Current Concepts in the Anatomy and Origin of Pharyngeal Diverticula

/STRU^NI RAD UDK 616.321-007.67-089 DOI:10.2298/ACI0901017S

Current concepts in the anatomy and origin of pharyngeal...... diverticula OM Skrobi}, AP. Simi}, NS Radovanovi}, BV [pica, PM Pe{ko Department of Esophagogastric Surgery, The First Surgical University Clinic, Clinical Center of Serbia, Belgrade, Serbia

The role of this paper is to present the current ANATOMICAL AND TOPOGRAPHICAL concepts in anatomy and etiopathogenesis of pha- CONSIDERATIONS ryngeal diverticula. Precise anatomical considerations highly emphasizing the weak anatomic areas The UES is defined as an area of high intraluminal pres- which predispose the pouch formation are dis- sure that forms a barrier between the pharynx and the cer- cussed. Focus exposed in details will also be given vical esophagus. This definition implies three responses: tone generation, phasic response activity, and sphincter rezime upon the structural and functional characteristics of the upper esophageal sphincter as well as to its opening. The UES relaxes and opens during swallowing, physiological states, architecture and dynamic func- allowing the passage of food and liquids into the esopha- tions. A brief review of hystorical and current perspec- gus, while at the same time provides a barrier against its tives regarding the origin of pharyngeal diverticula retrograde flow. By doing so, he represents an important has also been given. Special attention is given to the protective function preventing aspiration of acidic gastric abnormal cricopharyngeal function in patients with content into the respiratory tract on one side, and on the pharyngeal pouches in the terms of altered UES com- other entry of air into the esophagus. The UES also per- pliance, importance of gastroesophageal reflux and mits, by its physiologic relaxation, retrograde flow of ma- histopathologic changes of cricopharyngeal muscle. terial during belching, and vomiting. Anatomically observed, the pharyngoesophageal junc- Key words: Upper esophageal sphincter, Zenker tion or area encompassing the tone generation function of diverticula, etiopathogenesis the UES is sometimes referred to as the pharyngoeso- INTRODUCTION phageal segment or sphincter (PES) as well as upper esophageal high-pressure zone (UEHPZ). Although the he upper esophageal sphincter (UES) serves a range physiologic concepts of UES are mostly clear, the Tof important physiologic functions. Unlike its coun- anatomic components of these concepts are not. By the terpart in the distal esophagus, we are only beginning structural anatomy standpoint, the pharyngoesophageal to unravel the normal workings of this sphincter and junction or UES represents a musculocartilaginous struc- how its function is disturbed by disease. A clear under- ture composed of the posterior surface of the thyroid and standing on the exact etiopathogenesis of pharyngeal cricoid cartilage, the hyoid bone, and three muscles: infe- pouches, strangely enough, is still lacking. rior pharyngeal constrictor (IPC), cricopharyngeus (CP) Several theories exist concerning the formation of these and cranial or cervical esophagus (CE).1,2,3,4 (Figure 1). CP pulsion diverticula and mostly are centered upon the together with the cranial part of the cervical esophagus structural or physiological abnormality of the UES, espe- constitutes the lower third of the entire pharyngoeso- cially on its most prominent part the cricopharyngeal phageal high-pressure zone, while the IPC muscle ac- muscle (CP). counts for the remaining upper two thirds of the UES.4 In this paper we will highlight current knowledge and The physiologic function of the UES is mainly based on review the literature concerning anatomy and physiology the sole activity of cricopharyngeal muscle. The CP is a of the pharyngoesophageal junction, with a special em- striated muscle attached to the cricoid cartilage that is in phasis on the cricopharyngeal muscle pathophysiology in average 1.9 cm in length in males and 1.6 cm in fe- the spectrum of pharyngeal pouches. males.1,3 CP forms a c-shaped muscular band that pro- duces maximum tension in anteroposterior rather than lat- 18 OM Skrobi} et al. ACI Vol. LVI

eral directions. The CP is suspended between the cricoid processes, surrounds the narrowest part of pharynx, and extends caudally where it blends with the circular muscle of the cervical esophagus. Two sets of CP muscle fibers have been identified: the horizontally oriented fibers (pars fundiformis), which occlude the esophageal introitus, and an oblique band of fibers (pars obliqua), which are responsible for propulsion of the bolus. Both types of fibers of CP extend from the lateral aspect of the cricoid cartilage to the posterior midline raphe, where they blend superiorly with the IPC.5 The horizontal fibers of the CP en- circle the upper esophagus, forming a sling between the two sides of the cricoid cartilage.6 The inferior pharyngeal constrictor muscle extends from the oblique line of the thyroid cartilage to insert into the posterior midline pharyngeal raphe, a fibrous band ex- tending from the base of the skull, to which all of the bands of constrictor muscles are attached. Unlike the IPC, the pars fundiformis of the CP has no median raphe.3,4 Killian’s triangle, also known as dehiscence, through which pharyngoesophageal Zenker diverticula occur, represents an anatomical triangular area of sparse muscula- ture of the IPC, bordered superiorly by the firm oblique fibers of the IPC and inferiorly by the horizontal fibers of the CP, mostly lying in the posterior midline just above the cricopharyngeal sling and below the pharyngeal raphe.7,8,9,10 The cervical esophagus begins at the lower border of the FIGURE 1. cricoid cartilage and contains predominantly striated mus- ANATOMY OF THE PHARYNGOESOPHAGEAL JUNC- cle fibers, but occasionally smooth fibers are found in the TION. center of the muscle. The muscle fibers are arranged in two layers: the external layer containing longitudinal, and the internal layer containing circular or transversely arranged fibers. The inner circular layer blends superiorly with the cricopharyngeus. The longitudinal layer, however, diverges at its upper end approximately one to two cm from the CP, forming two bands that swing laterally and anteriorly around the esophagus to attach to a com- mon tendon behind the cricoid cartilage. Therefore, the posterior esophageal wall between these two diverging bands is the single circular layer of muscular fibers. This forms the second potentially weak area, known as Laimer’s triangle or the Laimer-Haeckerman area.11 The external longitudinal layer courses down the length of the entire esophagus. At its distal end the longitudinal fibers become more oblique and end along the anterior and posterior gastric wall.12 The internal circular FIGURE 2. layer of the esophageal muscle originates at the level of TYPES OF PHARYNGEAL DIVERTICULA AND THEIR cricoid cartilage and in descending forms incomplete cir- LOCATION. A) ZENKER DIVERTICULA, B) LAIMER DI- cles down to the esophagogastric junction. VERTICULA, C) KILLIAN-JAMEISON DIVERTICULA Another space of weakness at the pharyngoesophageal AND D) LATERAL PHARYNGEAL DIVERTICULA. junction is the Killian-Jamieson area. This is a muscular gap in the posterolateral wall located between the oblique pharyngeal fibers and inferiorly by the upper circular fi- and transverse fibers of the cricopharyngeal muscle. Some bers of the esophagus through which course the inferior authors describe this area as the space of the cervical laryngeal nerve, the inferior laryngeal artery, and laryn- esophagus inferior to the cricopharyngeus and lateral to geal lymphatics. the longitudinal muscle of the esophagus just below its in- In this area a Killian-Jamieson diverticulum can be sertion on the posterior lamina of the cricoid cartilage. formed13. It is important to differentiate this type of diver- This area is bounded superiorly by the lowest crico- ticulum from Zenkers, since the treatment approach is Br. 1 Current concepts in the anatomy and origins of 19 pharyngeal diverticula

tion, and conventional wisdom holds that the CP is the major muscle of the UES. Several studies have investigated the separate role of CP, IPC and the cervical esophagus in the unique functioning of the UES.14,15 In rest, both IPC and CP muscle contribute equally, express- ing the similar neuromuscular activity which fluctuates in association with changes in the intraluminal pressure.16,17 Some of the intrinsic pressure of the UES is possibly contributed by the infracricoid esophagus, but continuous activity has not been recorded.15,16,17 UES contraction and relaxation during retching and vomiting occur by the si- multaneous action of the CP, IPC, and proximal cervical esophagus.16,18 During swallowing and belching, CP shows the most prominent drop in pressure and active re- laxation15,18, while on the other hand CP and IPC both show active contractility during coughing and sneezing19. UES contraction in response to esophageal or pharyngeal distension occurs mainly with the action of CP.15 Taking all this facts in account, of all UES muscles only the cricopharyngeal functions is present in all physiologi- FIGURE 3. cal states. CP is composed of striated muscle of small av- INERVATION OF THE PHARYNGOESOPHAGEAL JUNC- erage diameter fibers (25-35 m) which are not oriented in 20,21,22 TION a parallel fashion. These fibers are of predominantly slow twitch (type I), an oxidative skeletal muscle type important for maintenance of basal tonicity.23,24,25 The pres- ence of some fast twitch fibres (type II) allows rapid contraction during swallowing, belching and vomiting.19-22 Compared with other striated muscles, the CP has abun- dant (about 40%) connective tissue (dominated by elastic elements) and larger cell membrane of a muscle cell or sarcolemma (the CP muscle fibers are smaller than most striated muscle fibers and therefore have more sarcolemma).24,27-29 These structural characteristics as well as the network arrangement of muscle fibers and connective tissue could account for the passive elastic behavior.21 Such a histological specificity results in characteristics similar to Starling’s law of cardiac muscle where the tension increases as the muscle is distended. The maximal tension in CP is generated at 1.7 times its basal length.15 This elasticity of CP serves several functions: a) CP distends as a bolus is pushed through the sphinc- 15 FIGURE 4. ter without the need for active relaxation , THREE-DIMENSIONAL PRESSURE PROFILE OF THE UP- b) rapid closure is aided after passage of material through the UES and basal tone is generated at all diame- PER ESOPHAGEAL SPHINCTER ILLUSTRATING THE ters without additional neural input.24,25,26,27 SHORT AXIAL ZONE OF MAXIMAL PRESSURE AND The CP receives innervation from the pharyngeal THE MARKED RADIAL ASYMMETRY. plexus, which is supplied by three major nerves: vagus completely different13 In the pharyngolaryngeal area a nerve branches including the pharyngeal branch of the va- typical lateral pharyngeal or pharyngolaryngeal pouches gus nerve (also referred to as the pharyngoesophageal also can be found. They originate at the weak point of the nerve (PEN), superior laryngeal nerve (SLN), and recur- thyrohyoid membrane and are mainly considered congeni- rent laryngeal nerve (RLN)), the glossopharyngeal nerve tal in origin.(Figure 2) (GPN) and sympathetic nerve fibers from the superior cervical ganglion. Although many nerves appear to pro- NEUROMUSCULAR COMPLEXITY AND THE BIO- ject to the CP, the PEN provides the major motor innerva- PHYSICS OF THE UES tion of the CP.28,29 The motor innervation of the IPC is supplied primarily by the pharyngeal branch of the vagus Despite decades of sophisticated studies, there is still a nerve through the pharyngeal plexus.30 controversy over precisely which muscles comprise the predominant function of UES. The location and structure of the CP muscle appears well suited to sphincter func- 20 OM Skrobi} et al. ACI Vol. LVI

Many studies have attempted to trace nerve fibers through the pharyngeal plexus to the IPC, but because this innervation is through a plexus of interconnecting nerves, it is not possible to definitively determine which branch exactly supplies the IPC. The entire IPC muscle has a single vertical band of motor end plates that corresponds to the location of the pharyngeal plexus (Figure 3). On the other hand the cervical esophagus is mainly innervated by the RLN. The terminal branches travel around the esophagus in a circular fashion and appear to cross the midline both anteriorly and posteriorly.31,32,33,34 ARCHITECTURE AND DYNAMIC FUNCTION OF THE UES The upper esophageal sphincter is usually closed by resting muscle tone and opened during swallowing by relaxation of muscle fibers together with cephalic displacement of the larynx, creating a negative pressure. The clos- FIGURE 5. ing or resting pressure of the UES varies with the circum- NORMAL STATIONARY MANOMETRIC FINDINGS OF 35,36,37 stances under which the measurements are made. THE UES The pressure profile of the UES shows axial asymmetry with a sharp increase and gradual decrease in pressure moving inferiorly through this zone, as well as marked radial asymmetry. These intrasphicteric pressure caracteris- tics have been best described by Welch and colleges who constructed a three-dimensional pressure profile of the UES.38 The pressure applied in the antero-posterior plane is three times greater than at the lateral plane, with a disloca- tion of the peak pressures along the anterior and the posterior aspects. Upper esophageal high pressure zone meas- ures between 2.5 and 4.5 cm in length, and the peak pressure manifest itself bellow the upper border of the high pressure zone, one cm anteriorly and two cm posteriorly.39 Resting pressures in normal subjects have been reported to be with high variations, between 35 and 200 mmHg. At the level of CP muscle this pressure is measured to be in average 55-75 mmHg in anteroposterior direction and 40, 41 20-30 mmHg transversaly. (Figure 4) FIGURE 6. During deglutition the UES converts rapidly from a MANOMETRIC TRACINGS OF IMPAIRED RELAXATION closed state to an open state to allow passage of the swal- OF THE UES IN PATIENTS WITH ZD. lowed bolus into the esophagus. During this opening the lumen assumes an oval cross section, after which it closes hibited. Because of its attachment to the larynx, which as the bolus leaves the pharynx. Relaxation and opening moves with deglutition, the UES moves upward 2 to 2.5 of the UES occur during deglutition, rumination, vomit- cm. ing, and belching.4 Following swallow initiation, approxi- In addition, the pressure applied by the onrushing bolus mately 0.2 to 0.3 seconds prior to the onset of UES open- can push open the lumen of the UES. Therefore, it is pos- ing, transient inhibition of vagal input to the muscular sible for the UES to relax without opening and open with- components of the UES leads to a loss of active tension in out relaxing. the sphincter region. Full sphincter relaxation is observed in the period of 0.5 On swallowing, the UES high-pressure zone falls to to 1.2 seconds and with passage of the hypophrayngeal resting atmospheric pressure and remains open to accom- contraction the sphincter closes with a contraction that modate bolus transport though the sphincter area. This re- creates a pressure that is often twice as high as the resting laxation is brought about by cessation of vagal nerve pressure of the UES itself, called "postrelaxation contrac- stimulation and by upward displacement and elevation of tion"1,3. Based on normal data from our motility labora- the larynx by the suprahyoid muscles (geniohyoid, mylo- tory, a deglutitive UES nadir pressure less than 10 mmHg, hyoid, and thyrohyoid) which pull the UES aborally. In- when measured by a sleeve sensor and during a "dry swal- deed, activation of these muscles can decrease intralumi- low", is considered a complete UES relaxation. (Figure 5). nal pressure within the UES even when the tone is not in- Subsequent to these phenomena, the degree of actual UES Br. 1 Current concepts in the anatomy and origins of 21 pharyngeal diverticula

opening is determined by a balance among three forces: Westrin et al45 suggested that two abnormalities predis- UES muscle tension, intrabolus pressure, and external pose formation of the posterior pharyngeal diverticulum: traction forces on the cricoid cartilage. anatomic weakness of the posterior pharyngeal muscula- It has been documented that manometric tests failed to ture adjacent to UES and/or muscular dysfunction of the detect any abnormality in even 40 per cent of patients UES. We previously described anatomical configuration with Zenker’s diverticulum, There are several reasons of UES, and emphasized the potentially weak areas. But why manometric testing may fail to detect pharyngoeso- the Killians triangle as a congenital weakness can not it- phageal function abnormalities in Zenker’s diverticulum: self explain the formation of the diverticula. ZD usually a) CP, which roughly corresponds to the UES, generates occur in the individuals aging between 60 and 70 years, asymmetric pressures with a considerable variability in and during the decades as the normal part of aging, swal- each of the axes, lowing mechanism can be altered. b) contractions of the pharyngeal striated muscle cause Age related changes include: increased hypopharyngeal pressure events to be much faster and greater in amplitude pressure, decreased number of cells in the Auerbach’s than in the distal esophagus, plexus, need for multiple swallows to effectively clear the c) the UES is extremely mobile and moves proximally oral cavity and diminished coupling between the oral and nearly 1 cm during swallowing, thus causing the record- pharyngeal phase of swallowing.46 It has been postulated ing site to "drop out" if it is placed in the central part of that excessive contraction of the pharyngeal and CP mus- the UES. cles creates the necessary conditions for herniation of the This "dropping out" of the recording site may explain esophageal mucosa trough the weak areas of pharyn- the apparently "normal" relaxation observed by previous goesophageal junction. This kind of possible etiopatho- researchers.42 Dent43 proposed and Kahrilas44 adapted the genesis of the ZD has been called the "neuromuscular manometric sleeve concept which is effective in UES dysfunction theory".45 pressure measurements despite the movement during the In his work concerning the origins of ZD Peters47 using deglutition. However, this method did not provide satis- specialized cricopharyngeal manometric recordings, pos- factory measurements concerning the pharyngeal contrac- tulated that the pathophysiology of pharyngeal pouches tion and UES relaxation. Castell et al34 proposed position- involves "altered compliance of the cricopharyngeus mus- ing the recording sensor above the high-pressure zone of cle" detected as impaired sphincter opening or raised in- the sphincter for that purpose, thereby allowing the trabolus pressure. Hypopharyngeal intrabolus pressure is opened sphincter in its upward excursion, to be studied. the low-pressure domain (2-10 mmHg) within the bolus itself, which is registered before the onset of the major CRICOPHARYNGEAL DISFUNCTION AND THE ORI- pressure upstroke caused by the advancing hypo- GINS OF PHARYNGEAL DIVERTICULA pharyngeal contraction (100 mmHg). It can be appreciated that intrabolus pressure will vary Upper esophageal sphincter relaxation, indeed the entire as a function of the resistance to bolus flow offered by the repertoire of pharyngeal and cricopharyngeal motor UES, and that the major determinant of such resistance is events during deglutition, originates in the medullary sphincter diameter. In ZD, combined radiographic and swallow center. Hence, it is not surprising that the major- manometric studies have confirmed normal pharyn- ity of identifiable disorders underlying failed UES relaxa- gosphincteric coordination, normal resting UES tone, and tion and manifesting as a pharyngeal or cervical complete UES relaxation during the swallow. Those stud- dysphagia most commonly arises from neurogenic or ies demonstrated that opening of the UES was restricted, myogenic diseases. In these diseases dysphagia is fre- and as a result that hypopharyngeal intrabolus pressure quently a part of wider neurologic syndrome, making it had increased. Hence, as originally suggested by Zenker necessary for the clinician to consider a wide range of di- himself, diverticulum formation is due to a poorly compli- agnostic possibilities and appropriate investigations. In ant but normally relaxing UES that cannot fully distend this paper our main objective was to present possible during the process of sphincter opening. Shaw et al sup- pathophysiologic pathways in origin of pharyngeal and ported these finding of poor UES compliance and added pharyngoesophageal diverticula, or intrinsic cricopha- that hypopharyngeal intrabolus pressure is a useful indica- ryngeal muscle disfunction leading to cervical dysphagia. tor of upper sphincter compliance which normalizes after Pharyngeal diverticula as already mentioned may be surgery.48 posterior, posterolateral, or lateral, but the most com- Why is UES opening restricted in patients with ZD? monly encountered type is the posterior pulsion or Histopathologic studies of the CP and IPC muscles, re- Zenker’s diverticulum (ZD). After more than a century of trieved at the time of cricopharyngeal myotomy in pa- debate and investigation there is no general consensus re- tients with ZD, showed myopathic features including garding the exact etiology of ZD. For years most widely muscle fiber degeneration and necrosis, phagocytosis, and accepted mechanisam of the ZD development has been a increased fibroadipose tissue replacement confined to the functional disturbance of the pharyngoesophageal seg- CP muscle. These morphologic changes in the CP muscle ment, mainly a combination of increased resting pressure do influence the contractile and elastic properties of the of the sphincter, lack of complete relaxation, and in par- muscle and probably account for its restricted opening. 49 ticular, incoordination of the hypopharynx and upper esophageal sphincter. (Figure 6) 22 OM Skrobi} et al. ACI Vol. LVI

When compared with the normal CP muscles, the mus- golaryngeal reflux. In the past, most research investiga- cles in patient with ZD demonstrates histologic and bio- tions have concentrated their efforts on focusing on the chemical abnormalities consistent with fiber dropout (due pathophysiology of the UES in the spectrum of pharyn- to necrosis, as evidenced by scattered degenerative fi- goesophageal diverticula. In the future studies, the role bers), greater fiber size variability, and marked increase in not only of the CP or pharyngoesophageal junction has to fibroadipose tissue replacement leading to decreased mus- be investigated, and a special emphasis of the whole cle-connective tissue ratio. Fatty replacement of muscle foregut must be taken into account. By making this kind fibers and increased type I muscle fibers, which are highly of approach to the several century old problems, we shall oxidative slow twitch and are responsible for tonic con- increase our knowledge on the subject of wider spectrum traction, have also been found in the CP muscle of pa- of entities in the possible origins of pharyngeal pouches. tients with ZD. Another issue that has been debated for years is the role SUMMARY of pathologic gastroesophageal reflux in etiology of crico- SAVREMENI KONCEPT ANATOMIJE I PATOFIZIOLO- pharyngeal spasm and formation of ZD. Association be- GIJE FARINGEALNIH DIVERTIKULUMA tween GERD and ZD was firstly recognized when Smiley 50 et al reported increased incidence of hiatal hernia among Cilj ovog rada je da se prika‘u osnovi anatomije i pa- the patients with ZD. Same author performed esophageal tofiziologije gornjeg ezofagealnog sfinktera (GES) u cilju manometric studies in patients with endoscopicaly con- razmatranja etiologije faringealnih divertikuluma. Rad firmed GER, and found significantly elevated resting po~inje sa detaljnim anatomskim prikazom anatomije pressure of the UES. Interestingly enough in these pa- GES-a i posebnim osvrtom na anatomski slabe regije kao tients the resting pressure of UES decreased after the an- predisponiraju}a mesta za nastanak diveritkuluma. Nakon 51 tireflux surgery. The problem with this study was unreli- toga bi}e prikazane strukturalne i funkcionalne karakteris- able manometric equipment and the difficulties with tech- tike mi{i}a koji sa~injavaju GES, a potom i fiziologija nique of the UES resting pressure measurement, which we gornjeg ezofagealnog sfinketra, njegova arhitektonika i 36,43,44 previously described. dinami~ka funkcija. Iznosimo pregled istorijskih i aktuel- Results of Simleys study were compromised by later nih koncepta etiopatogeneze divertikuluma. Ukaza}emo manometric studies of UES in patients with ZD, using the na zna~aj poreme}ene krikofaringealne funkcije u smislu 52 constant perfusion manometric device. No significant oslabljene komplijanse GES-a, kao i histopatolo{kih elevation of CP muscle resting pressure was found in pa- promena krikofaringealnog mi{i}a. Predo~en je i zna~aj tients with reflux esophagitis or symptoms of GERD. patolo{kog gastroezofagealnog refluksa u genezi diver- The higher incidence of GER among the patients with tikuluma kroz pregled literature koja se odnosi na ovu ZD was also reported in numerous studies and it counted problematiku. from 22% to up to 95%.53,54,55,56,57 These studies are diffi- Klju~ne re~i: gornji esofagealni sfinkter, Zenkerov cult to compare because there is no standardization in divertikulum, etiopatogeneza GERD diagnosis. 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