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The American Journal of Surgery (2009) 197, 439–446

linical Surgery-International

he impact of age, vitamin D3 level, and incidentalarathyroidectomy on postoperative hypocalcemia afterotal or near total thyroidectomyesim Erbil, M.D.a,*, Umut Barbaros, M.D.a, Berna Temel, M.D.b,mit Turkoglu, M.D.c, Halim Issever, Ph.D.d, Alp Bozbora, M.D.a,elçuk Özarmagan, M.D.a, Serdar Tezelman, M.D.a

Department of General Surgery; bDepartment of Endocrinology; cDepartment of Biochemistry; dDepartment of Health

ublic, Istanbul University Istanbul Medical Faculty, Istanbul, Turkey

AbstractBACKGROUND: Hypocalcemia caused by transient or definitive hypoparathyroidism is the most

frequent complication after thyroidectomy. We aimed to compare the impact of incidental parathy-roidectomy and serum vitamin D3 level on postoperative hypocalcemia after total thyroidectomy (TT)or near total thyroidectomy (NTT).

PATIENTS: Two hundred consecutive patients with nontoxic multinodular goiter treated by TT andNTT were included prospectively in the present study. Group 1 (n � 49) consisted of patients with apostoperative serum calcium level �8 mg/dL, and group 2 (n � 151) had a postoperative serumcalcium level greater than 8 mg/dL. Patients were evaluated according to age, preoperative serum25-hydroxy vitamin D (25-OHD) levels, postoperative serum calcium levels, incidental parathyroid-ectomy, and the type of thyroidectomy.

RESULTS: Patients in group 1 (n � 49) were hypocalcemic, whereas patients in group 2 (n � 151)were normocalcemic. Preoperative serum 25-OHD levels in group 1 were significantly lower than ingroup 2 (P � .001). The incidence of hypoparathyroidism was significantly higher following TT(13.5%) than following NTT (2.5%) (P � .05). The risk for postoperative hypocalcemia was increased25-fold for patients older than 50 years, 28-fold for patients with a preoperative serum 25-OHD levelless than 15 ng/mL, and 71-fold for patients who underwent TT. Incidental parathyroidectomy did nothave an impact on postoperative hypocalcemia. The highest risk of postoperative hypocalcemia wasfound in the patients with all of the above variables.

CONCLUSIONS: Age, preoperative low serum 25-OHD, and TT are significantly associated withpostoperative hypocalcemia. Patients with advanced age and low preoperative serum 25-OHD levelsshould be placed on calcium or vitamin D supplementation after TT to avoid postoperative hypocal-cemia and decrease hospital stay.© 2009 Elsevier Inc. All rights reserved.

KEYWORDS:Hypocalcemia;Total thyroidectomy;Incidentalparathyroidectomy;Vitamin D

tets

* Corresponding author. Tel.: �90 212 5331784; fax: �90 212319771.

E-mail address: yerbil2003@yahoo.comManuscript received November 23, 2007; revised manuscript January

a, 2008

002-9610/$ - see front matter © 2009 Elsevier Inc. All rights reserved.oi:10.1016/j.amjsurg.2008.01.032

Total thyroidectomy (TT) is now the preferred option forhe management of benign multinodular goiter.1,2 Postop-rative hypocalcemia is the most frequent complication af-er TT, and it continues to challenge even experiencedurgeons since it often extends the duration of hospital stay

nd increases the need for biochemical tests.3–6

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The causes of hypocalcemia after TT are multifactorial,nd some of these factors include iatrogenic surgical traumao the parathyroid glands, incidental parathyroidectomy, theumber of functioning glands left behind, extent of surgery,xperience of the surgeon, hyperthyroidism, retrosternaloiter, concomitant neck dissection, and thyroid car-inoma.5–10

Familiarity with parathyroid anatomy and experience aref crucial importance in thyroid surgery. However, inciden-al parathyroidectomy may occur even in the hands of theost experienced thyroid surgeon. The incidence of inci-

ental parathyroidectomy ranges from 5%–20%. Inciden-ally, excised parathyroids are reported in intrathyroid loca-ions in up to 40%–50% of cases.10–14 In most cases, only

parathyroid gland is inadvertently resected with the thy-oid. Although some studies suggest that incidental para-hyroidectomy does not correlate with postoperative hy-ocalcemia, its clinical relevance is not yet clear.10–14

Vitamin D plays a critical role in calcium homeostasis.15

fter it is acquired by either sunshine or diet, it is convertedo 25-hydroxy vitamin D (25-OHD) in the liver. Serum5-OHD is thought to be biologically inactive. However, itrovides the most reliable parameter reflecting the vitamin

status of the body.15–17 In Turkey, more than 30% ofifferent groups of subjects have vitamin D deficiency.18,19

nsufficiency in calcium absorption due to low vitamin Doncentration leads to an increase in parathyroid hormonePTH) secretion. Increased PTH stimulates the synthesis ofalcitriol and thereby improves calcium absorption effi-iency.

The aims of this prospective clinical study are: (1) toompare the impact of age, serum vitamin D3 level, andncidental parathyroidectomy on postoperative hypocalce-ia after TT or near total thyroidectomy, and (2) to deter-ine which risk factors are important for hypocalcemia

ncidence. To the best of our knowledge, our study is therst prospective study performed to detect the impact ofge, preoperative serum 25-OHD level, and incidental par-thyroidectomy on postoperative hypocalcemia after TTr NTT.

aterials And Methods

atients

A total of 200 consecutive patients with nontoxic multi-odular goiter treated by bilateral TT and bilateral NTT inhe Department of Surgery at the Istanbul Faculty of Med-cine between January 2006 and January 2007 were in-luded prospectively in the present study.

The main indications for surgery included large goiterith a compressive effect for all patients. Patients withyperthyroidism, substernal goiter, previous thyroid or neckperations, or concomitant parathyroid disease, as well as

hose who refused to participate in this study, were excluded a

rom the present study. None of the patients had signs orymptoms indicating metabolic bone disease, and none ofhe patients were on medications, such as oral calcium/itamin D supplementation, anti-resorptive agents, hormoneeplacement therapy for postmenopausal women, anabolicgents, thiazide type diuretics, or antiepileptic agents,nown to affect serum calcium metabolism. The study planas reviewed and approved by our institutional ethical

ommittee, and informed consent was obtained for all pa-ients.

All thyroid procedures were performed by experiencedndocrine surgeons using the conventional clamp-and-tieechnique. Vessel sealing systems including ultrasonic dis-ectors, electrothermal bipolar vessel sealers, and titaniumlips were not used. TT was performed by extracapsularissection. NTT was performed by the capsular dissectionethod, and less than 1 g of remnant tissue was left around

he Berry ligament. For the remnant tissue, we estimatedhat 1 cm3 equaled 1 g. Recurrent laryngeal nerves werearefully identified and dissected. All parathyroid glandsdentified and preserved with meticulous dissection for theirlood supply. After resection, the thyroid gland surface wasarefully examined for the presence of parathyroid tissue.arathyroid glands were autotransplanted using a standard

echnique. Pathology reports were reviewed specifically forhe presence, location (ie, extracapsular or intrathyroid),umber, size, and histological characteristics of removedarathyroid glands; the results were recorded.

Serum calcium, 25-OHD, alkaline phosphatase, creati-ine, and albumin levels were determined the day beforeurgery. Serum calcium levels were measured 24 hoursostoperatively. The lowest postoperative serum calciumevel was determined for all patients. Serum calcium con-entration was adjusted for serum albumin.

Two hundred patients were divided into 2 groups accord-ng to their postoperative calcium levels. Patients in group 1n � 49) had postoperative serum calcium levels �8 mg/dL,hereas patients in group 2 (n � 151) had serum calcium

evels greater than 8 mg/dL. Hypocalcemia was defined asserum calcium concentration of �8 mg/dL. Patients with

symptomatic hypocalcemia showed only laboratory find-ngs, whereas patients with symptomatic hypocalcemia hadlinical symptoms in addition to laboratory findings. Theresence of clinical symptoms or signs of hypocalcaemiaere reported, including facial paresthesia, positive Ch-ostek’s or Trousseau’s signs, and muscular spasm. Serumalcium levels for hypocalcemic patients were measuredvery 12 hours until the serum calcium levels stabilized. Allatients developing asymptomatic hypocalcemia werereated with oral calcium (3–6 g/d). Symptomatic hypocal-emia was treated with parenteral calcium and an oral 1,25-ihydroxy vitamin D3 (calcitriol) supplementation of 1–1.5g/d. Those patients with asymptomatic hypocalcemia wereischarged on oral calcium, whereas patients with symp-omatic hypocalcemia were discharged on oral calcium

nd/or calcitriol at doses modified relative to serum calcium

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oncentration. The latter patients were monitored weeklyntil their serum calcium and PTH levels normalized.

iochemical analysis

Serum calcium, alkaline phosphatase, creatinine, and al-umin levels were determined with an auto-analyzer (Cobasntegra 800, Roche Diagnostics, Basel, Switzerland). Serum5-OHD levels were determined from an immunoradiomet-ic assay using the commercially available 25(OH)-vitamin

3 RIA CT kit (BioSource Europe, Nivelles, Belgium).ormal ranges of biochemical parameters were 8.5–10.5g/dL for serum calcium, 90–260 U/L for serum alkaline

hosphatase, 0.6–1.5 mg/dL for serum creatinin, 3.5–5 g/dLor serum albumin, and 6–46 ng/mL for serum 25-OHDoncentrations.

tatistics

Data were analyzed using SPSS 11.0 for WindowsSPSS Inc, Chicago, IL). Results were expressed as mean �D. Comparisons of data used the Wilcoxon signed-rank

est, chi-square test, and logistic regression analysis. Resultsere considered statistically significant when the 2-tailed Palue was less than .05.

esults

The mean (�SD) age for all patients was 44.4 � 12ears (range 17–72 years). The female/male ratio was 5.2/1n � 168/32). The means (�SD) for serum albumin, creat-nine, calcium, alkaline phosphatase, and 25-OHD levelsere 3.7 � .06 g/dL, .8 � .03 mg/dL, 8.8 � .03 mg/dl, 158 �4 U/L, and 27.1 � 13 ng/mL, respectively. The postop-rative serum calcium level was lower than the preoperativeerum calcium level (8.8 � .3 mg/dL vs 8.2 � .7 mg/dL,� .001).Incidental parathyroidectomy was found in 16 patients

8%). One and 2 parathyroids were incidentally removed in3 (81%) and 3 (19%) patients, respectively. Parathyroidissue was found in intrathyroidal (53%) and extracapsular47%) locations. The mean size of the incidentally excisedarathyroids was 4 � 1.6 mm (range 2–8 mm). In allatients, the parathyroid tissue was histologically normal.

TT was performed in 52 patients (26%) and NTT in 148atients (74%). There was no operative mortality. The in-idence of transient vocal cord paralysis was 4% (8/200).ersistent vocal cord paralysis and hypoparathyroidismere not encountered in our series. In the histopathologic

valuation, papillary thyroid cancer was detected in 27atients (13.5%); 22 of these patients (81.4%) had papillaryicrocarcinoma (�1 cm). The mean (�SD) size of the

umor was 5.3 � 3.6 mm (range 2–13 mm). s

valuation of patients according toostoperative hypocalcemia

For 49 (24.5%) group 1 patients, the serum calcium levelas less than 8 mg/dL at 24 hours after the operation. Of

hese 49 patients, 36 (73%) developed symptomatic hy-ocalcemia and 13 (27%) developed asymptomatic hy-ocalcemia. Age and serum alkaline phosphatase levelsere significantly higher in group 1 than in group 2 (57.1 �years and 278.32 � 78 U/L vs 40.3 � 10 years and 119.11 �

5 U/L, P � .001). There was no significant difference inreoperative serum albumin, creatinine, or calcium leveletween groups 1 and 2 (3.5 � .4 g/dL, .9 � .2 mg/dL, and.6 � .4 mg/dL vs 3.6 � .4 g/dL, .8 � .2 mg/dL, and 8.7 �

7 mg/dL, P � .05). Preoperative serum 25-OHD and post-perative serum calcium levels were significantly lower forroup 1 patients than group 2 patients (7 � .2 mg/dL and1 � 7 ng/mL vs 8.7 � .3 mg/dL and 32.3 � 10 ng/mL,� .001). No difference in the rate of incidental parathy-

oidectomy was found between groups (10.2% vs 7.2%,� .05); however, the rate of TT for hypocalcemic patientsas significantly higher than that for normocalcemic patients

43/49 [87.7%] vs 9/151 [5.9%], P � .001) (Figure 1). Hos-ital stay was significantly longer in group 1 (4.2 � 1.1 days,ange 2–8 days) than group 2 (1.4 � .3 days, range 1–2 days)P � .001). In female patients, the ratio of postoperativeypocalcemia was found to be significantly higher when com-ared to male patients (27.9% vs 6.25%, P � .01).

valuation of patients according to preoperativeerum 25-OHD level

A total of 33 patients had serum 25-OHD levels �15g/mL (6.5 � 1.3 ng/mL), and a total of 167 patients hadevels greater than 15 ng/mL (31.1 � 10 ng/mL). Postop-rative serum calcium levels in patients with serum 25-HD levels �15 ng/mL were significantly lower than those

n patients with serum 25-OHD levels greater than 15g/mL (6.9 � .2 mg/dL vs 8.5 � .5 mg/dL; P � .01). Aotal of 33 of the 33 (100%) patients with serum 25-OHDevels �15 ng/mL and 16 of the 167 (9.5%) patients withevels greater than 15 ng/mL developed hypocalcemia. Theatio of postoperative hypocalcemia was significantly higheror patients with serum 25-OHD levels �15 ng/mL than itas for patients with levels greater than 15 ng/mL (P �

001). The ratio of symptomatic hypocalcemia was signifi-antly higher for patients with serum 25-OHD levels �15g/mL than it was for patients with levels greater than 15g/mL (83% vs 25%; P � .03). Age and serum alkalinehosphatase levels were significantly higher for patients witherum 25-OHD levels �15 ng/mL than they were for patientsith levels greater than 15 ng/mL (58.4 � 7 years and69.87 � 80 U/L vs 41.7 � 10 years and 136 � 65 U/L,� .001) (Figure 2). In the female patients, preoperative

erum 25-OHD levels were found to be significantly lower

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442 The American Journal of Surgery, Vol 197, No 4, April 2009

hen compared to male patients (23.3 � 10.8 ng/mL vs6.8 � 7.9 ng/mL, P � .001).

valuation of patients according toncidental parathyroidectomy

The rate of incidental parathyroidectomy for patientsndergoing TT was significantly higher than that for pa-ients undergoing NTT (14/49 [28.5%] vs 2/151 [1.3%],

igure 1 Comparison of hypocalcemic and normocalcemic patieB), preoperative serum vitamin D3 level (C), and total thyroidectine in the bar).

� .001). The number of parathyroid glands identified c

uring a thyroidectomy (ie, more or fewer than 2) didot influence the rate of unintended parathyroidectomyP � .05).

orrelations

There was a positive correlation between the serum cal-ium level and serum 25-OHD level (rs � .538, P � .0001),hereas there was a negative correlation between serum

cording to age (A), preoperative serum alkaline phosphatase leveltio (D). Box plot of the parameters shows the median (horizontal

nts acomy ra

alcium level and age (rs � �.468, P � .0001) and female

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ender (rs � �.160, P � .02) and serum alkaline phospha-ase level (rs � �.506, P � .0001) and TT (rs � �.605,

� .0001) (Figure 3). We did not find a correlation be-ween the serum calcium level and incidental parathyroid-ctomy.

ogistic regression analysis

Patient age, preoperative serum alkaline phosphataseevel, 25-OHD level, and the type of thyroidectomy werendependent significant variables in the development of hy-

igure 2 Comparison of patients with low and normal preoperaalcium level (B), preoperative serum alkaline phosphatase level (Chows the median (horizontal line in the bar).

ocalcemia after thyroidectomy. The risk for postoperative T

ypocalcemia was increased 25-fold for patients older than0 years (odds ratio [OR] 25.5; 95% confidence intervalCI] 9.3–69.3), 28-fold for patients with a preoperativeerum 25-OHD level less than 15 ng/mL (OR 28.4; 95% CI1.9–67.4), and 71-fold for patients who underwent TT (OR1; 95% CI 25.3–198.9). The risk for patients older than 50ears who underwent TT increased 85-fold (OR 85.6; 95% CI4.04–112.9); the risk for patients older than 50 years witherum 25-OHD levels lower than 15 ng/mL increased 75-foldOR 75.2; 95% CI 58.99–94.01); the risk for patients witherum 25-OHD levels lower than 15 ng/mL who underwent

rum vitamin D3 level according to age (A), postoperative serumpostoperative hypocalcemia ratio (D). Box plot of the parameters

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T increased 123-fold (OR 123; 95% CI 102.23–146.76); the

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isk for patients with all three characteristics increased 182-old (OR 182; 95% CI 156.52–210.45) (Figure 4).

ollow-up

Thirteen of 49 patients with asymptomatic hypocalcemiaere treated with oral calcium supplementation only. Thirty-

ix patients with symptomatic hypocalcemia were treatedith parenteral calcium, oral vitamin D3, and calcium sup-lementation until they were discharged. Symptomatic pa-ients (n � 36) were treated parenteral calcium and calcitriol

igure 3 Relationship between the postoperative serum calciureoperative serum alkaline phosphatase level (C), and type of th

upplementation. Treatment was discontinued during the t

rst week for 13 patients with asymptomatic hypocalcemia.reatment was discontinued during the second, third,

ourth, and fifth week for 10, 9, 11, and 6 of the 36 patientsith symptomatic hypocalcemia, respectively.

omments

We investigated the prediction value of age, preoperativeerum 25-OHD, and incidental parathyroidectomy on post-perative hypocalcemia after total and near total thyroidec-

el and preoperative serum vitamin D3 level with (A), age (B),tomy (D).

omy. We found that age, preoperative low serum 25-OHD,

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nd TT were significantly associated with postoperativeypocalcemia. Incidental parathyroidectomy did not impactostoperative hypocalcemia. A positive correlation wasound between the serum calcium level and serum 25-OHDevel, whereas negative correlations were observed betweenhe serum calcium level and age, serum alkaline phospha-ase level, and TT. According to a logistic regression anal-sis, age, serum 25-OHD level, and TT were significantndependent variables associated with postoperative hy-ocalcemia. The risk for postoperative hypocalcemia foratients undergoing TT was higher than that for patientsith preoperative low serum 25-OHD levels and advanced

ge. The highest risk of postoperative hypocalcemia wasound in the patients with all of the above variables.

Postoperative hypocalcemia is one of the most frequentomplications after TT.3,4 In several studies, the incidencef hypoparathyroidism varied from 1.6% to above 50%.3–10

he causes of hypocalcemia after TT are multifactorial, andome of these causes include injury, devascularization, andnintentional excision of parathyroid glands, the number ofunctioning glands left behind, the extent of surgery, thexperience of the surgeon, hyperthyroidism, retrosternaloiter, concomitant neck dissection, and thyroid car-inoma.5–10

Recently, there has been a great deal of interest in iden-ifying perioperative factors that can predict the develop-ent of hypocalcemia after thyroidectomy.20–25 Intraoper-

tive or postoperative serum PTH measurements are usefulor the identification of patients who are at risk for hypocal-emia.23–25 Symptomatic hypocalcemia usually contributeso the length of patients’ hospital stay. Some authors em-irically propose routine oral calcium and/or calcitriol ad-inistration for patients undergoing TT to enhance the

ikelihood of early hospital discharge.20,21 In our study, theospitalization period was longer for hypocalcemic patientshan for normocalcemic patients.

TT and NTT have emerged in recent years as a surgicalption in the surgical treatment of patients with multinod-lar goiter, and it is particularly useful in endemic iodine-

igure 4 Risk factors for postoperative hypocalcemia accordingo a logistic regression analysis.

eficient regions.1,2 TT was the highest risk factor for post- p

perative hypoparathyroidism.4–7 In our study, the rate ofT for hypocalcemic patients was significantly higher than

hat for normocalcemic patients.Incidental parathyroidectomy is not uncommon during

hyroidectomy.11–14 Almost half of the parathyroid glandsre found within the thyroid gland, so some inadvertentarathyroidectomies are unavoidable. The clinical signifi-ance of incidental parathyroidectomy during thyroid sur-ery is somewhat obscure. The question of how many para-hyroids must be preserved to maintain a normal serumalcium level remains unresolved. Most authors believe that

single functioning gland is enough to restore normalarathyroid activity, but others believe that the integrity oft least 3 glands is necessary.5–8,12–14 In our study, noignificant correlation was found between incidental para-hyroidectomy and clinical and biochemical hypocalcemia.espite some controversy, most authors agree that identi-

ying parathyroid glands during thyroid surgery can result inlower incidence of hypocalcemia.5–10 However, the ability

o identify parathyroid glands during surgery did not haven impact on the rate of hypocalcemia in our study.

Vitamin D has a critical role in calcium homeostasis.itamin D deficiency has been frequently documented inedically ill and free-living populations.16,17 In Turkey,ore than 30% of different groups of subjects have vitamindeficiency.18,19 Advanced age is reported to be a major

isk factor for vitamin D deficiency. Aging is associatedith alterations in vitamin D metabolism. Studies havebserved (1) an age-related decrease in renal 1-� hydroxy-ase activity and intestinal calcium absorption, and (2) ange-related decline in the cutaneous accumulation of 7-de-ydrocholesterol, which is converted into previtamin-D3 byolar ultraviolet radiation. Insufficient calcium absorptionue to low vitamin D concentrations leads to an increase inTH secretion. Increased PTH stimulates the synthesis ofalcitriol and thereby improves calcium absorption effici-ncy.15–17 We hypothesized that patients with preoperativeormal serum vitamin D levels can compensate for postop-rative hypocalcemia due to parathyroid injury without clin-cal and laboratory indications of hypocalcemia. High fre-uency of vitamin D deficiency could be responsible for theelatively high frequency of temporary postoperative hy-ocalcemia in our study. To the best of our knowledge, ourtudy is the first prospective study performed to detect thempact of the preoperative serum 25-OHD level, age, andncidental parathyroidectomy on postoperative hypocalce-ia after TT or NTT. We found that advanced age and low

reoperative serum 25-OHD were significantly associatedith postoperative hypocalcemia.In conclusion, age, serum 25-OHD levels, and TT were

ound to be significant independent determinants of postop-rative hypocalcemia. However, incidental parathyroidec-omy did not have an impact on postoperative hypocalce-ia. The risk of postoperative hypocalcemia for patients

ndergoing TT was higher than that for patients with low

reoperative serum 25-OHD levels and advanced age. Be-

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446 The American Journal of Surgery, Vol 197, No 4, April 2009

ause postoperative hypocalcaemia may delay a patient’sischarge and add to the cost of the procedure, patients withdvanced age and low preoperative serum 25-OHD shoulde placed on calcium or vitamin D supplementation after TTo avoid postoperative hypocalcemia.

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