High-Speed Digital Imaging of Neoglottic Vibration After Total Laryngectomy

Objectives  To establish the applicability of digital high-speed imaging in studying neoglottic mucosal vibration after total laryngectomy and to perform a structured evaluation of the recordings using a standardized assessment form to gain insight about the anatomical and morphologic characteristics of the neoglottis.

Design  Evaluation of a new clinical tool and description of clinical disorders in a patient survey.

Setting  The Netherlands Cancer Institute, Amsterdam.

Patients  Forty-six patients who underwent laryngectomy, 36 who underwent standard total laryngectomy and 10 who underwent a partial or total pharynx reconstruction (ie, myocutaneous pectoralis major flap [n=4], free radial forearm flap [n=2], tubed gastric pull-up [n=3], and full gastric pull-up [n=1]).

Intervention  Digital high-speed imaging, using a 90° rigid laryngoscope, of the neoglottic vibration in prosthetic tracheoesophageal speakers after total laryngectomy.

Main Outcome Measures  Digital high-speed imaging might overcome some of the problems of stroboscopy in studying irregular voices and could, therefore, be expected to give more insight into the anatomical and morphologic characteristics of the neoglottis.

Results  Digital high-speed recordings could be obtained in 44 of 46 patients. Using a structured evaluation form, a wide variability in anatomical and morphologic features could be established.

Conclusions  Digital high-speed imaging appeared to be a useful tool in studying the irregular vibrations of the neoglottis. Evaluation by the structured evaluation form gives a good idea about the wide variability in anatomical and morphologic features of the neoglottis.

IN THE PAST 2 decades, vocal rehabilitation of laryngectomies is performed increasingly by prosthetic tracheoesophageal (TE) voice. In several studies^1-3 comparing esophageal with TE voice, it was found that TE voice is more similar to normal voice than esophageal voice. However, comparing TE with normal voice reveals that TE voice is still considered as deviant from normal voice.^1-4 To gain more insight into the underlying mechanism of voice production in patients who underwent total laryngectomy and into the factors that are influencing the quality of the voice, it is necessary to extend our knowledge of the anatomical and morphologic characteristics of the new voice source. This new voice source is often referred to as the pharyngoesophageal segment, pseudoglottis, or neoglottis. Herein, the term neoglottis will be used.

In TE voice restoration, a surgical fistula is created between the trachea and the esophagus, in which a voice prosthesis is inserted. A voice prosthesis acts as a 1-way valve, allowing air from the trachea to pass into the esophagus, and preventing food and saliva from entering the lungs. By occluding the tracheostoma, pulmonary air is directed through the valve into the esophagus. On speaking, the air passing the esophagus sets the neoglottis into vibration. After standard total laryngectomy with primary closure of the pharynx, in general, constriction of the cricopharyngeal muscle narrows the neoglottis and allows formation of a vibrator for voice.⁵ The variable lengths of the narrowing of the neoglottis suggest contribution from the inferior pharyngeal constrictors in some patients.⁵ It can be expected that differences between TE voices are related to differences in the anatomical and morphologic characteristics of the neoglottis.^5-7

Studies of the anatomical and morphologic characteristics of the neoglottis have been performed by videofluoroscopy,^5,7-12 stroboscopy,^12-14 and fiberoptic visualization.^12,15 In laryngeal voicing, stroboscopy is a common method used to visualize vocal fold vibration. With stroboscopy, a virtual slow motion of the rapid vibration is acquired by subsequent light flashes that are slightly out of phase with the fundamental frequency of the vocal fold vibration. Stroboscopy is thus dependent on triggering based on the fundamental frequency extracted from the electroglottographic signal or the acoustical signal of the voice source. "Frequency-independent" visualization methods like high-speed imaging¹⁶ or videokymography¹⁷ are available, which were already used in studying pathological laryngeal voices.^17-21 The advantage of these frequency-independent techniques is the possibility of studying irregular vibrations by performing recordings with many (≥2000) frames per second. These techniques are, to the best of our knowledge, not yet used to investigate anatomical and morphologic characteristics of the neoglottis. In the present study, we investigated whether high-speed imaging is useful as a technique to investigate various characteristics of the neoglottis after total laryngectomy. We used high-speed imaging and not videokymography since we were interested in the anatomical and morphologic features of the entire neoglottis, which can indeed be achieved by visualization in full frames but not by a single scanning line.

The subjects were 46 patients who underwent laryngectomy (35 men and 11 women). Informed consent was received from all subjects. The age of the subjects varied from 46 to 82 years (mean, 67 years). All patients were using TE voice (Provox voice prosthesis; ATOS Medical AB, Hörby, Sweden).^22,23 Stoma occlusion was performed with a valve heat and moisture exchanger (ATOS Medical AB)²⁴ in 44 patients, and with a hands free speech valve (Inhealth Technologies, Carpinteria, Calif)²⁵ in 2 patients. The postoperative follow-up was longer than 6 months in 42 patients and less than 3 weeks in 4. The median postoperative follow-up was 3 years 2 months (range, 2 weeks to almost 18 years). A standard total laryngectomy was performed in 36 patients. In 4 patients, the pharynx was reconstructed partially with a pectoralis major myocutaneous flap; and in 2 patients, a circumferential defect of the pharynx was reconstructed with a tubed free radial forearm flap. Four patients underwent a total laryngopharyngoesophagectomy, which was reconstructed with a full gastric pull-up procedure in 1 patient and with a tubed gastric pull-up procedure in 3 patients. A unilateral radical neck dissection was performed in 14 patients and a bilateral neck dissection in 7; in 25 patients, no neck dissection was performed at all. During surgery, a myotomy of the cricopharyngeal muscle was performed in 8 patients. A neurectomy of the pharyngeal nerve plexus was performed in 22 patients. Imaging of the neoglottis was performed with a unique digital high-speed camera system.¹⁶ This system consisted of a personal computer (Pentium 166 MHz; WIS GmbH, Nuremberg, Germany) and a camera head with a digital charge coupled device sensor chip, which has a resolution of 128 by 128 pixels at 256 gray values and a maximal spectral sensitivity in the far red and near infrared range. The recording rate was 2000 frames per second, enabling a sufficient oversampling with respect to the expected fundamental frequencies. The camera was used in combination with a 90° rigid endoscope (model 4450.57; R. Wolf, Knittlingen, Germany) and a cold light source (model 482; Karl Storz, Tuttlingen, Germany). The patients were asked to produce a sustained /a/ sound. As in normal indirect laryngoscopy, patients were asked to put out their tongue to reveal the cranial opening of the neoglottis. In 12 patients, local anesthesia (10% lidocaine hydrochloride spray) was used during the high-speed recording examination.

During the recording process, each picture was written into a circularly organized semiconductor memory of 256 megabytes. The recording was stopped by a posttrigger signal. By this procedure, all frames recorded during the preceding 8 seconds were held in the camera memory. Sequences containing relevant parts of phonation were stored on a computer hard disk. For permanent storage, the image sequence is copied onto a compact disk (CD-ROM). Once stored, the recording can be replayed at any delayed speed, down to single frame display, using a software program (Winplay Speedcam Version 1.10; Fraunhofer Institute for Integrated Circuits, Erlangen, Germany, available at http://www.iis.fhg.de).

An adapted version of the stroboscopic assessment form suggested by Hirano and Bless²⁶ was used for visual evaluation. It consisted of 3 image quality variables and 7 temporal and morphologic characteristics of the neoglottis (Table 1). In a first trial session, 6 raters (1 ear, nose, and throat specialist; 1 phoniatrician [M.T.]; 1 resident [B.M.R.O.d.C.]; 1 speech therapist; 1 phonetician/speech therapist [C.J.v.A.]; and 1 computer scientist/image processing specialist [T.W.]) blinded for the clinical data judged the recordings independently of each other. Afterward, the results were discussed, and a final rating form was composed (Table 2). In the actual rating, the recordings were, in 4 rating sessions of 2 hours each, judged by 3 raters (1 phoniatrician [M.T.]; 1 resident [B.M.R.O.d.C.]; and 1 phonetician/speech therapist [C.J.v.A.]) who reached consensus of opinion in all cases. For the judgments, a replay speed of 25 single frames per second was used.

Acquiring high-speed images was possible in 44 of 46 patients. The absence of color, the low resolution, and the light power available sometimes limited the overall quality of the recordings; however, even with these limitations it was possible to obtain useful recordings in all but 2 patients. In one patient who underwent standard total laryngectomy, the investigation was not possible because of a high gag reflex. In another patient who underwent a full gastric pull-up procedure, no useful recordings could be obtained and only dark images could be acquired due to the dispersion of the light in the wide neoglottis.

Different shapes and vibration patterns of the neoglottis were seen. Even in the patients in whom data were recorded shortly after surgery, mucosal vibrations could be identified. The only difference in patients with a longer postoperative follow-up was the clearly visible presence of fibrin deposits on the sutures. During TE phonation, saliva is driven upward by the expiratory airflow, which sometimes interacts with the mucosal vibration. Four figures with examples of a vibrating neoglottis are shown. In each figure, the sequence of the subsequent frames in time is from the upper left frame, in horizontal direction, to the lower right frame. In the upper part of each frame the posterior wall is situated; in the lower part, the anterior wall. Right and left are shown as in normal endoscopic investigation. An example of a circular vibrating neoglottis, with a clear mucosal wave, is given in Figure 1. The dark circular area at the right side of the first frame is the lumen of the neoglottis. The brighter semicircular structures above and below the lumen are mucosal folds of the neoglottis. The left esophageal wall is not completely visible. During the subsequent frames, the lumen enlarges and reaches a circular shape, until in frame 23 a new opening in the depth appears. From frame 14 to 20, an irregular brighter structure (mucosal wave) develops and moves toward the anterior mucosal fold.

Besides the circular neoglottis shown in Figure 1, split, triangular, and irregular shapes were seen. In Figure 2, an example is given of a triangular neoglottis; and in Figure 3, an example of a side-to-side split neoglottis is given.

In the patients with a circumferential pharyngeal reconstruction with a radial forearm flap, a complete gastric pull-up, or a tubed gastric pull-up, neoglottic vibrations also could be seen. In Figure 4, an example of a vibrating neoglottis of a patient after a total laryngopharyngoesophagectomy with a tubed gastric pull-up reconstruction is given.

All recordings were judged for quality by the following variables: assessability, brightness, and focus. When more recordings were stored for one patient, the recording with the best consensus judgments for these 3 variables was chosen for further evaluation. The results that are given herein are the results of consensus judgments for all 44 patients for whom evaluable recordings were stored. It appeared that the assessability was good in 22 recordings, fair in 9, moderate in 10, and poor in 3. Brightness was good in 34 recordings, fair in 9, and moderate in 1. The recordings were focused in 24 cases, slightly unfocused in 18, and unfocused in 2. The number of recordings that are slightly unfocused is relatively high; because of large individual differences in the level of the vibrating part, it was not always possible to adjust the focus of the endoscope before or during the phonation optimally. An overview of the results of the judgments of the overall quality of the recordings is given in Table 3.

There were 35 evaluable patients who underwent a standard total laryngectomy. The results of the frequency analysis of the results of the consensus judgments are given in Table 4.

In most patients, there was only a little to a moderate amount of saliva visible, although in a few cases it was more extensive or even obstructing the neoglottis. The origin of the neoglottis was clearly visible in approximately two thirds of the patients; in one third of the patients, it was not clearly visible, which is the case when the neoglottis seems to be situated at a deeper level or when it is obstructed by saliva. The shape of the neoglottis was variable: irregular or left-to-right split shapes were seen most often. The location of the vibration was mostly situated at 2, 3, or more walls. There was a strong or weak mucosal wave visible in half of the patients, and no mucosal wave was seen in the remaining half. Sometimes a mucosal wavelike movement of saliva was seen, resulting in collection of saliva at the upper part of the neoglottis, which was not judged as a mucosal wave. In two thirds of the patients, an irregular vibration of the neoglottis was seen. In half of the patients, the open phase of vibration was longer than the closed phase of vibration. The closed phase was never judged as longer.

There were 9 evaluable patients who underwent a total laryngectomy with a partial or total reconstruction of the pharynx. A large variation in the different characteristics of the neoglottis was seen. The small patient group and subgroups prohibit drawing any meaningful conclusions. Results of the consensus judgments for the 3 small subgroups are given in the right side of Table 4.

The first aim of this study was to establish the applicability of digital high-speed imaging in studying characteristics of the neoglottis in patients after total laryngectomy. From this study, it can be concluded that useful images giving realistic visual information about the vibration of the neoglottis can be collected for further evaluation. The clinical applicability of digital high-speed imaging would be improved if images were in color, the resolution were higher, and the light power were stronger. However, already with the presently available equipment, useful recordings could be obtained in most of the patients studied. There are, to the best of our knowledge, no earlier reports about the use of this technique in studying the neoglottis and, thus, no studies are available for comparison. However, a few articles report on the use of stroboscopy in these voices. Damsté¹³ stated that the neoglottis in esophageal voice, just like the vibration of the normal glottis, could be observed by the aid of a stroboscope, but that conditions must be favorable: a purely periodical vibration and a patient capable of retaining air in the esophagus sufficiently long to permit the introduction of a mirror. He succeeded in a few patients, and saw "serpentine movements" over a great depth (1.0-1.5 cm); the duration of the opening of the upper mucous membrane folds was only short in proportion to the duration of the closed phase. Hammarberg and Nord¹² studied 4 TE speakers using videofluoroscopy and fiberendoscopy. In one of these patients, who had short sequences of regular vibrations of the neoglottis, it was possible to register stroboscopic images. These indicated a pattern of successive closures and openings of the segment. Omori et al¹⁴ studied the dynamics and origin of the neoglottis in 25 TE shunt speakers by videofluoroscopic, strobofiberscopic, and electromyographic studies. With stroboscopy, in 18 patients they observed regular vibration, and in 7 patients, irregular vibration of the neoglottis. In 24 patients, the direction of opening and closure of the neoglottis was anterior-posterior; in one patient, it was left-right. They did not report any problems pacing the stroboscopic light flashes in the irregular TE voices.

Although this is not confirmed by Omori et al,¹⁴ the statement of Damsté¹³ that stroboscopy is only possible in clearly periodic voices seems reasonable. Kitzing²⁷ stated that a necessary condition to get the stroboscopic effect is that the vibrations be (quasi) periodic during the time of observation, and that in case of aperiodicity of the voice source a blurring of the images originates. This is also confirmed by a study performed by Woo et al,²⁸ in which the role of stroboscopy as a clinical tool was studied in pathological vocal fold phonation. It appeared that 17.4% of the recordings were of poor quality. A major cause for this was the inability of the patients' voice to pace the stroboscope. From various studies, it has become clear that, although TE voice seems to be more stable,²⁹ TE and esophageal voice are often irregular.^4,30,31 Irregularities in the acoustic or electroglottographic signal used for pacing the stroboscope cause a mistriggering of the stroboscopic light flashes. Furthermore, when an electroglottographic signal is used in laryngectomies to trigger the stroboscopic light flashes, the pressure of the electroglottographic electrodes in the neck may cause deformation of the neoglottis. We must, therefore, conclude that methods studying the neoglottis should be independent of triggering based on the fundamental frequency. Digital high-speed imaging and videokymography might, therefore, be more suitable to give reliable information about the vibratory pattern of the neoglottis. In a recent study, Schutte et al¹⁸ stressed that digital high-speed imaging is a powerful method for evaluating the vocal fold vibration. However, this is still nonstandard, complex equipment, which is at the moment not readily available for everyday clinical practice. As digital technologies become rapidly available at lower costs, it can be expected that a digital high-speed system will be available for clinicians and voice laboratories at costs comparable with those of the more sophisticated stroboscopy units.

The second aim of this study was to develop an instrument to describe the characteristics of the neoglottis, and to use this instrument to evaluate the anatomical and morphologic characteristics of the neoglottis in the recordings of this patient group. In analogy to the evaluation of stroboscopic images,²⁶ an assessment form for visual assessment was used. Although this is a subjective method to describe the characteristics of the neoglottis, the evaluation form appeared to be useful to describe the visible characteristics of the recordings, and to reach consensus of opinion among the 3 raters.

The results of the consensus judgments show a wide variability in the anatomical and morphologic characteristics of the neoglottis. This wide variation was one of the most striking observations of the study, since it was expected from the study by Omori et al¹⁴ that most vibrations would be in the anterior-posterior direction. However, in this study, the neoglottis appeared to show a wide variation in shape and location(s) of vibration, even among patients with the same type of surgical intervention. This variability in the nature of the neoglottis can be explained by patient-to-patient differences in surgical invasion and reconstruction, as stated by Qi and Weinberg,³² who found a wide variability in the nature of the voicing source signals. The evaluation of the neoglottic vibration after reconstructive surgery shows that neoglottic mucosal vibration also takes place in these voices. The appearance of neoglottic vibration shortly after surgery shows that this vibration is immediately present when vocal rehabilitation is started.

In this ongoing research project, evaluations of videofluoroscopic images and perceptual evaluation and acoustical analysis of the voice quality will be performed in addition to digital high-speed imaging. Relations between these different measurements might give more insight into the role of the different characteristics of the neoglottis in alaryngeal voice quality.

Quantitative evaluation of the high-speed recordings of the neoglottis, providing objective measurements of shape, periodicity, and fundamental frequency, is currently under way and already proved on recordings of the neoglottis of a few patients.³³ Objective criteria obtained by quantitative evaluation may provide useful information about the fundamental frequency and periodicity of the voice source.

In general, digital high-speed recording is a useful tool for obtaining more insight into the anatomical and morphologic characteristics of the neoglottis. The use of a structured assessment form is suggested to perform standardized evaluation.

Accepted for publication March 11, 1999.

This study has been partially supported by grant Ey 15/8-1 from the Deutsche Forschungsgemeinschaft, Bonn, Germany; the Institute for Functional Research into Language and Language Use, Amsterdam, the Netherlands; and the Department of Speech and Language, Catholic University of Nijmegen, Nijmegen, the Netherlands.

Presented in part at the Third European Study Group for Functional Surgery Following Laryngectomy Congress, Arcachon, France, May 26, 1998; and at the 24th International Association of Logopedics and Phoniatrics Congress, Amsterdam, the Netherlands, August 24, 1998.

We thank Louis C. W. Pols, PhD, and Florien J. Koopmans–van Beinum, PhD, for their critical review of the manuscript; and all the patients for their participation in this study.

Reprints: Frans J. M. Hilgers, MD, PhD, Department of Otolaryngology–Head and Neck Surgery, The Netherlands Cancer Institute/Antoni van Leeuwenhoek Huis, Plesmanlaan 121, 1066 CX Amsterdam, the Netherlands (e-mail: fhilg@nki.nl).