Total Compared with Subtotal Thyroidectomy in BenignNodular Disease: Personal Series and Review ofPublished ReportsGiuseppe Pappalardo,1 Antonio Guadalaxara,1 Fabrizio Maria Frattaroli,1 Giovanni Illomei1 andPaolo Falaschi2

From the 12nd Surgical Clinic - Policlinico Umberto I, University of Rome “La Sapienza”, Italy and 2Department of InternalMedicine, 2nd University of Naples, Italy

Eur J Surg 1998; 164: 501–506

ABSTRACTObjective: To evaluate the outcome after total and subtotal thyroidectomy for the treatment of single and multinodular goitresin two comparable groups of patients.Design: Prospective randomised study.Setting: University hospital, Italy.Subjects: 141 Patients operated on for benign goitre from 1975–85.Interventions: 69 Patients were randomised to have total thyroidectomy and 72 subtotal thyroidectomy by standard techniques.Main outcome measures: Temporary or permanent palsy of the recurrent laryngeal nerve, temporary or permanent hypo-parathyroidism, recurrence of the goitre, and the incidence of iatrogenic injuries after completion thyroidectomy.Results: Patients were followed up for a median of 14.5 years (range 10–21). After total thyroidectomy 2 patients (3%)developed temporary palsy of the recurrent laryngeal nerve but there were no permanent lesions; and 24 (35%) developedtemporary and 2 (3%) permanent hypoparathyroidism. After subtotal thyroidectomy 2 (3%) developed temporary and 1 (1%)permanent palsy of the recurrent laryngeal nerve; and 13 (18%) developed temporary and 1 (1%) permanent hypopara-thyroidism. In addition, there were 10 recurrent goitres (14%). After completion thyroidectomy (n = 9) there were 2 cases oftemporary and 1 of permanent palsy of the recurrent laryngeal nerve, and 2 cases of temporary and 2 of permanenthypoparathyroidism.Conclusion: Total thyroidectomy is the procedure of choice for the treatment of benign nodular goitre.

Key words: multinodular goitre, total thyroidectomy, subtotal thyroidectomy, goitre recurrences, complications.

INTRODUCTION

The surgical treatment of benign thyroid disease is stillcontroversial. Except for single hyperfunctioningadenomas, which can be successfully treated bylobectomy (20), subtotal and total thyroidectomy arenow the surgical options available for all other thyroiddiseases. Despite numerous studies on operativestrategies, we know of no clear evidence about whichof these two options is best.

Many authors (3, 12, 22) favour the subtotal proce-dure in the treatment of benign multinodular disease,because of its lower incidence of iatrogenic injuries(recurrent nerve palsy and hypoparathyroidism), andthe supposed postoperative autonomous euthyroidstatus. Other authors advocate total thyroidectomy(8, 17, 19, 27), because the incidence of iatrogenicinjuries is similar to the subtotal procedure (8). Theincidence of permanent recurrent laryngeal nerveinjuries after the total and subtotal procedures variesfrom 0–1% (12, 8) and from 0–1.3%, respectively

(8, 26). The incidence of permanent hypoparathyroid-ism ranges from 0–3.8%, and from 0–0.2%, respec-tively (12, 8). Recurrence that requires further resec-tion is a relevant factor in choosing the operation.Even in the case of apparent single colloid nodulesthere is a basic alteration to the entire gland, which issusceptible to recurrence in the parenchymal remnantafter partial excision, under thyrotropic stimulus(28, 30, 37, 40). Alternating phases of cellular hyper-plasia and colloid involution bring about nodularevolution in response to inadequate hormonogenesis,as the residual parenchyma has the same character-istics as the excised portion of gland (8, 37). Teuscheret al. (37) have shown that the development of agoitre is at least in part affected by local controlfactors which are independent of both thyroidstimulating hormone (TSH) and hypothalamic-pitui-tary feedback, and consequently not inhibited bysuppression with L-thyroxine. Reported recurrencerates after subtotal resection range from 0–43% (3, 8)(Table I). Suppressive doses of L-thyroxine seem to

1998 Scandinavian University Press.ISSN 1102–4151 Eur J Surg 164

ORIGINAL ARTICLE

reduce the number of recurrences rather than preventthem.

A significantly higher incidence of recurrence wasfound when the follow-up was by ultrasonographyrather than simple clinical examination (4, 5, 14, 16).

The aim of this study was to evaluate the outcome ofthe two operations in the treatment of benign nodularthyroid diseases in two comparable randomised groupsof patients, operated on by the same surgeons andfollowed up for at least 10 years.

PATIENTS AND METHODS

Between 1975 and 1985 we did 141 thyroidectomies inpatients with benign goitres. We included in the studyunilateral and bilateral multinodular euthyroid goitres.Patients with Graves’ disease, Plummer disease,thyroiditis, hyperfunctioning single adenoma, or cancerwere excluded. The patients were randomly assigned tohave total thyroidectomy (n = 69) or subtotal thyroid-ectomy (n = 72).

We thought that a 10 year follow-up was necessaryto evaluate recurrence rate of subtotal resection so thelast thyroidectomies included in this study were done in1985. The median follow-up was 14.5 years (range 10–21).

The two groups were comparable as regards age(median 48 years, range 25–67, compared with 50,range 27–70) and sex (49 women and 20 men com-pared with 51 women and 21 men). Table II shows theindications for operation. Thyroidectomies were doneby the same group of surgeons according to a standardtechnique. Recurrent laryngeal nerves were isolatedbilaterally and the blood supply of the inferior para-thyroid glands was preserved by ligating individualbranches of the inferior thyroid arteries next to theparenchyma. In the subtotal group lobectomy was donewith contralateral subtotal resection leaving 3–5 g(about 1.5–2 cm3) on the less affected side. Totalthyroidectomy comprised extracapsular removal of thethyroid lobes and the pyramidal lobe, with preservationof the parathyroid glands, recurrent laryngeal nerves,and the external branches of the upper laryngeal nerves

as for the subtotal procedure. The integrity of the vocalcords was evaluated preoperatively and after extuba-tion by the anaesthetist. A further examination wasmade before discharge from hospital by an otolaryn-gologist in all patients with dysphonia.

In the subtotal group the rate of injuries to therecurrent nerve, hypoparathyroidism, and recurrenceswere the only variables evaluated. Permanent injury tothe recurrent nerve was considered as palsy of the vocalcord diagnosed by an otolaryngologist that lasted formore than six months postoperatively. If it lasted lessthan six months it was temporary. Temporary hypo-parathyroidism was defined as a fall in the serumcalcium concentration (less than 2.1 mmol/L) correctedaccording to the serum albumin concentration, andpermanent hypoparathyroidism as the need for oralvitamin D and calcium six months after operation tocorrect low serum calcium concentrations. We diag-nosed a recurrence when physical examination orfollow-up ultrasound scan showed nodular involve-ment or an enlargement of the residual thyroidremnant.

Serum calcium concentrations were measured pre-operatively in every patient and on the first and thirdpostoperative day. All patients were discharged takingL-thyroxine 1.5–2.25�g/kg body weight daily. Thedose of L-thyroxine was subsequently adjusted depend-ing on the concentration of circulating TSH. Higherdoses of L-thyroxine were prescribed for patients whohad subtotal resections (TSH <0.8 mU/L) and lowerdoses to patients who had total thyroidectomy and toolder and postmenopausal patients with the risk of

Table I.Reported recurrence rates (%) after subtotal thyroidectomy

Recurrence rate (%)

First author Year Reference numberPostoperativethyroxine

No postoperativethyroxine

Mean duration offollow-up (years)

Jarnerot 1973 18 1.5 15 not statedBerchtold 1983 3 12 42 not statedGeerdsen 1986 14 9.5 11.3 9Anderson 1990 2 5 43 10Campana 1992 8 0 10.7 not statedBistrup 1994 6 14.5 21.8 9

Table II. Indications for operation for multinodulargoitre

Data are expressed as number (%) of patients.

Thyroidectomy

Total(n = 69)

Subtotal(n = 72)

Bilateral 55 (80) 53 (74)Unilateral 14 (20) 19 (26)

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iatrogenic osteoporosis. Each patient was followed upat 45 days, 6 months, and then every year and hadserum calcium assay, and measurement of parathyroidhormone, triiodothyronine (T3), thyroxine (T4) andTSH concentrations at 3 and 6 months and then everyyear. Thyroid ultrasonography was done every 6months after subtotal resection. If recurrence wassuspected clinically and ultrasonographically, a131Iscan was done.

In cases of recurrence completion thyroidectomywas the procedure indicated.

RESULTS

No patient died and there were no bilateral injuries tothe recurrent laryngeal nerves, no need for earlyreoperation, and no difference in the postoperativestay in hospital (median 3 days, range 2–4 days). Nopatients were lost to follow-up. Iatrogenic lesions areshown in Table III. One patient had a mild tetanic crisisthat resolved promptly after intravenous calciumgluconate.

All patients were followed-up after 10–21 years(median 14.5 years). The serum TSH concentrationwas suppressed in all patients as the compliance withtaking thyroxine was good. Ten patients in the subtotalgroup developed recurrences (14%) (Table IV).

There was a good correlation between clinicalexamination and ultrasound study in patients whodeveloped recurrences. No malignant transformationwas found in the recurrences. Nine of 10 patients (90%)with recurrences had completion thyroidectomy after7–15 years (median 10.5); one patient refused opera-tion and is being treated medically. The incidence ofcomplication after completion thyroidectomy washigher than after primary total thyroidectomy (TableV).

DISCUSSION

It is difficult to evaluate the results of thyroid surgeryfor benign disease mainly because of the long follow-up required for a complete assessment of the outcomewhen there may be a 20–30 year delay beforerecurrence (20). Our results showed a similar incidenceof temporary and permanent injuries to the recurrentlaryngeal nerve and permanent hypoparathyroidismafter the two operations but there was an increasedincidence of temporary hypoparathyroidism after totalthyroidectomy. The incidence of recurrence (14%)after subtotal thyroidectomy is considerable but similarto those reported elsewhere.

In recent years there has been a change in thesurgical treatment of benign thyroid disease consistingof a progressive increase in total thyroidectomy from

4% in 1970, to 40% in 1990 (20). The increase wasmainly in operations for multinodular goitre where thepercentage of patients treated by total thyroidectomynow exceeds 80% (20). This may be explained bysurgeons’ increasing confidence in the procedure andmoreover by poor long term results with the subtotalprocedure. Complications evaluated by us and otherauthors (8, 10, 35, 39) after total thyroidectomy, in-dicate a low incidence of hypoparathyroidism andpermanent injuries to the recurrent laryngeal nerveentirely comparable to those observed after subtotalresection. Routine isolation of the recurrent nervessignificantly decreases accidental injuries (7, 23, 36).Surgical experience, as postulated by Reeve et al. (34),has a key role in reducing iatrogenic damage to the

Table III. Iatrogenic lesions that developed postopera-tively

Data are expressed as number (%) of patients.

Thyroidectomy

Total(n = 69)

Subtotal(n = 72)

Palsy of recurrentlaryngeal nerve:

• Temporary 2 (3) 2 (3)• Permanent 0 1 (1)

Hypoparathyroidism• Temporary 24 (35) 13 (18)*• Permanent 2 (3) 1 (1)

* p = 0.03, Fisher’s exact test.

Table IV. Number (%) of recurrences after subtotalthyroidectomy for multinodular goitre

Unilateral(n = 19)

Bilateral(n = 53)

Total(n = 72)

7 (13) 3 (16) 10 (14)

Table V. Iatrogenic injuries when total thyroidectomywas done as the primary procedure and when it wasdone as a completion procedure

Data are expressed as number (%) of patients.

Primaryprocedure(n = 69)

Completionprocedure(n = 9)

Palsy of recurrentlaryngeal nerve:

• Temporary 2 (3) 2 (22)• Permanent 0 1 (11)

Hypoparathyroidism• Temporary 24 (35) 2 (22)• Permanent 2 (3) 1 (11)

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503Thyroidectomy for benign disease

recurrent laryngeal nerves. Furthermore, the surgeonwho has completed a well designed training pro-gramme and who has become proficient as a traineewill remain proficient despite practising in a provincialhospital (32). Martensson and Terins (24) maintain thatsuch injuries are directly related to the extension of theoperation.

Some authors (17, 26) consider that “almost totalthyroidectomy” (unilateral or bilateral salvage ofminimal peritracheal thyroid tissue) is the treatmentof choice in multinodular goitre. This procedure wouldadd the advantages of total (no recurrences) to those ofsubtotal thyroidectomy (low incidence of temporaryand permanent hypoparathyroidism). Demard et al.(11) reported 5.7% temporary hypoparathyroidism andno permanent recurrent nerve injuries with thistechnique. In our opinion no advantages are offeredby this procedure, compared with total thyroidectomy,with the possible exception of the incidence of tem-porary hypoparathyroidism, which however, is easilymanaged medically. The correct surgical technique fortotal thyroidectomy could reduce the incidence of bothtemporary and permanent hypoparathyroidism. Toprevent temporary hypoparathyroidism it is importantto ligate the inferior thyroid vessel close to the thyroidcapsule. The identification of vascularised parathyroidtissue is essential to avoid permanent hypoparathyroid-ism. If the parathyroid blood supply is uncertainimplantation of the gland into the deltoid or sterno-cleidomastoid muscles is advisable (25).

The recurrence rate observed in our study (14%)confirms the incidence reported elsewhere. Ambrosi etal. (1) found that recurrences were inversely related tothe extent of resection. Piraneo et al. (31) reported a39% recurrence rate after enucleating excision, 27%after lobectomy, 20% after lobectomy and contralateralenucleating excision, and 4% after subtotal resection.

The role of postoperative hormone suppression onthe incidence of recurrence is not completely clear.Patients given suppressive doses of L-thyroxine post-operatively are thought to have a lower incidence ofrecurrence (Table I). Hormones that induce inhibitionof TSH may prevent or significantly reduce the residualparenchymal stimulation, thereby lowering the inci-dence of recurrence. However, this hypothesis has notbeen confirmed by other authors (1, 5, 15, 40). Geerd-sen and Hee did not report any relationship betweenserum TSH increase and recurrence (13); the latter maybe related to the production of insulin-like growthfactor (IGF-I) and epidermal growth factor (EGF) bythe thyroid remnant (15). The 14% recurrence ratefound after subtotal resection suggests that anysuppressive regimen was only partly effective inreducing the incidence of recurrence.

A key issue emerging from recent data is the

question of how a nodular goitre attains the capacityfor growth independently of TSH. The most plausiblehypothesis is that nodular growth may be caused by thepresence in the adult thyroid of less differentiated cellswith a higher than average natural growth potential,some of which may replicate in the absence of TSH(29). In contrast to the normal gland, in which TSH isclearly the main factor that regulates follicular cellgrowth, additional mechanisms or growth factors havea crucial role. IGF-I, which stimulates proliferation ofthyroid follicular cells through specific receptors, isone of many growth stimulators (EGF) T cell growthfactor � (TGF-�), and fibroblast growth factor (FGF),and inhibitors (TGF-�) that act independently of, but inconcert with, TSH (38). In this study we did completionthyroidectomies after a median interval of 10.5 years,so that the clinical evidence of these recurrences, withhormone treatment, becomes relevant after a period upto 10 years. As regard other complications, iatrogenicinjuries are not related to duration of follow-up; wehave considered permanent laryngeal nerve palsy andpermanent hypoparathyroidism as palsy of the vocalcord and the need to give vitamin D and calcium orallysix months after operation, respectively.

Another element supporting total thyroidectomy as aprimary option is the incidence of iatrogenic injuriesafter completion thyroidectomy; the risks are up to tentimes greater (33). Injuries to the recurrent laryngealnerve and permanent hypoparathyroidism after reo-peration range from 3.1% to 12%, and from 3.7% to25% (7, 9, 33, 35), respectively, and were 1/9 for bothpermanent recurrent nerve injuries and hypoparathyr-oidism in our series.

Even though we did not see any malignant transfor-mation in the thyroid remnant after subtotal resection,it ranges from 4% to 17% in other series (21).

In conclusion, according to some reports (8, 17, 27)and in our experience, total thyroidectomy does notsignificantly increase the incidence of iatrogenicinjuries in unilateral and bilateral multinodular thyroidgoitres. Subtotal thyroidectomy is not sufficient tomaintain a euthyroid state in most patients and isfollowed by recurrence, the incidence of whichincreases with time. Completion thyroidectomy has ahigher incidence of iatrogenic lesions compared withprimary thyroidectomy.

Total thyroidectomy therefore seems to be theprocedure of choice in most patients with diffusebenign thyroid disease. Subtotal resection may beindicated in older patients because of the delay inclinical evidence of recurrence.

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RESUMEBut: Evaluer le devenir de deux groupes comparables depatients apre`s thyroıdectomie totale et subtotale pour goitreuni ou multinodulaireType d’etude: Prospective, randomise´e.Provenance: Hopital universitaire, Italie.Patients: Cent quarante et un patients ope´res d’un goitrebenin entre 1975 et 1985.Methodes: Apres tirage au sort, 69 patients ont eu unethyroıdectomie totale et 72 une thyroı¨dectomie sub-totaleselon une technique standardise´e.Principaux criteres de jugement: L’existence d’une paralysierecurentielle temporaire ou de´finitive, l’existence d’unehypoparathyroı¨die temporaire ou de´finitive, la recidive dugoitre, et l’incidence des complications iatroge`nes apre`stotalisation de la thyroı¨dectomie.Resultats: Les patients ont e´te suivis pendant 14,5 ans enmoyenne (extreˆmes 10–21). Apre`s thyroıdectomie totale, 2patients (3%) ont eu une paralysie re´curentielle temporairemais Il n’y a eu aucune atteinte de´finitive; et 24 patients onteu une hypoparathyroı¨die temporaire (35%) et 2 (3%) unehypoparathyroı¨die definitive. Apres thyroıdectomie sub-totale, 2 patient (3%) ont eu une paralysie re´curentielletemporaire et un patient (1%) une paralysie re´curentielledefinitive; et 13 patients ont eu une hypoparathyroı¨dietemporaire et 1 (1%) une hypoparathyroı¨die definitive. Deplus il y a eu 10 re´cidives de goitres (14%). Apre`s totalisationde thyroıdectomie (n = 9) il y a eu 2 cas de paralysierecurentielle temporaire et un cas de paralysie re´curentielledefinitive, et 2 cas d’hypoparathyroı¨die temporaire et 2 casd’hypoparathyroı¨die definitive.Conclusions: La thyroıdectomie totale est le proce´de dechoix pour le traitement des goitres nodulaires be´nins.

ZUSAMMENFASSSUNG:Ziel: Beurteilung des Outcomes nach totaler und subtotalerSchilddrusenresektion in der Behandlung der mononodula¨-ren und der multinodula¨ren Knotenstruma in zwei vergle-ichbaren Patientengruppen.Studienanordnung: Prospektive randomisiserte Studie.Studienort: Universitatskrankenhaus, Italien.Patienten: 141 in den Jahren 1975–1985 wegen einerbenignen Stuma operierte Patienten.Methoden: 69 Patienten wurden in die Gruppe mit totalerSchilddrusenresektion randomisiert und 72 Patienten wurdenin eine mit subtotaler Schilddru¨senresektion randomisiert.Das operative Vorgehen erfolgte jeweils in der Standard-technik.Endpunkte: Temporare oder dauernde Rekurrenzparese,temporarer oder dauernder Hypoparathyroidismus, Rezidiv-struma, Inzidenz iatrogener Scha¨den nach Beendigung derSchilddrusenresektion.Ergebnisse: Der Median des Nachbeobachtungszeitraumsbetrug 14,5 Jahre (Spannweite 10–21 Jahre). Nach totalerSchilddrusenresektion entwickelten 2 Patienten (3%) einetemporare Rekurrenzparese, persistierende Rekurrenzpare-sen wurden nicht gesehen. 24 Patienten (35%) entwickelteneinen tempora¨ren und 2 Patienten (3%) einen dauerndenHypoparathyroidismus. Nach subtotaler Schilddru¨senresek-tion entwickelten 2 Patienten (3%) eine tempora¨re und 1Patienten (1%) eine permanente Rekurrenzparese. 13 Pa-

tienten entwickelten einen tempora¨ren und 1 Patient (1%)entwickelten einen permanenten Hypoparathyroidismus.Weiterhin sahen wir 10 Rezidivstrumen (14%). Nach Rest-thyroidektomie (n = 9) sahen wir 2 Fa¨lle von tempora¨rer und1 Fall von permanenter Rekurrenzparese. In 2 Fa¨llen wurdein dieser Untergruppe ein tempora¨rer und in 2 Fa¨llen einpermanenter Hypoparathyroidismus gesehen.Schlußfolgerungen: Die totale Schilddru¨senresektion ist dasVorgehen der Wahl in der Behandlung der benignenKnotenstruma.

������E����� ����� ��������� ����� ��������� ������������� � �������� � ���� ��� ��������������� �� �� � ���� � ������ � ������� �����!������� ����� ����� " ���������� ������� ������� ����������!������ #��� ������� ��������$ ����%!������� &'& �� ���$ ��� ������� �� �������������������� �� �� �� �� �� � ���� � &()* ��&(+* ����!�� ��� ,( �� ����� ��� ������ ����� ��%��������� � �������� )- ��% ������������� �������� � ������������ ������ ���������!����� ����� ����� . ������� � �����%������ �� ���� ������ �� ��$ � ������� � �����%��������� �� �����$ � �� �� ���$ ��������%� ������� ��� �/���� ����� � ��������!���������"� ���� ��� ���������� � � ����������% &'!* ��� 0��� ��� �� &1 ��� �� -& ����2! "������������� � �������� � - �� ����� 03%2 �����% � ������� �� �� ���� ������ �� ��������� ��$ �� ���� ������� ������ �����%����� �� ���!# -' �� ����� 03*%2 �����% � ������� � -�� ����� 03%2 �����%���� ����� �� �����!"���� ������������ � �������� � - �� �����03%2 �����% �����%���� � & �� ���� 0&%2�� ��������� �� �� ���� ������ �� ������� �� ��;� &3 �� ����� �����% � ������� � & �� ������ ��������� ����� �� �����! # &1 �� �������� ������ � �� �� ��� 0&'%2! "���� ���� 4���% � �������� 0n = (2 ��� ������ � - ����%�� ������� � & ����� �� ��������� �� �� ����� ������ �� ������� �� ��$ � - ����%� ������� ������� � - ����%� �����%���� ����� ��� �����!��� ��� 5�������% � ��������% %��%���% �������� ���� � ��% ����% ��� ������������ ������������!

Submitted November 15, 1996; submitted after revisionAugust 7, 1997; accepted August 20, 1997

Address for correspondence:Giuseppe Pappalardo, M.D.Via Sebastiano Conca, 11I-99197 RomeItaly

Eur J Surg 164

506 G. Pappalardo et al.