RECURRENT LARYNGEAL NERVE PARALYSIS

The purpose of this paper is to present a revised conception of the causes and mechanism of recurrent laryngeal nerve paralysis. The explanation is based on the fact that, at times, these nerves divide into two or more branches prior to entering the larynx. This division may occur at any point in the recurrent course from the clavicle to the cricothyroid articulation. The statement that the recurrent laryngeal nerve has been found to divide in the extra laryngeal areas could not be news to those familiar with the literature on this subject. This is a report on the dissection of 100 cadavers. It confirms the division of the recurrent laryngeal nerves in the extra laryngeal space. The information obtained from these 100 dissections not only offers a simple, practical and tenable explanation of the elementary and bizarre type of traumatic laryngeal paralysis but should assist in avoiding these paralyses.

report is one of a female aged 25 years. In September 1930, she discovered a small lump in the upper and outer quadrant of her left breast. Three months later this was removed and was considered benign by the pathologist. The wound healed promptly, only to break down after five months, giving rise to an ulcerated area which steadily increased in size. During July 1932, enlarged lymph glands were noticed in the axilla. A biopsy was done and carcinoma diagnosed. In October, she consented to receive a course of deep X-ray therapy. Two months later, January 3rd, 1933, she was admitted to the Victoria General Hospital with a " discharging sore of the left breast " and " swollen and painful neck ". Her recent history was to the effect that her neck had become swollen and painful for about two weeks and that she had experienced hoarseness, a choking feeling at times, together with some difficulty in both swallowing and breathing. In addition, she had had a dry cough for three months. Although her appetite was poor, she claimed that she had not lost weight, and inspection showed her to be well nourished and of good colour.
Examination showed an ulcer of the breast i£ by 2 inches, with a ragged, indurated, and reddened margin with a sloughing base and a sero-purulent discharge. The left axillary glands were enlarged. The left supraclavicular glands were palpable with more or less general swelling of the deep tissues of the neck. Physical examination showed the lungs to be apparently normal. X-ray of the spine and long bones was negative. X-ray of the lungs suggested the possibility of malignant involvement. Dr. H. K. MacDonald, to whose care she was committed, referred her to Dr. R. Evatt Mathers for laryngeal examination, and the writer found a completely immobile left vocal cord with no evidence of new growth. Following a course of deep X-ray therapy, she was discharged on January 19th, 1933, improved so far as the neck and throat were concerned. Fullness of the neck had subsided, but the glands remained tender. Readmitted on March 19th, with severe dyspnoea. Fluid was aspirated from the left pleural cavity and temporary relief followed. Distress soon recurred and death took place the following day. Post mortem was refused.
A lump in the lower and inner quadrant of the right breast had developed between the time of discharge on January 19th and readmission on March 19th. A slight drooping of the left upper eyelid had been noticed for three weeks. 222 The explanation offered by Dr. Turner may be briefly stated. The external lymph drainage of the breast flows, for the most part, first to the lymph glands in the axilla, then to the subclavian lymph glands which lie at the apex of the axilla and posterior to the costo-coracoid membrane and below the clavicle, and finally empties into the blood circulation at the junction of the internal jugular and subclavian veins. In his original article he wrote : Some of the efferent vessels of the axillary subgroups, however, do not pass into the subclavian glands, but, passing superficially to the clavicle, ascend directly to the supraclavicular glands, in which they terminate. Oelsner regards this as an important and constant arrangement (writer's italics).
The internal drainage, Dr. Turner points out, pierces the chest wall and is conveyed by the internal mammary or retrosternal lymph channel, which is separated from the mediastinal pleura by a fine layer of cellular tissue, as it passes upwards behind the costal cartilages and in close contact with the dome of the pleura to empty into the vessels at the root of the neck. Again referring to the intra-thoracic or internal route, ending in the great veins of the neck, Dr. Turner continues : Some aberrant efferents of the retro-sternal glands, however, pass over the clavicle and drain directly into the supraclavicular glands (writer's italics).
Thus, it would appear that the supraclavicular collection of lymph glands may be infected by breast cancer cells by either route. These glands have many efferent channels besides the two mentioned and along which cancer cells may find their way, but only one has any bearing upon the matter under discussion. I will also quote the paragraph from the address of Mr. W. Sampson Handley, entitled " Lines of Advance in Surgery of Breast Cancer." 11 It seems doubtful whether any direct vascular connection exists between the pre-tracheal glands of the thorax and the supraclavicular glands. In many cases the pre-tracheal efferent trunks discharge directly into the great veins, and the avenue of permeation into them is thus cut off. It would appear that the only constant lymph-vascular connection of the supraclavicular glands with the thorax is by way of the efferents of the small recurrent laryngeal chain of glands.

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Presumably it is the pressure that results from extension of the cancer cells to the lymph glands along this recurrent laryngeal lymphatic pathway, that gives rise to vocal cord paralysis.
Dr. Turner bases his explanation of the crossed paralysis on the intimate relationship that exists between the peripheral lymphatics of the mamma and those of the overlying and adjacent cutaneous lymph vessels and the continuity across the mid-line of nearby cutaneous lymphatics. Thus, cancer cells from the medial portion of a breast could cross over and reach the axillary glands of the opposite side. In some cases (Oelsner reports that he met it twice in nine subjects) there exists a decussation of collecting trunks which pass anterior to the clavicle, to terminate in the supraclavicular gland of the opposite side.
Assuming the anatomical information to be both complete and correct, it comes to this, that all cancer cells, by whichever lymphatic route the extension may take place, must pass anterior to the clavicle to reach the supraclavicular lymph glands. If this be the case, it would seem one is justified in concluding that if the lymph channels crossing the clavicle were destroyed at a sufficiently early stage, a case could be guarded against laryngeal paralysis and secondary deposits in the mediastinum.
The idea that an operation could hold such possibilities seemed worthy of further enquiry.
In answer to questions regarding the lymphatic channels passing anterior to the clavicle, which is so stressed by Dr. Turner, Professor Rouviere wrote 12 : The passage of lymphatics uniting the axillary glands to the supraclavicular glands in front of the clavicle must be very rare. I have never observed it. The lymphatic channels that very often unite the axillary glands to the supraclavicular glands pass normally under the clavicle and anterior to the subclavian vein.

Again :
Neither my collaborators nor I have ever seen a lymphatic channel uniting the internal mammary chain to the supraclavicular glands, pass anterior to the clavicle.
In his recently published and exhaustive text on the lymphatic system, 13 which contains not only the researches of himself and his collaborators, but also a thorough survey of the literature, Professor Rouviere writes : It is not rare to see the large collecting trunks of the intrathoracic glands not opening directly into the internal jugular or subclavian veins, but terminating in a gland of the internal jugular and transverse cervical chain near the jugulo-subclavian union.
The intrathoracic glands include the internal mammary chain. On page 167 he specifically states that the internal mammary lymph trunk in some cases ends in the lowest gland of the internal jugular chain. The transverse cervical refers to the lowest elements of the supraclavicular group.
It would appear that the view that some efferent channels pass from axillary to supraclavicular glands anterior to the clavicle has been mistakenly attributed to Oelsner, as the following quotation shows, 14 pages 147-48 : A direct union of the anterior thoracic glands or of the lymph trunks of the thoracic integument itself with the so-called supraclavicular glands, I have never been able to demonstrate, but I cannot deny the possibility of this union, as it has been found by Sappey and also by Grossmann, and since, in carcinoma of the breast, the glands of the supraclavicular group here and there show up as infected and hardened. I should be inclined, however, to consider this course of the efferent vessels of the anterior thoracic glands to have arisen abnormally either in consequence of the original developmental arrangement (Anlage) or, as is more probable, because of the blockage of the main stream by carcinomatous emboli or by inflammatory processes, has caused the formation of new anastomoses.
The anterior thoracic glands of Oelsner are situated in the second intercostal space under or lateral to the border of the pectoralis major. They obtain a large amount of lymph from the mammary gland and transmit it to higher glands in the axilla.
Oelsner's conception of the termination of the lymph channels from the axilla (p. 147), I4 is that the subclavian lymph trunk opens into the venous angle (i.e. subclavian and internal jugular) either directly or after passing by way of another gland which is superior and dorsal to the subclavian vein.
It would seem, however, that there is a direct route passing anterior to the clavicle, between the breast and the 225 supraclavicular glands, for among the afferents of the transverse cervical chain mentioned by Professor Rouviere, are : Vessels that have come directly from the superficial tissues of the antero-lateral region of the neck, of the anterior thoracic wall in particular of the mammary region, and sometimes also from the upper limb 13 (p. 58). And again : One or two vessels which arise below and near the clavicle are conveyed upwards, pass in front of the clavicle and open into a subclavicular (sousclaviculaire) gland 13 (p. 199).
The distinction to be noted is that these trunks are subordinate collecting trunks of the cutaneous lymph plexus. This plexus is continuous with the lymphatics of the mammary gland, but these trunks are not recognized as in any way a regular route of lymph drainage from the mammary gland.
Professor Rouviere, when writing regarding the route of possible involvement, sent me the following : I do not think that the cancerous infection passes through the mediastinum to reach the ganglia of the recurrent chains. The pathogenic agent may follow, in fact, a shorter and more direct way. It may go thus : 1. From the breast to the axillary glands and to the internal mammary glands.
2. From the internal mammary axillary glands to the glands of the internal jugular chain and of the transverse cervical chain. Now the inferior glands of the internal jugular chain frequently receive efferent vessels from the ganglia of the corresponding recurrent chain. These internal jugular glands, once being infected by the cancer, the conditions for the retrograde propagation are realized, the infection will have only a very short way to go to reach the glands of the recurrent chain.
The recurrent laryngeal chain is continuous with the para-tracheal or latero-tracheal group, 13 page 178, which extends to the bifurcation, the very centre of the mediastinum. It would, therefore, appear that the contention that the recurrent laryngeal chain is the connecting link between what is outside and what is inside the mediastinum holds good, provided the term " recurrent laryngeal chain " is used in the wider sense. This applies to the right side, particularly, where the recurrent nerve is more of a cervical than a thoracic structure, and the glands concerned would be more properly 226 named the paratracheal. The supraclavicular glands may be involved, but their being or not being involved does not necessarily have any bearing upon the extension of disease via the para-tracheal (in part recurrent) chain, as this link is by way of the jugular chain.
If the supraclavicular lymph glands were an important link, it would not be unreasonable to expect the corresponding recurrent chain and nerve to be more commonly involved. In four cases, Case VI 1 -5> 9> IO , in each instance the right breast was diseased, the right supraclavicular glands were enlarged, but it was the left cord that was paralysed. In Case I 1 no glands on either side of the neck were palpable, and in 4 a case of bilateral paralysis, they were palpable only on one side and in 8 another of bilateral paralysis, " A t no time was there tangible enlargement of the glands of the neck, although a little fullness could be felt in the left posterior triangle." Including the writer's case, seventeen cases will have been reported, in which one breast has been diseased, nine right and eight left, and among these, eleven cases of crossed paralysis occurred, four on the right and seven on the left.
The cutaneous lymphatics : Which arise near the inner periphery of the mamma have been shown by Rieffel and Oelsner to terminate in the axillary glands of the opposite side (Dr. Turner's italics).
If this observation be correct, and this route followed in cases of crossed paralysis, then it would be expected that the contralateral axillary glands would be enlarged at least once in the eleven cases reported, even if a palpable gland is evidence of well-established cancerous disease. Two observations are made : Darling 3 : No definite glands palpable in either axilla. Carter 4 : " No palpable glands in either axilla " (the right axillary contents were cleared out three years previously).
Regarding the termination of the decussating cutaneous lymph trunks in the supraclavicular glands of the opposite side, which pass anterior to the clavicle, as so clearly depicted in Dr. Turner's illustrations, Oelsner's statement is that the 227 lymph trunks cross to the axilla of the opposite side, 14 page 139, but he makes no mention of any other gland group. It is unfortunate that the drawings used in connection with Dr. Turner's original article should be misleading, especially in their emphasis on the passing of the trunks anterior to the clavicle.
No enlarged glands could be felt above the right clavicle. Hard more or less fixed gland above the inner end of left clavicle. Enlarged gland above left clavicle. Left supraclavicular glands were enlarged. Above the inner end of the left clavicle a large hard gland could be palpated. Enlarged hard glands above the right clavicle. No glandular enlargement was detected aboveleft clavicle. A large hard gland in the posterior triangle of the neck immediately above the right clavicle. Small hard gland immediately behind the left clavicle. At the time of operation, November 12th, " no affected glands could be detected." No observation recorded at time of second operation the 16th of May following. Mass of hard glands in the right supraclavicular fossa. Left supraclavicular fossa tender to firm palpation, multiple small glands could be felt. Breast.
Right. At operation twelve months earlier, the axillary and supraclavicular glands on the right side were found enlarged and were removed. The right supraclavicular glands felt " shotty ". A fullness was noticed in the posterior triangle above the right clavicle. A hard mass was felt extending forwards beneath the sterno-cleido-mastoideus.
The supraclavicular glands on the right side were hard and slightly enlarged. Left supraclavicular glands palpable with more or less general swelling of the deep tissues of the neck.
Following the suggestion of Dr. Turner, I have listed case 8 as really one of tumour of the left breast with both homo-lateral and contra-lateral paralysis, in view of the fact that the right mamma had been removed sixteen years and the left but two years before laryngeal examination was required, and that at that time the left cord was paralysed, to be followed after only fourteen months by the right.
To be dogmatic on the basis of a review of seventeen cases, reported with varying degrees of detail, without a single post mortem and with a system for a background so prolific in 229 variations as the lymphatic, would, of course, be folly. Until more cases are reported and post mortems obtained and performed with the specific object of throwing light on this phenomenon, we must be content with speculation. At the moment, one is inclined to believe that in the majority of cases the infection travels via the substernal route or by way of the axilla and infraclavicular glands to reach the internal jugular chain, which in turn has as an afferent, the para-tracheal distribution.
On the right side the jugulo-subclavian angle is very much on the level of the lower border of the right subclavian artery, consequently retrograde extension must pass horizontally inwards or probably upwards in order that a gland be involved to make pressure on the recurrent laryngeal nerve, whereas extension either upwards or downwards would fulfil the requirements of the left side.
Professor Rouviere (page 179) states that at the level of the left innominate (brachio-cephalic) vein there is a definiteand constant connection between the right and left paratracheal lymphatic chains. This may be the route taken to give rise to crossed paralysis. If the right paratracheal glands were infected, the cancer cells could pass to the left side at this level and the recurrent nerve be interfered with without widespread mediastinal disease.
Again, the substernal or internal mammary chains can be connected at various levels behind the sternum or, as suggested by Dr. Turner, the intermammary cutaneous plexus may play a part.

Summary
The writer is reporting a case of recurrent laryngeal paralysis, secondary to cancer of the breast, and reviewing the sixteen previously reported. The explanation of this phenomenon put forward by Dr. A. Logan Turner in his original article in 1921, and which has prompted all subsequent reports, is examined and questioned in the light of more recent knowledge of the anatomy of the lymphatic drainage of the breast and its connections. The conclusion arrived at is that the explanation suggested is subject to correction in its essential points.
It would be difficult for me to express adequately my appreciation of the help received from Dr. H. Rouviere, Professor of Anatomy, Faculty of Medicine, Paris, and Dr. Donald Mainland, Professor of Anatomy, Dalhousie University, Halifax, Canada, without whose aid this paper could not have been written.
L'auteur rapporte un cas de paralysie du larynx d'origine recurrentielle, secondaire a un cancer du sein. II passe en revue 231 seize cas qui ont ete publies anterieurement. II examine l'explication de ce phenomene donnee par le Dr. Logan Turner en 1921 dans son article original qui a inspire toutes les observations consecutives, et il discute cette explication a la maniere de nos plus r^centes acquisitions sur le systeme sympathique du sein et ses connexions. Sa conclusion est que l'explication proposee est sujette a revision dans ses points essentiels.