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N:Cases and medico-legal aspects regarding bilateral iatrogenic injury of the recurrent laryngeal nerve

Rosario Barranco1, Tommaso D�Anna1, Antonina Argo1*,Francesco Cupido2, Gianfranco Cupido3 Paolo Procaccianti1 .
1 University of Palermo, Department of Biopathology, Medical Biotechnologies and Forensic Section of Legal Medicine, 129, del Vespro Street, 90127, Palermo, Italy.
2 University of Palermo, Department of Surgery, Oncology and stomatologic, 5, L. Giuffr�, Street, 90127, Palermo, Italy.
3 University of Palermo, Department of Experimental Biomedicine and Clinical Neuroscience, Section of Otolaryngology, 129, del Vespro Street, 90127, Palermo, Italy.
* Corresponding Author:  HYPERLINK "mailto:antonella.argo@libero.it"antonella.argo@libero.it

Key words: Thyroidectomy, Recurrent Laryngeal Nerve Palsy, Professional Liability, Guidelines

ABSTRACT
On the basis of the observation of 5 cases of recurrent nerve paralysis in patients undergoing surgical thyroidectomy, the authors evaluate the medicolegal implications related to the onset of this serious complication deriving from surgical operations in the thyroid gland. We describe the possible surgical techniques to preserve and not damage the RLN, in the course of a surgical procedure involving the thyroid gland. The medicolegal evaluation examines the possibility to detect, in the different cases analyzed, a surgical malpractice that might entails the existence of a professional responsibility, distinguishing this situation from cases in which the error can be defined as "excusable." We also have considered the importance of informed consent and of the medical chart, which is the main tool to evaluate the conduct of the surgeon.

INTRODUCTION
Injury of inferior or recurrent laryngeal nerve (RLN) is one of the most frequent and important complications during thyroid surgery. It occurs on average with a rate of 12% among all complications arisen in subjects undergoing such operations, with a range, according to the different cases, which goes from 0 to 20% [1]. The recurrent nerve innervates all the intrinsic muscles of the larynx, except the cricothyroid muscle, which is innervated by the superior laryngeal nerve, having, therefore, a fundamental role in normal laryngeal physiology. The lesion of this nerve impacts heavily on the social life of the patient, both for the occurrence of a deficit of the phonatory function, both primarily for disorders of ventilation and for the possible episodes of ingestion in the airways, due to the lack of occlusion of the glottis[2].
The patient, for the reasons given, is severely limited in the workplace and in his social life. Because of the problems exposed, the lesion of this nerve emerges as subject of medicolegal interest, in the case of medical professional liability. An accurate isolation of the nerve, in fact, cancels or reduces the risk of injury [3].The bilateral paralyses, differently from the unilateral, are very rare. Transient lesions of the recurrent nerve are described in the literature with a rate ranging between 2.6 and 5.9%, of which those permanent fluctuate between 0.5 and 2.4%. Several pathogenic mechanisms may compromise its anatomical and functional integrity, from the real dissection to the thermal damage caused by electrocautery in its closeness. The ischemic damage may be due to stretching, compression, crushing, entrapment in ligation or perineural devascularization [4].
In view of the numerous intraoperative technical schemes designed to trace and preserve the RLN, the surgeon is required to have an appropriate level of expertise, diligence and prudence, in order to trace the recurrent neural structures and protect them. This procedure can not be, logically, detached from a deep and detailed knowledge of the anatomic relationships between the recurrent nerves and the adjacent anatomical structures.
It is not easy to implement a surgical plan able to protect the RLN during a thyroid surgical operation, since its course possesses an extreme variability. The left recurrent nerve detaches from the vagus when the latter has already reached the chest cavity, it loops around the aortic arch and it connects with the pericardium, with the left atrium, with the pulmonary veins, with the left main bronchus and with the tracheobronchial lymph nodes. It courses along the anterior surface of the esophagus, in correspondence of the tracheoesophageal sulcus, connecting with the posteromedial portion of the left side lobe of the thyroid. The right lobe, instead, arises from the vagus in the neck, loops around the subclavian artery, it connects with the right pleural dome and it courses obliquely up to the larynx, connecting with the right border of the esophagus and with the posteromedial portion of the right lateral lobe of the thyroid. The inferior laryngeal nerves course at the back of the lateral lobes of the thyroid, and crosses, generally, the inferior thyroid artery, before entering the  larynx, where they split into two branches, the anterior one supplying the constrictor muscles of the glottis and the posterior branch that innervates the back cricoarytenoid muscle, abductor of the vocal cords.
Traditionally, adhesion of the nerve to the thyroid lobes would be an important factor that predisposes to injuries of the RLN, especially in cases where the nerve is attached to the thyroid capsule. In these cases, the greater risk is represented by the stretching or tearing of the nerve during the dissection of the thyroid lobe, when this is dislocated in front.
The rather irregular anatomy of RLN is more stable in terms of its distal segment adjacent to the cricothyroid junction, in fact, based on surgical experience gained over the years; this was the point where you should start tracing the nerve to minimize the risk of damage, because they are less subjected to anatomical variations [5]. The regular anatomical relationship between the Zuckerkandl�s tubercle and the RLN, at his entrance into the posterior laryngeal wall, focuses on the possible use of this region as an atomical landmark of the nerve. However, the inconstant presence of such anatomical element in the totality of the patients does not allow considering this investigation devoid of possible drawbacks[6]. Another landmark in the research of the recurrent nerve, may be established by the suspensory ligament of Berry, by reason of the fact that the RLN penetrates the laryngeal musculature laterally to this structure, without ever crossing it [7].
There is an important anatomical relationship also with the inferior thyroid artery, which provides however, a high variability; it is not uncommon, in fact, to detect dissimilar conditions, not only in different subjects, but also between the two sides, in the same subject. This great variability in the relationship between nerve and artery limits the possibility of considering the inferior thyroid artery as a single point of landmarks to trace the nerve [8].
Progresses made in recent years have allowed us to interpret electrophysiological data of intraoperative recurrent nerve and indeed the use of monitors for electromyography allows recording spontaneous or evoked potentials. Intraoperative monitoring of the recurrent laryngeal nerve has been recognized as a method to be used in thyroid surgery, allowing a reduction in the risk of the recurrent nerve injuries. These methods have the advantage of succeed in identifying the nerve through an assessment of action potentials and not through labor intensive visual methods. However these methods are burdened by the possibility of observing false negatives for the incorrect placement of the endotracheal electrode and also false positives due to stimulation with large electrical pulses, able to circumvent the axonal gap [9]. The methods so far described can be readily used by the surgeon only and exclusively in cases where the basic pathology of thyroid has not subverted the normal anatomy, such as it may happen in case of neoplasia of the thyroid gland in advanced stage: in this case due the infiltrative process, the neural structures result to be diverted in comparison with the normal anatomic path, therefore it is extremely difficult to trace and preserve the RLN. In addition, a meticulous surgical evaluation can not but take into account the possibility of facing anatomical abnormalities of the nerve course.
In a good percentage of cases one can observe a non-recurrence of right inferior laryngeal nerve ,that reaches the laryngeal musculature without looping around the right subclavian artery .This irregularity habitually is associated to a retroesophageal right subclavian artery (lusory artery), whose highlight must therefore be an inevitable indication of the presence of the said abnormality. Another possible abnormality is the extralaryngeal bifurcation of the recurrent nerve before crossing the inferior thyroid artery: the awareness of this likely event should prompt the surgeon, alerted by the discovery of a too thin structure of the recurrent, to search both the bifurcation and the second branch of the RLN [9]. 
In order to wise up on the matter of professional liability it is crucial to prove the offense or the damage, the error that caused it, and the causal link, as well as the subjective requirement of fault. It is known that the medicolegal evaluation in such situations presupposes a method of assessment ex ante, by which we reconstruct the clinical conditions prior to the surgery and those successive to the health service, including also the technical equipment available and the environmental circumstances [10]. It is also necessary to determine the degree of difficulty of the surgery and the possible presence of conditions, which, in the specific case, might make the preservation of the RLN extremely complicated These contingencies could be an important, if not crucial, aid in the analysis of the case, when the medical record and the surgery chart of the patient have been carefully compiled, noting all the anamnestic and objective patient-related records 
The bilateral lesion of the RLN can occur in a complete or incomplete way, with different symptoms according to the different syndromes.
Complete manifestations are Ziemssen�s syndrome and Riegel�s syndrome. In the first one, twovocal cords are immovable in abduction, so that therefore there is a phonatory diplegia [11]. In these cases the dysphonia is quite progressive and consequently the main symptom is aphony. This symptom can be associated with deglutition disorders and events of ab ingestis pneumonia, as a result of a dilated rima glottidis.
Riegel's syndrome is characterized by the position of the vocal cords immobilized in adduction in the median position. In these cases, the larynx is completely paralyzed, with profound alteration of both the movements of abduction and adduction. The symptom that dominates the case is the inspiratory dyspnea as the inspired air tends to further bring closer the two hypotonic vocal cords.
The symptomatology is characterized, also, by the laryngeal stridor, by cornage( respiratory distress) and by tirage (inspiratory retraction), which is characterized by peculiar retraction  at the level of the jugular notch  and of the supraclavicular dimples, during the inspiratory phase. You can also associate a dysphonia, caused by the constant intermediate position of the vocal cords, which annuls the vibration effect. 
The inspiratory dyspnea may occur in an underhand manner and thus be well tolerated at rest; however it tends to get progressively worse or otherwise it can occur acutely and suddenly, with vocal cords in remarkable adduction, with a clinical case of considerable seriousness, such to fear the onset of a asphyxiating syndrome.  
Among the incomplete laryngeal diplegiae we must include Gerhardt�s syndrome, characterized by a paralysis that affects only the rear cricoaritenoyd muscles, with a laryngoscope and symptomatic frame similar to the one of Riegel syndrome but less severe. The two vocal cords are in a paramedian position separated by a space of about 1-2 mm [11]. Voice timbre is not altered, but since its intensity is never strong, voice is easily exhaustible and tired. The inspiratory dyspnea dominates other symptoms when there is no vocal function damaged.
From a therapeutic point of view, cases not responding to steroids  and neurotrophic therapy [12] need surgical interventions to be performed at least after about 6 months, since up to that time a functional recovery of the vocal cords is possible and desirable. 
Paralysis in abduction can be corrected surgically in order to reduce the glottal space, by means of median thyrotomy and internal subchondral graft of fragments of auricular cartilage.In conditions of respiratory failure paralysis in adduction require a tracheotomy in order to avoid an asphyxiating syndrome; after the tracheotomy it will be possible to intervene to enlarge the laryngeal respiratory space by sectioning the arytenoid cartilages or by means of a posterior cordotomy [13, 14].


CASES
In the light of the analysis and evaluations above exposed, we analyzed 5 cases of bilateral lesion of the RLN of iatrogenic nature (post-thyroidectomy), arrived in personal clinical experience and medicolegal valuation practice. The subjects in question were all females: 3 had undergone thyroidectomy because of a diffuse goiter, 2 suffering from an infiltrative thyroid neoplasm. In all the cases we have analyzed there were no permanent or transitory pathologies related to an injury of recurrent nerve.
In 4 out of these 5 cases, this was the first surgery involving thyroid, devoid, therefore, of the increase of the risk of lesions of the recurrent nerve typical of the re-operated patients [15]. Only one subject had previously undergone surgery on the thyroid gland. All patients had undergone a total thyroidectomy and only one subject underwent a subtotal one. Both techniques do not present fundamental differences in the risk of iatrogenic lesion of the nerve. The two cases of malignant thyroid neoplasy had been subjected to a satellite lymphadenectomy, which greatly increases the risk of damaging the recurrent nerves [2]. In cases of diffuse goiter no outcome showed any abnormality of the normal anatomy of the RLN, in addition no difficulty has been described in their collecting. Patients suffering from malignant neoplasy, instead, presented a rather altered anatomic frame with infiltration of the nervous structures. The period between the surgery and the onset of symptoms referable to a bilateral recurrent lesion is quite similar in all the 5 cases taken into consideration: all, in fact, showed a symptomatic follow up in the immediate post surgery period. 
Patients at the time of first observation showed in all the cases a dyspnea of inspiratory and expiratory nature of more or less serious level; moreover, three subjects suffered from nocturnal stridor associated with cornage (inspiratory stridor) and tirage (respiratory distress). In all the cases the diagnosis was reached by a fibreoptic laryngoscope with flexible endoscope: during the examination, vocal cords appeared immobilized, static in paramedian position, determining a considerable reduction of the respiratory space. Due to a severe dyspnoeic symptomatology, such to fear the onset of an asphyxiating syndrome, all patients underwent an immediate tracheotomy. Subsequently, after 6 months - period necessary to verify a possible spontaneous recovery (or partial) of at least one of the two paralyzed vocal cords [16] - all patients examined underwent a laser cordectomy, in order to provide an increase in  glottic space.
DISCUSSION
Recognizing that an erroneous action is likely to be due to a negligent conduct performed by the health professional, as regards bilateral lesions of the recurrent nerve subsequent to a thyroid surgery, is often not easy to appreciate, especially in cases where the documentation regarding the medical record is rather incomplete, making consequently difficult the opportunity to express an opinion, if not of certainty, at least of high probability.
The realization of the existence of a professional liability, first of all, starts from the verification of the causal link between surgery and the occurred lesion of inferior laryngeal nerves. In this sense, it is indispensable to evaluate the functionality of the recurrent nervous structures prior to the surgery: the finding of a pre-existing damage, pointed out by anamnestic and documentary records or by pre operation  laryngoscopic findings, might bring into question ,up to exclude it, the causal link between conduct  and event arisen from alleged medical negligence .
A precise and accurate analysis requires a correct chronological positioning of the lesion and of its subsequent symptoms. In fact, bilateral lesions of the RLN that occur, later, are often a result of compressive phenomenas caused by visible and big scars, that have nothing to do with the work of physician; consequently, in these situations, it is hard  to find a malpractice, due to negligence, imprudence and / or inexperience. These considerations, of course, can not be accepted when the bilateral nervous lesion has occurred later, for example because of an avoidable infectious complication, in case of nerve compression due to the presence of a hematoma consequent to a bleeding which could have been stopped if the health professional had put in place suitable procedures, or in case of a drainage in continuous aspiration placed badly.
Paralyses occurring in the immediate post operation period, are generally attributable to a nervous lesion occurred during surgery, therefore the presumption of a medical conduct not responding to the leges artis, assumes a definitely higher importance. In this regard it is desirable to identify the etiology of the lesion. In most cases, we can detect the cause of intraoperative damage in an erroneous identification and wrong isolation of nerves, attributable to multiple factors, such as anomalies during the course, precocious ramifications, incongruous handling, excessive bleed due to a little careful ligation of the arterial branches which , making the operation field not bloodless, prevents an easy identification of nerve structures. In addition, the close relation between these structures and the inferior thyroid vessels can lead the inattentive surgeon to include the nerve branches in the vessel ligation causing extensive damage of a blunt-compressive nature [17].
The medicolegal judgment must take into consideration the fact that the intraoperative recurrent nerve lesions may have a different degree of severity: the neurotmesis determines a permanent loss of nerve functionality, the axonotmesis causes an irreversible limitation, and finally the neurapraxia causes an alteration of the vocal cords, often recoverable in full, within a few months. It is therefore essential to evaluate and assess the severity of functional impairment not earlier than 6 months, when the reduction of laryngeal function is no longer susceptible of improvement or worsening [17]
The evaluation of records and of informed consent assume a fundamental value. Comprehensive, complete and truthful information, certainly exclude an alleged offence related to a violation of the right to self-determination of the patient; but it neither reduce or exclude the surgeon's fault related to an error that occurred during the surgical procedure. Among other things the consent appears frequently in an imperfect form for a number of reasons, among which the most significant is represented by the fact that health professional tends to diminish and minimize this moment of comparison and communication with the patient [18, 19]. The physician, often, conceives informed consent, in the perspective of defensive medicine, as a tool of self-defense and not as a manifestation of the will to use one's own body that may exclude specifically the wrongfulness of the fact.
In iatrogenic lesions of the RLN, the medicolegal evaluation is based mainly on an analysis of medical records and of the attached surgical register, as it represents the main element of the defense of the surgeon, who must write clearly and in a complete way all the data related to the patient and to surgical procedures. It is an important element of defense to record in the medical case all those conditions which have made extremely difficult the isolation of the RLN; these difficulties are basically to be referred to the possible presence of a malignant neoplasy that, infiltrating the neural structures, prevents their safeguard, or to the case of reoperation in which it is possible to observe altered anatomical relationships between the neural structures and the adjacent tissues. In these circumstances, the omitted description of these elements is equivalent to their absence.
The presence of pre existent conditions favourising the onset of a bilateral recurrent lesion, or of a very high degree of technical difficulty, may cause the surgical mistake to be defined as �excusable�, concept which can be applied in a medical context, in the event of an intrinsic scientific uncertainty which makes comprehensible and absolvable those negative outcomes not deriving from serious mistakes or by an inobservance of particular preventive rules [20]. These cases are to be distinct from those where, without any problem of isolation of inferior laryngeal nerves, the lesion of these nervous structures is attributable to inexpert, negligent or imprudent practice of the surgeon. In absence of pre existences and of different causes justifying the lesion, the performance of the physician is considered, according the criterion of exclusion, the only moment which might have affected the course of the surgery operation that, if carefully performed, would not have damaged the inferior laryngeal nerves.   
Finally, international guidelines of British Thyroid Association and of American Thyroid Association underline the need to trace and protect the RLN during surgery on thyroid. The physician on the basis of his experience and of the anatomic-surgical situation must be capable of choosing the technique most suitable to the specific case. In case of particular technical difficulties the guidelines suggest to use the   intraoperative monitoring of inferior laryngeal nerves. [21-24].
As regards the cases above described, the onset of symptoms in the immediate post-operative period is indication of a nervous lesion occurred during the surgical intervention. In the two cases of neoplasy on the thyroid gland, records regarding the medical case and the surgical chart have pointed out a deep alteration of the normal loco-regional anatomy, because of the diffuse infiltration of the cancer issue, making extremely hard the possibility to trace and protect inferior laryngeal nerves also through the intraoperative monitoring of the recurrent laryngeal nerve.
In the 3 remaining cases, the absolute benignity of the thyroidal pathology, the laryngoscopic preoperative elements , as well as the absence of annotations  in the surgical chart and in the medical case  demonstrative of an objective difficulty in the isolation of inferior laryngeal nerves and the onset of a symptomatology in the immediate post-operation period have underlined real elements of censure in the conduct of the surgeon, who has neglected international guidelines , which impose a severe scrupulousness in the identification and protection of the recurrent laryngeal nerve. Therefore, all the factors listed appear to be enough to suppose the existence of a professional liability of the surgeon.

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