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Chernobyl and public health

BMJ 1998; 316 doi: https://doi.org/10.1136/bmj.316.7136.952 (Published 28 March 1998) Cite this as: BMJ 1998;316:952

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Overestimation of Thyroid Cancer Incidence after the Chernobyl Accident

Thyroid carcinoma (TC) in children and adolescents is the only type
of malignancy, significant increase of which in consequence of Chernobyl
accident (CA) is regarded to be proven (1-5). Reaction of scientific
community to the reports on its drastic increase, started 4 years after
the CA, was sceptical: it had been assumed that radiation from Iodine-131
is less carcinogenic to the thyroid than external radiation, and that a
latent period for thyroid carcinoma after an exposure should be around 10
years. There was also uncertainty about accuracy of the diagnoses (6).
High incidence and the short induction period were designated as unusual
in the UNSCEAR 2000 report, where it is also stated that the number of
thyroid cancers in children and adolescents exposed to radiation is
considerably higher than expected on the basis of previous knowledge. It
is assumed that other factors may be influencing the risk (1). Improved
diagnostics, registration and reporting were named among factors that
could have contributed to the increased cancer incidence after the CA (3).
It is also noteworthy that exposures to the Iodine-131 from medical
procedures have not demonstrated convincing evidence of an increased
thyroid cancer risk (7).

Previously we reviewed several publications overestimating radiation
induced abnormalities after CA (8-11). This article is based on experience
of histopathological practice in the former Soviet Union (12), visiting
cytological and histopathological laboratories, interviewing physicians in
the northern regions of Ukraine. Besides, information from Russian-
language professional literature can shed more light on the issue. All
quotations below are verbatim translations.

The following figures can give an estimate of the incidence increase.
In Ukraine before CA, about 12 cases of TC were registered in children and
adolescents yearly. During 5 years preceding the CA (1981-85), a total of
59 cases of thyroid carcinoma were diagnosed among patients younger than
18 years. By the year 1997, the total number of thyroid carcinoma cases,
registered in Ukraine in children and adolescents, was 577 (13). In
Belarus, TC incidence in some areas increased after the CA from 0,04 to 20
-50 cases pro 100.000 children (14). From 1992 to 2002 in Belarus, Russia
and Ukraine more than 4000 cases of thyroid cancer were diagnosed among
persons who had been children and adolescents at the time of the accident
(15).

These figures are doubtful for a pathologist acquainted with
diagnostic practice of that time. Coverage of population at risk after the
CA by medical examinations was improved. Ultrasonic thyroid screening was
performed in the population at risk, especially children and adolescents,
and large number of thyroid nodules was found. Equipment of
histopathological laboratories was poor and outdated; excessive thickness
of histological sections hindered reliable assessment of diagnostic
criteria. Gross dissection (“cutting up”) of surgical specimens was often
made with blunt autopsy knives, without rinsing specimens with running
water, which can result in tissue deformation, contamination by cells and
tissue fragments, leading to artefacts, hardly distinguishable from tumour
microembolism or angioinvasion. It could have contributed to high
frequency of tumour cell finding in blood vessel lumina (45 %) reported in
post-Chernobyl paediatric TC (14). In many laboratories celloidin
embedding was used, not allowing reliable evaluation of nuclear changes in
papillary thyroid carcinoma, in particular, the ground-glass nuclei.
Russian pathologists, having experience with thyroid tumours from
radiocontaminated areas, pointed out the “low quality of histological
specimens, impeding assessment of nuclei” (16).

False-positive diagnosis of TC was not excluded after cytological and
histological examination. If a thyroid nodule is found during ultrasonic
screening, a fine-needle aspiration biopsy (FNA) is usually performed.
Thyroid FNA cytology is known to be accompanied by a certain percentage of
inconclusive results (so-called grey zone): figures about 10-20 % are
reported from modern clinical centres (17), but in the former Soviet Union
percentage was higher, one of the causes being absence of modern
literature in hospitals and laboratories. Data about sensitivity of the
FNA in detecting post-Chernobyl childhood TC can be found in the
dissertation of A.Iu. Abrosimov (18), a well-known Russian specialist in
this area: “In a definite or presumptive form, diagnosis of carcinoma was
established in 161 from 238 cases”, whereas papillary carcinoma was
diagnosed correctly by FNA in 69,5 % and its follicular variety - only in
36,5 % of cases. As it follows from the context, presumptive diagnoses
were included among correctly diagnosed cases. After receiving a
cytological report in a presumptive form (“atypical cells” or “suspicion
of carcinoma”), depending on the nodule size, a lobectomy or subtotal
thyroid resection is performed, and the surgical specimen is sent for
pathological examination. Histopathological differential diagnosis of
thyroid nodules is again a problematic area. High quality of specimens,
required for adequate evaluation of nuclear changes in papillary
carcinoma, was not always achieved at that time. For search and evaluation
of malignancy criteria of a minimally-invasive follicular carcinoma
(capsular and vascular invasions) great number of sections can be needed,
which have not always been made. Besides, it is known from praxis that
after a radical removal of a presumed carcinoma, a pathologist can be
inclined to confirming malignancy even in case of some uncertainty.

Moreover, in the 1990s some diagnostic criteria of TC were hardly
known in the former Soviet Union, were not mentioned by Russian-language
handbooks and monographs in use at that time (19-20). The minimally-
invasive follicular carcinoma and its diagnostic criteria were absent in
the Russian-language literature. One of the most significant diagnostic
criteria of papillary carcinoma - ground-glass or cleared nuclei - was
mistranslated as something like “watch-glass nuclei moulded together”
(yadra v vide pritertykh chasovykh stekol) and presented by the most
authoritative Russian-language handbook of tumour pathology (20) as a sign
not only of papillary, but also of follicular TC, for which it is not
characteristic. Description of this phenomenon does not agree with
international literature. Nuclear changes, characteristic of papillary
carcinoma, are not visible in the illustrations of this handbook. Even
less understandable comparison with a sand-glass (another mistranslation
of the “ground-glass”) can be encountered.

Recently edited in Russia “Atlas of human tumour pathology” (22)
contains misleading information. It is written with reference to thyroid
nodules: “In severe dysplasia appear cell groups with clearly visible
atypia. Therefore, 3rd grade dysplasia is considered as an obligate pre-
cancer, which histologically is hardly distinguishable from carcinoma in
situ”. Nuclear atypia (enlargement, hyperchromatism, pleomorphism) is not
regarded in modern literature as a malignancy criterion of follicular and
papillary thyroid nodules, and the concepts of carcinoma in situ and
dysplasia are not applied to them (23). Cases of false-positive TC
diagnosis, caused by misinterpretation of nuclear atypia as a malignancy
criterion, are known. Follicular and solid varieties of papillary TC
prevailed in children and adolescents after the CA (5,21). Diagnosis of
these subtypes of papillary carcinoma is largely based on the nuclear
criteria, inadequate assessment of which can result in false-positive
conclusions, for example, in case of well-differentiated tumours of
uncertain malignant potential (24) or benign papillary nodules (25).

Physicians of histopathological and cytological laboratories in
northern Ukraine usually agreed that improved diagnostics, screening and
oncological alertness contributed to high incidence figures of post-
Chernobyl TC. Elevated interest to radiation induced malignancy as a topic
for research and publications, sometimes coupled with economic interests
(foreign help, international scientific cooperation etc.) was pointed out
as a motive for biased interpretations and fabrication of data. It should
be noted that foreign research partners, having scrupulously performed
expensive modern tests, can find themselves formally embroiled in
scientific misconduct, if their ex-Soviet peers have committed
falsification, misinterpretation, or arbitrary selection of data or
material.

Overestimation of post-Chernobyl malignancies and other radiation
induced abnormalities of the bladder and kidneys, probably resulting from
non-random case selection, was reported previously (8-11). It would be
logical to presume by analogy the same attitude also to the thyroid, the
more so, as scientific misconduct has been not uncommon in Soviet science
(26-29). “Multiplication of cases” (making several cases from one) for
elevation of statistics, which would be difficult to disclose even by
external check-ups and verifications, was pointed out by some
pathologists.

Remarkable observations about post-Chernobyl attitude to thyroid
nodules can be found in Russian-language literature: “Practically all
nodular thyroid lesions in children, independently of their size, were
regarded as potentially malignant neoplasms, requiring urgent surgical
operation”; “Aggressiveness of surgeons contributed to the shortening of
the minimal latent period” (30). Obviously, it was not the matter of true
latency shortening but of early detection. Data about verification by
expert commissions of post-Chernobyl paediatric TC in Russia provided
further evidence for false-positivity: “As a result of histopathological
verification, diagnosis of TC was confirmed in 79,1 % of cases (federal
level of verification – 354 cases) and 77,9 % (international level – 280
cases)” (18). Obviously, false-positive diagnoses remained undisclosed in
cases not covered by verification.
Another evidence in favour of false-positivity: incidence of paediatric TC
in Bryansk region, the most radiocontaminated area in Russian Federation,
having increased from zero (1986-89) up to 9 cases in 1994 and 8 in 1995,
decreased back to zero in 2001 and 1 case yearly in the subsequent 2002-
2003 years (31), disagreeing with prognoses that radiation-induced TC
morbidity in Bryansk region inhabitants, who had been children or
adolescents at the time of CA, would grow nearly exponentially until 2021
and beyond (32). These data can be explained by false-positivity in the
early period after CA with subsequent improvement of diagnostic accuracy.
In this connection, lack of statistically significant TC increase in
children born after the CA can be understood: the data pertaining to them
originated from a later period, “oncological alertness” affected these
children to much lesser degree, and there were no motives to artificially
enhance the figures.

Research on post-Chernobyl pediatric TC is in a cul-de-sac: the data
documenting its dramatic increase are felt to be inflated, but to prove it
with figures would be not easy today. Arguments presented in this article
do not suffice to deny completely the TC increase in children and
adolescents after the CA but allow concluding that high figures were at
least in part caused by improved detection of thyroid nodules with
occasional false-positive conclusions about malignancy. Besides, latent
carcinomas and borderline lesions, including well-differentiated tumours
of uncertain malignant potential (24), found by echo-screening and
diagnosed as malignancies, could have additionally contributed to the high
figures.

References:

1. UNITED NATIONS. Sources and effects of ionizing radiation. UNSCEAR
2000 Report to the General Assembly, Vol. 1. Sources and effects of
ionizing radiation. United Nations, New York, 2000. p. 15

2. IPHECA (International Programme on the Health Effects of the
Chernobyl Accident). Medical Consequences of Chernobyl Accident. Geneva,
WHO, 1995

3. Cardis E. Current status and epidemiological research needs for
achieving a better understanding of the consequences of the Chernobyl
accident. Health Phys. 2007; 93: 542-546

4. Balonov M. Third annual Warren K. Sinclair keynote address:
retrospective analysis of impacts of the Chernobyl accident. Health Phys.
2007; 93: 383-409

5. Nikiforov Y, Gnepp DR. Pediatric thyroid cancer after the
Chernobyl disaster. Pathomorphologic study of 84 cases (1991-1992) from
the Republic of Belarus. Cancer. 1994; 74: 748-66

6. Williams ED. Chernobyl and thyroid cancer. J Surg Oncol. 2006; 94:
670-7

7. Holm LE. Thyroid cancer after exposure to radioactive 131I. Acta
Oncol. 2006; 45: 1037-40

8. Jargin SV. Over-estimation of radiation-induced malignancy after
the Chernobyl accident. Virchows Arch. 2007; 451: 105-106

9. Jargin SV. Re: Involvement of ubiquitination and sumoylation in
bladder lesions induced by persistent long-term low dose ionizing
radiation in humans and Re: DNA damage repair in bladder urothelium after
the Chernobyl accident in Ukraine. 2007; 177: 794

10. Jargin SV. On the overestimation of Chernobyl NPP accident
consequences. Med Radiol and Radiation Safety (in Russian). 2007; 52 (1):
73-74

11. Jargin SV. On the overestimation of Chernobyl NPP accident
effects: urinary bladder tumors. Med Radiol and Radiation Safety (in
Russian). 2007; 52 (4): 83-84

12. Omutov M., Jargin SV. The practice of pathology in Russia.
Abstracts of the 21st European Congress of Pathology. Virchows Archiv
2007, 451(2): 277

13. Tronko MD, Bogdanova TI, Komissarenko IV, Epstein OV, Oliynyk V,
Kovalenko A, et al. Thyroid carcinoma in children and adolescents in
Ukraine after the Chernobyl nuclear accident: statistical data and
clinicomorphologic characteristics. Cancer. 1999; 86: 149-56

14. Demidchik EP, Tsyb AF, Lushnikov EF. Thyroid carcinoma in
children. Consequences of Chernobyl accident (in Russian). Moscow:
Meditsina; 1996

15. Chernobyl’s Legacy: Health, Environmental and Socio-Economic
Impacts and Recommendations to the Governments of Belarus, the Russian
Federation and Ukraine. Vienna: IAEA; 2006

16. Abrosimov AIu, Lushnikov EF, Frank GA. Radiogenic (Chernobyl)
thyroid cancer (in Russian with English summary) Arkh Patol. 2001; 63(4):
3-9

17. Chow LS, Gharib H, Goellner JR, van Heerden JA. Nondiagnostic
thyroid fine-needle aspiration cytology: management dilemmas. Thyroid.
2001; 11: 1147-51

18. Abrosimov AIu. Thyroid carcinoma in children and adolescents of
Russian Federation after the Chernobyl accident. Dissertation (in
Russian). Obninsk; 2004

19. Bomash NIu. Morphological diagnostics of thyroid diseases (in
Russian). Moscow: Meditsina; 1981

20. Kraievski NA, Smolyannikov AV, Sarkisov DS (Editors). Patho-
morphological diagnostics of human tumors. Handbook for physicians (in
Russian). Moscow: Meditsina; 1993

21. Bogdanova TI, Kozyritskiĭ VG, Tronko ND. Thyroid pathology
in children. Atlas (in Russian). Kiev: Chernobylinterinform; 2000

22. Paltsev MA, Anichkov NM. Atlas of human tumour pathology (in
Russian). Moscow: Meditsina; 2005

23. Rosai J. Rosai and Ackerman’s Surgical Pathology. v. 1, p. 515-
594. Edinburgh: Mosby; 2004

24. Fonseca E, Soares P, Cardoso-Oliveira M, Sobrinho-Simões M.
Diagnostic criteria in well-differentiated thyroid carcinomas. Endocr
Pathol. 2006; 17(2):109-17

25. Khurana KK, Baloch ZW, LiVolsi VA. Aspiration cytology of
pediatric solitary papillary hyperplastic thyroid nodule. Arch Pathol Lab
Med. 2001; 125(12):1575-8

26. Jargin SV. Examples of plagiarism from the former Soviet Union.
Dermatopathology: Practical & Conceptual 2008, 14 (2): 19. Available
from: http://derm101.com

27. Jargin SV. (2003) Scientific misconduct and International Co-
operation. BMJ Rapid Responses; published online 18 November 2003:
http://www.bmj.com/cgi/eletters/322/7281/274#40883

28. Jargin SV. Cell culture as a testing system for lipid-lowering
substances. Abstracts of the 3rd Intercontinental Congress of pathology.
Virchows Arch 2008, 452 (Suppl 1), S34

29. Russian Pathology: per Scientiam ad Veritatem.
(http://www.freewebs.com/ruspat1/; 08/10/2008)

30. Bogdanova T., Zurnadzhy L., Tronko M. et al. Pathology of thyroid
cancer in children and adolescents in Ukraine having been exposed as a
result of the Chernobyl accident. International Congress Series. 2007;
1299: 256-262

31. Parshkov EM, Sokolov VA, Proshin AD, Kurnosova LV.
Characteristics of thyroid cancer incidence in children residing in radio-
contaminated areas (in Russian). In: Chernobyl legacy. Proceedings of the
scientific and practical conference. Kaluga; 2006. Issue 4; p. 132-134

32. Tsyb AF, Ivanov VK, Matvienko EG. Medical radiological
consequences of Chernobyl accident for the population of Russia. Ibid. p.
13-21

Competing interests:
None declared

Competing interests: No competing interests

11 October 2008
Sergei V. Jargin
Pathologist
Clementovski per 6-82; 115184 Moscow, Russia