original papers

Adv Clin Exp Med 2013, 22, 3, 387393

ISSN 18995276

Copyright by Wroclaw Medical University

Maciej Bagaj1, ad, f, Sylwester Gerus1, bd, Urszula Dorobisz2, c, e,

Tadeusz ukieczuk3, c, e, Beata Wikiera4, c, e

Thyroidectomy in Children:
Changing Trends and Surgical Strategies
Tyreoidektomia udzieci: zmieniajce si trendy epidemiologiczne
istrategie postpowania chirurgicznego
Department of Pediatric Surgery and Urology, Wroclaw Medical University, Poland
Department of Radiology, Wroclaw Medical University, Poland
3
Department of General Surgery, Wroclaw Medical University, Poland
4
Department of Pediatric Endocrinology, Wroclaw Medical University, Poland
1
2

A research concept and design; B collection and/or assembly of data; C data analysis and interpretation;
Dwriting the article; E critical revision of the article; F final approval of article; G other

Abstract
Background. Surgical thyroid pathology is an uncommon problem in children and due to environmental factors
may be locally-specific. Until the mid-90s, Lower Silesia had been regarded as aregion of endemic goiter but since
then abetter system of iodine prophylaxis has been introduced.
Objectives. To assess changing trends in the epidemiology of surgical thyroid diseases in children and to examine
whether they have influenced potential alterations of operative strategies during the study period.
Material and Methods. The medical records of all children operated on for thyroid disease between 1993 and 2010
in the university pediatric surgical center were retrospectively reviewed. The data regarding the indications for
thyroidectomy, details of surgical management and outcome were collected and analyzed in three periods of time
19931998, 19992004 and 20052010.
Results. There were 46, 63 and 41children operated on in the analyzed periods of time, respectively, with no significant differences regarding their age and gender. Preoperative thyroid ultrasound scan showed nodular lesions
within the thyroid gland in 145children (94.7%). The frequency of unilateral and bilateral nodular lesions was basically similar throughout the whole study. There has been asignificant decrease in subtotal resections from around
63% in the first period to less than 16% in the other two periods of the study. The reverse trend can be clearly seen
with regard to unilateral total lobectomy. Since 1999, total lobectomy or total thyroidectomy has been performed
in more than 80% of the children. Nodular goiter was the most common indication for surgical operation followed
by follicular adenoma. Malignant disease was recorded in 7children (4.6%).
Conclusions. The gradual decrease of the number of children with surgical pathology of the thyroid gland seems
to reflect an effective iodine prophylaxis. Depending on the extent of thyroid disease, unilateral lobectomy, either
alone or coupled with partial or total resection of the contralateral lobe should be astandard surgical procedure in
children (Adv Clin Exp Med 2013, 22, 3, 387393).
Key words: thyroid, children, thyroidectomy, goiter, thyroid nodule.

Streszczenie
Wprowadzenie. Chirurgiczne schorzenia tarczycy s rzadkie udzieci. Na ich wystpowanie maj wpyw czynniki
rodowiskowe. Do lat 90. XX w. Dolny lsk by uznawany za obszar endemicznego wola, od tego czasu zosta
jednak wprowadzony lepszy iskuteczniejszy system profilaktyki jodowej.
Cel pracy. Ocena zmiennych trendw epidemiologicznych schorze chirurgicznych tarczycy udzieci oraz wykonanie oceny, czy miay one wpyw na zmian strategii postpowania chirurgicznego.
Materia imetody. Przeprowadzono retrospektywn analiz dokumentacji medycznej dzieci poddanych leczeniu
chirurgicznemu wlatach 19932010 wreferencyjnym orodku uniwersyteckim chirurgii dziecicej. Szczegowej

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M. Bagaj et al.

ocenie poddano wskazania do zabiegu operacyjnego, szczegy zabiegu oraz wyniki leczenia. Dane byy oceniane
ianalizowane wtrzech okresach: 19931998, 19992004 i20052010.
Wyniki. Wanalizowanych okresach operowano odpowiednio 46, 63 i41dzieci bez istotnych rnic statystycznych
w odniesieniu do wieku i pci pacjentw. Zmiany guzkowe wykazano na podstawie przedoperacyjnego badania
USG u145dzieci (94,7%). Czsto wystpowania zmian obejmujcych jeden pat lub oba paty bya zbliona we
wszystkich analizowanych okresach badawczych. Odsetek resekcji subtotalnych bardzo wyranie zmniejszy si
z63% wpierwszym okresie do mniej ni 16% wtrzecim okresie. Odwrotny trend obserwowano wodniesieniu do
jednostronnego usunicia pata tarczycy. Od 1999roku cakowite usunicie co najmniej jednego pata byo wykonane uponad 80% dzieci. Najczstszym wskazaniem do leczenia chirurgicznego byo wole guzkowe oraz gruczolak
pcherzykowy. Nowotwory zoliwe odnotowano tylko u7dzieci (4,6%).
Wnioski. Stopniowe zmniejszanie czstoci wystpowania schorze tarczycy leczonych chirurgicznie u dzieci
wydaje si wynika ze skuteczniejszego programu profilaktyki jodowej na terenie Dolnego lska. Jednostronna
totalna lobektomia uzupeniona oczciowe lub cakowite wycicie drugiego pata powinna by przyjta jako standardowy zabieg chirurgiczny udziecka ze schorzeniem chirurgicznym tarczycy (Adv Clin Exp Med 2013, 22, 3,
387393).
Sowa kluczowe: tarczyca, dzieci, tyreoidektomia, wole, wole guzkowe.

Surgical thyroid diseases are relatively uncommon in children. Although the indications for their
operative management are predominantly based
on ahigher risk of malignancy in this age group,
strategies applied by pediatric surgeons frequently
follow those used in adult patients. Aunique feature of thyroid pathology is the fact that due to
environmental factors it may be locally-specific.
Iodine deficiency must be numbered as one of the
most important factors involved in the etiology of
diseases of the thyroid gland in the pediatric population[1, 2]. Until the mid-90s, Lower Silesia had
been regarded as aregion of endemic goiter. Since
then an effective system of iodine prophylaxis has
been introduced in Poland[3]. Taking these facts
into consideration, the authors have undertaken
a 18-year retrospective review of their experience
with thyroidectomy in children. The authors specifically aimed to assess changing trends in the epidemiology of surgical thyroid diseases in children
from Lower Silesia and to examine whether they
have influenced potential alterations of operative
strategies during the study period.

Material and Methods

The medical files of all children who underwent operative treatment due to disease of the
thyroid gland between 1993 and 2010 at the University Department of Pediatric Surgery in Wroclaw were selected from the hospital database and
subjected to a detailed analysis. The Department
of Pediatric Surgery is the only center offering an
operative management of thyroid pathology in
children in the south-west region of Poland, which
has more than 3.5 million inhabitants. All of the
children were referred to the surgical department
by apediatric endocrinologist. Preoperative diagnosis included hormonal studies, ultrasound scan
of the thyroid gland and fine-needle aspiration

biopsy in all patients. Thyroid scintigraphy was

part of the routine work-up during the first years
of the study period. Later it was ordered routinely
in the cases presenting with hyperthyreosis only.
Indications for an operative procedure were established by an endocrinologist and surgeon together.
During the first two years of the study period, the
operative procedures were performed by or under
supervision of the surgeon from the Department of
General Surgery of the Wroclaw Medical University. Since 1995 all operative procedures have been
performed by the senior author (MB).
The data regarding the patients demographics, previous medical history, clinical presentation
of thyroid disease, and the results of hormonal
and imaging studies were selected and analyzed in
all patients. The details of the surgical procedure
were extracted from the operative notes. Three
basic categories of thyroidectomy were arbitrarily
accepted for the purpose of this study, namely:
partial, subtotal and total resection, each referring
either to one lobe or to the entire gland. In each
case the final diagnosis was made by the pathologist examining the resected specimen. In order to
comply with the principal aim of the retrospective
study, all data was analyzed separately in the three
6-year consecutive periods; 19931998, 19992004
and 20052010.
Statistical significance between frequencies
was calculated by the chi-square test 2df with Yates
correction with acorresponding degree of freedom
df (df=(m1)*(n1), where mnumber of rows,
n number of columns) or if the expected value
was less than 5, by aFisher exact test (F).
A p value of less than 0.05 was required to
reject the null hypothesis. Statistical analysis was
performed using the EPIINFO Ver. 3.5.2 software
package (CDC, Atlanta, Georgia, USA).

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Thyroidectomy in Children
Table1. Pathological anatomy of the thyroid gland assessed on the preoperative ultrasound scan

Tabela1. Zmiany anatomiczne gruczou tarczowego ocenione na podstawie przedoperacyjnego badania ultrasonograficznego
Years
(Lata)

Total
(Ogem)

Only one lobe affected

(Tylko wjednym pacie)

Both lobes affected

(Zmiany wobu patach)

Diffuse
(Zmiany rozsiane)

single lesion
(pojedyncza
zmiana)

multiple lesions
(mnogie
zmiany)

single lesion
(pojedyncza
zmiana)

multiple
lesions
(mnogie
zmiany)

single lesion
(pojedyncza
zmiana)

multiple
lesions
(mnogie
zmiany)

enlargement
(powikszenie)

19931998

46

18 (39.1%)

8 (17.4%)

2 (4.3%)

12 (26%)

6 (13%)

19992004

63

29 (46%)

9 (14.2%)

7 (11.1%)

4 (6.3%)

12 (19%)

2 (3.1%)

20052010

41

16 (39%)

3 (7.3%)

6 (14.6%)

5 (12.2%)

11 (25.6%)

Table2. Surgical procedures performed in the analyzed periods of time (sub subtotal, part partial, tot total lobectomy)
Tabela2. Rodzaj leczenia operacyjnego udzieci wanalizowanych okresach (sub subototalna resekcja, part czciowa
resekcja plata, tot calkowite usunicie pata)
Years
(Lata)

Procedure (lobe/lobe)
(Typ zabiegu (pat/pat))
sub/sub

sub/

sub/part

part/part

part/

tot/

tot/tot

tot/sub

tot/part

19931998

21

N=46

45.6%

4.3%

13.04%

4.3%

8.7%

8.7%

15.2%

19992004

31

N=63

11.1%

6.3%

1.6%

49.2%

9.5%

14.3%

7.9%

20052010

14

N=41

9.7%

7.3%

34.1%

14.6%

7.3%

21.9%

4.9%

Results
One hundred and fifty children constituted the
study group. Their age ranged from 7 to 18 years
(mean 14.8). Three children were operated on twice
because of the recurrence of nodular goiter after initial subtotal resection and therefore the total number of operations was 153. There were 116 girls
(77.3%). The incidence of surgical thyroid disease
among boys in the analyzed periods was 19.6%,
25.3% and 22.5% respectively (p>0.05). There were
no statistical differences when the mean age of the
patients in each study period was studied. Preoperative thyroid ultrasound showed nodular lesions
within the thyroid gland in 145 children (94.7%).
In 8children the thyroid gland showed diffuse enlargement of both lobes. Table1 illustrates the distribution of pathological lesions of the gland in the
analyzed patients when assessed by preoperative
ultrasound scan. Comparing all three studied periods, two trends could be detected, namely decreasing number of children with diffuse enlargement of
the thyroid gland and slowly increasing incidence
of thyroid disease affecting both lobes. Only when

comparing the first and the third period were the

differences statistically significant, with ap-value of
0.0172 and x=13.8.
One hundred eleven children (74%) were euthyroid on initial presentation. In thirty-three children (22%) hormonal studies revealed hyperthyroid status. Only six children (4%) suffered from
hypothyroidism. When this data is analyzed in the
three periods of study, the incidence of euthyroid
patients rose from 63% to 76.2% between 1999 and
2004 and up to 87.7%. The distribution of patients
with hyperthyroidism was 37.2%, 18.75% and
12.2%, respectively.
In Table2, surgical procedures were summarized in the three studied periods. During the first
years, subtotal resection of the thyroid gland was
the preferable operative option regardless of the
extension of thyroid disease. This was the principle applied by the adult surgeons supervising
the first procedures performed in the clinic. It had
been followed by the authors until around 1998
unless there were indications for another type
of thyroid resection. During this period, thyroid
scintigraphy was aroutine preoperative study. The

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M. Bagaj et al.

rence of nodular disease prompted total left lobectomy six years later. The second patient had
right total and left partial lobectomy in 2001 due
to alarge single nodule in each lobe. In 2009 she
had the left lobe totally excised because of recurrence of the disease with multiple nodules within
the residual thyroid tissue. The last patient had
asingle large nodule in the left lobe and multiple
smaller nodular lesions within the right lobe and
subsequently had atotal left lobectomy and partial
excision of the right lobe. Pathology revealed follicular adenoma and nodular goiter. Due to recurrence of multiple nodules in the right lobe, it was
subsequently excised in 2008.
The results of pathological examination of the
resected specimens of the thyroid gland are presented in Table3. They include 3 specimens from
the re-operated children as well. Statistical analysis
did not reveal any significant trend with regards
to incidence of particular pathology throughout of
the study period.

lobe containing cold nodules was routinely sent for

intraoperative pathological assessment (frozen section). Most children operated in the first 2 periods
of the study had preoperative fine needle thyroid
biopsy performed in the local hospital either by
the radiologist or attending pathologist. In cases
of suspicion of malignant disease, unilateral lobectomy with intraoperative pathology was an initial
operative step. Total thyroidectomy was indicated
in children with confirmed malignancy. Unfortunately, in 3 of the first 5 patients with thyroid
carcinoma, the initial cytology was negative and all
had subtotal resection of the thyroid gland. These
patients underwent reoperation within two weeks
of the primary operative procedure with completion of total thyroidectomy and modified bilateral
cervical lymphadenectomy. Papillary carcinoma,
follicular carcinoma and medullar carcinoma were
finally diagnosed in these cases respectively. Since
1999, all patients in whom FNB revealed suspicious
cells or raised suspicion of follicular lesion underwent at least unilateral lobectomy. Such strategy
was subsequently transferred for patients with unilateral pathology of the thyroid gland, even in cases
of benign preoperative cytology. Statistical analysis has revealed significant differences between the
first and other two periods of the study with regard
to subtotal and total procedures (p < 0.05). The
differences between the two latter periods were not
significant (p=0.127).
Three patients with subtotal resections were
re-admitted for surgical management because of
the recurrent nodular goiter. The first patient with
multiple bilateral nodular lesions underwent total
right and subtotal left lobectomy in 1997. Recur-

Discussion
The limited experience of pediatric surgeons
in the treatment of thyroid pathology when compared to that of general surgeons is well reflected
in the medical literature [4, 5]. Because most pediatric patients with thyroid pathology are adolescents, they are frequently operated on by general
surgeons or endocrine surgeons in medical centers
for adults as well. The approach varies from country to country and depends on the general principles of the medical care system in agiven region.

Table3. Results of pathology reports in the operated children. NG nodular goiter, FA follicular adenoma,
G-B Graves-Basedov, SL lymphatic thyroiditis, hyperplastic hyperplastic goiter, Inv involutive goiter,
Dysh dyshormonogenetic goiter, CA thyroid carcinoma, NL neurilemmoma
Tabela3. Wyniki bada patologicznych tarczycy uoperowanych dzieci. NG wole guzkowe, FA gruczolak pcherzykowy, G-B choroba Graves-Basedowa, SL limfatyczne zapalenie tarczycy, hyperplastic wole hyperplastyczne, inv wole
inwolucyjne, dysh wole dyshormonogenetyczne, CA rak tarczycy, ML neurilemmoma
Years
(Lata)

19931998

Number
(Liczba)

46

%
19992004

63

%
20052010
%

41

Diagnosis
(Rozpoznanie)
NG

FA

FA
+NG

G-B

SL

hyper- Inv
plastic

Dysh

CA

Cyst

NL

18

10

39.1

21.7

6.5

8.7

4.3

10.8

2.2

4.3

2.1

24

16

38.1

25.4

6.3

6.3

9.4

1.6

1.6

6.3

3.1

1.6

20

48.8

12.2

14.6

2.4

4.8

9.8

2.4

2.4

2.4

Thyroidectomy in Children

Moreover, thyroid pathology in children reflects

more than that in adult patient environmental
etiology. Ionizing radiation, either therapeutic or
accidental, has for decades been regarded as the
most important carcinogenic factor[1]. Iodine deficiency is a well known cause of endemic goiter
and in the geographic areas with poor iodine supplementation, the prevalence of thyroid diseases is
still high. All these above mentioned factors indicate that the epidemiological and clinical aspects
of the surgical diseases of the thyroid gland in children may vary not only between various countries
but may change with time in the same country as
well. Present study seems to provide a very good
example of such unique features of pediatric thyroid pathology. The territory of Lower Silesia was
known as an endemic goiter region until the late
80s. Anationwide schedule of iodine salt supplementation was introduced in the 90s [3]. The
authors started their program of surgical management of children with thyroid disease in 1993. Initially, all patients were operated on by acombined
team consisting of ageneral surgeon and pediatric
surgeon. Since 1996, all children have been operated on by the same pediatric surgeon with an interest in endocrine surgery. The presented series of
patients therefore reflects the personal experience
of asingle surgeon and gives aunique opportunity
to objectively assess the changing trends in thyroid
surgery during the last two decades. This is one of
the largest series of children with surgical thyroid
pathology reported in the literature from asingle
center. Surgeons from Boston reviewed 175 consecutive children who underwent thyroid surgery
but their study period was 35years[6]. The Canadian Pediatric Thyroid Nodule Study Group published the data collected from 9 centers and during the 6-year period between 2000 and 2005, one
hundred and forty-one children underwent surgery for thyroid nodules[7]. Astl et al. presented
114children subjected to thyroid surgery between
19912000 in Prague. The average number of patients per year is similar to present authors but it
must be emphasized that the authors represented
various departments aimed principally to treat
adult patients[8]. The variability of epidemiological data renders an objective comparative analysis
almost impossible. Reviewing their own study, the
authors want to stress that the number of patients
with surgical pathology has been consistently decreasing since around 2002, presently less than 10
per year. This trend cannot be proved statistically
yet, but it seems obvious that iodine supplementation has played amajor role. The low incidence of
thyroid cancer in Lower Silesia deserves aseparate
comment. Firstly the authors did not notice any
rise in incidence of thyroid pathology in children

391
with relation to the Chernobyl accident. Secondly,
alow number of children with cancer of the thyroid gland seems surprising low when compared
to the similar studies from other pediatric surgical centers. The incidence of cancer among the
children subjected to surgical management and
reported from various centers worldwide ranged
from 8% to 43%[7, 9, 10]. Such adifference might
result from amuch lower number of children with
benign nodules among all patients treated operatively in these studies. It may well be that some
children are operated on by general surgeons and
they are simple lost from the pediatric surgical records by changes to their characteristics. Prokurat et al. presented the results of a collaborative
retrospective study on thyroid cancer in children
treated in Poland between 20002005. They were
able to collect the data of 107 children aged less
than 18years operated on in 14 pediatric surgical
centers [11]. It does not seem therefore that the
incidence of thyroid cancer in children in Lower
Silesia has been underreported.
All children reported by the authors had an ultrasound of the thyroid gland. The authors regard
this diagnostic study as the most important preoperative imaging modality. It makes it possible
to precisely assess the morphology of the thyroid
gland and cervical lymph nodes and to plan the
operative strategy. The retrospective analysis did
not reveal significant differences with regard to
pathological anatomy between the children operated on in the three study periods. The frequency
of unilateral and bilateral nodular lesions was basically similar throughout the whole study. The apparently rising trend for higher incidence of unilateral or bilateral single lesion was not statistically
significant. The number of children with diffuse
enlargement of the gland decreased, which might
reflect the better results and efficacy of other modalities of treatment. Despite all these above-mentioned results, there are discernible changes in operative strategy throughout the study period. Two
basic facts must be regarded as the most important.
First, in three of the first five children with thyroid
carcinoma, afine-needle biopsy was false-negative
and subsequently they were subjected initially to
subtotal resection of the thyroid gland. Secondly,
one child with multinodular goiter, who had had
subtotal resection of the left lobe gland, developed
recurrent nodular disease six years later and she
required secondary resection of the residual gland
tissue. These events prompted the authors to introduce amore aggressive operative approach. First,
the authors began to perform fine needle biopsy
at their institution together with a radiologist familiar with thyroid anatomy and pathology. Since
2002 unilateral lobectomy has become aminimal

392

M. Bagaj et al.

extent of thyroid resection and the authors have

abandoned bilateral subtotal resection. In children
with unilateral pathology, total excision of the affected lobe is performed while the contralateral lobe
remains intact. In children with bilateral benign
nodules, one-side lobectomy with partial excision
of the contralateral gland is carried out, unless the
extent of pathological changes dictates its subtotal
or total resection. Children with thyroid carcinoma are scheduled for total thyroidectomy coupled
with lymph node dissection and the authors do
not offer gland-sparing procedures in cases of malignancy. An analysis of their own results clearly
indicates that there has been asignificant decrease
in subtotal resections from around 63% in the first
period to less than 16% in the other two periods of
study. The reverse trend can be clearly seen with
regard to unilateral total lobectomy. Unfortunately the surgeons from other centers did not present
such a comparative analysis of their own results
in various periods of time. Scholz et al., reviewing
their 35-year experience, noted that 2/3 of children
underwent unilateral lobectomy or local excision
and subtotal bilateral lobectomy was performed in
barely 6.8% of them. It is worth emphasizing that
10 of 52 children with thyroid cancer underwent
completion thyroidectomy after the initial unilateral lobectomy[6]. In their material 3 of 7children
with thyroid cancer required early re-surgery. The
authors believe that even in cases of false-negative
preoperative diagnostic studies it is much safer to
perform unilateral reoperation than to risk bilateral injury to vital structures. Astl et al. from Prague
report an aggressive surgical approach in children
with non-malignant disease. The majority of these
patients had total thyroidectomy or hemithyroidectomy performed[8]. On the other hand it should
be emphasized that more than one third of these
patients had Graves-Basedov disease or Hashimotos toxicosis. In their surgical material the authors
report a very low incidence of such pathology,
which again illustrates well adifferent therapeutic
approach to patients with the same pathology applied in various centers. Asimilar operative strategy was presented by surgeons from Denver. The
children with thyroid nodules had unilateral resection, while in those with suspicion of malignancy,
genetic abnormalities, Graves disease or Hashimotos thyroiditis, total resection was performed[4].
In other clinical studies from the last decade, their
authors report that total unilateral or bilateral

resection of the thyroid gland were procedures

of choice leaving subtotal resections reserved for
selected cases only[7, 8, 12]. Conversely, in older
papers the number of children undergoing less
aggressive resection like nodulectomy, partial or
subtotal resections is much higher[13, 14].
The introduction of a more aggressive operative policy by the authors does not seem to be linked
to changes in thyroid pathology in their patients.
Throughout the study, children with nodular goiter
and follicular adenoma prevail. A rising incidence
of nodular pathology during the last period is accompanied by asimilar decrease in the number of
children with follicular adenoma. Interestingly, the
number of patients with follicular adenoma associated with nodular goiter increased two fold in the
last years. The incidence of other surgical pathologies was uniformly low. It is again alocally specific
distribution of surgical thyroid diseases in children
as other authors present frequently different data.
Some of them put the focus on thyroid cancer in
children, only omitting benign diseases. In the Canadian collaborative study, children with cancer
constituted 43% of patients within the whole group.
Among those with benign disease, patients with
follicular adenoma prevailed with arate of 68%[7].
The rate of nodular goiter of 16.1% was significantly
lower compared to present population of patients.
Karazugel et al., in their retrospective study of
137children, showed asimilar prevalence to present
authors of benign pathology of the thyroid gland of
93.6%, but they did not specify the final histological
diagnoses in this subset of patients[10]. Hung et al.
presented 71 patients with solitary thyroid nodule
and found the highest rate of follicular adenoma
followed by carcinoma[15].
Summarizing authors near 20-year experience,
it should be stressed that the introduction of iodine
prophylaxis has proved effective and is reflected in
the decreasing number of children with surgical
thyroid pathology. This trend refers predominantly
to children with follicular adenoma. Secondly, ultrasound scan and fine-needle biopsy have proved
to be diagnostic studies of the highest impact on the
choice of asurgical approach with cytology aimed
at detecting malignancy. Ultrasound dictates the
mode of surgical management in children with
benign cytology. Regardless of the extent of thyroid disease, unilateral lobectomy, either alone or
coupled with resection of the contralateral lobe has
become astandard surgical procedure in children.

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Address for correspondence:

Maciej Bagaj
Department of Pediatric Surgery and Urology
Wroclaw Medical University
M.Skodowskiej-Curie 52
50-367 Wrocaw
Poland
E-mail: maciej.baglaj@umed.wroc.pl
Conflict of interest: None declared
Received: 24.09.2012
Revised: 24.02.2013
Accepted: 13.06.2013