Seediscussions,stats,andauthorprofilesforthispublicationat:http://www.researchgate.net/publication/50598240

GermanAssociationofEndocrineSurgeonspracticeguidelinesforthesurgicaltreatmentofbenignthyroiddisease

ARTICLEinLANGENBECKSARCHIVESOFSURGERY·MARCH2011

ImpactFactor:2.19·DOI:10.1007/s00423-011-0774-y·Source:PubMed

CITATIONS

45

READS

87

21AUTHORS,INCLUDING:

PeterGoretzki

LukaskrankenhausNeuss

301PUBLICATIONS3,280CITATIONS

SEEPROFILE

ChristianScheuba

MedicalUniversityofVienna

77PUBLICATIONS2,003CITATIONS

SEEPROFILE

ThomasSteinmüller

149PUBLICATIONS3,478CITATIONS

SEEPROFILE

ArnoldWTrupka

KlinikumStarnberg,

78PUBLICATIONS1,662CITATIONS

SEEPROFILE

Availablefrom:ChristianScheuba

Retrievedon:15November2015

ORIGINAL ARTICLE

German Association of Endocrine Surgeons practiceguidelines for the surgical treatment of benignthyroid disease

Thomas J. Musholt & Thomas Clerici & Henning Dralle &

Andreja Frilling & Peter E. Goretzki &Michael M. Hermann & Jochen Kußmann &

Kerstin Lorenz & Christoph Nies & Jochen Schabram &

Peter Schabram & Christian Scheuba & Dietmar Simon &

Thomas Steinmüller & Arnold W. Trupka &

Robert A. Wahl & Andreas Zielke & Andreas Bockisch &

Wolfram Karges & Markus Luster & Kurt W. Schmid &

The Interdisciplinary Task Force “Guidelines” of theGerman Association of Endocrine Surgeons

Received: 18 January 2011 /Accepted: 1 March 2011 /Published online: 22 March 2011# Springer-Verlag 2011

AbstractIntroduction Benign thyroid disorders are among the mostcommon diseases in Germany, affecting around 15 millionpeople and leading to more than 100,000 thyroid surgeries

per year. Since the first German guidelines for the surgicaltreatment of benign goiter were published in 1998,abundant new information has become available, signifi-cantly shifting surgical strategy towards more radical

Author contributions All of the authors were involved in theconception and design of the guidelines, in data acquisition, analysis,and interpretation, and in drafting and critical revision of themanuscript.

T. J. Musholt (*)Section of Endocrine Surgery, Clinic of General and AbdominalSurgery, University Medical Center,Gutenberg University—Mainz,Langenbeckstr. 1,55101 Mainz, Germanye-mail: musholt@uni-mainz.de

T. ClericiDepartment of Surgery, Kantonsspital St. Gallen,CH-9007,St. Gallen, Switzerland

H. Dralle :K. LorenzDepartment for General, Visceral and Vascular Surgery,Martin-Luther University Halle-Wittenberg,Ernst-Grube-Str. 40,06120 Halle (Saale), Germany

A. FrillingDepartment of Surgery and Cancer, Imperial College London,Hammersmith Hospital,Du Cane Road,London( W12 0HS, UK

P. E. GoretzkiSurgical Department 1, Lukaskrankenhaus Neuss,Preussenstr. 84,41456 Neuss, Germany

M. M. HermannDepartment of Surgery, Kaiserin-Elisabeth-Spital,Medical University of Vienna,Huglgasse 1–3,Vienna, Austria

J. KußmannClinic for Endocrine Surgery, Schön Klinik Hamburg–Eilbek,Dehnhaide 120,22081 Hamburg, Germany

C. NiesDepartment for General and Visceral Surgery,Niels-Stensen-Kliniken, Marienhospital Osnabrück,Bischofsstr. 1,49074 Osnabrück, Germany

Langenbecks Arch Surg (2011) 396:639–649DOI 10.1007/s00423-011-0774-y

interventions. Additionally, minimally invasive techniqueshave been developed and gained wide usage. Thesecircumstances demanded a revision of the guidelines.Methods Based on a review of relevant recent guidelinesfrom other groups and additional literature, unpublisheddata, and clinical experience, the German Association ofEndocrine Surgeons formulated new recommendations onthe surgical treatment of benign thyroid diseases. Theseguidelines were developed through a formal expert consen-sus process and in collaboration with the German societiesof Nuclear Medicine, Endocrinology, Pathology, andPhoniatrics & Pedaudiology as well as two patientorganizations. Consensus was achieved through severalmoderated conferences of surgical experts and representa-tives of the collaborating medical societies and patientorganizations.Results The revised guidelines for the surgical treatmentof benign thyroid diseases include recommendationsregarding the preoperative assessment necessary todetermine when surgery is indicated. Recommendationsregarding the extent of resection, surgical techniques, andperioperative management are also given in order tooptimize patient outcomes.Conclusions Evidence-based recommendations for the sur-gical treatment of benign thyroid diseases have beencreated to aid the surgeon and to support optimal patient

care, based on current knowledge. These recommendationscomply with the Association of the Scientific MedicalSocieties in Germany requirements for S2k guidelines.

Keywords Benign goiter . Thyroid disorders . Surgery .

Diagnostic procedures . Surgical techniques . Postoperativecare

Introduction

Benign thyroid disorders are among the most commondiseases in Germany, affecting about 15 million people andleading to more than 100,000 thyroid surgeries annually[10].

The German Surgical Society published its first guide-lines for the surgical treatment of benign goiter in 1998 [3].Since those recommendations appeared more than a decadeago, abundant data have been published and experience wasgained regarding benign thyroid disorders and theirmanagement (for recent reviews, see, e.g., [1, 34, 35, 38,39, 44, 46, 56]). These data and this experience signifi-cantly shifted surgical strategy towards more radicalinterventions. Additionally, minimally invasive techniqueshave been introduced and have become widely used. Thesecircumstances demanded an updating of the guidelines.

J. SchabramDepartment of Surgery, St. Josefs Hospital,Liebigstr. 24,35338 Giessen, Germany

P. SchabramRatajczak & Partners—Solicitors—Berlin•Cologne•Essen•Freiburg•Meissen•Munich•Sindelfingen,Heinrich-von-Stephan-Str. 25,79100 Freiburg, Germany

C. ScheubaDivision of General Surgery, Department of Surgery,Medical University,Währinger Gürtel 18–20,1090 Vienna, Austria

D. SimonDepartment of General and Visceral Surgery, Bethesda Hospital,Heerstrasse 219,47053 Duisburg, Germany

T. SteinmüllerDepartment of Visceral and Endocrine Surgery,DRK-Kliniken Berlin-Westend,Spandauer Damm 130,14050 Berlin, Germany

A. W. TrupkaDepartment of Surgery,Kreiskrankenhaus Starnberg GmbH Oßwaldstr. 1,82319 Starnberg, Germany

R. A. WahlDepartment of Endocrine Surgery,Burgerhospital Frankfurt am Main e.V,Nibelungenallee 37–41,60318 Frankfurt, Germany

A. ZielkeDepartment of Surgery, Klinikum Offenbach GmbH,Starkenburgring 66,63069 Offenbach, Germany

A. BockischDepartment of Nuclear Medicine, University Hospital of Essen,Hufelandstr. 55,45122 Essen, Germany

W. KargesDivision of Endocrinology and Diabetes,RWTH University Hospital Aachen,Pauwelsstrasse 30,52074 Aachen, Germany

M. LusterDepartment of Nuclear Medicine, University of Ulm,Albert-Einstein-Allee 23,89081 Ulm, Germany

K. W. SchmidDepartment of Pathology, University Hospital of Essen,Hufelandstr. 55,45122 Essen, Germany

640 Langenbecks Arch Surg (2011) 396:639–649

The German Association of Endocrine Surgeons(Chirurgische Arbeitsgemeinschaft Endokrinologie[CAEK]) therefore undertook to develop a revised setof state-of-the-art, evidence-based, practical recommen-dations. This set of recommendations would be developedhrough a formal expert consensus process. In this task, theCAEK was assisted by four medical organizations, namely,the German Society of Nuclear Medicine, the GermanSociety of Endocrinology, the German Society ofPathology, and the German Society of Phoniatrics &Pedaudiology, as well as by two patient organizations,“Schmetterlinge e.V.” and “Ohne Schilddrüse Leben e.V.” It ishoped that the new guidelines will help surgeons tooptimize the quality and cost-effectiveness of care ofpatients with benign thyroid disorders. Before therecommendations are presented, however, the creationprocess will be described.

Creation process

The guidelines were formulated through the followingsteps:

Literature review and synopsis development The 1998German Surgical Society guidelines [3] and the results ofa literature review were used as starting points. A PubMedsearch with the key words “guidelines” + “thyroid” +“surgery” was conducted for the 2000–2010 period. Thesearch revealed 292 matches, but only a small fraction ofthe publications [6, 7] comprised evidence-based guidelinesaddressing thyroid surgery, and most matches were there-fore of limited value. Post-1998 original reports of clinicalstudies on surgical treatment of benign thyroid diseases andrecently published meta-reviews of this literature [1, 34, 35,38, 39, 44, 46, 56] also were consulted. It should be notedthat the original reports were predominantly retrospectiveanalyses (US Agency for Health Care Policy and Research[AHCPR] evidence level III) and only in exceptional caseswere randomized prospective studies (AHCPR evidencelevels I or II).

Synopses were prepared by topic comparing the 1998German Surgical Society recommendations to guidelinesfrom other groups and to meta-reviews. The major guide-lines used for comparison were those of the AmericanAssociation of Clinical Endocrinologists and the AssociazioneMedici Endocrinologi [4], the European Thyroid Association[37], the British Thyroid Association (http://www.british-thyroid-association.org/news/Docs/Thyroid_cancer_guidelines_2007.pdf), and, especially, the American ThyroidAssociation (ATA) [6, 7]. The ATA recommendations, whichcover the medical as well as the surgical treatment ofmalignant as well as benign thyroid disease, are the only

current guidelines based on methodical literature evaluationwith level of evidence assessment.

Draft manuscript development by the CAEK GuidelinesTask Force Based on the synopses, a first draft of theCAEK guidelines was developed. The manuscript wascirculated among the CAEK Guidelines Task Forcemultiple times for review and comment. In every round ofreview, the Task Force Coordinator (TJM) registered eachTask Force member’s opinions regarding all draft state-ments and recommendations as well as the member’ssuggestions for alternative positions or wording. Eachround of comments was integrated into succeeding draftsof the guidelines manuscript.

Five consensus conferences moderated by the TaskForce Coordinator were held in which the drafts and thecore statements were discussed in depth and internalevidence (unpublished studies, expert experience) wasconsidered. After the discussion of each topic, a vote wastaken, which usually resulted in agreement by more than75% of Task Force members. In seeking consensusregarding the recommendations, the Task Force emphasizedthe level of evidence, ethical aspects, patient preferences,clinical relevance, risk/benefit ratios, and applicability.

Finalization of draft manuscript with assistance of othermedical societies and patient organizations The manuscriptapproved by the Task Force after the five consensusmeetings was circulated to all Task Force members as wellas to representatives of the collaborating medical societiesand patient organizations enumerated above. The TaskForce members and representatives had the opportunity tocomment, object, and submit alternative proposals. All ofthese individuals then participated in a final consensusconference featuring a moderated discussion, voting on thecontroversial points, and a final vote on the entiremanuscript. All recommendations were accepted by “strongconsensus” (agreement of >95% of participants) or by“consensus” (agreement of >75% of participants).

CAEK membership review and approval of manuscript Themanuscript approved in the final consensus conferencewas circulated to all CAEK members, who were giventhe opportunity to object and submit suggestions oralternative proposals. Based on this CAEK memberfeedback, a final draft was prepared. This draft wasapproved by the CAEK General Assembly at its annualbusiness meeting held in Lodz on 28 November 2009and by the Board of Directors of the German Society forGeneral and Visceral Surgery. The German-languagemanuscript is available at the Association of theScientific Medical Societies in Germany website (http://www.awmf.org/leitlinien.html).

Langenbecks Arch Surg (2011) 396:639–649 641

Recommendations

Preamble

Benign thyroid diseases encompass all non-malignantalterations of the thyroid which are accompanied bydisorders of morphology, function, or both. The aim ofdiagnostic procedures in this setting is to clarify the natureof the thyroid disease and to describe all morphological andfunctional alterations, taking into account the therapeuticpossibilities. The indication for surgical treatment in agiven patient is based on the results of that individual’sdisease-specific examinations and localization proceduresand on consideration of any non-operative treatmentalternatives and possible complications of surgical proce-dures. The aim of surgical treatment is the safe and certainpermanent elimination of the underlying thyroid disease. Asa rule, the treatment necessitates additional procedure-specific diagnostic examinations to optimize the planningand execution of the operation, as well as perioperativefollow-up to record complications related to the surgery.Foremost among such complications are temporary orpermanent laryngeal function disorders secondary to nerveinjuries (e.g., to the recurrent laryngeal nerve) or temporaryor permanent parathyroid disorders (hypocalcemia, hypo-parathyroidism). Additional surgical risks are postoperativebleeding, potentially accompanied by respiratory distress;predominantly temporary postoperative swallowingdisorders; numbness in the area of the mobilized skinflap; and scar tissue development within the area of the skinincision. Increased operative risk is generally a given when thehistory includes prior neck surgery. Moreover, for neckoperations involving large goiters that extend beyond theanatomical thyroid bed, e.g., into the area of the perivascularsheath or into the upper mediastinum (sternotomy)—corresponding risks must be considered.

For each procedure, the patient information and informedconsent should include an individualized appraisal of the risksas well as explanations regarding the pros and cons of theparticular therapeutic options and the rationale for surgicaltreatment. The information and informed consent also shoulddescribe intraoperative circumstances that could require achange in the preoperatively defined surgical plan, the risk ofrecurrence of the thyroid disorder, and the postoperative care.

Preoperative diagnostic procedures

R1 Preoperative laryngoscopic examination of vocal cordfunction is recommended in general. Especially inpatients with clinical dysphonia or after previous surgeryin the neck area, such examination is indispensable.

R2 To exclude concomitant hyperparathyroidism, theserum calcium concentration should be determined

preoperatively. An increased calcium concentrationrequires further preoperative evaluation.

R3 Determination of the basal serum calcitonin concentra-tion prior to thyroid surgery allows the early detection ofmedullary thyroid carcinoma. In the event of anincreased basal calcitonin level, a stimulation test shouldbe performed for further diagnostic differentiation.

R4 Fine needle aspiration cytology (FNAC) is recommendedif a non-surgical approach is under consideration, if thethyroid nodes are suspicious on imaging, if there issuspicion of malignancy in the neck lymph nodes, or if alocally invasive growth is present, for which a cytologicaldiagnosis is of importance for planning the operation.

Patient’s history and clinical assessment

The patient’s medical history, including familial predisposi-tions and the clinical assessment, aids in determination of theindication, in risk appraisal, and in operation planning. Thehistory also helps clarify the risk of malignancy.

Neck ultrasound

Ultrasound examination of the neck area is part of theroutine diagnosis of thyroid diseases [35]. Ultrasonographyprovides information on the size and the structure of theorgan and detects signs of malignancy, especially in thepresence of nodular lesions or extrathyroidal pathologicalchanges such as enlarged lymph nodes [17, 18]. A sono-graphic examination performed by the surgeon may behelpful for planning the resection.

Scintigraphy

In addition to ultrasonography, thyroid scintigraphy isrecommended for the planning and execution of theoperation, for example:

1. For the functional assessment of nodes and to differentiatebetween a focal or disseminated autonomy

2. In case of suspected intrathoracic or dystopic goiter3. Before surgery for a recurrent disease

Additional imaging

For planning of the surgical procedure, additional imagingby magnetic resonance imaging or computed tomographywithout contrast enhancement is recommended in cases of:

1. Suspicion of retrovisceral, retrosternal, or intrathoracicgoiter based on clinical or imaging (ultrasound/scintig-raphy) findings or both

642 Langenbecks Arch Surg (2011) 396:639–649

2. Tracheal deviation/stenosis3. Local infiltrative processes

Laryngoscopy

Preoperative laryngoscopic examination of vocal cord func-tion is recommended. Especially in patients with clinicaldysphonia and after previous surgery in the neck area,laryngoscopy is indispensable and can be supplemented byfurther examinations. These studies serve, on the one hand, asquality control and, on the other hand, to confirm any pre-existing impairments, which must be factored into thedecision-making regarding the indication for surgery and intothe planning of any surgical intervention [16, 40, 47].

Calcium

To exclude concomitant hyperparathyroidism, serum calciumconcentration should be determined preoperatively. Anincreased calcium concentration requires further preoperativeevaluation.

Calcitonin

The determination of the basal serum calcitonin concentra-tion facilitates the early detection of medullary thyroidcarcinoma and is recommended in particular before surgeryfor nodular thyroid diseases [8, 24, 42].

Commercially available calcitonin tests have assay aswell as age- and gender-specific reference ranges. Theinterpretation of the test result should also take into accountfactors influencing calcitonin levels, such as renal failureand drug interactions.

In cases of increased basal calcitonin, a calcitonin stimula-tion test, e.g., with pentagastrin or calcium, is recommendedfor further differential diagnosis, particularly between C-cellhyperplasia and medullary thyroid carcinoma [9].

FNAC

FNAC of a suspicious thyroid node is appropriate fordefining the risk of malignancy [27]. This procedure isparticularly indicated if non-surgical treatment of the lesionis being considered. The informative value of FNAC islimited to the sampled node. FNAC is not suitable for theexclusion of micro-carcinoma. With respect to encapsulatedfollicular tumors, FNAC cannot distinguish between follicularadenoma and carcinoma.

For planning and execution of the surgical procedure,FNAC is recommended in case of:

1. Suspicious thyroid nodes based on clinical or imagingresults or both

2. Suspicious neck lymph nodes3. Locally invasive growth

A FNAC finding of a follicular neoplasm or otherevidence or proof of malignancy is an indication forsurgery.

Definition of resections

1. Enucleation: excision of a node along its capsule2. Node excision: resection of a node along with a small

margin of normal thyroid tissue3. Resection of the isthmus: resection of the pretracheal

thyroid tissue4. Subtotal lobe resection: partial resection of a thyroid

lobe leaving a tissue remnant of 1 to 4 mL5. Near-total lobe resection: partial resection of a thyroid

lobe leaving a tissue remnant of less than 1 mL6. Hemithyroidectomy/lobectomy: complete resection of

a thyroid lobe including the thyroid isthmus and thepyramidal lobe

7. Hartley–Dunhill resection: hemithyroidectomy pluscontralateral subtotal resection leaving a tissue remnantof 1 to 4 mL located at the upper pole or posteriorly

8. Bilateral subtotal resection: partial resection of boththyroid lobes leaving a bilateral tissue remnant of 1 to4 mL each

9. Near-total thyroidectomy: the almost complete resec-tion of the thyroid leaving a total tissue remnant ofless than 2 mL

10. (Total) thyroidectomy: the complete resection ofboth thyroid lobes including the thyroid isthmusand the pyramidal lobe without leaving a tissueremnant

Procedures 3–10 listed above are partially or completelyextracapsular resections. Procedures 1 and 2 are intra-capsular resections in which the thyroid tissue is removedwhile the thyroid capsule is largely left behind. Proceduresother than those listed here are defined in the surgical reportby specifying the location and amount of thyroid remnant.

Indications for surgery

R5 The indications for surgery in benign thyroid diseasesare suspicion of malignancy, local discomfort, dys-topic localization, or hyperthyroidism that cannot becontrolled with conservative measures. When deter-mining the indication, alternative treatment optionssuch as radioiodine therapy should be considered.

R6 The indications for surgery of recurrent goiter aresimilar to those for primary surgery of goiter, but theincreased risk of complications should particularly betaken into account.

Langenbecks Arch Surg (2011) 396:639–649 643

Solitary nodules

Nodules with signs of malignancy A nodule with signs ofmalignancy is an indication for surgery.

Nodules without signs of malignancy In the absence ofsigns of malignancy, solitary nodules can be treatedsurgically or medically or can be observed, depending ontheir size and clinical symptoms [10, 19].

Toxic nodules Solitary toxic nodules (unifocal functionalautonomy, “hot” nodule) can be surgically removed, treatedwith radioiodine ablation, or observed, depending on thesize, clinical symptoms, and laboratory test results (thyroid-stimulating hormone, TSH). When a toxic nodule issymptomatic and contraindications for surgery are absent,surgical resection is an effective treatment option with lowrisks, regardless of the nodule size.

Cystic lesions Cystic lesions with signs of malignancy arean absolute indication for surgery. When there are localsymptoms but no signs of malignancy, either surgery or atrial of conservative treatment are a valid approaches. Incase of asymptomatic cysts without signs of malignancy, aprimary “watch and wait strategy” or a conservativetreatment is recommended. In the event of recurrencefollowing conservative treatment, a surgical intervention isfrequently indicated.

Multinodular goiter

Depending on the size, clinical symptoms, and laboratorytest results (TSH), multinodular goiter can be treatedsurgically, with radioiodine, or medically or can beobserved. Indications for surgery are signs of malignancyor necessity for exclusion of malignancy, local discomfort,or subclinical or manifest thyrotoxicosis.

In the case of extended retrosternal goiter or dystopiclocalization, surgery may be indicated even in theabsence of goiter symptoms or of signs suggestive ofmalignancy.

Immunogenic thyrotoxicosis—Graves’ disease

If, during primary conservative therapy, the indication foran ablative treatment arises, surgery and radioiodinetherapy are viable alternatives. A surgical approach ispreferred with varying degrees of urgency depending on theindividual situation or symptoms in cases of thyroidgrowth, endocrine ophthalmopathy, suspected malignancy,(serious) side effects and intolerance of thyrostatic therapy,

refractory or severe hyperthyroidism, or rejection of radio-iodine therapy by the patient [12, 46].

In children and adolescents, surgery is the treatment ofchoice for definitive cure.

Iodine-induced thyrotoxicosis

Iodine-induced thyrotoxicosis or other forms of thyrotoxiccrisis may demand surgery, even if the patient is hyperthy-roid, when these conditions are uncontrolled and emergentor refractory to conservative treatment or when suchtreatment causes severe side effects [25].

Thyroiditis

In and of itself, the Hashimoto’s thyroiditis type ofautoimmune thyroiditis is not an indication for surgery.Indications arise when there are signs of malignancy and, ifappropriate, when local symptoms are not controlled bymedical treatment.

In view of its frequent spontaneous remission, subacutegranulomatous thyroiditis (de Quervain’s thyroiditis) rarelypresents an indication for surgery. However, surgery isindicated when signs of malignancy are apparent andpossibly when recurrent pain necessitates repeated gluco-corticoid therapy.

In the case of the rare Riedel’s (invasive fibrous)thyroiditis, signs of malignancy or mechanical symptoms(tracheal obstruction) can require surgery [26].

Recurrent goiter

Indications for surgery are the same as stated in the sections“Solitary nodules” to “Thyroiditis”. However, the increasedrisk of complications and the possibility of preexistinginjuries, particularly of the recurrent laryngeal nerve, of theparathyroids, or of both, must be taken into account.

Resection procedures

R7 In most cases, when thyroid nodules are suspected tobe malignant, a hemithyroidectomy should be per-formed, principally to obviate the need for a secondsurgical procedure should malignancy be verified onlypostoperatively.

R8 (Total) thyroidectomy or near-total thyroidectomyshould be the goal in the event of complete nodulartransformation of the thyroid tissue or of multiplenodules in both thyroid lobes.

R9 When surgery is indicated in Graves’ disease, a (total)thyroidectomy should always be considered.

644 Langenbecks Arch Surg (2011) 396:639–649

Solitary nodules

In the case of solitary nodules without signs of malignancy,a node excision with resection of a small margin of normalthyroid tissue, a subtotal lobe resection, or a hemithyroidec-tomy is advised, depending on the size and the intrathyroidallocalization of the nodule.

When solitary nodules show signs of malignancy, ahemithyroidectomy should be performed in almost allcases. The rationale is to obviate the need for anipsilateral re-operation and thereby to eliminate theincreased risk of perioperative complications associatedwith such procedures [10].

Multinodular goiter

In the past, a high recurrence rate (up to 40%) was observedfollowing tissue-sparing thyroid resections [1, 34]; there-fore, (total) thyroidectomy has become widely used forbilateral multinodular goiter in recent years [50].

The traditionally preferred approach of preservingnormal-appearing thyroid tissue can be considered inindividual cases as a resection strategy that is guided bymorphology and preserves thyroid function. Leavingbehind thyroid nodules should be avoided or should bejustified by special circumstances because these lesionsare the main cause of recurrences needing re-operation.On the other hand, the risk of surgery-related complica-tions increases with the extent of the resection. For thesereasons, the choice of the extent of resection entailsbalancing the potential disease-related risks against thepotential surgical risks in each individual case. In thepresence of complete nodular transformation of thethyroid tissue or multiple nodes in both thyroid lobes,either (total) thyroidectomy or near-total thyroidectomyshould be the aim.

Tissue-sparing procedures must be justified.

Surgical treatment of hyperthyroidism

In the surgical treatment of hyperthyroidism, preoperativeachievement of a euthyroid state should be the aim. Amanifestly hypothyroid metabolic condition resultingfrom thyrostatic medication should be avoided since thiscondition may be associated with disorders of primaryhemostasis [30].

The surgical approach to unifocal autonomy in thepresence of hyperthyroidism is equivalent to the approachto solitary nodules without signs of malignancy. Formultifocal autonomy in the presence of hyperthyroidism—a disorder analogous to multinodular goiter withouthyperthyroidism but with bilateral multinodular transfor-

mation—(total) thyroidectomy or near-total thyroidectomyis preferred [39, 46].

When surgery is indicated for Graves’ disease, (total)thyroidectomy should be the aim. This procedure ispreferred, particularly on immunological grounds, if aco-existing active endocrine ophthalmopathy is presentand, on general grounds, to avoid persistence orrecurrence [46]. For moderate or severe endocrineophthalmopathy, perioperative corticosteroid administra-tion should be considered.

Recurrent goiter

The aim of the surgical strategy for recurrent goiter is theelimination of the nodule or other areas of tissue with themost suspicious pathology, the prevention of anotherrecurrence, as well as the preservation of the function ofthe recurrent laryngeal nerve and the parathyroid glands.The most severely affected side should be addressed first.Contralateral resection should only be carried out if,following resection of the primary side, the anatomicaland functional preservation of the recurrent laryngeal nervecan be anticipated [11].

Surgical technique

R10 Careful, i.e., non-skeletonizing, vascularization-preserving preparation of the recurrent laryngealnerve reduces the risk of injury and should be afundamental rule in both primary surgery andsurgery for recurrence. The visible anatomic courseof the nerve before and after resection should bedocumented.

R11 In every thyroid resection with a possibility ofimpairing the anatomical or functional integrity ofthe parathyroid glands, the aim is to ensure thatvulnerable parathyroid glands are reliably identifiedand preserved in situ in a well-vascularized state.Parathyroid glands that are reliably identified asdevascularized or that have been accidentally re-moved should be cut into small pieces and auto-transplanted into the neck muscles.

R12 An intraoperative frozen section is recommended inthe event of pre- or intraoperative suspicion ofmalignancy. If during surgery of a node with signsof malignancy no intraoperative frozen section ispossible, the patient must be informed of thiscircumstance and its potential consequences, e.g.,completion thyroidectomy.

R13 For all minimally invasive techniques, the sameprinciples on the determination of the indication,

Langenbecks Arch Surg (2011) 396:639–649 645

avoidance of complications, and choice of resection typeapply as that with conventional surgical procedures.

Preservation of the recurrent laryngeal nerve

Functional disorders of the recurrent laryngeal nerve areassociated with impairments of phonation, swallowing, andbreathing. Bilateral pareses of the recurrent laryngeal nervefrequently necessitate tracheotomy.

The risk of damaging the recurrent laryngeal nerve isdetermined by the extent of the resection and the individualanatomical variant of the nerve course. The delicate, i.e.,the non-skeletonizing, vascularization-preserving prepara-tion of the recurrent laryngeal nerve reduces the risk ofinjury and should, as a general rule, be carried out in bothprimary surgery and surgery for recurrence [5, 28]. Thevisible anatomic course of the nerve should be documentedbefore and after resection.

As an exception to this need for documentation,identification of the recurrent laryngeal nerve may beomitted if the anterior resection plane is located ventral ofthe anterior lamella at a safe distance from the nerve course[49]. Non-identification of the recurrent laryngeal nervemust be justified and documented.

Intraoperative neuromonitoring does not replace butrather serves only as a complement to the gold standardof visual nerve identification [14, 21, 31, 51, 53]. Neuro-monitoring can confirm the identity of the recurrentlaryngeal nerve. Additionally, by providing periodictransfer signal assessment, this procedure can renderprobable the functional preservation of the recurrentlaryngeal nerve. To record the entire course of therecurrent laryngeal nerve, it is necessary to stimulatethe vagal nerve before and after the resection. The safestmethod to differentiate between action potentials andartifacts is to record electromyograms. A significantreduction of the risk of recurrent nerve injuries byapplication of neuromonitoring has so far only beendemonstrated in redo interventions [13, 31]. The mainbenefit is the avoidance of bilateral nerve damage.

Preservation of the external branch of the superiorlaryngeal nerve

The external branch of the superior laryngeal nerve over-crosses, crisscrosses, or undercrosses the superior pole vesselsin close proximity to the superior thyroid pole [25, 33, 52].Damage to the nerve branch can result in dysphonia withimpaired vocal performance in the forms of a reducedfrequency range and rapid fatigue. In light of available data,a routine intraoperative identification of the nerve branchcannot be justified [36]. The specific anatomy should be

taken into account through careful preparation close to thecapsule of the upper thyroid pole.

Identification of the parathyroid glands

The need to protect the parathyroid glands during thyroidresection results from the subjective and objective con-sequences of hypoparathyroidism, which may significantlyimpair the quality of life [5]. Even today, a satisfactorysubstitute for parathyroid function is not always possible.The delayed effects of permanent hypoparathyroidism(impaired calcium and phosphate homeostasis, cataract,calcification of the basal ganglia, etc.) can be substantial.

The most common variants of the location of theparathyroid glands are described in numerous publications[2, 48, 55]. Because of the common blood supply of thethyroid and parathyroid glands via the inferior thyroidartery or superior thyroid artery, very careful dissectionmust be performed between the thyroid gland and theparathyroid glands to avoid compromising the blood flowto the latter, which is essential for their function [50]. Inevery thyroid resection that is associated with a potentialimpairment of the anatomical or functional integrity of theparathyroid glands, the aim is to ensure that vulnerableparathyroids are identified and preserved in situ in a well-vascularized state. Parathyroid glands that are reliablyidentified as devascularized or have been accidentallyremoved should be cut into small pieces and autotrans-planted into the neck muscles.

The surgical report should document the location ofthe preserved parathyroid glands as well as anyautotransplantation.

Approach to retrosternal/retromediastinal goiter

Retrosternal extension of a goiter into the posterior or anteriormediastinum or retrovisceral goiter require special attentionbecause of the increased risk of recurrent laryngeal nerveinjury caused by pulling the thyroid gland during mobilizationand because of the frequently altered course of the recurrentlaryngeal nerve secondary to these conditions [23]. Becauseits blood supply always derives from the neck, a pseudoen-dothoracic goiter or false endothoracic goiter, in contrast tothe rare true endothoracic goiter, very seldom requires apartial or complete sternotomy [56]. In case of a retrosternalgoiter, the aortic arch and right atrium are importantanatomical landmarks, which aid in the preoperative assess-ment of the need for sternotomy [23].

Intraoperative frozen section of thyroid tissue

The purpose of an intraoperative frozen section ofthyroid tissue is the intraoperative diagnosis of lesions

646 Langenbecks Arch Surg (2011) 396:639–649

suspicious for malignancy in order to avoid a two-stagecancer surgery with potential disadvantages for thepatient [43, 45]. The patient should be informed aboutthe methodological limitations of frozen section, inparticular, that with any frozen section analysis a defini-tive histopathological diagnosis may only be possible bypostoperative paraffin-embedded histology. The patientshould also be informed that a non-total thyroidectomymay require completion thyroidectomy.

If during surgery of a nodule with signs of malignancy nointraoperative frozen section is possible, the patient must beinformed of this circumstance and its potential consequences(e.g., completion thyroidectomy).

From a surgical point of view, intraoperative frozensection is recommended for the following indications:

1. Thyroid nodules that are suspicious for malignancybased on preoperative clinical, imaging, or cytolog-ical results

2. Intraoperative suspicion of malignancy of the thyroid orlymph nodes

3. Less-than-total thyroidectomy

Minimally invasive procedures

These procedures comprise a variety of cervical andextra-cervical access techniques intended to optimize thecosmetic result in the neck. Depending on the method,specific issues arise concerning informed consent.Results allowing a preliminary evaluation are so far onlyavailable for minimally invasive video-assisted surgery.According to current data, the risk of complications isnot increased [32, 41, 44]. Preconditions for performingminimally invasive procedures are an extensive experi-ence with conventional open thyroid surgery and appro-priate patient selection, for example, with respect tothyroid volume and node size. For all minimally invasivetechniques, the same principles apply to the determinationof the indication, avoidance of complications, and choiceof resection type as those that apply with conventionalsurgical procedures. The inclusion and exclusion criteriafor choosing a minimally invasive procedure versus aconventional procedure and for choosing between differ-ent minimally invasive techniques have not yet beenclearly defined.

Histological assessment of the surgical specimen

Proper histopathological examination of the surgical spec-imen should be performed without exception. Especially incases with signs of malignancy, a diagnosis within 48–72 his desirable to permit any required completion operation tobe carried out on a timely basis.

Postoperative monitoring and follow-up

R14 A check of vital signs and wound conditions isrequired within the first 8 h after thyroid resection.

R15 Postoperative laryngoscopic assessment of laryngealfunction is required and is used to record postoper-ative dysfunctions.

R16 The determination of serum calcium concentrationis recommended on the first and second postoper-ative days or whenever clinical symptoms arepresent.

Postoperative monitoring

Postoperative monitoring is performed to detect acutecomplications. In particular, a check of vital signs andwound conditions is required because of the risk ofpostoperative bleeding in approximately 1% of cases,predominantly within the first 8 h [15]. Such follow-upensures the timely performance of any necessary surgicalrevision and addresses the threat to life which is alwaysassociated with postoperative bleeding.

Postoperative assessment of laryngeal functionand approach in the event of dysfunction

Postoperative laryngoscopic assessment of laryngeal func-tion is required and is used to record postoperativedysfunction. Such evaluation permits the early initiationof any necessary therapeutic measures and is also anindispensable tool for quality assurance.

In the event of postoperative vocal cord dysfunction,further diagnostic evaluation and, if appropriate, therapy arerecommended. Patients with bilateral recurrent nervepareses are at a high risk of needing a tracheotomy. Thesepatients therefore require controlled inpatient monitoringand supportive measures until undisturbed respiration isestablished with or without tracheotomy.

Postoperative monitoring of parathyroid functionand approach in the event of dysfunction

Postoperative monitoring of serum calcium and PTHconcentration helps detect insufficient parathyroid hormonesecretion and allows the early initiation of substitutiontherapy. Such monitoring is also an important tool forquality assurance.

Serum calcium concentration should be measured on thefirst and second postoperative days or in the presence ofclinical symptoms. Early postoperative determination ofparathyroid hormone levels can provide information aboutthe expected severity of hypocalcemia [22, 54].

Langenbecks Arch Surg (2011) 396:639–649 647

The necessity, dose, and duration of calcium administrationand, if needed, vitamin D administration are based on theclinical symptoms and the serum calcium concentration.Because of the possible long-term consequences (e.g.,cataract, basal ganglia calcification), even an asymptomaticlong-term postoperative hypocalcemia should be treated.Regular laboratory monitoring is required to avoid dosageerrors and, if applicable, to allow for the patient to be weanedoff the treatment.

Postoperative monitoring of thyroid remnant morphology

In the event of relevant residual thyroid tissue, diagnosticimaging procedures to monitor the morphology arerecommended [38]. Any residual or recurrent nodes withgrowth or with signs of malignancy appearing duringfollow-up should be subjected to additional diagnosticprocedures and, possibly, to treatment.

Postoperative prophylaxis against recurrence and thyroidhormone substitution

Postoperative thyroid-specific drug therapy is used tomaintain a euthyroid metabolic state and in the presenceof residual thyroid tissue to prevent recurrence. Generally,individualized postoperative prophylaxis is initiated imme-diately regardless of the final pathological findings, aimingat a TSH level in the middle of the normal range.Depending on the expected thyroid function, the levothyr-oxine can be administered with or without iodine supple-mentation [20, 29, 34]. The medication requires regularmonitoring of thyroid function markers. To this end, testing4–6 weeks after surgery to assess the effectiveness of themedication has proven to be beneficial.

Conflicts of interest None.

References

1. Agarwal G, Aggarwal V (2008) Is total thyroidectomy the surgicalprocedure of choice for benign multinodular goiter? An evidence-based review. World J Surg 32:1313–1324

2. Akerstrom G, Malmaeus J, Bergstrom R (1984) Surgical anatomyof human parathyroid glands. Surgery 95:14–21

3. Anonymous (1998) Leitlinie zur Therapie der benignen Struma.In: Mitteilungen der Dt. Ges. f. Chirurgie. Stuttgart

4. Anonymous (2006) American Association of Clinical Endocrinolo-gists and Associazione Medici Endocrinologi medical guidelines forclinical practice for the diagnosis and management of thyroidnodules. Endocr Pract 12:63–102

5. Brauckhoff M, Gimm O, Weiss CL et al (2004) Multipleendocrine neoplasia 2B syndrome due to codon 918 mutation:

clinical manifestation and course in early and late onset disease.World J Surg 28:1305–1311

6. Cooper DS, Doherty GM, Haugen BR et al (2009) RevisedAmerican Thyroid Association management guidelines forpatients with thyroid nodules and differentiated thyroid cancer.Thyroid 19:1167–1214

7. Cooper DS, Doherty GM, Haugen BR et al (2006) Managementguidelines for patients with thyroid nodules and differentiatedthyroid cancer. Thyroid 16:109–142

8. Costante G, Meringolo D, Durante C et al (2007) Predictive valueof serum calcitonin levels for preoperative diagnosis of medullarythyroid carcinoma in a cohort of 5817 consecutive patients withthyroid nodules. J Clin Endocrinol Metab 92:450–455

9. Doyle P, Duren C, Nerlich K et al (2009) Potency and tolerance ofcalcitonin stimulation with high-dose calcium versus pentagastrinin normal adults. J Clin Endocrinol Metab 94:2970–2974

10. Dralle H (2007) Thyroid incidentaloma. Overdiagnosis andovertreatment of healthy persons with thyroid illness? Chirurg78:677–686

11. Dralle H, Pichlamayr R (1991) Decrease of risks in reoperation forbenign struma. Chirurg 62:169–175

12. Dralle H, Sekulla C (2004) Morbidity after subtotal and totalthyroidectomy in patients with Graves’ disease: the basis fordecision-making regarding surgical indication and extent ofresection. Z Ärztl Fortbild Qualitätssich 98(Suppl 5):45–53

13. Dralle H, Sekulla C, Haerting J et al (2004) Risk factors ofparalysis and functional outcome after recurrent laryngeal nervemonitoring in thyroid surgery. Surgery 136:1310–1322

14. Dralle H, Sekulla C, Lorenz K et al (2008) Intraoperativemonitoring of the recurrent laryngeal nerve in thyroid surgery.World J Surg 32:1358–1366

15. Dralle H, Sekulla C, Lorenz K et al (2004) Ambulatory and briefinpatient thyroid gland and parathyroid gland surgery. Chirurg75:131–143

16. Farrag TY, Samlan RA, Lin FR et al (2006) The utility ofevaluating true vocal fold motion before thyroid surgery.Laryngoscope 116:235–238

17. Frates MC (2008) Ultrasound in recurrent thyroid disease.Otolaryngol Clin North Am 41:1107–1116

18. Frates MC, Benson CB, Charboneau JW et al (2006) Managementof thyroid nodules detected at US: Society of Radiologists inUltrasound Consensus Conference statement. Ultrasound Q22:231–238, discussion 239–240

19. Gough J, Scott-Coombes D, Fausto Palazzo F (2008) Thyroidincidentaloma: an evidence-based assessment of managementstrategy. World J Surg 32:1264–1268

20. Grussendorf M, Vaupel R, Reiners C et al (2005) The LISA trial-a-randomized, double-blind, placebo-controlled four-arm study of1,000 patients with nodular goiter in Germany. Study design andfirst results of feasibility. Med Klin (Munch) 100:542–546

21. Hermann M, Hellebart C, Freissmuth M (2004) Neuromonitoringin thyroid surgery: prospective evaluation of intraoperativeelectrophysiological responses for the prediction of recurrentlaryngeal nerve injury. Ann Surg 240:9–17

22. Hermann M, Ott J, Promberger R et al (2008) Kinetics of serumparathyroid hormone during and after thyroid surgery. Br J Surg95:1480–1487

23. Huins CT, Georgalas C, Mehrzad H et al (2008) A newclassification system for retrosternal goiter based on asystematic review of its complications and management. Int JSurg 6:71–76

24. Karges W, Dralle H, Raue F et al (2004) Calcitonin measurementto detect medullary thyroid carcinoma in nodular goiter: Germanevidence-based consensus recommendation. Exp Clin EndocrinolDiabetes 112:52–58

648 Langenbecks Arch Surg (2011) 396:639–649

25. Kochilas X, Bibas A, Xenellis J et al (2008) Surgical anatomy ofthe external branch of the superior laryngeal nerve and its clinicalsignificance in head and neck surgery. Clin Anat 21:99–105

26. Lorenz K, Gimm O, Holzhausen HJ et al (2007) Riedel’s thyroiditis:impact and strategy of a challenging surgery. Langenbecks Arch Surg392:405–412

27. Lundgren CI, Zedenius J, Skoog L (2008) Fine-needle aspirationbiopsy of benign thyroid nodules: an evidence-based review.World J Surg 32:1247–1252

28. Machens A, Holzhausen HJ, Thanh PN et al (2003) Malignantprogression from C-cell hyperplasia to medullary thyroid carcinomain 167 carriers of RET germline mutations. Surgery 134:425–431

29. Mann B, Buhr HJ (1998) Surgical therapy of benign thyroid glanddiseases. Zentralbl Chir 123:2–10

30. Marongiu F, Cauli C, Mariotti S (2004) Thyroid, hemostasis andthrombosis. J Endocrinol Investig 27:1065–1071

31. Mazal W (2003) Dissection of the recurrent laryngeal nerve withneuromonitoring—forensic aspects. Eur Surg 35:268–271

32. Miccoli P, Minuto MN, Ugolini C et al (2008) Minimally invasivevideo-assisted thyroidectomy for benign thyroid disease: anevidence-based review. World J Surg 32:1333–1340

33. Mishra AK, Temadari H, Singh N et al (2007) The externallaryngeal nerve in thyroid surgery: the ‘no more neglected’ nerve.Indian J Med Sci 61:3–8

34. Moalem J, Suh I, Duh QY (2008) Treatment and prevention ofrecurrence of multinodular goiter: an evidence-based review of theliterature. World J Surg 32:1301–1312

35. Morris LF, Ragavendra N, Yeh MW (2008) Evidence-basedassessment of the role of ultrasonography in the management ofbenign thyroid nodules. World J Surg 32:1253–1263

36. Morton RP, Whitfield P, Al-Ali S (2006) Anatomical and surgicalconsiderations of the external branch of the superior laryngealnerve: a systematic review. Clin Otolaryngol 31:368–374

37. Paschke R, Reiners C, Fuhrer D et al (2005) Recommendations andunanswered questions in the diagnosis and treatment of thyroidnodules. Opinion of the Thyroid Section of the German Society forEndocrinology. Dtsch Med Wochenschr 130:1831–1836

38. Phitayakorn R, Mchenry CR (2008) Follow-up after surgery forbenign nodular thyroid disease: evidence-based approach. World JSurg 32:1374–1384

39. Porterfield JR Jr, Thompson GB, Farley DR et al (2008) Evidence-based management of toxic multinodular goiter (Plummer’s disease).World J Surg 32:1278–1284

40. Randolph GW, Kamani D (2006) The importance of preoperativelaryngoscopy in patients undergoing thyroidectomy: voice, vocalcord function, and the preoperative detection of invasive thyroidmalignancy. Surgery 139:357–362

41. Schabram J, Vorlander C, Wahl RA (2004) Differentiatedoperative strategy in minimally invasive, video-assisted thyroidsurgery results in 196 patients. World J Surg 28:1282–1286

42. Scheuba C, Kaserer K, Weinhausl A et al (1999) Is medullarythyroid cancer predictable? A prospective study of 86 patientswith abnormal pentagastrin tests. Surgery 126:1089–1095,discussion 1096

43. Schmid KW, Ladurner D (1997) Intraoperative diagnostic frozensection of the thyroid gland. Pathologe 18:98–101

44. Sgourakis G, Sotiropoulos GC, Neuhauser M et al (2008)Comparison between minimally invasive video-assisted thyroid-ectomy and conventional thyroidectomy: is there any evidence-based information? Thyroid 18:721–727

45. Sheu S-Y, Frilling A, Betzler M et al (2005) Der intraoperativeGefrierschnitt der Schilddrüse - Indikation, Verlässlichkeit, Limit-ierungen. Viszeralchirurgie 40:174–179

46. Stalberg P, Svensson A, Hessman O et al (2008) Surgicaltreatment of Graves’ disease: evidence-based approach. World JSurg 32:1269–1277

47. Steurer M, Passler C, Denk DM et al (2002) Advantages ofrecurrent laryngeal nerve identification in thyroidectomy andparathyroidectomy and the importance of preoperative andpostoperative laryngoscopic examination in more than 1000nerves at risk. Laryngoscope 112:124–133

48. Thompson NW, Eckhauser FE, Harness JK (1982) The anatomyof primary hyperparathyroidism. Surgery 92:814–821

49. Thomusch O, Machens A, Sekulla C et al (2000) Multivariateanalysis of risk factors for postoperative complications in benigngoiter surgery: prospective multicenter study in Germany. World JSurg 24:1335–1341

50. Thomusch O, Sekulla C, Dralle H (2003) Is primary totalthyroidectomy justified in benign multinodular goiter? Results ofa prospective quality assurance study of 45 hospitals offeringdifferent levels of care. Chirurg 74:437–443

51. Thomusch O, Sekulla C, Machens A et al (2004) Validity of intra-operative neuromonitoring signals in thyroid surgery. LangenbecksArch Surg 389:499–503

52. Timmermann W, Hamelmann WH, Meyer T et al (2002)Identification and surgical anatomy of the external branch of thesuperior laryngeal nerve. Zentralbl Chir 127:425–428

53. Timmermann W, Hamelmann WH, Thomusch O et al (2004)Effectiveness and results of intraoperative neuromonitoring inthyroid surgery. Statement of the Interdisciplinary Study Group onIntraoperative Neuromonitoring of Thyroid Surgery. Chirurg75:916–922

54. Trupka A, Sienel W (2002) Autotransplantation of at least oneparathyroid gland during thyroidectomy in benign thyroid diseaseminimizes the risk of permanent hypoparathyroidism. ZentralblChir 127:439–442

55. Wang C (1976) The anatomic basis of parathyroid surgery. AnnSurg 183:271–275

56. White ML, Doherty GM, Gauger PG (2008) Evidence-based surgicalmanagement of substernal goiter. World J Surg 32:1285–1300

Langenbecks Arch Surg (2011) 396:639–649 649