Portuguese Version

Year:  2001  Vol. 67   Ed. 6 - (8º)

Artigo Original

Pages: 809 to 817

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Cartilaginous tumors of the larynx

Author(s): Robert Thomé 1,
Daniela C. Thomé 2,
Cinthia R. C. Royg 3

Keywords: chondroma, chondrosarcoma, larynx, laryngeal neoplasms, laryngeal surgery

Abstract:
Introduction: Cartilaginous tumors of the larynx are uncommon, the cricoid cartilage being the most common site. The rarity of these tumors accounts for limited experience and, as a consequence, knowledge about them presents obscure points. Objective: To report surgical results as well as long-term follow-up on six patients with cartilaginous tumors of the larynx, 4 low-grade chondrosarcoma and 2 chondroma. Study design: Retrospective no randomized. Material and method: Five of the tumors were located in the cricoid and 1 in the thyroid cartilage. The patients had partial (4) and total laryngectomy (2), followed up from 6 to 30 years (average-19.5 years). Results: None of the patients presented metastasis or tumor-related death. Survival rate tumor-free at 5-years was 100% and at 20-years 67%, comorbidity being responsible for the decrease. Conclusions: Our results reinforce the concept for partial surgery as treatment modality, reserving total laryngectomy for large tumor or recurrence. Five-year follow-up may not be sufficient to observe recurrence in less aggressive chondrosarcoma.

Introduction

Few rare tumors have been more discussed in the literature than cartilaginous tumors of the larynx. Similarly to any other rare pathology, experience with these tumors has been gathered little by little, amounting to approximately 270 cases reported since the introduction by Travers39 to the Medico-Chirurgical Society of London, in 1816. The rare occurrence of these tumors is described in the literature: 31 cases of the Armed Forces Institute of Pathology in a 40-year period (1929 to 1969)18; 10 cases from the Massachusetts Eye and Ear Infirmary in a 30-year period17; 10 cases from the Department of Pathology of Temple University Health Sciences Center in a 35-year period2, and 47 cases from the Mayo Clinic in a 85-year period (1910 to 1995)22. The assessment of the real incidence of these tumors is difficult, because many studies, complying with their internal practices, use continuously the same basis of patients, resulting in contradicting results. For example:

1) out of the 47 patients with cartilaginous tumors reported by Lewis et al.22, from Mayo Clinic, in 1997, many had been previously reported by New29, 1918; Figi12, 1932; New30, 1935; New and Erich28, 1938; Goethals et al.13, 1963; Gorenstein et al.14, 1980; Neel and Unni26, 1982;
2) out of 31 patients presented by Hyams and Rabuzzi 18, 3 had been previously reported by Sirota and Hurwitz37 and by Brandenburg et al.4;
3) out of 8 patients with chondrosarcoma reported by Nicolai et al.31, 3 had already been presented by Ferlito et al.11;
4) Damiani and Tucker9 reported one case of a patient with chondroma treated with conservative surgery; three years and a half later, Lavertu and Tucker20 conducted total laryngectomy in the same patient because of recurrence.

Therefore, a detailed study to consider repetition of patients in subsequent studies may conclude that the incidence is even lower than previously reported in the literature.

Owing to its rarity, institutions and specialists have limited experience with such cases and, as a consequence, the literature provides innumerous studies reporting isolated cases or a small number of cases, basing the discussion on information collected from different retrospective studies. Figi12 emphasized that few specialists, even the most experienced ones, will find one case of cartilaginous tumor of the larynx during his or her professional life span.

Chondrosarcoma should be considered the most frequent cartilaginous tumor of the larynx. It is important to point out that until the 90's, chondroma was believed to be the most common, possibly because in the past the term was used to refer to any cartilaginous tumor. The terminology of chondrosarcoma was introduced by New30 in 1935, to designate malignant cartilaginous tumors. For this reason, the incidence of chondroma was wrongly estimated as 70 to 80% of all cartilaginous tumors for decades3, 7, 20, 27. Moreover, most cases published did not include follow-up, or they had a short period follow-up, and as demonstrated by larger groups of patients or by longer periods of follow-up, most chondromas turned out to be low-malignancy chondrosarcomas, such as histology studies of the recurrence proved years later5, 10, 20, 21, 26, 27, 31, 38. Long-time follow-up not only shows benign misinterpretation of the original tumor, but has also contributed to expand the knowledge about these tumors, helping the definition of surgery as the best approach to treat such cases, either as partial or total laryngectomy, depending on the localization and dimensions of the tumor, identification of prognostic value variables and the expected survival levels.

The present study aimed at presenting the surgical results and long-term follow-up of 6 patients with cartilaginous tumors of the larynx, 4 low-grade chondrosarcomas and 2 chondromas.

Material and Method

In the period between 1980 and 2000, 6 patients with cartilaginous tumors of the larynx were seen and operated by our clinic staff. There were 4 low-grade chondrosarcoma (1 thyroid cartilage and 3 cricoid cartilage tumors) and 2 cricoid cartilage chondromas. We analyzed data concerning the patients, the tumors, the surgery, results and follow-up. Patients' parameters included age, gender and race; tumor variables included localization, dimension and histology type; surgery-related factors were date, surgical approach and safety margins of the surgical piece; parameters related to outcomes included tumor recurrence and time of detection, cause and date of death, follow-up period and clinical status of the patient at the end of the study. Patients were all male Caucasian subjects ranging in age from 38 to 64 years, mean age of 50.1 years. The five cricoid cartilage tumors (3 chondrosarcomas and 2 chondromas) were apparently originated from the lamina, located on the posterior portion of the cartilage. In this group of patients, dyspnea and/or progressive hoarseness were the predominant symptoms. In one patient (case 3), no symptomatology related to the tumor had been noticed by the patient up to the moment he had to be submitted to general anesthesia for an orthopedic surgery and the team had difficulty to introduce the intubation probe. Duration of symptoms until diagnosis ranged from 6 months to 10 years (approximated mean of 3.4 years), and thyroid chondrosarcoma was the case that took the longest. Radiological study was performed in all patients to define the location and the extension of the tumors. In 67% of the patients, the images had diagnostic importance because of the pattern of popcorn-type calcification (Figure 1, A and B). In the patient with thyroid cartilage tumor (case 1), inspection and palpation of the neck showed a hardened mass, fixed to the thyroid, deforming the profile of the neck. In the patient, laryngoscopy revealed rounded smooth supraglottic bulging, recovered with intact mucosa, reducing the glottic chink and causing immobility of homolateral vocal fold. In the 5 patients with cricoid cartilage tumor, laryngoscopy showed submucous bulging of the posterior wall of the subglottic region, with rounded sessile smooth surface and recovered by intact mucosa. Among these patients, 2 cases (cases 4 and 5) presented reduced mobility of vocal folds and 3 patients (cases 2, 3 and 6) had preserved mobility. The dimension of the tumor varied from 1 to 6 cm (malignant, mean of 4.2cm; benign, mean of 1.5cm). Three patients (cases 1, 4, and 5) were submitted to tracheotomy, under local anesthesia, at the time of the direct laryngoscopy conducted to collect fragments of the tumor, and 3 patients (cases 2, 3 and 6) on the surgery day, before conservative laryngectomy.

Case 1 with thyroid chondrosarcoma and case 5 with cricoid cartilage tumor had to undergo total laryngectomy. Although they had probably been present for a long time, we observed that the tumors were confined to the laryngeal limits, pressing the structure without invading the external perichondrium.

Two patients with cricoid cartilage chondrosarcoma (cases 2 and 4) were submitted to subperichondral resection of all cartilage followed by termino-terminal thyro-tracheal anastomosis, and application of a stent. In the preoperative visit, both patients consented that total laryngectomy was to be performed if we considered it necessary during the surgery. After the resection of the arch and cricothyroid dearticulation, internal and external perichondrium of the lamina were detached until we surrounded the upper margin, avoiding as much as possible to open the cricoarytenoid articulations. The reduction of tension on the suture line of the anastomosis was reached through release of the larynx, combined with mobilization of the trachea followed by open dissection of the anterior wall up to the mediastinum. Before suturing the anterior-lateral walls of the anastomosis, we applied an endolaryngeal stent maintained in position for 4 weeks (case 2) and 8 weeks (case 4).

The 2 patients with cricoid cartilage chondroma (cases 3 and 6) were submitted to local resection of the tumor through laryngofissure. After the exposure of the tumor, a vertical incision was made including mucosa and internal perichondrium that recovered the tumor, going from the interarytenoid area up to 1cm below its lower limit. After the preparation of mucoperichondral flaps, the tumor was resected, going into the normal cartilage, around it and delimiting a clear line resulting from the difference in density of the tumor tissue and the normal cartilaginous tissue. The bed of the operative cavity, represented by the external periochondrium, was filled with reposition and suture of mucoperichondral flaps. We placed an endolaryngeal stent, maintained in place for 4 weeks.

Figure 1.



Figure 2.



Figure 3.

Results

Surgical margins were considered negative for tumors in the 6 patients. No patient presented metastasis or tumor-related death. Of the two patients with chondrosarcoma (cases 1 and 5) submitted to total laryngectomy, one died tumor-free 30 years after the surgery and the other is alive and asymptomatic 22 years later. As to the two patients with cricoid cartilage chondrosarcoma (cases 2 and 4) who had total resection of the cartilage with thyro-tracheal anastomosis, one of them (case 2) was submitted to total laryngectomy after recurrence 8 years later and remains tumor-free 21 years after the salvage surgery (that is, 29 years after the initial conservative surgery) and the other patient (case 4) died tumor-free 8 years after the surgery. Of the two patients with chondroma (cases 3 and 6) that were submitted to local resection with laryngofissure, one of them died (case 3) with no evidence of tumor 6 years after the surgery and the other (case 6) is alive and has been tumor-free for 20 years. In summary, follow-up range varied from periods of 30, 29, 6, 8, 22 and 20 years, respectively, after the initial surgery. The patient followed up the longest was case 1, with a 30-year follow-up period and case 3 was followed up for 6 years, the shortest period. Five-year survival was 100% and 20-year survival dropped to 67%, as a result of the action of co-morbidity. Up to the conclusion of the present study, 3 of the 6 patients, being that 2 of them had malignant tumors and 1 had a benign tumor, were alive and asymptomatic, with mean follow-up of 23.7 years.
Table 1 summarizes the data concerning patients, tumors, surgery, outcomes and follow-up.

Table 1.


Table 2.

Discussion

Although much has been discussed about cartilaginous tumors of the larynx, no definite cause has been related to its etiology. From classical theories, the most accepted one described the abnormal calcification of the laryngeal cartilages. Ossification in cricoid and thyroid cartilages starts from the third decade and increases with aging16, 19. The observation that cartilaginous tumors are more frequently seen in the elderly suggest a possible correlation between development of these tumors and alterations of the ossification process. The lamina of the cricoid cartilage is the most common localization of the cartilaginous tumors of the larynx,, followed by the inferior-lateral part of the thyroid cartilage. These areas correspond to the attachment of the main intrinsic and extrinsic muscles of the larynx. Progressive laryngeal ossification was attributed to the influence of mechanical stimuli produced by the contraction of these muscles15, 16, 19. Cartilaginous tumors of the larynx frequently affect more the hyaline cartilage than the elastic cartilage, and cases that affect arytenoid and epiglottis are extremely rare8, 17, 18 (arytenoid cartilage is a hyaline cartilage with a small portion of elastic cartilage in the vocal process, in the attachment of the vocal muscle, whereas the epiglottis remains non-ossified through the whole life). Brandwein et al.5 raised the hypothesis that the process of ossification could stimulate the occurrence of multipotential mesenchymal cells or cartilaginous debris, normally absent in mature cartilages, which would be the origin of the tumors. The review of literature has shown the reference to a congenital chondroma in a 56-day-old child reported by Montanari25. Simpson et al.36 reported a case of a 3-day-old child and Adler et al.1 in a 2-day-old girl. Therefore, congenital factor separates the logic of the etiology of these tumors in children and adults, thus, other etiological factors should be involved. The occurrence of two primary cartilaginous tumors (the second one developed years after the first one), reported by Wengraf40 is unique in the literature, but it is questionable, because it seems to be a late tumor affection.

Our reduced number of patients presented a prevalence of chondrosarcoma of 4 cases (67%), in accordance with the current literature findings5, 11, 22, 31. In the last study published by Mayo Clinic22, out of 47 patients, only 3 (6%) had chondroma. The fact that our patients were men, aged in average 50.1 years is also in accordance with the well-defined male predominance, of Caucasian subjects, frequently affected in the 5th and 6th decades of life. The localization of the tumors in our sample - 83% in the cricoid cartilage and 17% in the thyroid cartilage, is also in accordance with the literature data that says that cricoid cartilage is the preferred site, followed in decreasing order by the thyroid cartilage and rarely by arytenoid and epiglottis cartilages.

It was no surprise that 67% of our patients (cases 1, 2, 4 and 5) came to treatment only after long symptomatic periods of years, resulting in large tumors at the time of diagnosis. Early diagnosis of cartilaginous tumor of larynx is rare because growth is slow and patients do not value symptomatology; our patients had difficulties to define precisely the onset of the first symptoms. For this reason, it is understandable that 4 out of the 6 patients presented large tumors at diagnosis. Three patients (cases 1, 4 and 5) delayed the medical visit as much as possible, that is, up to the moment that breathing difficulty became unbearable. The perception of the subglottic narrowing when the nasogastric tube was being passed through one patient submitted to an orthopedic surgery was the first sign of the tumor, as reported by one of our patients (case 3), but it is not usual. A similar episode was reported by Lewis et al.22; Neis et al.27 and Schittek and James35. Correlation between age, tumor size and malignancy has been suggested by the literature5,18,31. Tumors that are larger than 3cm in diameter, predominantly in older patients, are associated with malignancy whereas tumors smaller than 1-2cm in diameter, at any age, affecting patients younger than those affected by chondrosarcoma, are related to benign characteristics. In our study, we recognized the correlation between size of tumor and malignancy, but we did not find any correlation between age group and tumor histology (Table 1).

The most controversial and confusing aspect of the diagnosis of cartilaginous tumors is the distinction between benign and low-grade malignant tumor based on the histology analysis of the biopsy. Although the criteria to define malignancy and benign aspects have been clearly established23, tumor samples obtained by the biopsy do not provide conditions to differentiate it because the histologic picture varies from one area to the other of the same tumor. The fact that the histologic pattern of malignancy is limited to certain tumor areas, that is, the malignant tumor presents areas with benign aspect, at least in part, could explain the reports of diagnosis of chondroma of the biopsy material, followed by definite diagnosis of chondrosarcoma at the histology of the surgical piece or the recurrence years later. Therefore, the recurrence after the resection of a tumor diagnosed as chondroma may be considered a chondrosarcoma until proven the contrary, and careful histology review is mandatory because of the possibility of underdiagnosing the malignancy. Based on the endoscopic analysis and the radiological imaging that is nearly pathognomonic of laryngeal cartilaginous tumors, the difficulty to collect enough material for the biopsy of a tumor of firm consistence, similar to bone consistence and recovered by intact mucosa, the presence of areas histologically different in the same tumor, limiting the validity of the diagnosis of chondroma in a biopsy, make us wonder how important the biopsy really is and whether it may not be skipped, since the preoperative distinction does not change the treatment plan. In our group, we had the correct original diagnosis in 4 of the 6 cases (67%) and underdiagnosis of malignancy in 2 cases (33%) of the samples of cricoid cartilage tumors, leading to final diagnosis based on the surgical piece (cases 2 and 4). The malignant transformation of a benign tumor that has been slowly developing for months or years, can not be excluded6, 27, 32. The authors that advocate this hypothesis argument that the prolonged evolution of a chondrosarcoma can be considered evidence that it has evolved during many years as a benign tumor. However, there is no conclusive evidence to support this argument.

Table 2 shows the correlation between chondrosarcoma and chondroma in our study.

Surgery is the appropriate treatment approach for primary or recurrent tumors. According to our results and based on the studied literature, we may state that conservative laryngectomy with safety margins is the treatment approach recommended for these tumors, reserving total laryngectomy for large tumors or recurrences in which the partial surgery is not feasible. Slow and localized growth of these tumors, the fact that tumor recurrence may be treated with partial or total surgery with no unfavorable impact to patients' lives17, 18, 20, 22, 27, and that survival rate is not longer with total laryngectomy instead of partial one20, support the use of conservative surgery as an initial procedure. Complete tumor surgical resection is an important factor to reduce the recurrence rates, but free-neoplasic margins are no guarantee that a recurrence will not develop one year or many years after the surgery, which was the case of one of our patients with chondrosarcoma (case 2). It is important to point out that even though the conservative surgery failed to eradicate the tumor, it was gratifying to have a functional larynx for a long time, before the recurrence happened. The survival of this patient has also shown that recurrence of chondrosarcoma after conservative surgery treated with total laryngectomy does not adversely influence the final outcome. This findings is in accordance with data reported by other studies5, 7, 20, 21. It is interesting to highlight that the survival of the 2 patients with chondrosarcoma (cases 2 and 4), wrongly diagnosed as having chondroma based on the samples from the biopsy, was not different from the outcomes of those correctly diagnosed with chondrosarcoma right from the beginning (cases 1 and 5). This observation reinforces what the literature5, 20, 21 says about the fact that non-diagnosed malignancy in the primary tumor does not interfere in the final outcome. In large cricoid cartilage tumors, resection of the cartilage with thyro-tracheal anastomosis proved to be an alternative technique for 2 patients (cases 2 and 4) with chondrosarcoma, who otherwise would have been submitted to total laryngectomy. The progress in cricoid cartilage tumor should overcome the argument that subtotal or total resection of this cartilage would not result in loss of the support necessary for the laryngeal patency 18, 20, 38. Cocke8, in 1962, collected 10 cases of cricoidectomy from a literature review and presented 100% cure and 60% laryngeal stenosis. However, he did not report the surgical technique employed. To repair the support of the laryngeal framework, after subtotal resection of the cricoid cartilage, a number of surgical techniques have been used: suture of the inferior cornun of the thyroid cartilage to the first tracheal ring and stent20, rib autologous graft27, flap of epiglottis cartilage and transposition of the flap of sternocleidomastoid muscle of superior pedicle to support the laryngeal lateral-posterior wall7, total skin graft3, endolaryngeal modeling34, and thyro-tracheal anastomosis 33. Link24 performed total exeresis of the cricoid cartilage by curettage, removing half of it in the initial tumor surgery and half in the recurrence, six years later. Since 70-80% of the laryngeal cartilaginous tumors arise from the cricoid cartilage, in our opinion, subperichondral resection followed by thyro-tracheal anastomosis may be considered an alternative technique to total laryngectomy.

Small tumors may be resected through laryngofissure. The reason for that lies in the fact that there is a clear line that surrounds the tumor, resulting from the difference in consistence between the tumor tissues and the normal cartilaginous tissue. Thus, the appropriate local resection margin should exceed the normal cartilaginous tissue, externally to the line, guaranteeing a safe surgical margin.

The concept of the external perichondral resection in the tumor site has been a controversial approach and it is not supported by the surgical findings of our four patients with cricoid cartilage tumors, since there was the presence of a cleavage plan between the intact perichondrium and the tumor. The external perichondrium represents the limit of a safe resection and any maneuvers beyond that point do nothing but add a further risk to the recurrent laryngeal nerve. The tumor should not be enucleated or submitted to curettage. In the past, local recurrence of the tumor was at least in part related to resection of the tumor by curettage5, 27, 31, and not because of lack of resection of the external perichondrium.

Owing to the potential recurrence of malignant tumors, the follow-up should be longer than 5 years; any period below that is not enough to detect recurrence, as demonstrated.

Since chondroma and low-grade chondrosarcoma present similar clinical picture, they are difficult to differentiate based on the histologic prognosis of the material collected in the biopsy. However, they are treated by the same surgical approach and have the same prognosis (despite the tendency for recurrence of the chondrosarcoma). Therefore, these are strong arguments for the combination of these two tumors in the same group. However, this argument can not be widely accepted because, despite the fact that the biopsy has limited validity in the diagnosis of chondroma, these two tumors are indeed distinct and may be differentiated in the examination of the surgical piece by a number of histologic characteristics.

Conclusion

Chondroma and low-grade chondrosarcoma present similar clinical picture and they are difficult to differentiate based on the histological fragments of the tumor obtained in the biopsy. However, not diagnosing malignancy does not have an adverse impact in survival. Localization and size of the tumor have a direct influence in the choice of partial or total surgery. Our results reinforced the concept that conservative laryngectomy should be the initial treatment approach, reserving total laryngectomy for the original tumor or recurrence, if the partial surgery is not feasible. Five-year follow-up may not be enough to observe recurrence of low-grade chondrosarcoma.

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1 Ph.D., Medical School, Universidade de São Paulo.
2 Post-Graduation under course, Discipline of Otorhinolaryngology, Medical School, Universidade de São Paulo.
3 Otorhinolaryngologist, Medical School, Universidade de São Paulo.

Address correspondence to: Robert Thomé - Alameda Itú 483 - São Paulo/SP - CEP 01421 - 000
Tel: (55 11) 288-9988; (55 11) 5579-3260 - Fax: (55 11) 284-3049; (55 11) 5081-4677
E-mail: rthome@dialdata.com.br

Study conducted in the private practice of Otorhinolaryngology and Head and Neck Surgery of the authors.

Study presented at the 102nd Annual Meeting of the American Academy of Otolaryngology-Head and Neck Surgery, September 13-16, 1998, San Antonio, Texas, U.S.A.

Article submitted on May 10, 2001. Article accepted on June 26, 2001.

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