Pediatric TC Before and After the Chernobyl Accident
Prior to CA, the registered incidence of pediatric TC had
been considerably lower in the former Soviet Union (SU)
than in other industrialized countries [17,18]. In the 1981-
1985 period, the TC incidence among children ≤15 years
old in the northern regions of Ukraine was 0.1 and in
Belarus it was 0.3 per million per year [18]. For comparison,
the US Cancer Registry reported the total incidence rate
for the period 2000-2004 equal to 85 per million per year,
~2.1% being diagnosed at the age ≤20 years. According to
the Tumor Registry in Germany, the incidence was 69 in
adults, 0.2 in children 0-9 years old, 0.4 in those aged 10-14
years, 1.4 in adolescents 15-19 years old and 2.0 per million
per year in total for those ≤20 years [19]. The TC incidence
grew with advancing age also in later reports from the
United States: 0.43 (5-9 years old) to 3.5 (10-14 years) and
15.6 (15-19 years) per million per year [20,21]. Of note,
the TC incidence in Belarus in people ≤18 years old has
remained at the enhanced level (15.7 per million per year in
2012) [22,23], although the radiation factor has no longer
been active, which indicates that other mechanisms e.g.
enhanced vigilance have contributed to the high figures. It
had been known prior to CA that screening can significantly
elevate the detection rate of TC [24].
The comparatively low detection rate of TC prior to CA is often disregarded in the literature. It was claimed, for example, that the frequency of sporadic TC in Belarus during the 1971-1985 period did not differ from the global statistics [25] with reference to [6], where no such statements were found. Balonov [26] wrote about the background TC incidence in children ≤10 years old of 2-4 cases per million per year in Belarus and Ukraine, which disagrees with the data cited above [18]. The relatively low TC frequency in the contaminated areas prior to CA indicates that there were neglected cancers among residents. The screening after CA found not only small nodules but also late-stage TC interpreted as rapidly growing radiogenic cancers developing after a short latent period. Besides, there was endeavor to be recognized as Chernobyl victims to gain access to health care and other provisions [27]. Cases from non-contaminated areas must have been averagely highergrade as there was no mass screening there. Accordingly, the first wave TC cases after CA were larger and of higher grade than those diagnosed later [28], when neglected cases had been sorted out by the screening. Pediatric TCs detected during first 10 years after CA were described as relatively low differentiated, aggressive, invasive and metastatic [29]. It can be argued that the screening cannot account for differences in the patients age as a significant increase occurred only in people exposed as children and adolescents. The mechanism was selection bias: children were given more attention, and they are accessible for screening at schools and preschools; mass checkups were performed in conditions of high alertness. As mentioned above, screening can significantly elevate the registered TC incidence [24] due to a reservoir of clinically silent cancers [30]. Obviously, mechanisms such as the counting of tumors with uncertain malignant potential and microcarcinomas among cancers, false-positivity, and the registration of nonexposed patients as radiation-exposed have contributed to the incidence rise. The relatively high prevalence of latent thyroid microcarcinomas in the population is known; as discussed previously, some of these cases have been overtreated [31]. The following statement can cause misunderstanding: 77% of primary tumors were larger than 1 cm, suggesting that these were not incidental TC detected by screening [32]. In fact, the screening detected not only small nodules but also advanced TC, neglected because of the incomplete coverage of residents by medical checkups prior to CA. This predictable phenomenon was confirmed by the fact that the first wave TC cases after CA were on average larger and higher-grade than those found later [28].
Considering the misinterpretation of late-stage TC as aggressive tumors caused by radiation, some features of supposedly radiogenic cancers must characterize, on average, a later stage of the tumor progression. For example, chromosomal rearrangements of the proto-oncogene Ret, especially Ret/PTC3 fusions, frequently found in TC of patients exposed to radiation after CA at a young age [5,33], were supposed to be markers of radiogenic TC [34,35]. In fact, as discussed previously, the Ret/PTC3 frequency among TC patients probably correlates with the average disease duration and tumor progression [36]. The cohort of pediatric papillary TC after CA with prevailing Ret/PTC3, detected during the first 10 years after CA, was deemed exceptional worldwide [37,38]. In sporadic papillary TC, Ret/PTC1 fusions are more frequent than for Ret/ PTC3 [39]. In fact, post-Chernobyl cancer is exceptional not worldwide but in more developed countries, where malignancies are detected relatively early. Similarly to the former SU, Ret/PTC3 was the most prevalent Ret fusion type among TC cases from India [40]. In particular, Ret/ PTC3 fusions were reported to be frequent in Kashmir [41]. On the contrary, pediatric TC in Japan has been different from that after CA, being averagely of lower grade [42]. The Ret fusions in the pediatric TC in Japan were found only in ~10.3%; expectedly, Ret/PTC1 was the prevailing Ret fusion type [43,44]. This certifies the relatively early diagnostics of TC in Japan. Along the same lines, more mutations were found in TC from contaminated areas of Russia compared with controls from Seattle [45]. Additional details are summarized in several previous papers [36,46].
No associations between Ret/PTC and radiation doses were reported in a research of nodular thyroid lesions in the areas of Russia contaminated after CA [47]. Correlations between individual doses and Ret/PTC among atomic bomb survivors [48] could have been caused by a bias similar to that discussed here as well as by higher doses. Note that for the low-LET (linear energy transfer) radiation, acute exposures are generally more efficient than the same doses protracted over a long time; an overview of literature was provided previously [49]. The enhanced frequency of Ret/ PTC was reported in papillary carcinomas from patients who had undergone radiotherapy in childhood. Many of these patients had been treated for cancer so that the doses were comparatively high [50]. The possibility that mutations such as Ret/PTC can be induced by radiation is not denied here. Of importance is the accumulation of mutations in parallel with the tumor dedifferentiation and their association with certain steps of the neoplastic progression, Ret/PTC3 - with a later step than Ret/PTC1 [36,46].
Epidemiological Studies
The main body of evidence in favor of the cause-effect
relationship between ionizing radiation and TC among
children and adolescents after CA has come from the
epidemiologic studies e.g. those regarded pivotal [16,51-54].
In the case-control study [52], a retrospective estimation
of doses was carried out by means of questionnaires. The
research by Davis et al. [53] was similar in design. The
Chernobyl victim syndrome [27] was a widespread
phenomenon: many patients strived for higher dose
estimates to support their status of Chernobyl victims and
could provide biased information. Moreover, cancer patients
tend to recollect circumstances related to the exposure
better than controls [55]. The low participation rate among
controls was of concern because of potential selection bias
[52]. Furthermore, no widespread prophylaxis by stable
iodine occurred in the most contaminated areas of Belarus
and the Russian Federation immediately after the accident.
The measures were taken months after the accident to
provide stable iodine to children [52]. Nonetheless, the
iodine supplementation was reported to reduce the cancer
risk approximately threefold [52], although there would be
no appreciable blockage of the radioiodine uptake by the
thyroid [7]. Other questionable aspects of the study design
[52], favoring an LNT-type dose-response relationship,
have been commented on previously [56].
Cohort studies applied interviews along with thyroid dosimetry to estimate individual doses. Dosimetry was performed within 2 months after the accident (t1/2 of 131I is about 8 days). The study design included, if indicated, repeated examinations in central clinics of Kiev or Minsk [16,54]. It can be reasonably assumed that persons with higher dose estimates would be more interested in further examinations on average. In the health care system of the former SU, the thoroughness of medical examinations sometimes depended on the patients initiative. The dosedependent participation of cases could have resulted in higher estimates of risk [16]. Other epidemiologic studies on the effects of low-dose low-rate radiation may be laden by the same bias and others [24,57]. Of note, a significant increase of benign thyroid nodules was found in individuals exposed as children or adolescents to the Chernobyl fallout [58-60]. The pathogenesis of benign lesions is different from that of papillary TC [61]. The commensurate frequency increase of both benign and malignant thyroid nodules is circumstantial evidence in favor of the role of non-radiation factors. Additional details are summarized in the previous paper [1].
Furthermore, detection of thyroid cancer is heavily dependent on the intensity of screening, which can elevate the detection rate manifold [24,62]. The screening effect, improved registration and other non-radiation-related factors have played their role in the post-Chernobyl incidence increase of TC [4]. Radio- and cancerophobia contributed to the overdiagnosis of cancer, which can be illustrated by the following citation from a Russianlanguage professional publication (verbatim translation): Practically all nodular thyroid lesions, independently of their size, were regarded at that time in children as potentially malignant tumors, requiring an urgent surgical operation [63]. Obviously, mass screening in the areas where pediatric TC had been rarely diagnosed before, in the atmosphere of radio- and cancerophobia, must have resulted in overestimation [14,15].
Some Aspects of Morphological Diagnostics
Mechanisms of the overdiagnosis of TC after CA have been
discussed previously [1,15,36,46]. If a definite conclusion
about malignancy cannot be made on the basis of a fineneedle
aspiration (FNA), a histological examination
is required. The surgical specimen is forwarded to the
department of pathology, where malignancy of a radically
removed lesion could have been confirmed also in case
of uncertainty, favored by the insufficient quality and
quantity of histological specimens. Cases of false-positive
diagnosis, caused by misinterpretation of nuclear atypia
as a malignancy criterion of thyroid nodules, are known
from practice. The overdiagnosis was favored by high
tumor expectancy and limited availability of foreign
literature. FNA was started later than ultrasonography,
which additionally contributed to the false-positivity
during the 1990s. Panel reexaminations with international
participation confirmed ~78% of histological diagnoses of
post-Chernobyl pediatric TC in Russia. The cytological
diagnosis of TC was confirmed histologically in 161 of 238
cases (68%), among them papillary carcinoma in 69.5%
[64]. The cutting up of surgical specimens was performed
in many institutions with blunt knives without access to
running water, which may lead to the tissue squashing,
displacement of cells and tissue fragments [65]. This can
explain, for example, the detection of malignant cells within
blood vessels in 45% of childhood TC cases [66]. During
the 1990s, celloidin embedding was still in use, where all
nuclei appear somewhat cleared or ground-glass-like
compared to paraffin-embedded specimens, which can
be misinterpreted as a diagnostic criterion of papillary
TC. False-positive cases, not covered by reexaminations,
remained uncorrected also because histological specimens were not always stored properly, some slides were missing
or taken for consultation etc. More details and references
are in several previous papers [1,64]. The misinterpretation
of late-stage malignancies as aggressive radiogenic cancers
had consequences for the therapy [31].
The monitoring of populations exposed to low-dose radiation is important but will hardly add much reliable information on the health risks. It can be reasonably assumed that the screening and increased attention of exposed people to their health will result in new reports on the elevated cancer detection rate in exposed populations. An alternative for future work would be large-scale animal experiments. The average life duration is known to be a sensitive endpoint attributable to radiation exposure. Further experiments with different animal species would lead to a better quantification of their radiosensitivity thus enabling more precise extrapolations to humans.
CONFLICT of INTEREST
The author declares no conflict of interest.
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