HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS		QUICK SEARCH:   [advanced] Author: Keyword(s): Year:  Vol:  Page:

This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Marc Riquet Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Riquet, M. Articles by Danel, C. Search for Related Content PubMed PubMed Citation Articles by Riquet, M. Articles by Danel, C.

Ann Thorac Surg 1998;66:920-922
© 1998 The Society of Thoracic Surgeons

---

Original articles: General Thoracic

Axillary lymph node metastases from bronchogenic carcinoma

^a Service de Chirurgie Thoracique, Hôpital Laennec, Paris, France
^b Laboratoire d’Anatomie Pathologique, Hôpital Laënnec, Paris, France

Accepted for publication April 7, 1998.

Address reprint requests to Dr Riquet, Service de Chirurgie Thoracique, Hôpital Laënnec, 42 rue de Sèvres, 75007 Paris, France

	Abstract

Top Abstract Introduction Material and methods Results Comment References

 
Background. Axillary lymph node metastases (ALNMs) from bronchogenic carcinoma are rare and their significance may be questioned. A surgical approach may allow a better understanding of the mechanism of their occurrence.

Methods. A retrospective study of 1,486 cases of surgically removed non–small cell lung carcinoma was performed. Twenty-two patients (1.5%) had extrathoracic nodal metastases. Nine of them were ALNMs (<1%). These cases form the basis of this study.

Results. In 1 patient ipsilateral ALNM was removed during a lung operation. It was a left non–small cell lung carcinoma invading the chest wall (T3 N2). In the other patients (n = 8) ALNMs were observed during postoperative follow-up; 4 underwent ALNM resection, 2 had radiotherapy, and 2 had symptomatic treatment only. For these 8 patients, in the TNM classification performed after an initial bronchogenic carcinoma operation, the lymph node status was, respectively, N0 in four cases, N1 in three cases, and N2 in one case. Survival ranged from 1 to 10 months, except for one patient who is still alive after more than 5 years. In this case, the ALNM was discovered 4 months after a right lower lobectomy for a T2 N0 adenocarcinoma.

Conclusions. Axillary lymph node metastases may be involved through direct chest wall invasion of bronchogenic carcinoma or retrograde spread from supraclavicular lymphnode block. However, another mechanism seems to be the systemic vascular route.

	Introduction

Top Abstract Introduction Material and methods Results Comment References

 
Axillary lymph nodes are an unusual site for metastasis of bronchogenic carcinoma (BC). Ochsner and DeBakey in 1941–1942 reviewed the literature on the extent of lymphatic spread in 1,298 cases of lung cancer [1]. They found that axillary lymph nodes were involved in 6.6% of the cases and added two of their own. Marcantonio and Libshitz in 1995 discussed this topic reporting 17 presumed cases of axillary lymph node metastases (ALNMs) identified by computed tomography [2]. They concluded that ipsilateral axillary lymph nodes are involved either through chest wall invasion or through retrograde spread from the supraclavicular lymph nodes. They also suggested that contralateral axillary lymph node involvement requires involvement of contralateral mediastinal and supraclavicular lymph nodes first with retrograde spread. To further discuss the possible pathways and significance of ALNM from BC, we reviewed the cases of ALNM observed in a department of general thoracic surgery over a period of 12 years.

	Material and methods

Top Abstract Introduction Material and methods Results Comment References

 
From January 1984 to December 1995, 1,486 patients underwent surgery for non–small cell lung carcinoma at the Department of Thoracic Surgery of Laënnec Hospital, Paris.

Before surgery, all patients underwent a thorough workup that included chest roentgenogram, fibrobronchoscopy, and chest and brain computed tomography. Mediastinoscopy was performed only in patients in whom a contralateral mediastinal lymph node metastasis (N3) was suspected.

Among these 1,486 patients, 190 (13%) had had previous surgical removal of extrathoracic malignant tumors: 45 cases involved BC metastasis and 145 involved other cancers.

For 63 patients only exploratory thoracotomy was performed. All other patients underwent lung and complete ipsilateral mediastinal lymph nodes resections. In 147 patients (10%) the cancer invaded the chest wall.

Follow-up was performed by either the chest physician or the thoracic surgeon; extrathoracic nodal metastases were recorded in 22 cases (1.5%): jugulo carotidian, n = 7; intraabdominal, n = 3; supraclavicular, n = 2; and groin, n = 1. Axillary lymph node metastases were encountered in nine cases (<1%) and form the basis of this report.

There were 8 men and 1 woman, with a mean age of 62 years (range, 45 to 75 years). Lung cancer was located in the right upper lobe twice, the right lower lobe once, the intermediary bronchus once, the left upper lobe three times, the left lobar bifurcation once, and the left lower lobe once.

	Results

Top Abstract Introduction Material and methods Results Comment References

 
In only 1 case were axillary lymph nodes found and removed at the time of the lung operation. The tumor was located in the left upper lobe and involved the chest wall. A left pneumonectomy was performed with en bloc third, fourth, and fifth rib resections and left axillary dissection. All ipsilateral mediastinal lymph nodes were removed. Histology revealed an undifferentiated large cell carcinoma with mediastinal and axillary lymph node metastases. Postoperative course was uneventful. The patient died 2 months later while receiving adjuvant radiotherapy.

The 8 other cases of ALNM were observed during postoperative follow-up. At the time of the lung operation 4 cases were N0, 3 were N1, and only 1 was N2; all N+ had adjuvant radiotherapy in the mediastinum and supraclavicular area. The ALNMs appeared between 4 and 37 months after the thoracic operation.

The ALNMs were bilateral in 1 case: a left-side T2 N0 squamous cell carcinoma presenting with nontumoral loose pleural adhesion. The ALNMs were ipsilateral in two cases: a right upper and left lower lobe adenocarcinoma. In both cases no tumoral loose pleural adhesions were present. In the 5 other cases ALNMs were contralateral. Loose pleural adhesions were found in only 1 of these cases.

Of these 8 patients, 6 presented with concomitant systemic metastasis: bone, n = 3; brain, n = 1; lung and liver, n = 1; and abdominal lymph node, n = 1. No recurrent mediastinal lymph node was found.

Four patients underwent ALNM palliative resection because of pain, and to confirm the diagnosis of malignancy. The size of the metastatic nodes ranged from 4 to 7 cm. In three cases, the histologic classification (two adenocarcinoma and one squamous cell carcinoma) was identical in lung and ALNM, but in one case it was different (adenocarcinoma in lung and squamous cell carcinoma in ALNM). Concerning survival, 1 patient died after 3 months (initially T2 N1) and 2 patients after 7 months (initially T2 N0 and T2 N1), and the fourth patient is still alive after 6 years (initially T2 N0). The four other patients had no surgical removal of ALNM; 2 patients received only symptomatic treatment (survival, 1 and 4 months); and 2 underwent radiotherapy (survival, 7 and 10 months).

	Comment

Top Abstract Introduction Material and methods Results Comment References

 
Metastasis of bronchogenic carcinoma to axillary lymph nodes is a very rare condition. One publication that deals with that topic and gives a possible explanation of the pathways mechanisms is by Marcantonio and Libshitz [2]. That study demonstrated that bronchogenic carcinoma may involve ipsilateral axillary lymph nodes through either chest wall invasion or retrograde spread from supraclavicular lymph nodes. Furthermore, Marcantonio and Libshitz stated that contralateral axillary involvement is always due to retrograde spread and therefore implies involvement of contralateral mediastinal and supraclavicular lymph nodes first. In their experience based on radiology, ALNMs coexist only in already locally far advanced disease with chest wall involvement or mediastinal or supraclavicular metastases, or both.

The first hypothesis that bronchogenic carcinoma may involve ipsilateral axillary lymph nodes through chest wall invasion is confirmed by only 1 of our cases of ALNM. That case would have been a contraindication to operation if it had not been incidentally encountered. However, that we observed ALNMs in eight other cases without chest wall invasion shows that the hypothesis raised by Marcantonio and Libshitz [2] cannot be the only explanation. Another hypothesis explaining ALNM occurrence by chest wall involvement was suggested by Spencer [3]. This hypothesis is that tumoral spread may occur through "newly developed lymphatic channels which arise in pleural adhesions" [3]; this has not been clearly demonstrated. In an anatomic study performed on 360 human cadavers [4], lung adhesions to the chest wall were frequently encountered but neolymphatics running within these adhesions were not observed. In 4 of the 8 other ALNM cases we described, there were loose pleural adhesions: The axillary adenopathies were ipsilateral in 2 cases, bilateral once, and contralateral once. All 4 patients were N0 at the time of lung resection. Therefore, the pleural adhesion hypothesis could explain only 2 of these cases but not the occurrence of contralateral axillary metastases. Furthermore, axillary metastases were seldom observed during lung operation, in contrast with the high proportion of pleural adhesions we observed (25% of 1,486 patients).

The second hypothesis raised by Marcantonio and Libshitz [2] concerns the retrograde spread mechanism. It refers to the presence of N3 supraclavicular metastases occurring in most cases with N2 or N3 mediastinal involvement. In those cases, they explained the occurrence of ipsilateral as well as contralateral axillary metastasis by retrograde spread from the ipsilateral supraclavicular N3 disease. Retrograde opacification of axillary lymph nodes from the ipsilateral supraclavicular nodes was observed in 2% of consecutive bipedal lymphangiograms they performed. This type of spread can occur only when the valvular competence of lymphatic vessels is lost. We observed such valvular incompetence at the level of the lymphatic vessels which drain the lymph from the lung into the thoracic duct. As we demonstrated, this is one explanation for postoperative chylothorax after a lung operation [5]. Nevertheless, chylothoraces occurred in less than 1% after lung and lymph node resections, demonstrating that retrograde flow remains an exception. In the case of ALNM involvement, this may be an explanation because valvular incompetence is supposed to be created by supraventricular N3 node lymph block [2]. This is rare and occurs only in far-advanced lung cancers. Furthermore, this does not explain eight of the cases we observed. Only 1 patient had N2 disease, and in that patient bilateral axillary lymph node metastases were present. Another explanation is therefore necessary.

A third hypothesis is that ALNMs could be of systemic origin. For instance, various locations of distant lymph node metastasis are possible. In order of frequency, we observed axillary (n = 9), jugulo carotidian (n = 7), intraabdominal (n = 3), supraclavicular (n = 2), and groin (n = 1) metastases. From an anatomic point of view, groin, axillary, and jugulocarotidian lymph nodes behave differently from intraabdominal and supraclavicular ones, which are normally present on the lymph pathways of the lung [4, 6, 7]. Groin metastases are exceptional and no lymphatic vessel continuity can explain their incidence. Therefore, these metastases are surely systemic in origin. The problem is the same regarding axillary and jugulo-carotidian metastases. Jugulo-carotidian nodes and their lymphatic vessels are not anatomically involved in lymph drainage of the lung and no anastomosis with lymph nodes cranial to the supraclavicular nodes is evidenced by lymphatic injection [7]. This implies a certain degree of independence between the one draining the head and neck and the other draining the thorax. Similarly, axillary lymph nodes do not receive lymph from the lungs but essentially from the upper limbs and the chest wall [8]. Therefore, metastasis in those locations may be of systemic origin. This raises the question whether such metastases occur at random or whether they settle because of special affinity to lymph node tissue. The rarity of distant node metastases unrelated to the anatomic lymph pathway from the lung does not favor the last hypothesis.

In conclusion, ALNMs may be explained in the case of invasion of the chest wall by a direct lymph pathway. Retrograde flow due to N3 supraclavicular blockade may also be an explanation in far-advanced cases of the disease. Nevertheless, our results suggest that the most likely mechanism for axillary node involvement is systemic vascular seeding. With that being the case, a more logical treatment would combine chemotherapy with either operation or radiotherapy.

	References

Top Abstract Introduction Material and methods Results Comment References

 

1. Ochsner A, DeBakey M. Significance of metastases in primary carcinoma of the lungs: report of two cases with unusual site of metastasis. J Thorac Surg 1941–1942;11:357–87.
2. Marcantonio D.R., Libshitz H.I. Axillary lymph node metastases of bronchogenic carcinoma. Cancer 1995;76:803-806.[Medline]
3. Spencer H. Pathology of the lung, vol. 2, 4th ed Oxford: Pergamon, 1995.
4. Riquet M. Anatomic basis of lymphatic spread from carcinoma of the lung to the mediastinum: surgical and prognosis implications. Surg Radiol Anat 1993;15:273-277.
5. Riquet M., Hidden G., Debesse B. Les collatérales du canal thoracique d’origine ganglio-pulmonaire: Etude anatomique et chylothorax après chirurgie pulmonaire. Ann Chir 1989;43:646-657.[Medline]
6. Riquet M., Etienne G., Debesse B., Chrétien J. Direct metastases of abdominal lymph nodes in bronchogenic carcinoma. J Thorac Cardiovasc Surg 1990;100:143-144.
7. Le Pimpec Barthes F., Riquet M., Hartl D., Hubsch J.-P., Hidden G. Cervical venous anastomoses of pulmonary lymphatic vessels. Surg Radiol Anat 1997;19:53-55.[Medline]
8. Rouvière H. Anatomie des lymphatiques de l’homme. Paris: Masson, 1932.

This article has been cited by other articles:

				S. Komatsu, Y. Ueda, D. Ichikawa, H. Fujiwara, K. Okamoto, S. Kikuchi, A. Shiozaki, K. Imura, R. Ohsawa, T. Ochiai, et al. Prognostic and Clinical Evaluation of Axillary Lymph Node Metastasis in Esophageal Cancer Jpn. J. Clin. Oncol., April 1, 2007; 37(4): 314 - 318. [Abstract] [Full Text] [PDF]

This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Marc Riquet Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Riquet, M. Articles by Danel, C. Search for Related Content PubMed PubMed Citation Articles by Riquet, M. Articles by Danel, C.