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782 W or l d J . S u r g . V o l . 10 , N o . 5 , Oc t ob e r 1986

Table 1. Histologic classification of excised thyroidglands (1957-1984).P a t i e n t s

Papillary carcinoma~ 226Follicular carcinoma 65Medullary carcinoma 21Hurthle cell carcinoma 16Anaplastic carcinoma 9Multinodular goiter 27Hashimoto's thyroiditis 10Graves' disease 30Total 404

a Includes follicular varient of papillary carcinoma.

Westland, Michigan). The records of 404 patientswere available for retrosp ectiv e review and analysisof technique of the operation performed, extent oft h e disease, pathologic findings of excised tissue,degree of recurrent laryngeal nerve injury, degreeof postoperative hypoparathyroidism, other periop-erative complications, and mortality.Total thy roid ecto my is defined as the surgeon' sattempt to perform an extracapsular removal of theentire thyr oid gland including pyramidal lobe whilepreserving the parathyroid glands, recurrent laryn-geal nerves, and external branches of the superiorlaryngeal nerves. R ecurr ent laryngeal nerve injurieswere considered accidental complications of tech-nique unless vocal cord paralysis was observedpreoperatively or the operating surgeon specificallyindicated that nerve excision was necessary toassure r emoval of the neoplasm. In the last 14 yearsof the study, more functioning nerves were left insitu, despite extensive disease, and well-different-iated carcinoma was " sh av ed " off the nerves toavoid their sacrifice. If these nerves failed to func-tion postoperatively, these were not consideredaccidental injuries. Recurrent laryngeal nerve in-jury was documented by either direct or indirectlaryngoscopy. In all patients, persistent hypopara-thyroidism was considered to be a direct result ofthe technique unless the patient had preoperativehypocalcemia. Postoperative hypoparathyroidismand vocal cord paralysis lasting 1 year or longerwere considered permanent; however, if recoveryoccurred before that time, they were consideredtransient. Only clinically symptomatic patientswere treated for their hypocalcemia. Records of alloperations were carefully reviewed for details ofsurgical technique and the extent of tumor involve-ment. These factors were correlated with operativecomplications. All patients with differentiated thy-roid carcinom as under went posto perat ive J31I scan-ning for documentation of the prese nce of residualthyroid tissue and/or metastases.

R e s u l t s

During the 27-year period, all 404 patients under-went total thyroidectomies either as an initial oper-ation in 264 patients (65.3%) or as a completionthyr oide ctom y in 140 patients (34.7%). Concomi-tant lymph node excisions ranging from local re-moval of 1 or more central compartment nodes tobilateral neck dissections were performed in 159(47.2%) of the 337 patients with th yroid cancer.Table 1 outlines the histological classifications ofthe resected specimens for the entire series. Thy-roid cancer was found in 337 patients (83.4%) andother benign conditions in 67 patients (16.6%).Total thyroidectomies were performed in the benignconditions listed for a variety of reasons includingprevious history of head and neck irradiation, asso-ciated suspicious nodules, Graves' eye disease, andchildren with Graves' disease.Recurrent laryngeal nerve injuries are shown inTable 2. A comparison is made between our previ-ously report ed exp erienc e from 1957 through 1969and our most recent experience from 1970 tomid-1984. All of the cases in our earlier ex perie ncehad thyroid cancer, while our most recent experi-ence includes both patients with cancer and the 67patients with benign conditions. Transient nerveinjury, lasting from a few days to 11 months,occurred in 25 patients (6.2%) of the entire series,but in only 4 patients (1.8%) in our last 220 cases.The incidence of permanent nerve injury for theentire series was 2.5%; howeve r, it was only 0.45%since 1970. The incidence of recu rrent laryngealnerves invaded by tumor or deliberately sacrificedat operation remained remarkably constant for theentire period of the series at 6.9%. One patient witha diffusely enlarged goiter had a right vocal cordparalysis preoperatively caused by traction on t h enerve by the goiter. Ne rve function recovered afterthyroidectomy. No patients suffered permanent bi-lateral nerve injury. Four patients, however, re-quired temporary tracheotomies for bilateral tran-sient vocal cord paralysis. One additional patient,operated on since 1970, sustained accidental divi-sion of 1 branch of a recurrent laryngeal nervewhich was immediately recognized and repairedprimarily at the original operation. The patient hadcomplete recovery of vocal cord function on theinvolved side within 6 months.Transient hypoparathyroidism occurred from 1day postoperatively and lasted up to 1 year, in 68(16.8%) of 404 patients (Table 3). Seven ty-s ix symp-tomatic patients were treated with calcium and/orvitamin D until their symptoms abated and theirserum calcium returned to normal levels. Patientswere considered to be permanently hypoparathy-roid if they required treatment longer than 1 year.

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J.K. H a r n e s s e t a l . : T o t a l T h y r o i d e c t o m y 7 8 3

Tab l e 2. Recurrent laryngeal nerve injury.1957-1969 1970-1984 Total series(184 patients) (220 patients) (404 patients)

Transient injury 21 (11.4%) 4 (1.8%) 25 (6.2%)Permanent injury 9 (4.9%) 1 (0.45%) 10 (2.5%)Nerves invaded by tumor or sacrificed 13 (7.1%) 15 (6.8%) 28 (6.9%)

Tab l e 3. Postoperative hypoparathyroidism.1957-1969 1970-1984 Total series(184 patients) (220 patients) (404 patients)

Transient 24 (13.0%) 44 (20.0%) 68 (16.8%)Permanent 10 (5.4%) 6 (2.7%) 16 (4.0%)

Temporary hypoparathyroidism was treated for amean duration of 25.5 -+ 20 weeks. The overallincidence of permanent hypoparathyroi dism for theentire series was 4.0%; however, this fell to 2.7%for the last 220 patients. In this later subgroup, 5 ofthe 6 patients were found at operation to haveextensive bilateral involvement by thyroid cancer.These patients had both local invasion and exten-sive nodal spread o f their tumors. Only 1 patientsustained permanent postoperative hypoparathy-roidism following total thyroidectomy for a local-ized cancer involving a single lobe. None of thepatients undergoing total thryo idectomy for benigndisease suffered permanent hypoparathyroidism.Tracheotomies were done as an emergency pro-cedure postoperatively in a total of 9 patients(2.2%). Only 3 of these were done in the last 220patients (1.4%). A total of 3 patients (0.74%) werereturned to the operating room over the past 27years for postoperative hemorrhage. This complica-tion has occurred in only 1 of the 220 patientstreated in the pas t 14 years (0.45%). Drains wererarely used in this series and then only after nodaldissections in the lateral neck rather than the cen-tral compartment. Infections were rare (0.5%) eventhough antibiotics were not used. In 1 patient, acellulitis developed which was treated withoutdrainage (antibiotics only). Another patient devel-oped a Staphylococcus aureus infection betweenthe superficial layer of the deep cervical fascia andthe platysma muscle which was treated by openingand draining the cente r of the wound. The operativemortality rate for the entire series was zero. Anydeaths from cancer of the thyroid occurred after thefirst 30 days postoperativel y.D i s c u s s i o nThe anatomy and vulnerability of the recurrentlaryngeal nerves during thyroidectomy have been

widely studied [16-18]. The compli cations ofthyroi dectomy for carcinoma increase with the ex-tent of disease found at operation, with reoperativesurgery, and with less experienced surgeons [6,10-13, 15].The debate over the use of total thyroidectomyroutinely for the t reatment of all differentiated thy-roid carcinoma continues. Total thyroidectomy hasalso been advocated for the treatment of certainbenign conditions including extensive colloid nodu-lar goiter, toxic nodular goiters, chronic thyroiditis,Graves' disease (especially in Graves' eye disease),and nodules associated with head and neck irradia-tion. Total thyroidectomy is perceived as a morehazardous operation primarily because of the addi-tional risk to the contralateral recurrent laryngealnerve and the potential risk of permanent postoper-ative hypoparathyroidism. Injury to the recurrentnerve on the side opposite a localized primarythyroid neoplasm is particularly unfortunate. Fur-thermore, there have been no series of cases withsufficient long-term follow-up to document statisti-cally improved survival with total thy roidectomy intreating differentiated thyroid carcinoma.With applied anatomic knowledge and improvedtechniques has come a reduction in the morbidity oftotal thyroidect omy. Jacobs et al. reported a 0%permanent recurrent laryngeal nerve injury rate in213 patients undergoing total thyroi dectomie s usingthe same techniques as utilized in this series [10].Scanlon and colleagues had 1 permanent nerveinjury in 245 total thyroidectomies [12]. Karlan etal. reported a 0% nerve injury rate in 1,000 consec-utive thyroid operations. Of these, 457 were totalthyroidectomies, but only 93 were performed formalignancy [7]. Recent reports by Martensson andTernins from Sweden and Starnes et al. from Bos-ton have been most disturbing [14, 15]. Martenssonreports a 14% incidence of permanen t nerve injuryafter operations for thyroid cancer or reoperationsfor benign disease. Starnes reports an incidence ofpostoperative complications that was 20 timeshigher with total thyroidectomy than with partialthyroidectomy. The numbers of patients undergo-ing total thyroidectomies in both these series weresmall and their collective experience with totalthyroi dectomy was limited.

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7 8 4 W o r l d J . S u r g . V o l . 1 0 , N o . 5 , O c t o b e r 1 9 86

Our own experience with recurrent laryngealnerve injury, especially over the past 14 years, hasbeen consistent with other large series coveringsimilar time periods [7, 10, 12]. The marked de-crease in transient nerve injuries from 11.4% in thefirst half of our series to 1.8% since 1970 is mostgratifying. Similarly, our decreased incidence ofpermanent accidental nerve injury from 4.9% to0.45% is equally rewarding. We believe that theseimprovements represent the full use by all of ourcolleagues at the University of Michigan of thetechniques advocated by Thompson et al. in 1973[19]. Only 1 patient sustained a permanen t nerveinjury in the last 14 years, and this was on the sideopposite a primary tumor. Of the 10 cases ofpermanent nerve injury for our entire series, 4occurred on the side opposite a primary neoplasm.Wade, Lore, and Riddell have detailed the vul-nerability of the recurrent nerve at the time ofoperat ion [16-18]. We particularl y agree with Lorethat the nerve is at greater risk of injury in theregion of the posterior suspensory ligament of thethyroid (ligament of Barry) where the nerve oftenpenetrates the ligament. This relationship was alsodetailed by Thompson et al. in 1973 [19]. We do notroutinely identify the recurrent nerve early in theoperative procedure as advocated by others [3, 4].As a dissection proceeds to the area of the ligamentof Berry, however, we typically identify the recur-rent nerve as it courses close to or through theligament. Routine identification of the nerve bothinitially and in the area of the ligament of Berryshould be practiced by less experienced surgeons.Also, when the course of the recurrent nerve isdifficult to follow because of extensive thyroidcarcinoma in the central compartment, the nerveshould be identified and traced from the thoracicinlet toward the larynx in order to prevent injury.Injury to the external branch of the superiorlaryngeal nerves should be avoided by carefuldownward mobilization of the superior pole of thethyroid gland. Anterior and posterior branches ofthe superior thyroid vessels are individually ligatedand divided as they course over the superior pole.This technique prevents injury to the externalbranch of the superior laryngeal nerves as they maycourse through the bifurcation of the superior thy-roid vessels.Nonrecurrent laryngeal nerves occur primarilyon the right because of an anomalous right subclav-ian artery arising directly from the aorta whichoccurs with a frequency of 0.3-1.0% reported in theliterature [20]. Theoretically, if the left subclavianwere to arise from a right-sided dorsal aorta, itshould be possible for an anomalous recurrentnerve to occur on the left side. Such a case was

discovered in a dissecting room cadaver but hasnever been reported in the clinical literature [16].Recently, Sanders and colleagues reported the first2 cases of right-sided nonrecurrent laryngeal nervesin addition to standard recu rrent nerves [21]. Theimportance of experience in thyroid surgery is againemphasized.Since 1970, the reported incidence of permanentpostoperative hypoparathyroidism following totalthyroidectomy has varied from 1.2% to 11% [6-10,12, 14]. Prevention of ischemia to the parathyroidglands is of paramount i mportance in avoiding thiscomplication. We take all branches of the inferiorthyroid artery on the capsule of the thyroid glandmedial to that artery's branches to the parathyroidglands in order to avoid compromised blood flow tothe parathyroids. The parathyroid glands are them-selves always carefully dissected away from thethyroid gland capsule starting at a point medial totheir blood ~pply and gently teasing them laterallyand posterior to the thyroid capsule. If a parathy-roid gland is inadvertently devascularized, it maybe immediately reimplanted in an adjacent sterno-cleidomastoid muscle.The risk of hypoparathyroidism increases withreoperation and extensive thyroid carcinoma [6].Nearly all of our cases of permanent hypoparathy-roidism occurred in patients with extensive bilateralthyroid carcinomas that involved the central com-partment and jugular lymph nodes and were asso-ciated with local invasion. Because of bilateralinvolvement and extensive local disease, nothingshort of total thyroidectomy would have been ac-ceptable therapy in these cases. Every effort shouldbe made in such cases to identify the parathyroidglands and to preserve their blood supply. Vascu-larly compromised glands should be reimplanted.Despite the most careful operative technique, asmall percentage of patients will suffer permanenthypoparat hyroidism as a result of legitimate effortsto eradicate extensive disease and achieve cure. Inour last 220~i~atients, permanent hypoparathyroid-ism occurred in 6 patients (2.7%), all but 1 of whomhad very extensive carcinoma.Total thyroidectomy remains the treatment ofchoice for thyroid cancer in our experience becauseof its excellent control of local spread of disease andbecause it facilitates the postoperative use of 1311therapy in those patients with extensive diffErenti-ated thyroid carcinomas. Its utility in the manage-ment of a variety of benign conditions of the thyroidgland is also noted. Postoperative complications arecurrently related primarily to secondary operationsand extent of disease. They decrease with experi-ence and meticulous attention to careful technique.

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J . K . H a r n e s s e t a l .: T o t a l T h y r o i d e e t o m y 7 8 5

R ~ s u m ~A u c o u r s d ' u n e p e r i o d e d e 2 7 a n s d e 1 95 7 ~ 1 98 4 ,q u a t r e c e n t t r e n t e p a t i e n t s o n t s u b i u n e t h y r o i -d e c t o m i e t o t a l e d a n s n o t r e e t a b l i s s e m e n t p o u r d e sl e s i o n s b e n i g n e s o u m a l i g n e s d u c o r p s t h y r o i d i e n .D a n s 8 3 . 4 % d e s c a s i l s ' a g i t d ' u n c a r c i n o m et h y r o i ' d i e n , n e c e s s i t a n t c h e z 4 7 . 2 % d ' e n t r e e u x u nc u r a g e g a n g l i o n n a i r e a s s o c i e . O n o b s e r v e u n e at -t e i n t e t r a n s it o i r e d u n e f f r e c u r r e n t l a r y n g e d a n s6 . 2 % d e s c a s s u r l a t o t a l i t e d e l a s e r i e . U n ep a r a l y s i e p e r m a n e n t e u n i la t e ra l e d e s c o r d e s v o c a l e ss u r v i e n t c h e z 2 . 5 % d e s p a t i e n t s o p e r e s , a l o r s q u ed u r a n t l e s 1 4 d e r n i d r e s a n n e e s u n s e u l p a t ie n tp r e s e n t e c e t t e c o m p l i c a t io n . A u c u n d e s c as d ep a r a l y s i e b il a te r a le p e r m a n e n t e d e s c o r d e s v o c a l e sn ' e s t o b s e r v e . U n e h y p o p a r a t h y r o i d i e t r an s i to i r ee s t c o n s t a t e e c h e z 1 6 . 8 % d e s p a t ie n t s a v e ch y p o p a r a t h y r o i ' d i e d e fi n i ti v e d a n s 4 . 0 % d e s c a s .L ' i n c i d e n c e d e l ' h y p o p a r a t h y r o i ' d i s m e d e f in it ift o m b e b . 2 . 7 % a u c o u r s d e s 1 4 d e r n i d r e s a n n e e s e te s t d i r e c t e m e n t l ic e /~ l ' e x t e n s i o n d u c a n c e rt h y ro ' l' d ie n c o n s t a t 6 l o t s d e l ' i n t e r v e n t i o n . L e s c o m -p l ic a t io n s p o s t o p e r a t o i r e s d i m i n u e n t a v e c l ' ex -p e r i e n c e d u c h i r u r g i e n e t a u g m e n t e n t l o t s d e sr d i n t e r v e n t i o n s e t l ' e x t e n s i o n d e s l e si o n s . L at h y r o i ' d e c t o m i e t o t a l e d e m e u r e p o u r l es a u t e u r s l et r a i t e m e n t d e c h o i x d u c a n c e r t h y r o i ' d i e n .

R e s u m e nE n e l l a p s o d e l o s 2 7 a f i o s e n t r e 1 95 7 y 1 98 4, c u a t r oc i e n t o s t r e i n t a p a c i e n t e s f u e r o n s o m e t i d o s at i r o i d e ct o m f a t o t al p o r e n f e r m e d a d m a l i g n a ob e n i g n a d e l a g l ~ in d u la t i r o i d e s e n n u e s t r a si n s t i tu c i o n e s . C f i n c e r t ir o i d e o f u e h a l l a d o e n 8 3 . 4 %d e lo s c a s o s , y 4 7 . 2 % d e e s t o s t u v i e r o n d i s e c c i o n e sg a n g l i o n ar e s c o n c o m i t a n t e s . L e s i d n t r a n s i t o r ia d e ln e r v i o r e c u r r e n t e l a r f n g e o o c u r r i6 e n e l 6 . 2 % d e l as e r i e to t a l . P a r f i li s i s p e r m a n e n t e u n i l a t e r a l d e l ac u e r d a v o c a l o c u r r i 6 e n 2 . 5 % d e l o s p a c i e n t e so p e r a d o s , m i e n t r a s s d l o u n p a c i e n t e ( 0 . 4 5% )p r e s e n t 6 e s t a c o m p l i c a c i d n e n l o s fi l ti m o s 1 4 a f io s .N i n g t i n p a c i e n t e p r e s e n t 6 p a r~ i li si s b i l a t e r a l p e r m a -n e n t e d e l as c u e r d a s v o c a l e s . H i p o p a r a t i r o i d i s m ot r a n s i t o r i o f u e o b s e r v a d o e n 1 6 .8 % d e lo s p a c i e n t e s ,y e l h i p o p a r a t i r o i d i s m o p e r m a n e n t e o c u r r i 6 e n el4 . 0 % . L a i n c i de n c i a d e h i p o p a r a t i r o i d i s m o p e r m a n -e n t e d e s c e n d i 6 a 2 .7 % e n l o s fi l t i m o s 1 4 a f i o s ya p a r e c i 6 d i r e c t a m e n t e r e l a c io n a d o c o n l a e x t e n s id nd e l c f in c e r t i r o i d e o h a l l a d a e n l a o p e r a c i d n . L a sc o m p l i c a c i o n e s p o s t o p e r a t o r i a s d i s m i n u y e n e nr e l a c i 6 n a la e x p e r i e n c i a d e l c i r u ja n o y s ei n c r e m e n t a n c o n l as r e o p e r a c i o n e s y c o n l ae n f e r m e d a d m u y e x t e n s a . L a t i r o id e c t o m f a to t alc o n t i m i a s i e n d o n u e s t r a f o r m a p r e f e r i d a de t r a t am i -e n t o p a r a c g m c e r t i r o id e o .

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