Eur Radiol (2005) 15: 13191325 DOI 10.

1007/s00330-005-2687-z

HEAD AN D NECK

Milton Melciades Barbosa Costa Hilton Augusto Koch

Lateral laryngopharyngeal diverticulum: anatomical and videofluoroscopic study

Received: 31 May 2004 Revised: 17 December 2004 Accepted: 21 December 2004 Published online: 9 February 2005 # Springer-Verlag 2005

This work was performed at the Laboratories of Digestive Motility of the Department of Anatomy and Radiology of the Federal University of Rio de Janeiro, Brazil. M. M. B. Costa (*) Laboratrio de Motilidade Digestiva e Imagem, S. F1-008, Departamento de Anatomia, Universidade Federal do Rio de Janeiro ICB/CCS/UFRJ, Rio de Janeiro, 21941-590, Brazil e-mail: mcosta@acd.ufrj.br Tel.: +55-21-25626467 Fax: +55-21-24172029 H. A. Koch Departamento de Radiologia, Universidade Federal do Rio de Janeiro ICB/CCS/UFRJ, Rio de Janeiro, Brazil

Abstract The aims were to characterize the anatomical region where the lateral laryngopharyngeal protrusion occurs and to define if this protrusion is a normal or a pathological entity. This protrusion was observed on frontal contrasted radiographs as an addition image on the upper portion of the laryngopharynx. We carried out a plane-by-plane qualitative anatomical study through macroscopic and mesoscopic surgical dissection on 12 pieces and analyzed through a videofluoroscopic method on frontal incidence the pharyngeal phase of the swallowing process of 33 patients who had a lateral laryngopharyngeal protrusion. The anatomical study allowed us to identify the morphological characteristics that configure the high portion of the piriform recess as a weak anatomical point. The videofluoroscopic study allowed us to observe the laryngopharyngeal pro-

trusion and its relation to pharyngeal repletion of the contrast medium. All kinds of the observed protrusions could be classified as lateral laryngopharyngeal diverticula. The lateral diverticula were more frequent in older people. These lateral protrusions can be found on one or both sides, usually with a small volume, without sex or side prevalence. This formation is probably a sign of a pharyngeal transference difficulty associated with a deficient tissue resistance in the weak anatomical point of the high portion of the piriform recess. Keywords Swallowing . Laryngopharynx . Diverticula . Pharyngeal pouch . Dysphagia

Introduction
There is not a clear consensus on the meaning of the lateral laryngopharyngeal protrusion. Sometimes it is defined as a diverticulum but it is more frequently defined as a pouch or bulge [1]. It is considered as rare [26] and also as common [1, 7]. It is usually considered as a pathological entity [1, 813] but it was already considered as a variation of the normal morphology [5]. The lateral laryngopharyngeal protrusion can be observed on frontal contrasted radiographs as an addition image on the upper portion of the laryngopharynx. It can be

seen on one or both sides and has variable size and morphology. To Liston [7] these kinds of protrusions pass through the thyrohyoid membrane and they are the most common type of lateral pharyngeal diverticula. Lateral laryngopharyngeal pouches were considered as different from the lateral laryngopharyngeal diverticula [1]. The diverticula formations are protrusions that appear as full barium bags, variable in size, connected to the pouch by a short neck [1, 5]. Although both lateral laryngopharyngeal pouches and lateral laryngopharyngeal diverticula are considered as different entities, they have their origin at the same weak point on the thyrohyoid membrane [8].

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Lateral laryngopharyngeal protrusions classified as pouches and even as small diverticula may occur without symptoms [1, 14]. There are descriptions of associated complaints with lateral laryngopharyngeal protrusions, classified as diverticula, like dysphagia [1], cervical aching and odynophagia [15], dysphagia and hoarseness [12], dysphagia, suffocation and cervical discomfort [14] and even the possibility of aspiration after swallowing [13, 16]. Bagatzounis and Geyer [17] suggested that a lateral pharyngeal protrusion could be the cause of laryngeal superior nerve neuralgia. The lateral laryngopharyngeal protrusion was considered as a well-known entity by Ekberg and Nylander [1]. But our literature review led us to believe that this theme remains open to new research. Therefore our goal is to characterize the anatomical region where the protrusion occurs and to define if it is a normal or a pathological entity.

did not have significant digestive complaints. They were studied using a 100% barium solution. The pharyngeal phase of the swallowing process of each patient was observed at least with three gulps in frontal incidence. Each gulps volume was defined according to each patients own capability [18]. Starting from an 80-ml graduated beaker filled with barium solution, each gulp was registered. The gulps varied from 8 to 20 ml with an average of 12 ml. The requested the patients to perform a discreet cervical extension during swallowing. Videofluoroscopic examinations were accomplished with an FR2 type UV 56 M Medicor instrument, with a D1912/50150 tube under the table, a Videomed 2 TV system, an RBV 23/13 type image intensifier and a 525-line pattern, 60 Hz, interlacement 2:1 Vidicon tube. Images were recorded in VHS with a CXE 1331 Samsung high-speed video/monitor system. The tapes were analyzed with a Panasonic AG1980 video recorder and a Panasonic CT1383-VY monitor.

Materials and methods

Our study was developed using anatomical pieces and patients who had a lateral laryngopharyngeal protrusion in full agreement with the ethical guidelines proposed by the World Medical Association (WMA, Declaration of Helsinki, 1995; amended by the 52nd WMA General Assembly, Edinburgh, UK, October 2000). We obtained 12 blocks containing tongue, hyoid, pharynx and larynx from adult corpses of both sexes (seven male and five female), without traumatic deformities or known diseases, fixed in 10% formaldehyde solution. The area to be dissected was the thyrohyoid membrane projection delimited on the top by the hyoid bone, on the bottom by the superior border of thyroid cartilage lateral lamina and, on both sides, by a longitudinal plane tangent to the superior horn of the thyroid cartilage. The dissections enabled the analysis of both sides of the thyrohyoid membrane. We carried out a qualitative plane-by-plane observation through macroscopic and mesoscopic surgical dissection. The morphological characteristics and anatomical correlation between regional structures were analyzed and registered as the result. Besides surgical instruments we used a D.F. Vasconcelos model 1628 surgical magnifying glass for the dissection procedure. From 170 patients subjected to videofluoroscopy for digestive complains, we found 33 had a lateral pharyngeal protrusion (16 males and 17 females aged between 28 and 87). Twenty-three had significant dysphagia complaints (ten related to stroke, seven to oral and pharyngeal functional impairment without evident neural compromising, three to tracheocutaneous fixation, one to a cricopharyngeal bar, one to cricopharyngeal compression by cervical osteophyte and one was related to a psychogenical cause). Six had esophageal emptying dysfunction (two related to stenosis, one to Nissen surgery, one to achalasia, one to extrinsic compression and one to colon transposition). Four

Results
The anatomical analysis of the piriform recess let us see that its superior extremity, above the superior border of the thyroid cartilage lateral lamina, comes in a deeper plane, forming a complementary recess. This superior depression, although more accentuated, was continuous with the remainder of the piriform recess. This was true in all the pharynxes analyzed, except in one man, on the right side, and in one female, on the left side, where we found a circular entrance of a little bag whose depth exceeded the limit of the neighboring areas configuring atypical depression (lateral laryngopharyngeal diverticulum) (Fig. 1). Over the thyrohyoid membrane external face, we found a triangular area where the superior laryngeal nerve and vasa passed through. The limits of this triangular area were determined on the top by the inferior margin of the greater horn of the hyoid bone, the anterior margin by the posterior border of the thyrohyoid muscle and at the bottom by the muscular fibers of the thyropharyngeal part of the inferior pharyngeal constrictor muscle (Figs. 2a, 3). The trans-illumination from the external surface of thyrohyoid membrane let us see an illuminated circular area projected on the upper portion of the piriform recess. The lower limit of this thin area is delimited by the superior border of the thyroid cartilage lateral lamina. The top limit is delimited by the intrapharyngeal portion of the stylopharyngeus muscle. This top limit is located on the level of a transverse plane that passes in the vallecula bottom limit (Figs. 2bd, 3). The superior fibers of the thyropharyngeal part cover and reinforce the posterior and inferior portions of the thyrohyoid membrane. In the same way, the internal surface of the thyrohyoid membrane has its superior limit reduced and

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Fig. 1 Posterior view of the frontal image where in a we see (1) over the projection of the superior horn of the thyroid cartilage on both sides and (2) over the aryepiglottic fold; the arrow (3) points to the laryngeal aditus. Between 1 and 2 we observe the normal superior depressed portion on the pirifom recess on both sides. In b on the left side of a female piece and in c, on the right side of a males piece, we can observe an atypical depression over the high portion of the piriform recess (lateral pharyngeal diverticulum)

reinforced by the inferior fibers of the stylopharyngeus muscle. Once the musculature related to the thyrohyoid membrane has been retracted, an irregular conjunctive thin area can be observed. This thin area has its anterior limit drawn by the posterior margin of the anterior thyrohyoid ligament, the top limit by the inferior margin of the greater horn of the hyoid bone, the back limit by the posterior thyrohyoid ligament and the superior horn of the thyroid cartilage, and the bottom limit by the superior border of the thyroid cartilage lateral lamina. This thin area let us see a passage foramen to the internal branch of the superior laryngeal nerve about 1 cm above its bottom limit. This foramen has been projected over a deeper plane of the thyrohyoid membrane. Forming this deeper plane, we could observe a thin area of the thyrohyoid membrane outlining the hole of the nervous passage (Fig. 4). From the piriform recess, this foramen and its outline are covered by a regional mucous membrane (Fig. 3b). We could not identify sex or side differences in this thin area constitution projected in the high segment of the piriform recess. On both sexes, the vertical position of the superior horn of thyroid cartilage forms an angle less than 90 with the superior border of its lamina. Nevertheless, we have found in two males and in one female anatomical

Fig. 2 Schematic drawings. a Right lateral view, where 1 shows the triangular area crossed by the laryngeal superior nerve. This triangular area is formed by the great horn of the hyoid bone (2), the thyrohyoid muscle (3) and the thyropharyngeal muscle (4). b Frontal posterior view of the laryngopharyngeal anterior wall, where arrows point to both sides of the superior depressed portion of the pirifom recess: 1 laryngeal aditus, 2 intrapharyngeal segment of the stylopharyngeal muscle.c Medial view of the sagittal plane highlighting the superior horn of the thyroid cartilage (1), the arytenoid cartilage (2), the epiglottis cartilage (3), the body of the hyoid bone (4), the thyrohyoid membrane (5), where an arrow points to the foramen of the internal branch of the superior laryngeal nerve and the superior laryngeal artery, the medial thyrohyoid ligament (6), a cut surface of the thyroid cartilage (7), the lateral thyrohyoid ligament (8) and the great horn of the hyoid bone (9). d Frontal posterior view of the laryngopharyngeal anterior wall, where 1 indicates the superior horn of the thyroid cartilage, 2 indicates the internal surface of lamina of the thyroid cartilage, 3 indicates the great horn of the hyoid bone, 4 indicates the internal surface of the thyrohyoid membrane and 5 indicates the laryngeal aditus. On both sides, arrows point to the passage foramen of the superior laryngeal nerve that it is represented on the right side.

pieces, both right and left superior horns of the thyroid cartilage on the backward oblique position. And we also have found one female piece, just on the right side, the same superior horn oblique position determining a wider thin area. One of these male anatomical pieces has presented an atypical bag on the right side of the piriform recess superior portion. The results of the videofluoroscopic analysis are shown in Tables 1, 2, 3 and 4. The appearance of the protrusions occurred during the pharyngeal phase when the pharynx was full of contrast medium. We could not relate any complaint associated with them. The protrusions disappeared with the pharyngeal emptying. In seven of our observations (12.5%), a discreet residual mark of the contrast medium could be identified after the pharyngeal emptying. The protrusions dimensions

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Table 2 Unilateral protrusion Side Sex/age Male/>50 Right Left Total 7 3 10 2 3 5 Male/50 1 1 Sex/age Female/>50 3 3 Female/50 1 1

Table 3 Bilateral protrusion Dominant side Fig. 3 a Right lateral view showing the triangular formation, where 1 indicates the laryngeal superior nerve, 2 indicates the great horn of the hyoid bone, 3 indicates the thyrohyoid muscle and 4 indicates the superior fibers of the thyropharyngeal muscle. b Sagittal section of the larynx and the laryngopharynx, where 1 marks the projection of the superior horn of the thyrohyoid cartilage, 2 the arytenoids cartilage, 3 the epiglottis, 4 the body of the hyoid bone and 5 over the tongue, with the white arrow pointing to the valeculla and the black arrow pointing to the trans-illuminated thin area on the top of the piriform recess. Sex/age Sex/age Male/>50 Male/50 Female/>50 Female/50 Right Left Similar Total 5 9 9 23 4 3 1 8 2 2 1 3 5 9 3 1 4

Table 4 Protrusion characteristics Without neck Convex form Conic form Narrow neck Wide neck 50 6 29 6 With neck 21 4 17

varied from 1.0 to 2.5 cm depending on the contrast intensity inside the bag. Swallowing with a contrast-full piriform recess, owing to previous medium retention, usually results in a more evident protrusion than that with less residual contrast volume or with no contrast medium retention (Fig. 5). During swallowing, observed through a radiological frontal sequence, the pharyngeal protrusion appears in a plane below the vallecula and, afterwards, it moves upward to the vallecula level becoming more evident.

Fig. 4 a Left lateral view showing an irregular thin area where the arrow indicates the internal branch of the superior laryngeal nerve entrance, 1 indicates the superior horn of the thyroid cartilage, 2 indicates the superior border of the lateral lamina of the thyroid cartilage, 3 indicates the superior laryngeal nerve and vessels and 4 indicates the posterior margin of the anterior thyroid ligament. The inset (b) details the internal branch of the superior laryngeal nerve entrance (arrow).

Table 1 Distribution Bearers Sex Age Protrusion Fig. 5 Images obtained through the pause function from a videofluoroscopic exam, where in a (frontal view) an arrow points to a unilateral pharyngeal diverticulum on the right side. b The same case, in oblique incidence, with the arrow pointing to the full bag. Male Female >50 50 Unilateral Bilateral Total 33 16 17 25 8 10 23 56

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Fig. 6 Sequence of images in frontal view obtained through the pause function from videofluoroscopic examination of the same pharyngeal swallowing phase, where in a the arrows point to right and left pharyngeal diverticula. The right one is bigger than the left one. In b, both diverticula show more contrast medium density than that observed in a. In the right diverticulum we can see a wide neck. The left one does not have a neck. In c, we can observe a diverticulum emptying. In d, both bags were empty.

Difficulty in swallowing with continuous effort in patients with contrast medium retention in the piriform recess let us see larynx elevation with a pharyngeal contrast residue flowing from the bottom to the top, filling in the lateral laryngopharyngeal protrusion (Fig. 6). In four cases we identified a posterior laryngopharyngeal diverticulum (Zenker) in association with the lateral laryngopharyngeal protrusion. In one case we found a bilateral tonsil recess protrusion associated with the bilateral laryngopharyngeal protrusion.

Discussion
Our anatomical study provided the morphological basis to define the lateral pharyngeal protrusion as a false diverticulum in the same way as the definition of the parietal protrusion observed in the alimentary tract [19, 20]. From our videofluoroscopic results, we could elaborate a simple statistical analysis showing 33 bearers of a lateral pharyngeal protrusion (19.41%) in 170 patients. A bilateral pharyngeal diverticulum was present within 73.5% of them. The lateral pharyngeal diverticula were most common in people aged 50 or older (75.75%). No sex (48.48% male and 51.52% female) nor side volume prevalence was detected. Unilateral protrusions could be found in five

patients (55.55%three males/two females) on the right side and in other four patients (44.45%three males/one female) on the left side. Bilateral protrusions had a larger volume on the right side in nine patients (36%six males/ three females) and in seven patients (28%three males/ four females) on the left side. Similar volumes were observed on both sides in nine patients (36%four males/ five females). Adding the bilateral pharyngeal protrusions and the unilateral ones, we have 56 in total, 35 (62.5%) configured as protrusions without a neck and 21 (37.5%) with a neck. The contrasted protrusions without a neck have a pouch wall continuous with its opening. They could be characterized as a convex bag in 29 (82.86%) observations and as a conical bag in six (17.14%). Within those 21 with a neck, the bulge was expanded in sack form with a more constricted opening that could be considered as wide in 17 cases (80.9%) and as narrow in four (19.1%). We could not identify sex no side anatomical differences in the thin area projected on the top segment of the piriform recess. However, we found two men and one woman with both right and left superior horns of the thyroid cartilage and one woman with a right horn of the thyroid cartilage with an oblique backward position. This morphology, with larger angles than those observed in other anatomical pieces, could imply a larger exposed dimension of the high segment of the piriform recess. Reinforcing this possibility, we found one male piece with an atypical bag on the right side of the superior portion of the piriform recess and a backward position in its right superior horn. But, in contrast, we found one female piece with the same atypical bag not having the backward horn position. The lateral pharyngeal diverticula are visualized as ears projected on the lateral level of the vallecula when visualized in frontal radiological images. The weak point where lateral diverticula arises in the thyrohyoid membrane has its superior limit on a lower level than a plane crossing the bottom of the vallecula, as we have described. This fact demonstrates that the lateral protrusion arises and increases during hyoid and larynx upward and forward displacement. At this moment, the thyrohyoid membrane loses tension, accentuating the regional weakness, allowing easier expansion of the diverticulum. The full bag will become empty by the subsequent stretching of the thyrohyoid membrane produced by its returning to the resting position. Additionally, the lateral pharyngeal protrusion with its wide perpendicular opening and the action of gravity completes its emptying. Therefore, it is not reasonable to believe that thyropharyngeal muscle contraction acts as an additional emptying mechanism, as considered by Ekberg and Nylander [1]. To Bachman et al. [5], 1-1.5-cm diameter protrusions without symptoms are variations of a normal morphology. For them, diverticula would be protrusions with variable sizes, appearing as lateral cavities replete of barium, con-

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nected to the pharyngeal lumen through a short neck. Ekberg and Nylander [1] considered that diverticula of the piriform recess would have a narrow neck and would be able to retain food. The morphological characteristics used as a basis to configure the lateral pharyngeal protrusion [1, 5] clearly show that all forms of the acquired protrusion in the superior portion of the piriform recess are variations of the same pathological entity. The differences depended on individual variations of local tissue resistance. In this way, compared with similar lesions observed in all extensions of the digestive tube, the lateral pharyngeal protrusion is a diverticuluum in a less resistant point on the thyrohyoid membrane. All laryngopharyngeal protrusions acquired, with or without a neck, are kinds of diverticulum. They are constituted by the pharyngeal internal layers passing through an enlarged thyrohyoid membrane hole, in a mechanism similar to that observed in the remaining alimentary tract. In conical, convex or sack form, with or without a neck, they represent the same pathology, although differing in development stage. The physiopathology of lateral laryngopharyngeal diverticula in young adults, owing to pressure increase caused by wind instruments [15, 21], supports the theory that there is an anatomically less resistant area in the superior portion of the piriform recess. In analogy with inguinal hernia physiopathology [22], it is reasonable to suggest regional tissue weakness as an individual characteristic and that this weakness accentuates with aging. Probably, the great incidence of lateral pharyngeal diverticula in older people can be explained by these facts. The swallowing flow direction and the funneled morphology of the laryngopharynx determine flux concentrations in the narrow distal segment of the pharynx without substantial distention of the pharynx superior areas under physiological conditions. When the pharyngoesophageal transition opens, permitting the appropriate pharyngeal flux transference to the esophagus, it allows the piriform recess superior area, which is anatomically less resistant, to stay protected. We understand that the lateral pharyngeal diverticulum is a consequence, not a cause, of dysphagia. We believe that this formation is probably a sign of pharyngeal transference mechanism dysfunction, associated with deficient tissue resistance in the high portion of the piriform recess, where we found a weak anatomical region, due to a passage foramen of the internal branch of the superior laryngeal nerve. We were not be able to attribute any symptom to this kind of diverticulum. Nevertheless, owing to a close relationship between the superior laryngeal nerve and the lateral pharyngeal protrusion, it is possible, as suggested

by Ettman and Ramey [12], that the diverticulum could be the cause of hoarseness or, even, as suggested by Bagatzounis and Geyer [17], the cause of an eventual neuralgia of the superior laryngeal nerve, as verified by Hankins [15] in a case. As a complementary consideration about symptoms we would like to consider that an extremely large protrusion may retain solid food and may cause symptoms. This uncommon large lateral laryngopharyngeal diverticulum can be produced by the professional use of a wind instrument as observed by Hankins [15] and Rommelfanger [21]. The lateral pharyngeal diverticula and the posterior pharyngeal diverticula (Zenker) certainly have the same physiopathological mechanism. The Zenker diverticula characteristics, consequences and easy image detection makes us believe that they are the commonest type of pharyngeal diverticula [2]. However, we found only four Zenker diverticula in association with our 33 lateral pharyngeal diverticula. This relatively high frequency of lateral pharyngeal diverticula highlights its importance as a signal of a dysfunction of the pharyngeal transference mechanism. A tonsil recess pouch is another protrusion to be considered in association with a lateral laryngopharyngeal protrusion. Bachman et al. [5] suggest that a tonsil recess without the tonsil itself provides limited resistance to the pharyngeal pressure. They consider that the tonsil itself complements the tonsil recess resistance. Removed or atrophic tonsils permit pouch production at a level above the hyoid bone. We could observe only one bilateral tonsil recess protrusion in association with lateral pharyngeal diverticula. We did not find any congenital lateral pharyngeal diverticula. They are a very rare cervical protrusion [23] with a fistula opening in the pharyngeal tonsil recess [24, 25]. Fowler [3] considered that a congenital lateral pharyngeal diverticulum could not be confused with an acquired lateral pharyngeal diverticulum.

Conclusions
The lateral pharyngeal diverticula acquired are pathological protrusions, are more frequent in older people and are visualized as ears, are projected at the vallecula level, and are usually bilateral, with small dimensions, without sex, volume or side prevalence. These kinds of protrusion result from a less resistant area in the high portion of the piriform recess. This less resistant area is the anatomical region, in the thyrohyoid membrane, where the internal branch of the superior laryngeal nerve passes to the laryngopharynx submucous.

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The lateral pharyngeal protrusions defined as a pouch or a bulge, with or without a neck, considered as diverticula, are both variations of the same pathological entity. They are

probably a sign of a pharyngeal transference difficulty associated with deficient tissue resistance in the weak anatomical area of the high portion of the piriform recess.

References
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