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American Journal of Otolaryngology–Head and Neck Medicine and Surgery 28 (2007) 316 – 320 www.elsevier.com/locate/amjoto Internal jugular vein preservation in neck dissection for pN1-N2c oral and oropharyngeal carcinoma Everton Pontes, MD, Joao Goncalves Filho, MD, PhD, Ivan Marcelo Goncalves Agra, MD, ˜ ¸ ¸ Andre Lopes Carvalho, MD, PhD, Jose Magrin, MD, PhD, Luiz Paulo Kowalski, MD, PhD4 ´ ´ Head and Neck Surgery and Otorhinolaryngology Department, Centro de Tratamento e Pesquisa Hospital do Cancer A. C. Camargo, ˆ -Fundacao Antonio Prudente ¸˜ Received 7 August 2006 Abstract Purpose: The aim of this study is to evaluate risk factors of neck recurrence in patients with pN1-N2 neck stage, submitted to a modified radical neck dissection with preservation of the internal jugular vein. Materials and methods: We reviewed the medical records of 72 patients with squamous cell carcinoma of the oral cavity (43 cases) and oropharynx (29 cases). The clinical stage of the neck was N1 in 23 cases and N2a-c in 49. Results: Neck recurrences occurred in 6 cases at the side in which the internal jugular vein was preserved. Neck recurrence did not have significant correlation with tumor site ( P = .391), T stage ( P = .999), N stage ( P = .203), adjuvant radiotherapy ( P = .999), number of positive lymph nodes ( P = .180), lymph nodes size ( P = .429), and extracapsular spread ( P = .400). Conclusions: Modified radical neck dissection with internal jugular vein preservation can be performed in selected patients with lymph node metastases, with no significant increase on the risk of neck recurrence. D 2007 Published by Elsevier Inc. 1. Introduction Lymph node metastases are common in patients with oral cavity and oropharynx squamous cell carcinomas, and classical or modified radical neck dissection (RND) remains as the gold standard of surgical management. The presence of metastatic nodal disease is the most important prognostic indicator in patients with squamous cell carcinoma of the head and neck . Since the classical publication of Crile in 1906 , the technique of RND has remained virtually unchanged for the treatment of clinically detected metastatic lymph nodes in patients with head and neck carcinomas . The RND is oncologically safe, but it usually results in significant functional and esthetic morbidity . Thus, since the 1960s, several authors have been suggesting a number of 4 Corresponding author. Head and Neck Surgery and Otorhinolaryngology Department, Centro de Tratamento e Pesquisa Hospital do Cancer ˆ A. C. Camargo, Rua Professor Antonio Prudente, 211, 01509-900 Sao ˜ Paulo, Brazil. Fax: +55 11 3341 0326. E-mail address: email@example.com (L.P. Kowalski). 0196-0709/$ – see front matter D 2007 Published by Elsevier Inc. doi:10.1016/j.amjoto.2006.10.002 modifications of the RND, aiming to reduce its morbidity [4,5]. The only modification that got universal acceptance was the preservation of the accessory nerve. There are several concerns about the safety of the preservation of the internal jugular vein [3,5-7]. It was considered an option only in the treatment of the less involved side of the neck of patients submitted to simultaneous bilateral neck dissections [8,9]. The preservation of the internal jugular vein could reduce the risk of intracranial hypertension , facial edema , as well as facilitate the reconstruction with microvascular free flaps. The purpose of our study was to evaluate the efficacy and feasibility of the preservation of the internal jugular vein in neck dissection for oral cavity and oropharynx squamous cell carcinoma patients with pN1-N2c neck stage. 2. Patients and methods This study includes all previously untreated patients with squamous cell carcinoma of the oral cavity or oropharynx, E. Pontes et al. / American Journal of Otolaryngology–Head and Neck Medicine and Surgery 28 (2007) 316 – 320 317 Fig. 1. Modified RND with jugular vein preservation. clinically N1 or N2 stage with pathologically confirmed lymph node metastasis (pN+), submitted to a modified RND with preservation of the internal jugular vein of one or both sides of the neck between 1990 and 2000. The patients were selected from the hospital database, and we retrospectively reviewed the medical records of 72 to obtain original pathologic reports and clinical information. Preoperative evaluation included clinical history and physical examination, oral cavity and oropharynx examination, indirect laryngoscopy or nasofibroscopy, palpation of the neck, thorax radiography, and computed tomography of the neck and upper aerodigestive tract. All tumors were restaged according to the 2002 TNM Classification of the Union Internationale Centre le Cancer (UICC)/American Joint Committee on Cancer. In this study, the patients were composed of 66 men (91.7%) and 6 women (8.3%), with mean age of 56 years (range, 33-82 years). The site of the primary tumor was the oral cavity in 43 cases (59.7%) and the oropharynx in 29 cases (40.3%). The T stage was as follows: T1 in 3 patients (4.2%), T2 in 3 patients (4.2%), T3 in 34 patients (47.2%), and T4 in 32 patients (44.4%). The neck Table 1 Type of ND Ipsilateral ND MRND MRND MRND MRND MRND MRND MRND RND (IJV (IJV (IJV (IJV (IJV (IJV (XI) + + + + + + XI) XI + SCM) XI) XI + SCM) XI) XI) Contralateral ND – – MRND MRND SOH MRND MRND MRND n (%) 26 2 8 1 17 2 3 13 (41.7) (2.8) (11) (1.4) (23.6) (2.8) (4.2) (18) clinical stage was N1 in 23 patients (31.9%), N2a in 11 patients (15.3%), N2b in 22 patients (30.6%), and N2c in 16 patients (22.2%). All patients in this series had clinically palpable lymph nodes suggestive of metastases and underwent a modified RND with the internal jugular vein preservation in, at least, one neck side (Fig. 1). We routinely preserved the internal jugular vein in neck dissection even in patients with clinical metastatic lymph node. The resection of the internal jugular vein is performed only when there is macroscopic invasion of the vein by the metastases or the primary tumor. In clinically negative contralateral side of the neck, a selective neck dissection (levels I, II, and III) was performed for patients with a high risk of contralateral metastases (tumors that crossed the midline or floor of the mouth carcinomas that approached midline). The surgical procedures included ipsilateral modified RND with preservation of internal jugular vein in 28 patients (39%) and bilateral neck dissection in 44 cases (61%), with preservation of internal jugular vein on both sides in 9 patients (12.5%) and on only one side only in 35 patients (48.5%). Of these, 17 patients (23.6%) had modified RND with preservation of internal jugular vein associated with selective neck dissection on the other side (supraomohyoid neck dissection). Neck dissection characteristics are showed in Table 1. For statistical analysis, the computer program SPSS 12.0 for Windows was used. Statistical analysis included v 2 or Fisher exact test to compare the study variables. The KaplanMeier method was used for actuarial survival analyses. Statistical significance was determined for a P value less than or equal to .05. 3. Results There were 81 modified RNDs with internal jugular vein preservation in this study group. The median number of (IJV + XI) (IJV + XI) (XI) (IJV + XI) (IJV + XI) SOH indicates supraomohyoid neck dissection; MRND (IJV + XI + SCM), modified RND with preservation of the accessory nerve, internal jugular vein, and sternocleidomastoid muscle; MRND (IJV + XI), modified RND with preservation of the accessory nerve and internal jugular vein; MRND (XI), modified RND with preservation of the accessory nerve; ND, neck dissection. Fig. 2. Percent of neck levels involvement by positive lymph nodes. 318 E. Pontes et al. / American Journal of Otolaryngology–Head and Neck Medicine and Surgery 28 (2007) 316 – 320 Table 2 Characteristics of the 6 patients with neck recurrence after modified RND with internal jugular vein preservation Patient 1 2 3 4 5 6 Tumor site Lower gum Oral tongue Base of the tongue Floor of mouth Oral tongue Floor of mouth 4 Number of positive lymph nodes. TNM stage T3N1M0 T2N2bM0 T3N2bM0 T3N2bM0 T4N2cM0 T4N2bM0 pN(+)4 2 5 24 5 4 9 Extracapsular spread Yes Yes Yes No Yes Yes Postoperative radiotherapy (PO RT) Yes Yes Yes No Yes Yes lymph nodes dissected was 47 per side (range, 15-150 lymph nodes). The number of positive lymph nodes ranged from 1 to 44 (median, 4 positive lymph nodes). Most metastatic lymph nodes were at the jugular chain. Levels II, III, and IV were involved in 86%, 25%, and 12.4% of the neck dissection specimens, respectively. All the 8 patients with level V involved had nodal metastases at other levels (Fig. 2). Extracapsular spread of nodal neck disease was demonstrated in 62.5% of the cases. Most of the patients (76.4%) underwent postoperative radiotherapy. The neck was irradiated bilaterally in all of these patients, with doses ranging from 4500 to 7000 cGy (median, 6000 cGy) according to the indication of treatment and to the patient’s tolerance. Neck recurrence was the major end point of this study and occurred in 15 patients (20.8%). It was diagnosed on the ipsilateral neck dissection with preservation of internal jugular vein in 6 patients (8.3%). Contralateral neck recurrences were diagnosed in 9 patients (12.5%). Of these, the neck recurrence occurred in 5 patients not initially submitted to a neck dissection, in 2 (11%) of the 18 patients Table 3 Analysis of the neck recurrences in the side of internal jugular vein preservation according to the variables studied Variable No recurrence Recurrence (%) 5 (11.6) 1 (3.4) 0 (0) 6 (9.1) 1 (2.9) 5 (13.2) 1 (5.9) 5 (9.1) 2 (4.3) 4 (15.4) 1 (3.7) 5 (11.1) 3 (7) 4 (10.3) P .391 Tumor site Oral cavity 38 Oropharyngeal 28 T stage T1-T2 6 T3-T4 60 N stage N1-N2a 33 N2b-N2c 33 Adjuvant radiotherapy No 16 Yes 50 Positive lymph nodes =4 44 N4 22 Extracapsular spread No 26 Yes 40 Lymph nodes size (cm) =3 40 N3 25 submitted to a modified RND without internal jugular vein preservation, and in 2 patients submitted to a supraomohyoid neck dissection. In these patients who underwent a modified RND without preservation of the internal jugular vein or supraomohyoid neck dissection, the T stage were 1 T4, 1 T3, and 2 T3. The interval between initial treatment and neck recurrence ranged from 4.6 to 30.7 months (mean, 11.8 months). Table 2 presents the characteristics of the patients with neck recurrence in the side of internal jugular vein preservation. Adjuvant radiotherapy was not performed in 4 patients with neck recurrence (2 ipsilateral and 2 contralateral). Neck recurrence in patients submitted to modified RND with preservation of the internal jugular vein did not have significant correlation with T ( P = .999) and N ( P = .203) clinical stages, adjuvant radiotherapy ( P = .999), number of positive lymph nodes ( P = .180), lymph node size ( P = .429) and extracapsular spread ( P = .400) (Table 3). During the study period, which ranged from 3.5 to 145 months (median, 19 months), 19 patients (26.4%) remained alive with no evidence of carcinoma recurrence. At the study closing date, 5 patients (6.9%) were alive with a recurrence, 34 (47.2%) died due to the disease, 12 (13.8%) died of non–cancer-related causes, and 2 (2.8%) were lost to follow-up. The survival rates at 5 years for the patients with and without preservation of the internal jugular vein were 45% and 17% ( P = .004), respectively (Fig. 3). .999 .203 .999 .180 .400 .429 Fig. 3. Overall survival of the patients with and without preservation of the internal jugular vein. E. Pontes et al. / American Journal of Otolaryngology–Head and Neck Medicine and Surgery 28 (2007) 316 – 320 319 4. Discussion The embryologic origin and strict anatomic relation between the cervical lymphatic system and the internal jugular vein have always been a great concern with regard to the preservation of this structure in the treatment of regional metastases of upper aerodigestive tract carcinomas. However, major veins are routinely preserved in axillary, mediastinal, or retroperitoneal dissections. Right from his first publications, Crile  has described the resection of the internal jugular vein as an imperative stage of neck dissection, and various authors have shared this opinion throughout the years, up to the present [3,11]. Furthermore, Djalilian et al  demonstrated that the direct invasion of the internal jugular vein by cervical metastasis increases the incidence of distant metastasis. The morbidity and mortality related to RND, however, have always been a major concern for head and neck surgeons. Martin et al , in 1951, described the complications related to RND, which was followed by other authors [13,14]. Gius and Grier  and Sugarbaker and Wiley , also in the 1950s, described facial edema and increased intracranial pressure after bilateral ligature of the internal jugular veins, resulting in headaches, alteration in the level of consciousness, coma, and in some cases, death. Reports of blindness as a result of radical cervical dissection with bilateral ligature of the internal jugular veins are less frequent but is described up to today . Genden et al , in a review article about complications of neck dissection, found that the simultaneous bilateral RND represents a significant risk for postoperative complications, and that the mortality resulting from it is about 17%. In view of this situation, several variations of the classical RND have been studied since the 1950s, with the intention of diminishing the morbidity and mortality of the procedure without harming the end-result of the treatment [4,5,18,19]. In our study, the incidence of postoperative mortality rate was 0%, demontrating the good evolution of patients submitted to RND with preservation of the internal jugular vein, even in our 18 cases of bilateral neck dissection. The knowledge from the studies of Lindberg , Byers et al , Medina and Byers , and Shah , that cervical metastases obey a preferential distribution depending on the primary site of the disease, had a remarkable impact in planning the therapeutic approach to the neck with carcinomas of the aerodigestive tract. The distribution of the lymph nodes involved by metastases of the mouth and oropharynx carcinomas in this series was in accordance with that described in the literature [23,24], with 86% of the cases involving level II and 25% of the cases involving level III. With regard to the presence of positive lymph nodes at level V (8 cases), this never occurred in isolation, and lymph nodes of the jugular chain were always involved. There has been a great proliferation of elective dissections in the N0 cases of various topographies  as well as in selected cases of stage N1 tumors of the oral cavity and oropharynx [22,25,26], without increasing the risk of loco regional control of the disease or reducing the expectance of survival rates. In cases of stages N2a-c cervical involvement, the modification of radical classical neck dissection, mainly with regard to preserving the internal jugular vein, has received unfavorable criticism from various authors [6,7,27]. The improvements in techniques for the reconstruction of defects resulting from radical resections of advanced head and neck tumors by means of microvascular free flaps had a significant impact in the functional and esthetic rehabilitation of these patients. In such cases, it is important to preserve appropriate vascular pedicles for the nutrition of these flaps. The preservation of the internal jugular vein in selected cases of bilateral metastases is considered safe, whenever there are no macroscopic evidence of its involvement by regional lymph node metastasis [8,9]. The main objective of jugular vein preservation is to diminish morbidity and promote vascular pedicles for microvascular reconstructions. The overall index of neck recurrences in the present study was 20.8% (15 patients). The main purpose of this study was to evaluate neck recurrence in a group of patients submitted to a modified RND with preservation of internal jugular vein and compare it with the literature report of neck dissection without internal jugular vein preservation. When analyzing the 81 modified RNDs in isolation, in which the internal jugular vein was preserved, regional recurrence occurred in 6 patients, which corresponds to 8.3% of the cases. Pearlman et al  described neck recurrence rates of 5% in patients with pN+ tumors of the upper aerodigestive tract, with lymph nodes of up to 3 cm, submitted to modified RND with preservation of the accessory nerve, sternomastoid muscle, and internal jugular vein. Khafif et al , comparing patients submitted to radical classical neck dissection and modified RND with preservation of the accessory nerve, sternomastoid muscle, and internal jugular vein in tumors of the head and neck, showed regional recurrences in 26% of the 315 patients submitted to radical classical neck dissection. In the 55 patients submitted to a modified RND with preservation of the accessory nerve, sternomastoid muscle, and internal jugular vein (all with pN+), 14 had neck recurrences (25%). Richards and Spiro  presented a regional recurrence rate of 18.6% in 39 patients with stage N2 and N3 tumors of the upper aerodigestive tract submitted to classical or modified RND with preservation of the accessory nerve, followed by radiotherapy. However, if only the recurrences in operated necks are considered, of the 43 dissections performed, there was recurrence in 4 patients (9.3%). Buckley and Feber , in a clinical review article of surgical treatment of cervical metastases from squamous carcinoma of the upper aerodigestive tract, all N+ neck stage, found a mean recurrence rate of 14.5% in patients treated with RND and of 7.4% in patients treated by modified RNDs types I and III. It is important to emphasize that of the 15 neck recurrences in the present study, only 6 occurred in necks in which the internal jugular vein was preserved, being equivalent to 8.3% of the total casuistic and 40% of the 320 E. Pontes et al. / American Journal of Otolaryngology–Head and Neck Medicine and Surgery 28 (2007) 316 – 320  Barbosa JF. Radical laryngectomy with bilateral neck dissection in continuity. Arch Otolaryngol 1956;63:372 - 83.  Magrin J, Kowalski LP. Bilateral radical neck dissection: results in 193 cases. J Surg Oncol 2000;75:232 - 40.  Sugarbaker ED, Wiley HM. Intracranial pressure studies incident to resection of the internal jugular veins. Cancer 1951;4:242 - 50.  Martin H, Del Valle B, Ehrlich H, et al. Neck dissection. Cancer 1951;4:441 - 99.  Djalilian M, Weiland LH, Devine KD, et al. Significance of jugular vein invasion by metastatic carcinoma in radical neck dissection. Am J Surg 1973;126:566 - 9.  Bocca E. Functional problems connected with bilateral radical neck dissection. J Laryngol Otol 1953;67:567 - 77.  Nahum AM, Mullaly W, Marmor L. A syndrome resulting from radical neck dissection. Arch Otolaryngol 1961;74:424 - 8.  Gius JA, Grier DH. 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Richards BL, Spiro JD. Controlling advanced neck disease: efficacy of neck dissection and radiotherapy. Laryngoscope 2000;110:1124 - 7.  Buckley JG, Feber T. Surgical treatment of cervical node metastases from squamous carcinoma of the upper aerodigestive tract: evaluation of the evidence for modifications of neck dissection. Head Neck 2001;23:907 - 15.  Smeele LE, Leemans CR, Reid CB, et al. Neck dissection for advanced lymph node metastasis before definitive radiotherapy for primary carcinoma of the head and neck. Laryngoscope 2000;110: 1210 - 4.  Clark J, Li W, Smith G, et al. Outcome of treatment for advanced cervical metastatic squamous cell carcinoma. Head Neck 2005;27:87 - 94. neck recurrences. In addition to this, of these 6 patients, 5 had N2b-N2c neck stage and presented with capsular rupture of the metastatic neck lymph nodes, cases theoretically with a worse prognosis, which suggests the need for a better selection of patients. There was no statistical correlation between the location of the primary tumor, the T stage, the N stage, the treatment with adjuvant radiotherapy, the number or size of the positive lymph nodes, as well as the presence of capsular rupture in the involved lymph nodes, in relation to cervical recurrence when the internal jugular vein was preserved. This is probably due to the small number of cases with regional recurrence analyzed in the present study and also possibly to the selection of cases and to the extension of the neck dissection including the adventitia of the preserved internal jugular vein. Overall survival in the present study was 45% in 2 years and 32% in 5 years, which is equivalent to the rates described by other authors, even in studies that do not include RND with preservation of the internal jugular vein and that which include pN0 patients. Smeele et al , studying patients with head and neck carcinomas with neck metastases submitted to neck dissection and adjuvant radiotherapy for the treatment of the primary tumor, described an overall survival of 43% in 2 years. Clark et al , analyzing patients with stage N2 and N3 carcinoma of the aerodigestive tract submitted to surgery followed by radiotherapy, achieved overall survival rates of 39% in 5 years. These results suggest that modified RND with preservation of the internal jugular vein is feasible in selected pN+ patients with carcinomas of the oral cavity or oropharynx, without significantly increasing the risk of loco regional failures, and it is associated with overall survival results compatible with data reported in the literature. References  Schuller DE, McGuirt WF, McCabe BF, et al. The prognostic significance of metastatic cervical lymph nodes. Laryngoscope 1980;90:557 - 70.  Crile GW. Excision of cancer of the head and neck. 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