A Study of 875 Cases of Thyroid Cancer Observed Over a Fifteen-Year Period (1975–1989) at the King Faisal Specialist Hospital and Research Centre
1995; King Faisal Specialist Hospital and Research Centre; Volume: 15; Issue: 6 Linguagem: Inglês
10.5144/0256-4947.1995.579
ISSN0975-4466
AutoresMohammed Ahmed, Basima Al Saihati, William Greer, Abdulrahman Al-Nuaim, Siema M. Bakheet, A Abdulkareem, Stig Ingemansson, Mohammed Akhtar, Mohammed Ashraf Ali,
Tópico(s)Multiple and Secondary Primary Cancers
ResumoOriginal ArticleA Study of 875 Cases of Thyroid Cancer Observed Over a Fifteen-Year Period (1975–1989) at the King Faisal Specialist Hospital and Research Centre Mohammed Ahmed, MD, FACP Basima Al Saihati, MD, MRCP William Greer, PhD Abdulrahman Al-Nuaim, MD, FRCPC Siema Bakheet, MD A. M. Abdulkareem, FRCS(C), FICS Stig Ingemansson, MD, PhD Mohammed Akhtar, and MD, FCAP, FRCP(A) Mohammed Ashraf AliMD, FRCP(C), FCAP Mohammed Ahmed Search for more papers by this author , Basima Al Saihati Search for more papers by this author , William Greer Search for more papers by this author , Abdulrahman Al-Nuaim Search for more papers by this author , Siema Bakheet Search for more papers by this author , A. M. Abdulkareem Search for more papers by this author , Stig Ingemansson Search for more papers by this author , Mohammed Akhtar Search for more papers by this author , and Mohammed Ashraf Ali Search for more papers by this author Published Online:1 Nov 1995https://doi.org/10.5144/0256-4947.1995.579SectionsPDF ToolsAdd to favoritesDownload citationTrack citations ShareShare onFacebookTwitterLinked InRedditEmail AboutAbstractThyroid cancer (TC) is a common malignancy encountered at King Faisal Specialist Hospital and Research Centre (KFSH&RC). Of 19,885 different malignant tumors seen during the period from 1975 to 1989, there were 875 cases (4.4%) of TC. Of 1374 tumors of endocrine glands seen during the same period, 67% were thyroid neoplasms. TC represented 7.5% (618 cases) of all neoplasms in the females, second only to breast cancer. All types of TC were seen, with papillary thyroid carcinoma (PC) being the most common (79%). Anaplastic, medullary, follicular (FC), malignant lymphoma and Hürthle cell cancer accounted for 5.4%, 5.3%, 4.3%, 3.6% and 0.9% respectively. The frequency of PC was very similar (16%) in each of the third, fourth and fifth decades. The relative frequency (RF) of different types of TC was highest for PC with a ratio of 18:1 between PC and FC, which could be the highest ever reported. There was a clearly progressive increase in the number of thyroid tumors referred between 1975 and 1989. Although this increase was evident for both sexes, it was more apparent for females. There was also a distinct increase ( P<0.01) in the RF of PC from 76% (1975 to 1980) to 85% (1986 to 1989) with a decrease in FC from 9% to 2.5% over the same time periods.IntroductionDifferentiated thyroid cancer (DTC) is a relatively common malignancy with a marked international variation in the incidence of the disease. Limited data are available on the incidence and clinicopathological features of TC from the Middle East.1–23 Pertinent information regarding the demographic, epidemiological, clinical and pathological features of TC from Saudi Arabia is needed to determine the prognostic factors and to develop effective management strategies.Information on the geographical distribution of cancer has been of great value for generation of epidemiologic hypothesis and formulation of concepts for the etiology of cancer. Such information would also be valuable for making global comparisons. Until a population-based tumor registry is established in Saudi Arabia and the figures for TC made available, the only other recourse is to analyze the experience emanating from large referral centers. It is in this context that we have embarked on a study of 928 consecutive cases of thyroid tumors, observed over a 15- year period (1975 to 1989) at the King Faisal Specialist Hospital and Research Centre. The specific aims of this work were: 1) To analyze the demographic features of patients with TC seen at our institution since its inception in 1975. 2) To classify and determine the crude relative frequency (CRF) of different thyroid tumors seen at KFSH&RC between 1975 and 1989. CRF is the proportion of a given type of cancer in relation to all cases in a clinical or pathological series. 3) To determine any possible trend in the CRF of different types of TC seen at our institution.Patients and MethodsSince its inception in November 1975, we have had 1500 cases of thyroid tumors at KFSH&RC. However, this study was restricted to a retrospective analysis of information obtained in 928 consecutive cases of thyroid tumors referred to our institution between November 1975 and December 1989. Following their clinical evaluation, histopathological studies were performed by at least two pathologists on unselected surgical material removed either at KFSH&RC or obtained from the referring hospital. Representative sections from surgically resected thyroid glands were fixed in 10% buffered formaldehyde solution and embedded in paraffin. Three-micron-thick sections were stained with hematoxylin and eosin. Additional special stains were performed when necessary. In selected cases, immunohistochemical staining for thyroglobulin, calcitonin, CEA antigen, cytokeratin and vimentin were performed for precise identification of the neoplasm.We have followed the World Health Organization (WHO) classification system.24 The structural features of the tumor were recorded, including the presence of "ground glass" nuclei and psamomma bodies and an estimate of the proportion of papillary, follicular and solid histological components of the tumor in the section examined. Tumors with mixed follicular and papillary structures were classified as papillary thyroid carcinoma (PC). Any tumor that had ground glass nuclei, psammoma bodies or papillary structures was also designated as PC. For the follicular carcinoma (FC), we did not include the follicular variant of PC, Hürthle cell carcinoma (HCC), poorly differentiated (insular) carcinoma and mixed medullary-follicular carcinoma.The histological criteria for diagnosing true FC included capsular and/or vascular invasion. Tumors in which more than half of the cell population was made up of Hürthle cells were classified as Hürthle cell tumors and only those that showed evidence of angio or capsular invasion were classified as HCC. Undifferentiated tumors containing follicular or papillary structures were considered to be anaplastic carcinomas. Tumors with sarcomatous features in which epithelial structures were identified were classified as carcinomas.ResultsDemographic FeaturesKFSH&RC is a highly specialized national center for the management of cancer in Saudi Arabia. TC is a common malignancy encountered at our institution. Of 19,885 different malignant tumors seen during the period from 1975 to 1989, there were 875 cases (4.4%) of TC. Of 1374 tumors affecting endocrine glands seen during the same period, 928 (67%) cases were those of thyroid neoplasms. TC occupied sixth rank order among the 25 most common malignancies seen at our institution. It accounted for 4.7% of all malignancies in males; however, it represented 7.5% (618 cases) of all neoplasms seen in females, second only to breast cancer.Histological Classification (Table 1)Table 1 Histological classification of 928 cases of thyroid tumors at KFSH&RC (1975–1989).Histological typeNumber (%) Benign Tumors (Adenomas)53 (5.7%) Follicular Adenomas39 (4.2%)Hürthle Cell Adenomas14 (1.5%) Malignant Tumors875 (94.3%) Papillary Carcinomas694 (79.3%) Follicular Carcinomas38 (4.3%) Medullary Carcinomas46 (5.3%) Anaplastic Carcinomas47 (5.4%) Hürthle Cell Carcinomas8 (0.9%) Lymphomas32 (3.6%) Unclassified10 (1.14%)Grand Total928 (100%)Among the 928 cases of thyroid neoplasms, there were 53 cases (5.7%) of benign (39 follicular and 14 Hürthle cell adenomas) and 875 cases (94.3%) of malignant thyroid tumors. Among the malignant tumors, there were 694 (79.3%) cases of PC. Anaplastic and medullary carcinomas (MTC) had about an equal distribution of 47 cases (5.4%) and 46 cases (5.3%) respectively. The next common malignancy was FC with 38 cases (4.3%) followed by malignant lymphomas (ML) with 32 cases (3.6%). HCC was found only in a minority of eight cases (0.9%) and there were 10 cases (1.14%) of unclassified thyroid malignancies; these were excluded from an extended analysis and the data is reported mainly for the remaining 857 cases.Sex DistributionIn accordance with the usual worldwide experience, there was a female dominance of all TC except the MTC. A sex ratio (female to male) of 2.5:1 for all thyroid tumors and of 2.4:1 for the malignant cases was seen. Patients with PC had a sex distribution of 2.6:1 and those with FC showed a 3.8:1 ratio. The female predominance is especially pronounced for the ML (5.4:1) and also for HCC (8:0). Anaplastic carcinoma was seen more commonly in females at a 1.8:1 ratio. Only MTC showed a slight predominance in males at a ratio of 1:0.5.Age at Diagnosis, Split by SexThe mean age at diagnosis for females was 42 years – eight years younger than male counterparts. PC occurred with the greatest frequency in both sexes at all age groups studied. The highest frequency distribution (421/857 cases; 49%) for TC was accounted for by PC occurring at a remarkably uniform frequency of 16% per decade for each of the third, fourth and fifth decades of life.Figure 1 shows a breakdown of distribution of patients with PC according to age and sex. Although more common among females throughout the second to the eighth decades of life, this sex difference was pronounced during the third, fourth and fifth decades, accounting for 329 cases (38.4%). There were 119 cases (13.9%), 113 cases (13.2%) and 97 cases (11%) of females in the third, fourth and fifth decades respectively.FIGURE 1 Age and sex distribution of papillary thyroid carcinoma (KFSH&RC experience, 1975-1989).Download FigureTrends in Relative Frequency (RF) of TCFigure 2 shows a clearly upward trend in the RF of TC between the three study periods. Between 1975 and 1980, a total of 122 patients with TC were seen in contrast to 305 cases between 1981 and 1985 and 430 cases between 1986 and 1989. This change in the trend was almost exclusively contributed to by an increase in the relative occurrence of PC for the three time segments studied.FIGURE 2 Trend in the occurrence of malignant thyroid tumors.Download FigureWhereas between 1975 and 1980, PC accounted for only 93 of 857 cases (10.9%) of TC, its RF increased to 234 (27.3%) and to 367 cases (42.8%) for the periods from 1981 to 1985 and 1986 to 1989 respectively (Table 2). PC accounted for 76.2% of TC seen during the period from 1975 to 1980. However, during the latest study period (1986 to 1989) it accounted for 85.3% of TC seen during that period. Thus, there was a distinct increase (P<0.01) in the RF of PC over these two periods, while there was a decrease in FC from 9% to 2.5% over the same time periods.Table 2 Trends in relative frequency of thyroid cancer at KFSH&RC.Histological Type1975–19801981–19851986–1989Papillary93234367Follicular111611Anaplastic111620Medullary42517Lymphoma31415 Grand Total122305430PC dominated over other histological types by a wide margin. When compared to anaplastic and MTC, PC occurred with a RF of 15:1. The relative occurrence of PC to FC was 18:1, PC to ML 21.7:1, and to HCC it was 87:1.Although the pattern of an increase in the number of TC cases seen over the study period held true for both sexes, it was especially pronounced for females (Figure 2). Whereas for the period from 1975 to 1980 there were only 77 females, for the subsequent periods from 1981 to 1985 and from 1986 to 1989 the number of females increased progressively to 202 and 331 cases respectively.DiscussionThis study represents a general overview of TC experience at KFSH&RC. Specific and in-depth issues on this subject have been and are continuing to be reported from our center.25–29 Our study is unique because it is the only one which has systematically analyzed more than 900 consecutive cases of thyroid tumors from a single center – an experience not available so far from anywhere in the Middle East1–23 and hardly paralleled by any single major referral center anywhere within the relatively brief period of 15 years.Published information available from Saudi Arabia and the Middle East so far on the subject of TC is not only severely limited in its scope and the number of cases studied,1–14,16–23 but also is biased insofar as they have included patients undergoing surgery for diverse reasons5,7–9,13,16,17,19,20 with findings of TC on retrospective analyses of surgically removed thyroid specimens.5,7,8,11,13,14,17 In previously published studies from the Middle East, the thrust has been to report the general experiences of cancers afflicting many different body organs (including the thyroid) in a comparatively small number of patients2–4,6,14,16–19 rather than a specific study addressing TC as such. Our study, in contrast, is free of the aforementioned problems. Previously published studies have drawn such untenable conclusions as the incidence of TC in the Saudi population is high, and comparable with countries in the region, and higher than that reported from the Western world,13 despite the absence of valid epidemiological data, including a lack of national cancer statistics.3 Several of the factors mentioned above have resulted in severe bias, leading to conflicting information in reported frequencies of TC and its different types in Saudi Arabia1,5,7–9,13,15–17 and other regions in the Middle East.18–23 Lack of adherence to and/or application of the WHO criteria in the classification of TC in several reported studies from Saudi Arabia have accounted for conflicting statistics for the different histological types with gross overrepresentation in the relative frequency of follicular TC. As reported previously,28 we have strictly followed the criteria of WHO. As part of this study, all 83 cases previously diagnosed as FC at our center were restudied with stricter fidelity to the WHO criteria; only 38 fulfilled the true criteria and the rest had to be reclassified as PC. We believe such efforts have provided improved quality and a sound basis for drawing valid conclusions.Although all histological types of TC were encountered at our institution, PC was the most common malignancy observed, at a higher frequency in all age groups studied. It accounted for about 80% of all TC in our series. Of some 25 retrospective analyses of 12,855 treated cases of DTC from North and South America, eight European countries and Japan, reported between 1980 and 1990, PC comprised 50% to 89% of all cases (average 74%).30 Approximately 12,500 new cases of TC occur annually in the United States, the majority of which are papillary.31Our data can be more meaningfully compared with information generated from major referral centers such as the Mayo Clinic. Of 1736 patients with DTC who underwent primary surgery at the Mayo Clinic between 1945 and 1985, almost 90% had PC.30 Experience from the Mayo Clinic is similar to that reported from France,32 Iceland,33 Japan34 and Norway.35 In the Mayo Clinic experience, the age at diagnosis ranged from five to 93 years, which is similar to our experience. The Mayo Clinic has reported 58% of patients with PC were between the ages of 30 and 59 years.30 This contrasts with our data of 68% and 48% of all TC accounted for by PC occurring between the ages of 20 and 69 years and between the ages of 20 and 49 years respectively. The mean patient age of 44 years at the Mayo Clinic compares well with our experience. Mazzaferri, however, has reported a mean patient age of 32.3 years in his US Air Force study.36Several series have reported female predominance (62% to 81%) from both the United States37,38 and Europe39– 41 but considerably less than the female to male ratios ranging from 9:1 to 13:1 reported from Japan.42,43 In our series, the female to male ratio for PC of 2.6:1 is in keeping with the American and European experience.37–41Over the years, we have witnessed a substantial increase in the number of TC cases seen at our center. The observed increase in the number of TC patients at our institution is explained predominantly by an increase in the number of patients with PC along with a decrease in the number of patients presenting with FC. Indeed, the RF of PC is greatest compared to all other histological types. The relative occurrence of PC to FC (18:1) is different from that encountered in the United States, Europe or South America and may be the highest ever reported. Of interest is our observation of a progressive decline in the relative occurrence of FC from 9% in the period from 1975 to 1980 to 5.2% in the period from 1981 to 1985 and finally down to 2.5% in the period from 1986 to 1989. These findings in the Middle East are new and in none of the previously published data from the area1–23 are we aware of such serial observations having been reported. FC accounted for only 4% of all our TC cases; however, it accounts for about 10% to 15% of all TC reported from the United States.44,45 Each year there are about 1350 newly diagnosed patients with FC from the United States.44,45A changing pattern of TC cannot really be examined without access to several important epidemiological factors, such as accurate assessment of changes in the population status. Changing trends in RF of TC may represent several factors, consisting of increased health awareness, a change in the methods of referrals to our institution, improved methods of detection or a real increase in the incidence of the disease. Our data do not permit us to dissect these several factors.Our data do not offer an explanation for an increased RF of PC. One possibility is the recent observation of an increase in the dietary iodine intake by the population,46 not withstanding the observation by Sulimani et al. that the iodine concentration in Saudi waters is very low, ranging from 4 μmol/L to 13 μmol/L, in contrast to the iodine content in the waters reported from the United States, which is relatively high, consisting of 30 μmol/L.47 It is quite likely that a state of iodine deficiency may have prevailed previously. However, this may have been more than compensated by the recently observed increase in the intake of iodine-rich food items by the Saudi population.46 Saudis have been known to customarily take large amounts of tea, which is rich in iodine content (32 μmol/cc). Additionally, in the last two decades they have also been consuming large quantities of imported foods and local seafoods which are rich in iodine content, apart from common use of iodized salt recently. Available data indicate that following the introduction of iodine prophylaxis in other areas of the world, there had been an increase in the RF of PC over FC.48–50 The same phenomenon may hold true for Saudi Arabia as well.Over the years, the population of Saudi Arabia has been variously reported to be seven million to 12.5 million.51 El-Akkad estimated in 1982 that the incidence of all cancers in Saudi Arabia to be 80 per 100,000 per year.52 The incidence rate of cancer among Saudis in the Eastern Province, determined by the regional tumor registry, was reported to be 40 for 100,000 per year in the period from 1987 to 1988 (personal communication with Dr. Tamimi by a coauthor, AMA). This figure is similar to that observed by the Kuwaiti National Registry.18 It appears, therefore, that the incidence rate for all cancers in Saudi Arabia may lie somewhere between these two figures of 40 and 80 per 100,000. Based on these estimates and a reported population of 12.5 million, the total annual number of expected new cancer cases in Saudi Arabia could be between 5000 and 10,000 per year. With an observed CRF of TC of about 4% for both sexes, the number of newly diagnosed TC cases would be expected to range from 200 to 400 per year. However, on an average only 100 new cases of TC are observed annually at our institution. Over a 15-year period, one would expect to see between 3000 and 6000 of TC in Saudi Arabia (assuming no changes in the incidence and population statistics). It is clear, then, that the magnitude of problem for TC we are witnessing at KFSH&RC represents only a fraction of the problem. 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Volume 15, Issue 6November-December 1995 Metrics History Accepted17 April 1995Published online1 November 1995 InformationCopyright © 1995, Annals of Saudi MedicineThis work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.PDF download
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