甲状腺的外文献1214

ORIGINAL ARTICLE
Recurrent laryngeal nerve landmarks revisited
Elham Asgharpour,MD,PhD,1Eva Maranillo,MD,PhD,1Jose Sa~n udo,MD,PhD,1Aran Pascual-Font,PhD,1Marc Rodriguez-Niedenfu¨hr,MD,PhD,1 Francisco J.Valderrama,PhD,1Fermin Viejo,MD,PhD,1Ian G.Parkin,MD,PhD,2Teresa V a zquez,PhD1*
1Department of Human Anatomy and Embriology I,Faculty of Medicine,Complutense University of Madrid,Madrid,Spain,2Cuschieri Skills Centre,University of Dundee, Dundee,United Kingdom.
Accepted27June2011
Published online11November2011in Wiley Online Library().DOI10.1002/hed.21882
ABSTRACT:Background.The aim of this work was to evaluate,to prove their reliability,the different surgical landmarks previously proposed as a mean to locate the recurrent laryngeal nerve(RLN). Methods.The necks of143(68male and76female)human adult embalmed cadavers were examined.RLN origin and length and its relationship to different landmarks were recorded and results compared with those previously reported.Statistical comparisons were performed using the chi-square test(significance,p .05).
Results.Mostly,RLN is located anterior to the tracheoesophageal sulcus (41.6%),posterior to the inferior thyroid artery(35.8%),lateral to Berry’s ligament(88.1%),below the inferior rim of the inferior constrictor muscle(90.4%),and entering the larynx before its terminal division (54.6%).
Conclusions.The position of the RLN in relation to those structures classically considered as landmarks is highly variable.The most reliable relationships are those with Berry’s ligament or the inferior constrictor muscle.V C2011Wiley Periodicals,Inc.Head Neck34:1240–1246, 2012
KEY WORDS:Berry’s ligament,inferior constrictor muscle,inferior thyroid artery,tracheoesophageal sulcus,extralaryngeal branching
More than100years ago,Emil Theodor K€o cher,consid-ered by many‘‘the father of thyroidectomy,’’remarked that a precise anatomic knowledge is necessary to avoid the lesion of the recurrent laryngeal nerve(RLN).In spite of this remark,1of the most frequent causes of recurrent laryngeal nerve paralysis after thyroid surgery is iatro-genic.The risk of lesion has been attributed to different causes such as glandular pathology,1,2improper surgical technique,1fixation of the nerve to neighboring struc-tures,3,4and,to a great extent,to close anatomic relation-ships that make its dissection difficult during thyroidectomy.
The RLN has been described closely related to the infe-rior horn of the thyroid cartilage,2,5–8thyroid gland,3,7,9–11 inferior thyroid artery,3,7,10Berry’s ligament,11–13or the in-ferior pole of the thyroid gland.7,10,11
To locate the RLN,different surgical landmarks have been proposed,but none of them is still universally accepted;these include:Simon’s triangle,14–16its relation with the inferior thyroid artery,15,16its relation with the in-ferior pole of the thyroid gland,9,11,15–20the disposition of the RLN at the base of the neck,21or its relation with Zuck-erkandl’s tubercle.22,23Alternatively,traction maneu-vers24,25or intraoperative electrophysiologic monitoriza-tion have also been proposed as a mean to avoid RLN lesion.26,27
On the other hand,there is great variability related with the extralaryngeal branching of the RLN.Some authors described1or2terminal branches,5,15,28–30but most of them described variable branching patterns with up to8ter-minal branches.4,6,7,11,20,31–38
Although many studies regarding the anatomy of the RLN in cadaveric or surgical samples have been published,most of them were not based on statistically reliable samples or did not include homogeneous criteria to analyze different anatomic relationships.Therefore,the aim of the present work was to analyze,in a large and homogeneous sample of human cadavers,the most relevant landmarks to identify the RLN,as well as to compare our results with those previously published trying to clarify the surgical anatomy of the RLN to facilitate its safe localization during surgical procedures. MATERIALS AND METHODS
The necks of143white human adult embalmed cadav-ers were examined.They included68male and76female cadavers,with an age at death ranging between64and 100years(mean age,81years).No pathology of the thy-roid gland was observed.All cadavers were inside the size and weight range established by Cambridge Univer-sity for the acceptance of body donation(weight from 44.5to85kg,and<180cm in height).They had been partially dissected by Cambridge preclinical medical stu-dents during3academic years and then further dissected by the authors using magnification.
*Corresponding author:T.V a zquez,Department of Human Anatomy and Embriology I,Faculty of Medicine,Complutense University of Madrid,Madrid, Spain.E-mail:tvazquez@med.ucm.es
Contract grant sponsor:Universidad Complutense de Madrid;contract grant number:UCM920547and FIS10-02721.
Due to the neck complexion or the way in which the cadaver was embalmed,the sample was slightly reduced when analyzing certain parameters.The exact size of the sample will be specified in the Results section for each parameter studied.All measurements were made with the head in a centered supine position.Paint was used to highlight the different anatomic structures shown in the figures.Statistical comparisons of the obtained results were performed using the chi-squared test(significance,p .05).
The different parameters analyzed were:the origin of the RLN and length from its origin to the point in which it entered the larynx(a flexible ruler was used for meas-urements),the relationship to the tracheoesophageal sul-cus;the RLN was considered to be in the sulcus when it was equidistant from trachea and esophagus,and anterior or posterior to the tracheoesophageal sulcus when it was closer to the trachea or esophagus,respectively,and the relationship of the RLN with the inferior thyroid artery, taking into consideration3different scenarios:the RLN is related with the main trunk of the inferior thyroid ar-tery,with its terminal branches,or with its secondary branches;the position in relation with the related vessel has also been recorded.
The relationship of the RLN to Berry’s(or Gruber’s) ligament,the relationship to the inferior constrictor mus-cle,and the number of extralaryngeal branches of RLN as well as their caliber and distances from their origin to the inferior rim of the thyroid cartilage and cricothyroid joint were also analyzed.
Finally,a meta-analysis including previously published results was carried out.The literature search was made trying to incorporate all previously published articles dealing with the current subject.The literature search extended beyond PubMed and other databases and included articles from the nineteenth to the twenty-first centuries.The meta-analysis was performed on those studies presenting surgical or cadaveric samples,exclud-ing case-report descriptions.
RESULTS
The left RLN originated from the vagus nerve in all 143necks,in all cases in an anteroinferior position in relation to the aortic arch.The RLN originated at a dis-tance between15and22cm(mean,19cm)from the ori-gin of the superior laryngeal nerve.Nonrecurrent laryn-geal nerves have not been observed on the left side.
The right RLN originated from the vagus nerve in an anteroinferior position to the subclavian artery at the level of the root of the neck in142of143cases(99.3%).The mean distance to the superior laryngeal nerve origin was 13.9cm(range,9.5to17.5cm).In1case(0.7%),the right RLN was nonrecurrent;it originated from the vagus nerve at the cricoid cartilage level and it was associated to a right retroesophageal subclavian artery.
The RLN length has been studied in214heminecks (108right,106left).It ranged from4to9.5cm on the right side(mean length,6.7cm)and from9to17.5on the left side(mean length,13.3cm).No differences by sex were observed.Relationship of the RLN to the tracheoesophageal sulcus
This parameter was studied in197heminecks(97right, 100left).The nerve was located anterior to the sulcus in 82cases(41.6%),in the sulcus in65cases(33%),and posterior to it in50cases(24.5%).This relationship was symmetrical in31%of cases,being the nerve anterior to the sulcus in14%of cases,inside the sulcus in12%,and posterior to it in5%of cases.When side distribution was analyzed,the RLN was mostly anterior to the sulcus on the right side,whereas on the left side it was found most frequently in the sulcus(p¼.003)(see Figure1).
RLN relation to the inferior thyroid artery
The whole sample(246heminecks)was used to study the relation to the inferior thyroid artery.The nerve was observed posterior to the artery in35.8%of cases,ante-rior to it in32.9%,and between its branches in30.1%.In 1.2%of cases the artery was surrounded by the nerve (Figures1and2A and2B).The same neurovascular pat-tern was observed bilaterally in41.4%of cases.
There is a statistically significant difference(p¼.0001)when this relationship is examined by sides,so the anterior position is more frequent on the right side, whereas the posterior position is more frequent on the left side.
In4cases(1.6%)the inferior thyroid artery was absent; in3cases it was replaced by a thyroid inferior mesenteric artery(IMA or Neubauer’s artery)(Figure2C).
RLN and Berry’s ligament relationship
The relation with Berry’s ligament was confirmed in 185heminecks belonging to100cadavers(92right and 93left).In most cases(88.1%),the RLN was lateral to the ligament(Figures3A and3C);in11.9%cases,the RLN pierced the ligament(Figure3B).
This relationship was symmetrical in79.8%of cases. No differences by sex or side were found.
Relation between the RLN and the inferior constrictor muscle of the pharynx
The RLN was found below the inferior rim of the infe-rior constrictor of the pharynx muscle in most cases (90.4%)(Figures3A and3B);in9.6%of cases the nerve pierced the muscular fibers(Figure3C).No differences between side and/or sex were found.
Extralaryngeal branching of the RLN
The extralaryngeal branching of the RLN was analyzed in142cadavers.The RLN entered the larynx before its division in54.6%of cases,a situation significantly more frequent on the left side(p¼.043)(see Figure4).The RLN branched into2rami in45.4%of cases(Figures 1A,1C,2A,2B,and3).The branching of the RLN was symmetrical in51.7%of cases.
The caliber of both branches was similar in all cases with no statistically significant differences between side or sex. The extralaryngeal division of RLN was located at a mean distance from the inferior horn of the thyroid carti-lage of1.33cm on the right side and1.26cm on the left
R ECURRENT LARYNGEAL NERVE LANDMARKS
side.Regarding the inferior rim of the cricothyroid joint,the nerve’s division level ranged between 0and 1cm in 48.7%of cases;between 1.1and 2cm in 42.5%of cases;between 2.1and 3cm in 7.5%of cases;and between 3.1and 4cm in 1.3%of cases.
DISCUSSION
In relation to the origin of the RLN,our results confirm those previously published.10,11,19,39The observed inci-
dence of nonrecurrent laryngeal nerve associated with a right retroesophageal subclavian artery (0.7%)is also similar to that observed by most authors.2,4,11,19,32,40,41Embryologically,the existence of this variation has been explained by the absence of development of the fourth right aortic arch.42
The length of the RLN between its origin and its en-trance into the larynx has only been previously studied by Liebermann-Meffert et al,24who reported mean lengths of 7cm on the right side and 13cm on the
left
FIGURE teral views showing different recurrent laryngeal nerve (rln)relations with tracheoesophageal sulcus and inferior thyroid artery (ita).(A)Right hemineck in which rln is located anterior to the tracheoesophageal sulcus and posterior to the ita.(B)Left hemineck.The rln runs in the tracheoesophageal sulcus and is located anterior to the ita.(C)Right hemineck.The rln is observed posterior to the tracheoesophageal sulcus and anterior to the ita.eln,external laryngeal nerve;icm,inferior constrictor of the pharynx muscle;sta,superior thyroid artery;t,trachea;tg,thyroid gland.[Color figure can be viewed in the online issue,which is available at
.]
FIGURE 2.(A)Lateral view of a right hemineck.The recurrent laryngeal nerve (rln)passes between the inferior thyroid artery (ita)branches.(B)Right hemineck,lateral view.The ita is surrounded by the rln branches.(C)The ita has been replaced by a Neubauer’s artery (ima).There is no relation between this artery and the rln.aa,aorta artery;bct,brachiocephalic trunk;eln,external laryngeal nerve;icm,inferior constrictor of the pharynx muscle;lcca,left common carotid artery;rcca,right common carotid artery;rsa,right subclavian artery;sta,superior thyroid artery;t,trachea;tg,thyroid gland.[Color figure can be viewed in the online issue,which is available at .]
A SGHARPOUR ET AL .
side,which are completely coincident with our observations.
Regarding the position of the RLN in the tracheoesopha-geal sulcus,we found the RLN anterior to the sulcus in most cases,which disagrees with the vast majority of authors.7,10,11,15,17,19,39This could be explained because,except for Skandalakis et al,19all other authors considered only 2possible positions,the nerve is in the sulcus or ante-rior to it,but the posterior position was not considered and those cases were therefore counted together with those located in the sulcus (Table 1).
The RLN was located anterior to the sulcus most fre-quently on the right side (p ¼.003),which confirms that,during surgery,the right RLN is more exposed than the left one.5,9–11,17,28We did not find any case in which the RLN was inside the thyroid gland’s parenchyma.10,19
Taking into consideration previously proposed classifi-cations,the relationship between the RLN and inferior thyroid artery has been summarized in 3patterns (Table 2).Our results show that there is a similar proportion of cases in which the RLN passes anterior to the inferior thyroid artery or between its branches,in which the RLN runs posterior to the artery more frequently in those cases.Although Hirata 44stated that there were sex differences regarding this relationship,he did not per-form any statistical analysis,and we did not find any such differences.
When analyzing the RLN by side,we found the left RLN located more frequently posterior to the artery,which agrees with previous reports.7,10,11,14,15,17,19,33,34,36,43,44Regarding the right RLN,it was observed more frequently anterior to the artery,contradicting previously published results of most authors that found it more frequently between the inferior thyroid artery branches.15,19,34,36,40,43–45
The relation of both RLNs with the inferior thyroid ar-tery was symmetric in 41.4%of cases,which disagrees with most studies 7,9,18,28,39,45;only 1previous author states that the asymmetric disposition is the
most
FIGURE 3.Relation of the recurrent laryngeal nerve (rln)with Berry’s ligament and inferior constrictor muscle of the pharynx.(A)Posterolateral view of a left hemineck.The rln runs lateral to Berry’s ligament and go into the larynx under the inferior rim of the inferior constrictor muscle of the pharynx.(B)Posterior view of a left hemineck.The rln pierces the Berry’s ligament fibers.(C)Lateral view of a right hemineck.The rln pierces the inferior constrictor muscle of the pharynx fibers running lateral to Berry’s ligament.bl,Berry’s ligament;icm,inferior constrictor muscle of the pharynx;tg,thyroid gland.[Color figure can be viewed in the online issue,which is available at .]
FIGURE 4.Left hemineck lateral view.The recurrent laryngeal nerve (rln)enters the larynx before its terminal division passing posterior to the inferior thyroid ,common carotid artery;ct,cricothyroid muscle;icm,inferior constrictor muscle of the pharynx;ita,inferior thyroid artery;t,trachea.[Color figure can be viewed in the online issue,which is available at .]
R ECURRENT
LARYNGEAL NERVE LANDMARKS
frequent.14In these bilateral cases,the3described pat-terns were distributed in a similar proportion.
The presence of an IMA thyroid artery was described in3cases where the inferior thyroid artery was absent, representing a lower incidence than previously described.2,7,11,28,34,45,46We have not found situations in which there was no relation between the RLN and the in-ferior thyroid artery,which arose from the parallelism on their courses.33
Although the RLN has been described as being most frequently between the fibers of Berry’s ligament36or medial to it,47the majority of authors described the RLN lateral or posterolateral to Berry’s liga-ment.7,10,11,13,19,47,48This situation was also observed in 88.1%of cases in the present study;in the remaining cases,the nerve was between the ligament’s fibers (11.9%).In contrast to previous reports,in the present study the RLN was never observed medial to Berry’s lig-ament47(Table3).
To our knowledge,no previous studies analyzed differ-ences by sex and/or side or bilaterality of this relation-ship.We have not observed any statistically significant differences by sex or side,but symmetrical disposition of the RLN regarding Berry’s ligament was present in 79.8%of cases,which contradicts those findings that described RLN lateral to the ligament in100%of cases.13,48
Even though the relationship of the RLN with the infe-rior constrictor muscle has been described as an impor-tant landmark to locate the nerve,most studies did not perform a statistical analysis.10,39,40,49,50Our findings are in accord with those of Wafae51and Schweizer and D€o rfl,20which located the RLN entering the larynx more frequently inferiorly to the muscle.
The terminal branching of the RLN observed in this study confirms that the nerve may enter the larynx as a unique trunk(54.6%of cases)or split into2branches (45.4%of cases),similarly to some of the previously published studies.5,15,28–30In our opinion,the observed discrepancies in the reports analyzing the terminal branching of the RLN are due to the fact that some authors included collateral branches as well as RLN ter-minal branches.
We have also observed that,most frequently,the left RLN does not present terminal extralaryngeal branching (p¼.043),a fact that has not been recorded in the litera-ture consulted.A bilateral disposition has been previously reported ranging between15%52and75%20;we found a symmetrical situation in51.7%of cases,in which the RLN is a unique trunk in both sides before entering the larynx,which is the most frequent situation(30.8%) (Table4).
The extralaryngeal division of the RLN took place at a mean distance from the inferior horn of the thyroid
TABLE1.Relation of the RLN with tracheoesophageal sulcus.
Author(s)Anterior to
the sulcus
In the
the sulcus
Posterior to
the sulcus
Berlin and Lahey17—44/44(100)—Berlin1049/140(35)91/140(65)—Armstrong
and Hinton7
16/40(40)24/40(60)—Bowden116/55(11)49/55(89)—Skandalakis et al1994/204(46)99/204(49)11/204(5) Steinberg et al3954/180(30)126/180(70)—
Al-Salihi
and Dabbagh15
36/212(17)176/212(83)—
Our results82/197(42)65/197(33)50/197(25) Meta-analysis337/1072(31)674/1072(63)61/1072(6) Abbreviation:RLN,recurrent laryngeal nerve.
Comparison with consulted bibliography.Numerical data represent the number of cases/total sample;percentage in parentheses.
TABLE2.Relation of the RLN with the inferior thyroid artery and its branches.
Author(s)Anterior to
the the artery
Between artery
branches
Posterior to
the artery
Berlin and
Lahey17
15/44(34)10/44(23)19/44(43)
Ziegelman915/42(36)15/42(36)12/42(29) Berlin1045/140(32)20/140(14)75/140(54) Simon1415/86(17)6/86(7)65/86(76) Armstrong
and Hinton7
34/1040(34)23/100(23)43/100(43) Morrison3355/200(27)52/200(26)93/200(47) Dufour et al4312/52(23)16/52(31)24/52(46) Bowden1111/55(20)20/55(36)24/55(44) Clader et al3410/96(10)38/96(40)48/96(50) Skandalakis
et al19
42/203(21)76/203(37)85/203(42)
Papadatos4096/478(20)191/478(40)191/478(40) Steinberg
et al39
58/180(32)12/180(7)110/180(61)
Al-Salihi and
Dabbagh15
49/212(23)49/212(23)114/212(54)
Hirata44148/784(19)273/784(35)363/784(46) Salama and
McGrath36
28/144(19)52/144(36)64/144(45)
Poyraz and
Çalguner45
8/48(16.7)22/48(45.8)18/48(37.5)
Our results81/246(33)77/246(31)88/246(36) Meta-analysis722/3110(23)952/3110(31)1436/3110(46) Abbreviation:RLN,recurrent laryngeal nerve.
Comparison with consulted bibliography.Numerical data represent the number of cases/total sample;percentage in parentheses.TABLE3.Relation of the RLN with Berry’s ligament.
Author(s)
Lateral to the
ligament
Between the
ligament fibers
Medial to
the ligament Berlin10105/140(75)35/140(25)—Armstrong
and Hinton7
30/40(75)10/40(25)—
Bowden1111/18(61)7/18(39)—Skandalakis et al19118/204(58)86/204(42)—Salama and
McGrath36
46/144(32)98/144(68)—Sasou et al1346/46(100)——
Caçir et al48130/130(100)——
Yalçin and Ozan4790/112(80)3/112(3)19/112(17) Our results163/185(88)22/185(12)—Meta-analysis739/1019(72)261/1019(26)19/1019(2) Abbreviation:RLN,recurrent laryngeal nerve.
Comparison with consulted bibliography.Numerical data represent the number of cases/total sample;percentage in parentheses.
A SGHARPOUR ET AL.
cartilage of1.33cm on the right side and1.26cm on the left side.No references regarding this measurement were found in the literature consulted.Most reports established the distance of RLN extralaryngeal division using the in-ferior rim of the cricothyroid joint as a reference;in this respect,our results are in accord with those establishing that the RLN branches are most frequently at a distance <2cm(Table5).
When the RLN divided extralaryngeally,the motor branch was located anterior and lateral,whereas the sen-sory branch,which constitutes Galen’s connection,runs posterior and medial.Although in most cases(58.9%)we found both branches having a similar caliber,our results compared with those previously published show high var-iability.This could be due to the different methodology used by previous authors.7,49CONCLUSIONS
Taking into account our findings,the position of the RLN in relation to those structures classically considered as landmarks for identification,is very variable.The most constant relationships are those with Berry’s ligament or inferior constrictor muscle.Distances to the thyroid carti-lage inferior horn or to the inferior rim of the cricothyroid joint could also be of interest,but extralaryngeal branch-ing of the RLN in almost half of the cases must be taken into account.
Although there are many landmarks to identify the RLN,the variability in these anatomic relationships should always be taken into consideration.A precise understanding of the variable topographical anatomy of the nerve in this region facilitates fast and safe nerve identification.
Acknowledgements
The authors thank Dr.X.Le o n for his valuable statistical advice.
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TABLE4.Extralaryngeal branching of RLN.
Author(s)No extralaryngeal
division
Extralaryngeal
branching
Dilworth50/66(0)66/66(100) Nordland2860/62(97)2/62(3) Stewart and Moore316/24(25)18/24(75) Weeks and Hinton62/17(12)15/17(88) Reed32479/506(95)27/506(5) Armstrong and Hinton727/100(27)73/100(73) Morrison33114/200(57)86/200(43) Williams290/100(0)100/100(100) Bowden1112/54(22)42/54(78) Clader et al3421/50(42)29/50(58) Pichler and Gisel300/100(0)100/100(100) Laux and Guerrier49114/200(57)86/200(43) Keros and Nemanic350/300(0)300/300(100) Al-Salihi and Dabbagh15158/212(75)54/212(25) Salama and McGrath3650/144(35)94/144(65) Schweizer and D€o rfl205/42(12)37/42(88) Sun et al46/100(6)94/100(94)
Çakir et al4854/130(41)76/130(59) Our results155/284(55)129/284(45) Meta-analysis1302/2821(46)1519/2821(54) Abbreviation:RLN,recurrent laryngeal nerve.
Comparison with consulted bibliography.Numerical data represent the number of cases/total sample;percentage in parentheses.
TABLE5.Extralaryngeal division of RLN.
Author(s)
Distance to cricothyroid joint
inferior rim,cm
0–11–22–33–4
Dilworth5——66/66(100)—Williams29——100/100(100)—Salama and
McGrath36
45/94(48)45/94(48)4/94(4)—
Schweizer and
D€o rfl20
—41/42(98)—1/42(2) Beneragamai
and Serpell38
16/77(21)41/77(53)19/77(25)1/77(1) Our results39/80(49)34/80(42)6/80(7)1/80(1)
Abbreviation:RLN,recurrent laryngeal nerve.
Comparison with consulted bibliography.Numerical data represent the number of cases/total sample;percentage in parentheses.
R ECURRENT LARYNGEAL NERVE LANDMARKS
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