAL FUNCTION The lack of objective data makes the subject of functional derangements of pharyngo-esophageal function a confused one. The literature is full of varying concepts regarding the nature of physiologic disturbances in this region. Ever since the suggestion by Kelly 14 in 1919 that there was "spasm" at the entrance to the esophagus in patients with the disease that later became known in Great Britain as the Paterson-Kelly syndrome and in this country as the Plummer-Vinson syndrome, a variety of proposals has been offered by the medical profession to explain abnormalities of function of this portion of the gullet. In addition to Kelly, a number of others have emphasized the role of cricopharyngeal spasm in certain swallowing disorders. In 1946, Lahey 17 directed attention to the cricopharyngeal muscle, implicating it in the etiology of esophageal diverticula and advised forceful dilation of the muscle as well as surgical excision. Negus 21 • 22 also advised dilation in patients with pharyngo-esophageal diverticula, although cricopharyngeal incoordination rather than spasm was considered as the cause of the pouch. Delayed relaxation of the sphincter was considered an important mechanism by Cross and associates. 6
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A related concept is that of cricopharyngeal achalasia in which, theoretically, the sphincter fails to relax. As early as 1926, Jackson and Shallow 12 postulated such a mechanism as being the cause of pharyngoesophageal diverticula. Asherson 2 is usually given credit for introducing the term achalasia in 1950 as applied to various neuromuscular disorders affecting the cricopharyngeus muscle. Sutherland30 revived the term in 1962 and implicated this mechanism in the development of pharyngo-esophageal diverticula. Belsey3 also used the term in explaining the development of diverticula in a paper written in 1966, although he seems to use the terms achalasia and spasm synonymously. Another form of incoordination of the sphincter is that of a "second swallow" against a closed sphincter. This concept stemmed from radiographic studies of the upper gullet and was invoked to explain the development of pharyngo-esophageal diverticula. 32 Another possible mechanism for which there is recent physiologic support is that of premature contraction of the sphincter. In 1961 Ardran and Kemp,! basing their findings on radiography of the upper food passages, described partial or complete closure of the cricopharyngeus sphincter before all of the ingested bolus had been displaced from the pharynx into the esophagus. Lund19 has also described similar findings in instances of pharyngo-esophageal diverticulum. Esophageal manometric studies carried out on patients with pharyngo-esophageal diverticula, to be described in detail later, have supported this concept of premature contraction of the sphincter in such individuals.9 In addition to these various concepts regarding disordered function of the cricopharyngeus muscle in patients with diverticula, it has from time to time been postulated that abnormal pharyngeal function may be secondary to a variety of neuromuscular disorders. The following section represents an attempt to classify these various conditions. Classification of Disorders Table 1 represents a tentative classification of abnormalities of pharyngo-esophageal function based on personal and published inforTable 1. Classification of Abnormalities of Pharyngo-Esophageal Function Central nervous system disease Bulbar poliomyelitis Cerebrovascular accident Diseases affecting muscular activity Muscular dystrophy Myasthenia gravis Thyrotoxic myopathy Postsurgical dysphagia Radical oropharyngeal surgery Idiopathic incoordination Pharyngo·esophageal diverticulum
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mation. It is not intended to be all inclusive but rather is limited to the conditions that are most likely to be encountered clinically. With the exception of pharyngo-esophageal diverticulum, objective physiologic data relative to the mechanisms responsible for upper esophageal dysphagia are notably lacking. Abundant evidence exists, however, that some individuals, after injury to the brain stem, such as occurs with bulbar poliomyelitis or after a cerebrovascular accident, have difficulties in swallowing. 4, 13, 19,31 Diseases that directly affect muscular activity also may result in swallowing difficulties. Most common among these diseases are muscular dystrophy, myasthenia gravis, and the myopathy of thyrotoxicosis.4, 18, 24, 25 Of 34 patients with local lesions of the brain examined radiographically by Silbiger and associates,27 27 had motility disturbances of pharyngo-esophageal function while one third of those with primary muscle disease were so affected. Abnormalities of sphincteric relaxation are said to characterize central nervous system lesions, while the muscle diseases result in failure to develop effective pharyngeal peristalsis. Cricopharyngeal myotomy has been employed in scattered instances of this sort with inconclusive results. Difficulty in swallowing has been reported after extensive operations on the oropharyngeal region. Spasm of the cricopharyngeus muscle was considered by Schobinger26 to be the cause of dysphagia after total laryngectomy. Ogura et al. 23 subsequently advocated routine cricopharyngeal myotomy in patients undergoing supraglottic laryngectomy. More recently Mladick and associates20 have emphasized the role of the cricopharyngeus muscle in the pathophysiology of dysphagia after certain major oropharyngeal resections and described the use of cricopharyngeal myotomy in 21 patients. Their indications included a variety of operative procedures, such as resection of half or more of the oral pharynx or hypopharynx, total glossectomy, epiglottectomy, supraglottic laryngectomy, and resection of half or more of the base of the tongue. Finally, my associates and J9 have recently described a type of incoordination in patients with pharyngo-esophageal diverticulum that may be significant etiologically and supports the earlier radiographic findings mentioned previously. Using esophageal motility studies, we carried out 21 observations of pressures in the pharynx and esophagus on 11 patients with pharyngo-esophageal diverticula and compared them with 21 patients who had a normal pharynx and upper esophagus. A zone of elevated pressure was detected at the pharyngo-esophageal sphincter in all patients with pharyngo-esophageal diverticula. The elevated pressure zone was slightly longer and the maximal pressures within it were slightly lower than those reported from normal individuals. With deglutition all of the patients studied had immediate sphincteric relaxation followed by contraction, although the magnitude of relaxation and its duration were slightly longer than normal and the amplitude of contraction was slightly less. These findings clearly exclude the possibility of cricopharyngeal achalasia being present in patients with this disease. However, all of the
559
UPPER ESOPHAGEAL SPHINCTER IN HEALTH AND DISEASE
Health
PE Diverticulum
PE Diverticulum
I
H2
Swallow
1"5 em J" Pressure
t
Figure 4. Deglutition pressures at pharyngo-esophageal junction in a normal person and in two patients with pharyngo-esophageal diverticula. Note that in health (left panel) the pharyngo-esophageal sphincter (PES) is open during the entire period of pharyngeal contraction. In the two patients with diverticula, part or all of the period of pharyngeal contraction occurs after closure of the sphincter (middle and right panels). (From Ellis, F. H., Jr., et aI., Ann. Surg. 170:342, Sept., 1969.)
patients were noted to have an abnormal temporal relationship between pharyngeal contraction and pharyngo-esophageal sphincteric relaxation and contraction. In these patients, sphincteric contraction occurred before completion of the contraction of the pharynx (Fig. 4). No such abnormality was observed in any of the normal patients studied. In other words, clear evidence for incoordination of the pharyngo-esophageal junction was identified in all of the patients with the abnormality under discussion, suggesting that this incoordination, whatever its cause, might be responsible for the development of the lesion. These findings have not been confirmed by other workers, however. Kodicek and Creamer 16 carried out successful studies on 5 patients with pharyngo-esophageal diverticula without evidence of any abnormality of function. Of considerable interest is the recent report of Hunt and associates l l showing that sphincteric resting pressures were elevated in most patients with a pharyngeal pouch, in contrast to our findings, which showed the pressures to be slightly lower than normal. This difference may be explained partially by the fact that in our series of cases only 1 patient had a hiatal hernia, while 28 of their 30 patients with pharyngeal pouches had a hernia. Smiley and associates 28 postulated that since cricopharyngeal resting pressures were found to be high in the presence of gastroesophageal reflux, pharyngeal pouches result from cricopharyngeal dysfunction secondary to reflux.
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CRICOPHARYNGEAL MYOTOMY The concept of purposely weakening the pharyngo-esophageal sphincter is not a new one. Reference has already been made to the use of forceful dilation in the management of patients with pharyngoesophageal diverticula. Endoscopic diathermy division of the septum or common wall between the esophagus and the diverticulum has been used by Dohlman and Mattsson 8 among others. The procedure of cricopharyngeal myotomy was a natural consequence of the introduction by Asherson 2 of the term "achalasia" as applied to various neuromuscular disorders affecting the cricopharyngeal muscle and, as indicated before, a number of reports have appeared in the literature describing the successful use of this operative procedure in such conditions. While Harrison 10 employed cricopharyngeal myotomy combined with inversion of the diverticulum in 3 patients who had pharyngeal pouches, Sutherland 30 was perhaps the first to use the technique alone in patients with this condition. Subsequently, Davis and associates 7 and Blakely and associates 4 each reported the cases of 2 patients with pharyngeal pouches successfully treated by cricopharyngeal myotomy. The most extensive experience with this technique is that of Belsey 3 who in 1966 reported its use in 32 patients with pharyngo-esophageal diverticula, most of whom had diverticulopexy performed at the same time. Of the 18 pa-
Figure 5. Technique of esophagomyotomy. A, Site of skin incision. B, Exposure of diverticulum. Dotted line indicates proposed myotomy site. C, Completed operation. (From Ellis, F. H., Jr., et ai., Ann. Surg. 170:343, Sept., 1969.)
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tients we reported in 1969,9 all had cricopharyngeal myotomy, 4 had diverticulopexy in addition, and 4 had diverticulectomy. All but one were improved by the operation. Others have advocated the use of cricopharyngeal myotomy whenever diverticulectomy is performed, as recurrences have been reported with diverticulectomy alone. 15 • 29 It has been my experience that cricopharyngeal myotomy is a successful procedure for patients with smallsize to medium-size pouches. Those with pouches larger than 5.0 to 6.0 cm. in diameter should have diverticulectomy performed.
Surgical Technique The technique of esophagomyotomy is illustrated in Figure 5. Access to the diseased area is obtained through a left oblique cervical incision bordering the anterior edge of the sternocleidomastoid muscle. The
Figure 6. Esophageal roentgenograms in patient with pharyngo-esophageal diverticulum. A and B, Before operation. C and D, Four days after esophagomyotomy. E and F, Ten months later. (From Ellis, F. H., Jr., et al., Ann. Surg. 170:346, Sept., 1969.)
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HENRY ELLIS, JR.
pharyngo-esophageal region is exposed by retraction of the carotid sheath laterally and the trachea and larynx anteriorly and to the right. After the diverticulum is freed to its neck, the transverse fibers of the cricopharyngeus muscle bordering the inferior margin of the neck of the diverticulum are easily identified and incised. The incision is carried down to the mucosa and is extended caudally onto the esophagus, the length of the incision averaging about 3.0 cm. After the myotomy, the esophageal and cricopharyngeal muscles are dissected from the underlying mucosa for about half the circumference of the mucosal tube to allow the mucosa to protrude freely through the incision. The cervical wound is then closed with interrupted sutures, with or without drainage. The patient is allowed free oral feedings and is discharged from the hospital in a few days. At the time of dismissal from the hospital, roentgenograms of the esophagus reveal that the diverticulum either is no longer identifiable or is considerably smaller than before surgery (Fig. 6). Postoperative motility studies disclose a reduction by 50 per cent in the resting pressures at the pharyngo-esophageal sphincter accompanied by a decrease in length (Fig. 7). While with deglutition, relaxation and contraction persist, the magnitude of each component is reduced. The abnormal temporal relationships existing between the pharynx and sphincter before operation are also present after operation (Fig. 8). Preoperative
I
25 em H20 Pressure
5
Days
After
Cricopharyngeal
Myotomy
o. T:.:,.'.,,-.--""""-_'IjIo-,._-----...-"""II--I"'"
. ...... Pne mo ral?h
Figure 7. Resting pressures at the pharyngo-esophageal junction in patient with pharyngo-esophageal diverticulum before esophagomyotomy (upper panel) and five days after surgery (lower panel). Note decrease in sphincteric pressure and shortening of sphincter after operation. (From Ellis, F. H., Jr., Ann. Surg. 170:347, Sept., 1969.)
563
UPPER ESOPHAGEAL SPHINCTER IN HEALTH AND DISEASE
Preoperative 25cm
Pressure
cm from Incisors:
PH A R YNX _/Wj3_"i'+-1' II PES_;,,;;18...._"'" Atmospheric - - - - 1" Pressure l' Swollow
Post Myotomy
I sec
1-1
" +-
Atmospheric- Pressure Swallow
I
Figure 8. Deglutition pressures at pharyngo-esophageal junction in patient with pharyngo-esophageal diverticulum before surgery (upper panel) and five days after esophagomyotomy (lower panel). Some patient as in Figure 7. Note occurrence of pharyngeal contraction after closure of pharyngo-esophageal sphincter (PES). This abnormal sequence is not altered by myotomy, but the amplitude of sphincteric contraction is markedly reduced, as is the amplitude of relaxation. (From Ellis, F. H., Jr., et ai., Ann. Surg.170:347, Sept., 1969.)
SUMMARY The act of swallowing involves a complex mechanism reqUITIng precise coordination of the tongue, larynx, pharynx, and upper esophagus. Esophageal manometry has identified as part of this mechanism a high pressure zone corresponding to the cricopharyngeus muscle and adjacent pharyngeal and esophageal musculatures. This zone has the characteristics of a sphincter. It relaxes with swallowing just before and including the period of pharyngeal contraction and subsequently contracts to initiate the primary peristaltic wave of the esophagus. Many conditions may disturb the coordinated events that characterize normal pharyngo-esophageal function. These include central nervous system lesions, conditions affecting muscle function directly, major oropharyngeal surgery, and the idiopathic sphincteric incoordination characteristic of pharyngoesophageal diverticulum. Much needs to be learned about the exact nature of the physiologic disturbance that exists in these various disease states before cricopharyngeal myotomy can freely be recommended. If sphincteric pressures are high or if relaxation is incomplete, the operation should be
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beneficial. It is particularly useful in the treatment of small-size to moderate-size pharyngeal pouches, conditions characterized by closure of the cricopharyngeal sphincter before completion of pharyngeal contraction. Cricopharyngeal myotomy alone is accompanied by a high rate of symptomatic improvement coupled with radiographic evidence of regression in size or disappearance of the diverticulum in almost all cases.
REFERENCES 1. Ardran, G. M., and Kemp, F. H.: The radiography of the lower lateral food channels. J. Laryng. 75:358-370 (April) 1961. 2. Asherson, N.: Achalasia of cricopharyngeal sphincter: record of cases, with profile pharyngograms. J. Laryng. & Otol. 64:747-758 (Dec.) 1950. 3. Belsey, R: Functional disease of the esophagus. J. Thorac. Cardiov. Surg. 52:164-188 (Aug.) 1966. 4. Blakely, W. R, Garety, E. J., and Smith, D. E.: Section of the cricopharyngeus muscle for dysphagia. Arch. Surg. 96:745-762 (May) 1968. 5. Code, C. F., and Schlegel, J. F.: Motor action of the esophagus and its sphincters. In Handbook of Physiology-Alimentary Canal. Section 6, Chapter 90. Bethesda, Maryland, American PhysiolOgiC Society, 1967, pp. 1821-1839. 6. Cross, F. S., Johnson, G. F., and Gerein, A. N.: Esophageal diverticula. Associated neuromuscular changes in the esophagus. Arch. Surg. 83:525-533 (Oct.) 1961. 7. Davis, M. V., Mitchel, B. F., and Adam, M.: Cricopharyngeal achalasia: variant of hypopharyngeal diverticulum syndrome. Texas J. Med. 62:47-49 (Feb.) 1966. 8. Dohlman, G., and Mattsson, 0.: The endoscopic operation for hypopharyngeal diverticula; a roentgencinematographic study. Arch. Otolaryng; 71 :744-752 (May) 1960. 9. Ellis, F. H., Jr., Schlegel, J. F., Lynch, V. P., et al.: Cricopharyngeal myotomyforpharyngoesophageal diverticulum. Ann. Surg. 170:340-349 (Sept.) 1969. 10. Harrison, M. S.: The aetiology, diagnosis and surgical treatment of pharyngeal diverticula. J. Lar. Otol. 72:523 -534 (July) 1958. 11. Hunt, P. S., Connell, A. M., and Smiley, T. B.: The cricopharyngeal sphincter in gastric reflux. Gut 11 :303-306 (April) 1970. 12. Jackson, C., and Shallow, T. A.: Diverticula of oesophagus, pulsion, traction, malignant and congenital. Ann. Surg. 83:1-19 (Jan.) 1926. 13. Kaplan, S.: Paralysis of deglutition, post-poliomyelitis complication treated by section of cricopharyngeus muscle. Ann. Surg. 133:572-573 (April) 1951. 14. Kelly, A. B.: Spasm at entrance to oesophagus. J. Lar. Otol. 34:285-289 (Aug.) 1919. 15. Kinley, C. E.: The management of hypo pharyngeal diverticulum. Canad. J. Surg. 9:27-32 (Jan.) 1966. 16. Kodicek, J., and Creamer, B.: A study of pharyngeal pouches. J. Laryng. 75:406-411 (April) 1961. 17. Lahey, F. H.: Pharyngo-esophageal diverticulum; its management and complications. Ann. Surg. 124:617-636 (Oct.) 1946. 18. Leach, W.: Generalized muscular diseases presenting as pharyngeal dysphagia. J. Laryng. 76:237-240 (March) 1962. 19. Lund, W. S.: A study of the cricopharyngeal sphincter in man and in the dog. Ann. Roy. ColI. Surg. Eng. 37:225-246 (Oct.) 1965. 20. Mladick, R A., Horton, C. E., and Adamson, J. E.: Cricopharyngeal myotomy: Application and technique in major oral-pharyngeal resections. Arch. Surg. 102:1-5 (Jan.) 1971. 21. Negus, V. E.: Pharyngeal diverticula; observations on their evolution and treatment. Brit. J. Surg. 38:129-146 (Oct.) 1950. 22. Negus, V. E.: The etiology of pharyngeal diverticula. Bull. Johns Hopkins Hosp. 101: 209-223 (Oct.) 1957. 23. Ogura, J. H., Saltzstein, S. L., and Spjut, H. J.: Experiences with conservation surgery in laryngeal and pharyngeal carcinoma. Laryngoscope 71 :258-276 (March) 1961. 24. Peterman, A. F., Lillington, G. A., and Jamplis, R W.: Progressive muscular dystrophy with ptosis and dysphagia. Arch. Neurol. 10:38-41 (Jan.) 1964. 25. Pierce, J. W., Creamer, B., and MacDermot, V.: Pharynx and esophagus in dystrophia myotonica. Gut 6:392-395 (Aug.) 1965. 26. Schobinger, R: Spasm of the cricopharyngeal muscle as cause of dysphagia after total laryngectomy. Arch. Otolaryng. 67:271-275 (March) 1958.
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27. Silbiger, M. L., Pikielney, R., and Donner, M. W.: Neuromuscular disorders affecting the pharynx. Cineradiographic analysis. Invest. Radiol. 2:442-448 (Nov.-Dec.) 1967. 28. Smiley, T. B., Carer, T. B., and Porter, D. C.: Relationship between posterior pharyngeal pouch and hiatus hernia. Thorax 25:725-731 (Nov.) 1970. 29. Smith, S., and Buchtel, B. C.: Pharyngo-esophageal diverticula and dysfunction of the cricopharyngeus muscle. Southern Med. J. 61 :826-828 (Aug.) 1968. 30. Sutherland, H. D.: Cricopharyngeal achalasia. J. Thorac. Cardiov. Surg. 43:114-126 (Jan.) 1962. 31. Wilkins, S. A., Jr.: Indications for section of the cricopharyngeus muscle. Amer. J. Surg. 108 :533-538 (Oct.) 1964. 32. Wilson, C. P.: Pharyngeal diverticula, their cause and treatment. J. Laryng. 76:151-180 (March) 1962. 33. Zaino, C., Jacobson, H. G., Lepow, H., and Ozturk, C. H.: Pharyngoesophageal Sphincter. Springfield, Ill., Charles C Thomas, 1970,209 pp.