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Incidental Parathyroidectomy During Thyroid Surgery Does Not Cause Transient Symptomatic Hypocalcemia
Aaron R. Sasson, MD;
James F. Pingpank, Jr, MD;
R. Wesley Wetherington, MD;
Alexandra L. Hanlon, PhD;
John A. Ridge, MD, PhD
Arch Otolaryngol Head Neck Surg. 2001;127:304-308.
ABSTRACT
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Objectives To identify any risk factors for incidental parathyroidectomy and to
define its association with symptomatic postoperative hypocalcemia.
Design Retrospective study.
Setting Tertiary referral cancer center.
Patients Consecutive patients who underwent thyroid surgery between 1991 and
1999. Patients who underwent procedures for locally advanced thyroid cancer
requiring laryngectomy, tracheal resection, or esophagectomy were excluded.
Interventions All pathology reports were reviewed for the presence of any parathyroid
tissue in the resected specimen. Slides were reviewed, and information regarding
patient demographics, diagnosis, operative details, and postoperative complications
was collected.
Main Outcome Measure Identification of parathyroid tissue in resected specimens and postoperative
symptomatic hypocalcemia.
Results A total of 141 thyroid procedures were performed: 69 total thyroidectomies
(49%) and 72 total thyroid lobectomies (51%) . The findings were benign in
68 cases (48%) and malignant in 73 cases (52%). In the entire series, incidental
parathyroidectomy was found in 21 cases (15%). Parathyroid tissue was found
in intrathyroidal (50%), extracapsular (31%), and central node compartment
(19%) sites. The performance of a concomitant modified radical neck dissection
was associated with an increased risk of unplanned parathyroidectomy (P = .05). There was no association of incidental parathyroidectomy
with postoperative hypocalcemia (P = .99). Multivariate
analysis identified total thyroidectomy as a risk factor for postoperative
hypocalcemia (P = .008). In the entire study group,
transient symptomatic hypocalcemia occurred in 9 patients (6%), and permanent
hypocalcemia occurred in 1 patient who underwent a total thyroidectomy and
concomitant neck dissection.
Conclusions Unintended parathyroidectomy, although not uncommon, is not associated
with symptomatic postoperative hypocalcemia. Modified radical neck dissection
may increase the risk of incidental parathyroidectomy. Most of the glands
removed were intrathyroidal, so changes in surgical technique are unlikely
to markedly reduce this risk.
INTRODUCTION
THYROIDECTOMY IS typically associated with low morbidity if it is performed
with the identification and preservation of the parathyroid glands and laryngeal
nerves. Permanent or temporary dysfunction may result from conscious sacrifice
or unintentional injury to these structures. Awareness of the anatomical relationships
of the parathyroid glands is important in preventing hypocalcemia. The reported
incidence of postthyroidectomy hypoparathyroidism ranges from less than 1%
to 15%.1, 2, 3, 4, 5
Despite even careful surgical technique, temporary parathyroid dysfunction
may result. Although several factors may be responsible for transient hypocalcemia,
technical considerations include devascularization, trauma, and unintentional
excision of 1 or more parathyroid glands. A recent study reported an incidental
parathyroidectomy rate of 11%, with the majority of parathyroid tissue found
in extracapsular locations.6 Reducing the unintentional
resection of parathyroid glands might reduce the incidence of permanent and
temporary hypocalcemia. Our goal was to investigate whether there is an association
between incidental parathyroidectomy during thyroid surgery and postoperative
hypocalcemia.
PATIENTS AND METHODS
We retrospectively reviewed all standard thyroid operations (total thyroidectomies,
subtotal thyroidectomies, and lobectomies) performed by a single attending
surgeon (J.A.R.) at the Fox Chase Cancer Center, Philadelphia, Pa, between
1991 and 1999. Operations that included a simultaneous modified radical neck
or central compartment node dissection were included in the analysis. Extensive
thyroid procedures undertaken for locally advanced thyroid cancer, eg, requiring
laryngectomy, tracheal resection, esophagectomy, or median sternotomy, were
not included in the study group. Procedures for hyperparathyroidism were excluded
from the study. Parathyroid tissue intimately involved with tumor was not
considered to have been unintentionally resected.
Pathology reports on all specimens were reviewed for the presence of
parathyroid tissue. Incidental parathyroidectomy was defined as parathyroid
tissue identified in the resected specimen and distant from the tumor. Parathyroid
tissue submitted separately for histological evaluation was not considered.
For all specimens in which incidental parathyroid tissue was found, the slides
were reviewed to identify their location (intrathyroidal, extracapsular, or
in the central node compartment). The number, size, and histologic features
of all foci of parathyroid tissue were also recorded.
Patient records were reviewed, and data concerning age, sex, and preoperative
diagnosis were obtained. Operative reports were examined, and information
regarding surgical procedure (total thyroidectomy or lobectomy), neck dissection,
parathyroid autotransplantation, and number of parathyroid glands identified
was collected. Any procedure in which a thyroid lobe was removed, including
completion thyroidectomy, was considered a lobectomy. Data were gathered on
symptomatic hypocalcemia, calcium replacement, and recurrent laryngeal nerve
function. Recurrent laryngeal nerve function was determined by laryngoscopy
in all patients before and after their procedure.
Comparisons were made for unintentional parathyroidectomy and postoperative
hypocalcemia. Predictors of both outcome measures were assessed by univariate
and multivariate analyses. Univariate analysis of continuous variables was
performed using a t test, and categorical values
were determined using the Fisher exact test. Stepwise multivariate analysis
was performed using logistic regression. All reported P values were 2-tailed, and exact probabilities are provided. Significance
was determined for P .05.
Fine-needle aspiration was performed on all dominant thyroid lesions.
A diagnosis of malignancy usually prompted a total thyroidectomy. Indeterminate
cytological findings were followed up with a lobectomy and isthmectomy, unless
intraoperative findings warranted a complete thyroid extirpation. Completion
thyroidectomy was performed when malignancy was documented in the lobectomy
specimen. Thyroidectomy was performed with extracapsular removal of the thyroid
lobes, including the pyramidal lobe if present. Also, central compartment
node clearance was regularly performed for carcinomas, and modified radical
neck dissection was performed if lateral cervical lymphadenopathy was detected.
Care was taken to preserve the recurrent laryngeal nerves and all parathyroid
glands along with their blood supply as they were encountered during resection.
The location and number of parathyroid glands identified were recorded in
the operative record. After resection, the thyroid gland surface was carefully
examined for the presence of parathyroid tissue. Parathyroid glands were autotransplanted
using a standard technique. Parathyroid autotransplantation was also applied
to any parathyroid gland whose viability or vascular supply appeared questionable.
RESULTS
A total of 141 thyroid operations were performed between 1991 and 1999.
Total thyroidectomy was performed in 69 cases (49%) and thyroid lobectomy
in 72 cases (51%). The findings were benign in 68 cases (48%) and malignant
in 73 cases (52%). The patients ranged in age from 16 to 85 years (median
age, 51 years). Patient demographics, diagnosis, operative procedures, and
postoperative complications are shown in Table 1.
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Table 1. Patient Demographics, Diagnosis, Operative Procedures, Pathological
Findings, and Postoperative Complications
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Histopathological analysis identified 21 cases (15%) with incidental
parathyroid tissue. Of these 21 cases, 10 (48%) were benign and 11 (52%) were
malignant. Total thyroidectomy had been performed in 12 cases (57%), compared
with thyroid lobectomy in 9 (43%). A concomitant modified radical neck dissection
was performed in 5 cases (24%). Also, in 2 cases (10%), parathyroid autotransplantation
had been performed. The results of univariate analysis of patient variables
and incidental parathyroidectomy are shown in Table 2.
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Table 2. Univariate Analysis of Incidental Parathyroidectomy
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Microscopic examination identified a total of 26 foci of parathyroid
tissue in these 21 cases. The majority of cases demonstrated a single site
of parathyroid tissue; however, there were 4 specimens in which multiple foci
of parathyroid tissue were identified. Careful review was carried out to ensure
that these specimens represented distinct parathyroid glands. Three parathyroidectomy
specimens were unavailable for size measurements. In the remaining specimens
(88%), the size of the parathyroid tissue was determined by measuring its
greatest dimension (mean ± SEM, 3.9 ± 0.4 mm). The median size
was 3.5 mm (range, 1.5-12.0 mm). Further histopathological inspection revealed
that the majority of the parathyroid tissues were histologically normal; however,
3 foci were hypercellular, 1 was hypocellular, and 1 was adenomatous.
The parathyroid tissue in the resected specimen was found to be intrathyroidal
in 50% of the cases. Intrathyroidal location was defined as parathyroid tissue
completely contained within the thyroid capsule or completely surrounded by
thyroid tissue. Parathyroid tissue was found adjacent to the thyroid capsule
in 8 (31%) of the 26 foci found, and 5 (19%) of the glands were identified
in the central compartment specimen. The central compartment was defined as
the area between the internal jugular veins laterally, the sternal notch inferiorly,
and the hyoid bone superiorly. Detailed information regarding location of
the parathyroid glands was available from the operative reports of all patients,
except 1. There was no association between intraoperative identification of
parathyroid glands and the risk of incidental parathyroidectomy. No difference
in the rate of unintended parathyroidectomy was found when fewer than 2 parathyroid
glands were identified and when 2 or more were identified during a lobectomy
(P = .68), and there was no difference noted when
2 or fewer parathyroid glands were identified and when 3 or more glands were
identified during total thyroidectomy (P = .45).
Hence, the ability to identify parathyroid glands during surgery did not have
an impact on the rate of unintentional parathyroidectomy. Of the patients
with incidental parathyroidectomy, only 1 developed transient hypocalcemia.
This patient had 2 foci of intrathyroidal parathyroid tissue removed.
Univariate analysis identified concomitant modified radical neck dissection
as a risk factor for unintentional parathyroidectomy (P = .05). A total of 15 concomitant neck dissections were performed,
and 5 (33%) of these were associated with an incidental parathyroidectomy.
A total of 6 foci of parathyroid tissue were found (1 patient had 2). Three
of the 6 foci were intrathyroidal and 3 were in the central compartment.
In the entire series, postoperative hypocalcemia occurred in 10 patients
(7%). Of these 10 patients, 9 had transient hypocalcemia (demonstrated by
resolution of their symptoms when calcium supplementation was discontinued).
The median time to recovery was 8 weeks or less (range, 4-44 weeks). One patient
(0.7%) from this series has permanent hypoparathyroidism with circumoral numbness,
requiring limited calcium supplementation without vitamin D 6 years after
a total thyroidectomy, modified radical neck dissection, and parathyroid autotransplantation
for metastatic papillary carcinoma. Of the 21 surgical cases with an incidental
parathyroidectomy, only 1 patient (5%) developed transient hypocalcemia. In
this study group, there was no correlation between symptomatic hypocalcemia
and incidental parathyroidectomy (P = .99).
Postoperative hypocalcemia (transient and permanent) developed in 9
(13%) of 69 patients with total thyroidectomies, compared with 1 (1%) of 72
patients with thyroid lobectomies (P = .008). The
patient who developed temporary hypocalcemia after her lobectomy did so after
a completion thyroidectomy and modified radical neck dissection for metastatic
medullary carcinoma. A preoperative diagnosis of malignancy was correlated
with postoperative hypocalcemia (P = .02). Also,
modified radical neck dissection (P = .07) and parathyroid
autotransplantation (P = .07) may be associated with
hypocalcemia.
Sixty-nine total thyroidectomies were performed. With respect to postoperative
hypocalcemia, no difference was seen when 2 or fewer parathyroid glands were
identified and when 3 or more were identified (P
= .99). Hence, intraoperative identification of parathyroid glands was not
predictive of postoperative symptomatic hypocalcemia. Also, no other factor
in this cohort was found to be associated with hypocalcemia and total thyroidectomy.
Autotransplantation of parathyroid tissue was more frequently performed in
the hypocalcemic group than in the normocalcemic group (44% vs 18%) but did
not reach statistical significance (P = .10).
Stepwise multivariate logistic regression analysis showed that total
thyroidectomy was strongly associated with postoperative hypocalcemia (P = .008; odds ratio, 10.5) and that there was an increased
risk of incidental parathyroidectomy associated with modified radical neck
dissection (P = .04; odds ratio, 3.4).
COMMENT
This retrospective study did not demonstrate any relationship between
incidental parathyroidectomy and symptomatic postthyroidectomy hypocalcemia.
The incidence of incidental parathyroidectomy in this series (15%) is comparable
to that (8%-19%) reported in other series.5, 6, 7, 8, 9
The importance of parathyroid identification and preservation during thyroid
surgery has been emphasized by surgeons.3, 4, 10
Even when the surgical technique is meticulous, unintentional parathyroidectomy
may ensue. The variable location of the parathyroid glands (and particularly
the intracapsular site of some) contributes to the risk of incidental parathyroidectomy.
In our series, half of the parathyroid glands removed unintentionally were
within the thyroid capsule. A recent study reported a similar rate of 42%.6 It is doubtful that improvement in surgical technique
could completely eliminate the risk of incidental parathyroidectomy. We failed
to find any association between intraoperative identification of parathyroid
glands and incidental removal of the glands. Dissection in search of all parathyroid
glands seems unwarranted.
The average size of a normal parathyroid gland is approximately 6 mm.3, 10 In our series, the average size of
excised parathyroid tissue was 3.9 mm. Some discrepancy in size may be explained
by the histopathological sampling and processing of the specimen. Serial sectioning
of the specimen may capture only a portion of the actual parathyroid gland.
This might explain the small fragments of parathyroid tissue found in some
specimens. It has been postulated by Lee et al6
that the thyroid disease may influence the ability to find parathyroid tissue
in a thyroid specimen. The number of sections obtained and the pathologist's
diligence in examining the specimen may increase the likelihood of identification
of parathyroid tissue. There was no difference in the rate of unintentional
parathyroidectomy between procedures conducted with a preoperative diagnosis
of malignant or benign thyroid disease. Information regarding preparation
and sectioning of individual specimens is not available.
In this study, univariate and multivariate analyses identified modified
radical neck dissection as a risk factor for unintentional parathyroidectomy.
Of the 120 patients without an incidental parathyroidectomy, 10 (8%) simultaneously
underwent a modified neck dissection. In contrast, 5 (24%) of 21 patients
in whom parathyroid tissue was found underwent a neck dissection. In this
subgroup, a total of 6 sites of parathyroid tissue were identified (1 patient
had 2 intrathyroidal foci): 3 were located in the thyroid gland and 3 were
in the central neck compartment. Advanced disease with cervical adenopathy
is often accompanied by gross central compartment nodal disease as well. Hence,
it is not surprising that with more extensive procedures, unintentional parathyroidectomy
occurs more frequently. Only 1 of the 5 patients developed transient hypocalcemia.
Increased awareness when dissecting the central compartment may reduce the
risk of unintentional parathyroidectomy, but oncological principles should
not be compromised. Inspection of the resected neck dissection specimen for
parathyroid tissue, anticipating possible autotransplantation, seems prudent.
Transient hypocalcemia is common after thyroid surgery. Biochemical
hypocalcemia has been reported in as many as 83% of cases, but symptomatic
hypocalcemia is seen much less frequently.9
Injury, devascularization, and unintentional excision of parathyroid tissue
have all been cited as causes of postoperative hypocalcemia. Although many
other factors have been studied, the cause of postoperative hypocalcemia is
probably multifactorial.1
The risk of severe postoperative hypocalcemia after total thyroidectomy
is often cited as a reason not to use this procedure to treat small thyroid
neoplasms.4 Two recent series reported incidences
of 0.3% to 5.0% for temporary hypoparathyroidism and 0% to 0.5% for permanent
hypoparathyroidism.2, 3 In this
study, univariate analysis identified a preoperative diagnosis of malignant
disease (P = .02) and total thyroidectomy (P = .008) as being significantly associated with transient
symptomatic postoperative hypocalcemia. Additional factors such as modified
radical neck dissection and parathyroid autotransplantation, although not
statistically significant, may also be associated with hypocalcemia (P = .07 for both). Simultaneous neck dissection is undertaken
to treat advanced thyroid malignancy. It is not surprising that surgery for
advanced disease may be associated with transient postoperative hypocalcemia.
Permanent hypocalcemia in this study was similar to that previously reported.2, 3 The 1 patient who developed permanent
hypocalcemia underwent a total thyroidectomy, modified radical neck dissection,
and parathyroid autotransplantation for an advanced papillary carcinoma.
Multivariate analysis identified total thyroidectomy as the sole predictor
of postoperative hypocalcemia (P = .008). Analyzing
the cohort of cases in which only total thyroidectomy was performed failed
to reveal any contributing factors. In contrast to other authors,2 we did not find an association between identifying
fewer than 3 parathyroid glands and hypocalcemia (P
= .99).
We reserve parathyroid autotransplantation for glands found on the thyroid
capsule after resection or for glands that are clinically devascularized during
the operation.10 A recent study of routine
parathyroid autotransplantation during thyroid surgery reported a 1% incidence
of permanent hypoparathyroidism.11 The authors
advocate complete parathyroidectomy and parathyroid reimplantation for patients
with familial thyroid cancer, many of whom have parathyroid hyperplasia. For
patients with nonfamilial disease, they attempt to preserve at least 1 parathyroid
gland in situ and routinely autotransplant 1 or 2 parathyroid glands. Hence,
the impact of the in situ glands, compared with the transplanted ones, on
calcium homeostasis could not be determined.
Incidental parathyroidectomy is not uncommon, occurring in approximately
15% of cases in this series. Half of the glands were found within the thyroid
gland, so some unintentional parathyroidectomies are probably unavoidable.
Total thyroidectomy and a diagnosis of malignancy do not increase the incidence
of unintentional parathyroidectomy, but simultaneous modified radical neck
dissection may be a factor. No association between incidental parathyroidectomy
and symptomatic hypocalcemia was found. Hence, unintentional parathyroidectomy
does not appear to contribute to postoperative hypocalcemia.
AUTHOR INFORMATION
Accepted for publication August 31, 2000.
From the Head and Neck Surgery Section, Department of Surgical Oncology
(Drs Sasson, Pingpank, and Ridge), and the Departments of Pathology (Dr Wetherington),
Radiation Oncology (Dr Hanlon), and Biostatistics (Dr Hanlon), Fox Chase Cancer
Center, Philadelphia, Pa.
Corresponding author: John A. Ridge, MD, PhD, Head and Neck Surgery
Section, Fox Chase Cancer Center, 7701 Burholme Ave, Philadelphia, PA 19111
(e-mail: ja_ridge{at}fccc.edu).
REFERENCES
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1. Demeester-Mirkine N, Hooghe L, Van Geertruyden J, De Maertelaer V. Hypocalcemia after thyroidectomy. Arch Surg. 1992;127:854-858.
FREE FULL TEXT
2. Pattou F, Combemale F, Fabre S, et al. Hypocalcemia following thyroid surgery: incidence and prediction of
outcome. World J Surg. 1998;22:718-724.
FULL TEXT
|
WEB OF SCIENCE
| PUBMED
3. Shaha AR, Jaffe BM. Parathyroid preservation during thyroid surgery. Am J Otolaryngol. 1998;19:113-117.
FULL TEXT
|
WEB OF SCIENCE
| PUBMED
4. Schwartz AE, Friedman EW. Preservation of the parathyroid glands in total thyroidectomy. Surg Gynecol Obstet. 1987;165:327-332.
WEB OF SCIENCE
| PUBMED
5. McHenry CR, Speroff T, Wentworth D, Murphy T. Risk factors for postthyroidectomy hypocalcemia. Surgery. 1994;116:641-648.
WEB OF SCIENCE
| PUBMED
6. Lee NJ, Blakey JD, Bhuta S, Calcaterra TC. Unintentional parathyroidectomy during thyroidectomy. Laryngoscope. 1999;109:1238-1240.
FULL TEXT
|
WEB OF SCIENCE
| PUBMED
7. Öhman U, Granberg PO, Lindell B. Function of the parathyroid glands after total thyroidectomy. Surg Gynecol Obstet. 1978;146:773-778.
WEB OF SCIENCE
| PUBMED
8. Murley RS, Peters PM. Inadvertent parathyroidectomy. Proc R Soc Med. 1961;54:487-489.
PUBMED
9. Wingert DJ, Friesen SR, Iliopoulos JI, Pierce GE, Thomas JH, Hermreck AS. Post-thyroidectomy hypocalcemia: incidence and risk factors. Am J Surg. 1986;152:606-610.
FULL TEXT
|
WEB OF SCIENCE
| PUBMED
10. Lore JM, Pruet CW. Retrieval of the parathyroid glands during thyroidectomy. Head Neck Surg. 1983;5:268-269.
FULL TEXT
|
WEB OF SCIENCE
| PUBMED
11. Olson JA, DeBenedetti MK, Baumann DS, Wells SA. Parathyroid autotransplantation during thyroidectomy: results of long-term
follow-up. Ann Surg. 1996;223:472-480.
FULL TEXT
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WEB OF SCIENCE
| PUBMED
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