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The Relative Roles of Endemic Goiter and
Socioeconomic Development Status in the Prognosis
of Thyroid Carcinoma
Fawzy Bakiri, M.D.
Fadila K. Djemli, M.D.
Lounis A. Mokrane, M.D.
Farid K. Djidel, M.D.
BACKGROUND. It generally is accepted that the prognosis of thyroid carcinoma is
more severe in areas in which goiter is endemic. It could be assumed that this
prognosis also is less favorable in developing countries.
METHODS. Clinical features and tumor histology of 1000 consecutive patients were
Services d’Endocrinologie and Services d’Anatomie-Pathologique, Centre Pierre et Marie Curie, Hôpital, Bologhine-Hammamet, (Pr A.
Chouiter, Pr A. Bouhadef), Algiers, Algeria.
studied. Patient data from the endemic area (EA) were compared with those from
the nonendemic area (NEA). In addition, patients from the years 1966–1981 (P1)
were compared with those from 1982–1991 (P2). It is obvious that the country’s
socioeconomic status and health care system improved between the two periods.
RESULTS. The anaplastic and follicular types of thyroid carcinoma were more frequent in EAs (14% and 42.13%, respectively) than in NEAs (6.25% and 38.40%,
respectively). The frequency of the anaplastic carcinoma during P1 (16.03%) decreased by half during P2 (7.79%), whereas the frequency of follicular carcinoma
remained stable (35.85% and 40.46%, respectively). Clinically, more advanced
stages (tumor size, local and distant disseminations) were observed in the study
country than in developed countries. A clearcut improvement was observed during
P2 whereas differences between the EA and NEAs were few. Survival rates (follicular
and papillary types only) were not found to be different between EAs and NEAs
(5-year survival: 81.44% and 75.32%, respectively; 10-year survival: 67.93% and
69.52%, respectively). A significant (P õ 0.01) increase was observed between P1
and P2 (5-year survival: 72.69% and 84.80%, respectively; 10-year survival: 58.77%
and 83%, respectively).
CONCLUSIONS. Compared with endemic goiter, low socioeconomic status appeared
to be the major factor accountable for the high prevalence of advanced stage cases
and anaplastic carcinomas. Iodine deficiency appeared to play a specific role in
the increased prevalence of follicular types of thyroid carcinoma. Cancer
1998;82:1146–53. q 1998 American Cancer Society.
KEYWORDS: thyroid carcinoma, endemic goiter, iodine deficiency, developing countries, Algeria.
The authors thank Mr. M. Boushaba for his patient work.
Address for reprints: Fawzy Bakiri, M.D., Service
d’Endocrinologie, Hôpital Bologhine—Hammamet, 16060 Algiers, Algeria.
Received January 9, 1997; revisions received
May 29, 1997, and September 8, 1997; accepted September 8, 1997.
ata on thyroid carcinoma in developing countries are scarce.
Many developing countries are iodine deficient and thus the site
of endemic goiter. Algeria, a moderately advanced country in the
World Bank classification, has a large area of endemic goiter in the
north, where the majority of the population is concentrated.
It generally is accepted that the prognosis of thyroid carcinoma
is more severe in endemic areas because of the higher prevalence of
more malignant histologic forms, especially the undifferentiated ones.
These conclusions arise from studies undertaken in developed coun-
q 1998 American Cancer Society
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Thyroid Carcinoma and Endemic Goiter/Bakiri et al.
tries with moderate endemic goiter such as Switzerland, Austria, and Germany.1 – 6
The aim of this study was to assess and compare
the respective influences of endemic goiter and socioeconomic status on the prognosis of thyroid carcinoma.
One thousand consecutive records of patients admitted to the endocrine wards of Algiers between 1967
and 1991 were processed. These wards receive all thyroid carcinoma cases in the country and perform all
the diagnosis and therapeutic surgical procedures. The
mean age of the patients was 46 { 16.87 (standard
deviation) years for 231 males and 769 females. The
assessment comprised the clinical features and the
tumor histology. The clinical study more specifically
dealt with the circumstances of the carcinoma discovery and the clinical status at the time of diagnosis: the
reason that led the patient to seek medical attention
(initial sign), the goiter volume according to the World
Health Organization (WHO) classification, its history,
and the presence of lymph nodes and/or distant metastases. The WHO classification of goiter volume was
because it was available in all the patients, whereas
the exact size of the tumor occasionally was missing.
(WHO classification: 0 Å no goiter; 1 Å thyroid slightly
enlarged, visible with head tilted back; 2 Å thyroid
enlarged, visible with neck in normal position; and
3 Å thyroid greatly enlarged). Survival analysis was
performed according to the method of Kaplan and
Meier. Survival assessment concerned papillary and
follicular types of carcinoma only and took into account disease specific deaths only. The histologic
study included 17 codes rearranged according to the
WHO classification of thyroid tumors in papillary, follicular, anaplastic, medullary, and other tumors. Nonepithelial tumors, malignant lymphomas, secondary
tumors, and miscellaneous tumors also were included
in the latter class. Unclassified carcinomas with unavailable surgical specimens and cases without histologic confirmation were excluded from the study.
According to the first and second WHO classifications of thyroid tumors,7,8 mixed papillary-follicular
carcinomas were regarded as papillary. Anaplastic carcinoma was defined as a highly malignant tumor comprised in part or wholly of undifferenciated tumor.
During the time period 1982 – 1983, all specimens were
reviewed by one pathologist. After this date, diagnoses
also were made by a second pathologist from another
hospital. Diagnoses routinely were discussed between
pathologists of each department. Only very difficult
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Evolution of Some Socioeconomic Parameters between the Two
Periods of the Study
Gross national product (millions
Pediatric mortality rate (%)
No. of inhabitants per physician
Numbers indicate annual means for each period and are taken from the Bulletins de l’Office National
de Statistiques.
slices were submitted to an interward interpretation.
The interobserver variation was not evaluated.
For the purpose of this study, the patients were
divided in 2 groups according to the date of admission
to the hospital: 385 patients hospitalized between
1966 – 1981 and 615 patients hospitalized between
1982 – 1991. The socioeconomic status and the health
coverage of the country clearly improved between
these two periods (Table 1): An important increase in
the gross national product occurred between the two
periods of the study. The improvement in the health
system coverage is illustrated by the 3.5-fold increase
in the patient-to-physician ratio and the decrease in
the pediatric mortality rate.
The 2.5-fold increase in the number of thyroid
carcinomas discovered per year reported in the current study is another consequence of this improvement. The cutoff of 1981 was chosen because the most
important increase in the national income occured
during the early 1970s. The possible effect on thyroid
carcinoma only could be observed several years later.
In addition, using 1981 as the cutoff allowed the composition of two statistically comparative cohorts. The
same therapeutic protocol was applied over the two
periods of the study. In papillary and follicular types
the objective was to obtain in all patients, regardless
of the extent of disease, no radioiodine uptake on body
scintigram and suppressed levels of thyroglobulin and
thyroid-stimulating hormone, using surgery, 131iodine, and levothyroxine suppressive therapy.
The patients also were classified independently of
the date of admission based on their origin from an
endemic area (n Å 581) or a nonendemic area (n Å
236). According to the WHO criteria,9 the endemic area
was defined on the basis of a high prevalence of goiter
and a mean urinary iodine excretion õ 50 mg/g creatinine. In the nonendemic area, the goiter prevalence
was õ10% and the mean urinary iodine excretion was
ú80 mg/g creatinine.10,11 One hundred eighty-three records were rejected from this second classification be-
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General Distribution of Histologic Subtypes (%)
No. of patients
Endemic area
(P Å 0.05)
(P Å 1.1004)
Nonendemic area
(P Å 2.10 )
(P Å 3.1003)
P Å 3.1002 vs. papillary.
Results are expressed as percentages of each patient class. Patients were classified according to the period of hospitalization, then according to their origin from an endemic or a nonendemic area. Because of
insufficient data, 183 patients were excluded from this second classification.
cause of insufficient information regarding the origin
of these patients from an endemic or nonendemic area
or on their iodine intake. Between the two study periods the socioeconomic development induced some indirect and slight increase in iodine intake. However,
our last evaluation before initiating salt iodine prophylaxis in 199112 showed that the urinary iodine excretion
was still very low in the endemic areas.
There was no significant difference in economic
development or health coverage between the two
areas. The age distribution also was similar in both
areas (according to the Bulletins de l’Office National
des Statistiques).
Statistical comparison between the two patient
groups used the chi-square test or the Student’s t test
when appropriate.
Tumor Histology
Table 2 shows the general distribution of histologic
subtypes. Anaplastic carcinomas were more frequent
in endemic than in nonendemic areas. A significant
decrease in the frequency of anaplastic carcinoma was
observed during the second period of the study. There
was no adjustment for age nor differences in the histologic classification of the anaplastic types between the
two periods of the study. There was a greater prevalence of follicular type carcinoma in the endemic area;
however, this frequency was significant only when differentiated forms were taken into account (53.6% in
the endemic area versus 44.00% in the nonendemic
area; P õ 0.05). In the endemic area, the prevalence
of follicular type carcinoma was higher than that of
the papillary type.
During the second period, a significant increase
in papillary type carcinoma was observed. The increase in follicular type was not significant.
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For all the tumor cell types, there was no significant difference in patient mean age between the endemic and the nonendemic areas (papillary and follicular types: 45 { 15.72 years vs. 44 { 16.09 years, anaplastic types: 58 { 13.88 years vs. 63 { 10.18 years). A
significant (P õ 0.001) decrease in the mean age of
the patients presenting with papillary and follicular
type carcinoma was observed between the 2 periods
of the study (46 { 16.15 years vs. 42 { 15.59), whereas
there was no significant difference in the age of the
patients with anaplastic type carcinoma (56 { 13.84
vs. 59 { 13.53 years). In both regions and both time
periods the mean patient ages were higher in the anaplastic carcinomas than in the differentiated types (P
õ 0.001).
The results of clinical evaluation are shown in Table 3.
Survival rates of differentiated thyroid carcinomas
are summarized in Table 4. No significant difference
was observed between the endemic and nonendemic
areas. A significant increase was obtained during the
second study period.
With regard to tumor histology (Table 2), our results
confirmed the higher prevalence of more malignant
types of thyroid carcinoma in the endemic goiter area,
with a significantly higher frequency of anaplastic carcinomas than in the nonendemic area.
Although high (14%), this frequency was lower
than the 28.4% anaplastic prevalence reported by Riccabona in Austria13 and the 24.5% and 25.7%, respectively, reported by Löhrs et al.4 and Heitz et al.14 in
Germany. This most likely is due to the younger age of
our population, because undifferentiated carcinoma is
more prevalent in older individuals. In addition, these
studies date from the 1970s and since that time the
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Thyroid Carcinoma and Endemic Goiter/Bakiri et al.
Clinical Features (%)
No. of patients
Age (yrs)
Initial sign
Cervical lymph node
Lung metastasis
Bone metastasis
Goiter size
Goiter duration (yrs)
Goiter management
Suppressive therapy
Preoperated goiter
Cervical lymph nodes
N1 / N2 / N3
Metastasis (at least one)
Endemic area
Nonendemic area
50 (P Å 0.01)
0.86 (P Å 0.01)
6.82 (P Å 7.1003)
4.67 (P Å 0.05)
12.55 (P Å 0.03)
38.01 (P Å 1.1005)
41.33 (P Å 1.1005)
34.82 (P Å 1.1005)
15 (P Å 0.001)
14 (P Å 0.01)
11.60 (P Å 5.1004)
7.79 (P Å 0.01)
46.30 (P Å 1.1005)
34.94 (P Å 9.1003)
30.65 (P Å 0.01)
SD: standard deviation.
Indicate rare localization of metastasis, symptoms related to multiple endocrine neoplasia or medullary carcinomas discovered in relatives, fortuitously discovered microcancers in surgical cure of hyperthyroidism,
and especially goiters found by physicians during consultations for diseases that are unrelated to the thyroid gland.
Results are expressed as percentages of each patient class. Patients were classified according to the period of hospitalization, then according to their origin from an endemic or a nonendemic area. Because of
insufficient data, 183 patients were excluded from this second classification.
Survival Rates of Patients with Papillary and Follicular Thyroid Carcinomas
(n Å 237)
5 years
10 years
15 years
P õ 0.01
P õ 0.01
(n Å 523)
Endemic area
(n Å 429)
Nonendemic area
(n Å 192)
Results are expressed as percentages of each patient class. Patients were classified according to the period of hospitalization, then according to their origin from an endemic or a nonendemic area. Because of
insufficient data, 183 patients were excluded from this second classification.
incidence of anaplastic carcinoma has decreased
worldwide15,16 to approximately 5% in developed
countries,17,18 including countries with previous iodine
deficiency such as Switzerland15 and Bavaria.19
In a comparative study in Brazil covering the period 1957 – 1977, Medeiros-Neto et al.20 found a 20%
frequency for anaplastic carcinoma in the endemic
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area and a frequency of 6% in the nonendemic area,
which is similar to our findings.
A clear-cut decrease in the frequency of anaplastic
carcinoma was noted in countries with endemic goiter
regardless of whether iodine supplementation was implemented.2,4,5,6,15,21,22
Anaplastic carcinoma is believed to originate from
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CANCER March 15, 1998 / Volume 82 / Number 6
differentiated carcinoma or other thyroid pathology.6,15,16 Therefore, the history of the tumor growth
would be an important variable. Indeed, we found a
history of goiter of shorter duration during the second
period of the study (Table 3). Although significant, this
decrease appears minimal compared with the 50% reduction observed in the frequency of anaplastic types
carcinoma during the same period. The duration that
elapsed before the initial examination was slightly
longer in the endemic region, confirming the delay in
seeking medical attention for neck swelling in these
areas.13 The mean delay of 11 years in the nonendemic
area remains noteworthy. However, interpretation of
history data obtained from patient questionnaires
must be interpreted cautiously.
Our histologic data also confirm the greater frequency of follicular types in endemic areas. The frequency of follicular type carcinoma was even higher
than that of the papillary forms, whereas in nonendemic countries the percentage of papillary type carcinoma was at least double that of follicular type.
The percentage of follicular tumors in the current study was similar to those reported in European
iodine-deficient areas,2,4,5 and clearly are higher than
those reported in the U.S.A. and the Scandinavian
countries.17,18,23 – 25
It is of interest to note that a high prevalence of
follicular type carcinoma (38.4%) also was found in
the nonendemic area. Medeiros-Neto et al.20 reported similar findings in Brazil (29% in the endemic
area and 24% in the nonendemic area). This may be
explained by a lower, although normal, iodine intake
in nonendemic Algerian and Brazilian areas compared with countries without iodine deficiency. Although high, our proportion of carcinoma of follicular type in the nonendemic area remains less than
that of the papillary type.
It is recognized that the prevalence of papillary
tumors increases with iodine supply,26 reaching 71%
in Iceland27 and 85% in Japan,28 two countries with
a large iodine intake.
In spite of the improved iodine intake, the incidence of follicular thyroid carcinoma still is high in
previously iodine-deficient European countries. The
most recent publications report 38.7% in Germany19
and 27% in Switzerland.15 This could contribute to
the high mortality rates for thyroid carcinoma reported in both countries.15
As in other studies in endemic countries5,14 we
found the prevalence of follicular type carcinoma to
be stable with time. The decrease in the anaplastic
type primarily resulted in an increase in papillary
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The unchanged frequency of follicular type carcinoma and the clear-cut decrease in the incidence
of anaplastic tumors, even in the endemic areas,
would indicate a difference in the factors that make
these two forms more frequent in endemic areas.
In developed countries without endemic goiter,
it has been suggested that the incidence of follicular
type carcinoma incidence is declining slowly.23,29
This trend could not be confirmed by the study by
Spitz et al.30 in a very large series from a U.S. cancer
survey program.
From a clinical point of view (Table 3), our patients sought medical attention at late stages of the
disease, even during the second time period (22.70%
had large goiter with obvious malignancy and,
79.79% had visible goiter). The percentage of most
voluminous goiter (T3) was higher in the endemic
area. Yet, the percentage of 26.06% of such a tumor
in the nonendemic area is noteworthy. The percentage of small goiter was similar in the endemic and
nonendemic areas. In developed countries the T1
type is predominant.17 – 19,31
Levothyroxine suppressive therapy for goiter
was administered more frequently during the second period of the study in both regions, reflecting
the improved access to medical care. This treatment
also was given to 39% of patients in a study by DeGroot et al.32
Patients who underwent previous surgery comprise those who were lost to surgical follow-up or,
less frequently, those who underwent an insufficient
or inconclusive pathologic examination. They were
relatively few considering the difficult pathologic diagnosis of follicular carcinoma that was so frequent
in our series. In the series by Reinwein et al.,19 9.8%
of the patients, with a papillary type predominance,
underwent previous surgery for goiter.
Greater than 33% of our patients had lymphatic
involvement on their initial presentation. This proportion was even higher during the first period. This
finding also was more frequent in the nonendemic
area, most likely in relation with the higher frequency of papillary forms that have a high propensity for lymphophylic extention.
Our data regarding lymph node metastases during the second period are comparable to those reported in large series (26.6% by Jensen et al. in the
U.S.;17 21.3% and 35.6%, respectively, in females and
males by Asklen et al. in Norway.18 However, there
was a higher prevalence of papillary type carcinoma
in these series. In papillary only series, lymph node
invasion was more frequent (35 – 40%).32,33 In the
nonendemic area in the current study, with only pre-
W: Cancer
Thyroid Carcinoma and Endemic Goiter/Bakiri et al.
dominant papillary type carcinoma, the rate of
lymph node invasion was 45.7%. It was 34.94% in
the endemic region with a predominance of follicular type carcinoma. Brennan et al.28 reported a
lymph node invasion rate of only 6% in their series
of follicular carcinomas. Therefore, our figures indicate a high prevalence of regional lymph node extention in our patients.
During the two study periods the same number
of patients initially being treated for cervical lymph
nodes. This was more frequent in the nonendemic
area. In the series by Reinwein et al.,19 21.1% of male
and 10.3% of female patients were treated for cervical lymph nodes. These percentages, higher than
those in the current study, indicate that less attention is given to swelling lymph nodes in our population.
Approximately 8% of our patients were treated
for distant metastases. This proportion of patients
who were first seen for metastases-linked symptoms
did not vary with time. There was no difference between the two areas of the study. Our percentages
clearly were high in spite of the paucity of comparative data in the literature. Approximately 0.8% of the
patients in the series by Reinwein et al.,19 all age ú
60 years, were first seen for distant metastases.
Distant metastases were found in 26.3% of the
patients on their initial admission. Despite the decrease observed during the second period, our proportion of 23.6% remains much higher than the 6 –
8% reported in the large thyroid carcinoma series
and even higher than the elevated frequency (13 –
16%) observed in follicular type only series.23,29 Distant metastases involvement was less frequent in
papillary type only series (2 – 7.5%).32,33
The high proportion of follicular and anaplastic
carcinomas in our populations may explain our data
in part. However, this was not reflected in differences between the endemic and nonendemic areas,
in which the frequency of metastases was identical.
Thus, delay in seeking medical attention related to
low socioeconomic development, may be the main
factor in the increased frequency of metastases with
the known pejorative effect on prognosis.
Surprisingly, similar percentages of patients
with distant metastases were reported from Bavaria,
a socioeconomically developed region, by Löhrs et
al.4 (21% of distant disease in patients with papillary
type, 29% in follicular type, and 38% in patients with
anaplastic type). This study included patients seen
between 1960 and 1975.
Finally, with regard to the survival rates in our
patients with papillary and follicular type carcino-
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02-25-98 13:05:01
mas (Table 4), there was no significant difference
between the endemic and the nonendemic areas.
This was observed despite the higher frequency of
follicular type carcinoma in the endemic area. However, we found a similar proportion of patients with
distant metastases in each region. This could explain
these results, although further studies are necessary
to compare the aggressiveness of follicular and papillary thyroid carcinomas in Algeria. Survival rates
increased between the two periods of study. The improvement in the health care system appears to be
the major factor improving patient prognosis due to
a reduced delay in seeking medical attention, therefore resulting in less widespread dissemination, a
younger age at diagnosis (Table 3), and less anaplastic tumors (Table 2). It is well known that age is a
major prognosis factor in thyroid carcinoma.
In Austria, Riccabona et al.3 reported a marked
improvement (from 10% to 60%) in the 10-year survival rate for thyroid carcinoma after iodine supplementation. In Bavaria, the 5-year survival rate doubled
during 2 consecutive periods without iodine supplementation (30% between 1960 and 1975 and 60% between 1976 and 1980).4 In a recent report from Switzerland,15 where iodine deficiency remained a health
problem until the 1940s, survival rates for thyroid carcinoma were 71% at 5 years and 57% at 10 years, without any differences between the 2 periods studied
(1974 – 1980 and 1981 – 1987). These three countries
have the highest mortality rate from thyroid carcinoma
in Europe.15
Our data show a better survival rate. These findings are the more striking because both Switzerland
and Austria are no longer iodine deficient34,35 and their
socioeconomic development and health system are by
far better than those in Algeria. One explanation for
our results could be the younger age of our patients,
although the difference is small compared with the
mean patient age reported in the largest series.2,5,15,18,19
This emphasizes the importance of young age as a
favorable prognostic variable, especially because our
patients presented with worse clinical diagnoses.
In other countries the reported survival rate in
large series of differentiated thyroid carcinoma was
ú90% at 5 years and 90% at 10 years,17,36 with papillary tumors rating still better, although slightly
smaller percentages were observed in follicular type
carcinoma (90% at 5 years and 87% at 10 years).17,23,29
The current data confirme the predominance of
anaplastic and follicular type carcinoma in endemic
areas. However, causal factors appear to be different
for each type because we observed a dramatic fall
in the frequency of the anaplastic type carcinoma
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CANCER March 15, 1998 / Volume 82 / Number 6
whereas that of the follicular type remained stable
with time. The higher frequency of anaplastic carcinoma in endemic areas more likely is linked to late
detection of thyroid tumors due to inadequate socioeconomic conditions and medical standards. On the
contrary, our results confirm that there is no effect
of socioeconomic development on the frequency of
follicular type carcinoma, indicating a specific role
for iodine deficiency. However, the results of studies
from countries with previous endemic goiter indicate that the frequency of follicular type carcinoma
remains high despite correction of iodine deficiency.
This sustained effect of iodine deficiency did not
retain significance and requires further studies for
explanation. Results summarized in Tables 3 and 4
obviously indicate a more important role for socioeconomic status compared with endemic goiter or
iodine deficiency in the severity of presentation and
final prognosis of patients with thyroid carcinoma.
Thus socioeconomic development plays a major role
in thyroid carcinoma prognosis, through earlier detection of less malignant forms at earlier stages of
extention and in patients with a younger age at presentation. Certainly, better management of the disease also plays an important role, although this was
not addressed in this study.
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