According to MacLennan (IARC), the following information is considered basic in a population-based cancer registry: date of diagnosis; basis of diagnosis; site of primary tumour; morphology; behaviour of tumour; source of information; place of residence; ethnic group; and personal information sufficient to ensure the recognition of an individual when the same person is reported more than once to the registry [
8]. All these items were registered in the AKR, except for ethnicity. Ethnicity could be of interest to register in AO due to the Nenets indigenous population (0.5% of total population), but this was made unattainable when the Russian Federation implemented the use of "Russian" as nationality for all in identity documents. No unique identification number existed in Russia, but the identification of the individual was fulfilled in the AKR by registering the full name, gender and birth date.
Quality
The AKR is a comprehensive registry in terms of important information about each cancer case, and had few data-entry errors. The pathology department at the OD works according to the classifications of the WHO International Histological Classification of Tumours, and the diagnostic procedures, equipment and skills were found to be fully adequate.
The correctness of incidence rates is influenced by the completeness of cover. The numerator in the rate estimates is deflated if not all cases of cancer in the official resident population were captured by the health system, and/or if the AKR did not receive reports about all diagnosed cases. The denominator, on the other hand, is incorrect if the health system of AO covered more or fewer people than the official population figures. The results of the controls carried out in Severodvinsk and Kholmogory indicate that the submission of cancer reports to the AKR was not fully complete, and that the reporting varied from district to district. There was no apparent explanation for the difference in reporting between the two clinics, which both had an oncologist. Incomplete reporting has also been found to hamper the estimations of cancer incidence in established systems with a long tradition of population based cancer registration, such as in Norway [
9]. On the other hand, a fully complete cancer registry is inconceivable.
The AKR is a population-based cancer registry that is meant to cover the population of AO. Conscripts and students from elsewhere were not included in the official population figures, and cancer cases among them were not registered. There were two sub-groups of the official population of which some members were likely to survive, or die, with an undiagnosed cancer, and thereby contribute to an underestimation of incidence rates; namely, the indigenous Nenets and the poor elderly. The former mainly live in the north, and those among them who lived traditionally on the tundra as herders and hunters were less likely to seek or receive medical care from the public health care system. Poverty in Russia increased markedly in the 1990s – especially among elderly. Although health services in Russia were free and without service fees, the transport to the doctor or hospital usually had to be paid by the individual. Distances in rural areas are vast, and travelling was often uncomfortable and relatively expensive. Persons of age 80 years or older had the opportunity to transport without paying by inquiring for a requisition in advance. However, it is not unlikely that an increasing proportion of the elderly died from, or with, an undiagnosed cancer. Nevertheless, the age-specific incidence rates, all sites combined, in the older age groups did not decline within the study period.
Other sub-groups that were included in the official population figures, but possibly not fully reported to the AKR, were professional military personnel and railway and shipyard workers. These groups had their own health care privileges or systems that did not sort under the health authorities in AO, but directly under the state. This meant that patients who could not be treated within their own health system were sent to Moscow for treatment. Reporting was also done directly to Moscow, but this ended in the late 1990s for shipyard and railway workers. The OD had contact with the patients from these groups only if referred to them, and subsequently these patients would also be included in the AKR. The immediate families of these workers could also use the same health care system. The shipyard workers were located the city of Severodvinsk (population 230 000), which was a closed city due to the construction of nuclear and naval vessels at the shipyard. Figures about the number of workers in each of these groups were not publicly available, so the number of missing cases in the AKR from these two groups of workers is not readily estimated. But presumably the reduced allocation of funds after the disintegration of the USSR had the effect that fewer workers were sent to Moscow for cancer treatment. Furthermore, the retirement age for shipyard workers was as low as 45 years for women and 50 years for men, meaning that the workers were retired before they were in the highest risk groups in terms of age for most cancer types. The retirement age for male military personnel was 55 years.
Another group of concern in terms of population coverage was emigrants. People moving from AO to somewhere else in Russia were likely to register change of address, and if not, the report forms, if diagnosed elsewhere, would have been forwarded to AO. But quite a few people have emigrated to other former Soviet republics or other countries, and these people had no incentive or requirement to register. According to official figures there was a net emigration from AO of about 6000 people per year on average in the study period [
10]. However, the first census since the disintegration of the USSR, which was held during the autumn of 2002, revealed that the actual population of AO was about 90 000 people lower than the official population figures, and that 2/3 of the deficit was among men [
11]. Thus, the net emigration had been more than twice the official figures – on average. Based on age in 2002, the largest population discrepancies for men were in the age groups 35–39 and 60–64, and in the age groups 10–14 and 60–64 for women. The underestimation in the reported overall incidence rates for the whole study period should then be less than four percent due to this population factor. But since the population discrepancy varied with age group and gender, the underestimation will be of a higher magnitude for some cancer types and lower for others. The discrepancy between the official population-figures used in the present rate estimations and the real population size was presumably accumulative over time since the disintegration of the USSR. Hence, the influence of an inflated denominator on the estimated incidence rates was likely small in the early years of the study period, and more profound in the rates for 2000 and 2001.
The findings and notions discussed above indicate that the reported rates are underestimations, especially among men. However, the relative magnitudes of the site-specific cancer incidences within a gender would only have been affected by underreporting of cases if the population sub-groups discussed above were unusually prone, or less disposed, to certain types of cancer. Cancers related to the elderly were presumably of most concern in this perspective, but in the shipyard there might have been exposure to asbestos.
The proportion of cancer cases that was not captured by the health system, or diagnosed cases not caught by the AKR, can be estimated by calculating the annual proportion of cases among not-previously-registered individuals that were obtained from death certificates. The completeness of cover may also be evaluated by comparing the incidence rates of the different cancer types. The number of cases that were registered based on death certificate was 419 (2.4%) among men and 538 (3.0%) among women. The proportion varied from <0.6 percent in the years 1993–94 and 2000–01 to 5 percent in the period 1995–99. The actual proportion-level is an indication of how well the system works, and if the system worked consistently the proportion should have been fairly constant. Thus, the ability of diseased people to seek examination and treatment, and/or the function of the system, appears to have been impaired during the years of severe economic hardship. A study by Shkolnikov et al found that cancer deaths in the older age groups were under-recorded in Russia – especially in rural areas [
12]. In Norway, the proportion of registered cases obtained from death certificates was 2.6 percent for both genders in 1993 [
7].
The analysis revealed that almost 80 percent of all cases were verified histologically or cytologically. In the former USSR as a whole, 69.8 percent of the diagnoses were verified microscopically in 1989, and the proportion of cases verified varied from 62.4 to 81.3 percent between the different republics or oblasts within the union [
1]. In the neighbouring country Norway, 86 percent of all cases since 1953 have been verified histologically [
13].
Cancer incidence
The age-adjusted cancer incidence among men, all-sites combined, was similar to the incidence in Norway. But among women the incidence was more than 30 percent lower in AO [
13]. However, one should be careful in comparing the incidence rates in Russia with western countries since the competing risks of disease and death were different. The magnitude of the large difference in cancer incidence between men and women in AO was likely not due to an underestimation of rates, as the mentioned possible causes of underestimation mainly concerned men. For most cancers, the site-specific incidences found in AO were comparable both in magnitude and relative magnitude to rates for Russia in 1990, as reported by the International Agency for Research of Cancer (IARC) [
14]. The total age-adjusted incidence among men was 284/100 000 in Russia vs. 267 in AO, while 170 vs. 151/100 000 among women (ICD-9: 173 was not included in these calculations). In comparison with the IARC-reported incidence, the site-specific incidence in AO among men was higher for oesophagus, and lower for larynx and testis cancer. Also women had a higher incidence of oesophagus cancer in AO, but the incidences of cancer of the lung, breast and cervix uteri were lower [
14]. Compared to the incidence of female genital cancers in St. Petersburg, the incidences of corpus uteri and ovary cancer were lower in AO, while the incidence of cervix uteri cancer was of similar magnitude [
15]. Interestingly, the rate of stomach cancer was relatively high and colon cancer low, just as in Norway 30–40 years ago when the rates were quite different from today [
16].
The age distribution in AO, as in Russia, is different than the world standard population. Compared to the world standard (and most Western-European populations), there were relatively few older men and children below 10 years of age, as well as a small World-War II generation (age 50 – 59 in the study period). On the other hand, the post-war generation was relatively large (age 35 – 49). Thus, the distribution in AO was pear-shaped, in contrast to the pyramid-shape of the world standard population and the fairly evenly distribution of most Western-European populations. This means that the age adjustment of the incidence rates in AO contributed to an over-estimation of the cancer types that were most likely to develop in the age groups that were relatively small, and vice versa, compared to the actual burden of those cancers in the society.
The reported incidence rates in AO contribute to the discussion and generation of hypotheses concerning the role of different life-style and environmental factors in the aetiology of different cancer types. The AKR provides data for estimations and interesting insight to the cancer incidence in a northern Russian population. Using the registry for further investigations into district and age-group-specific differences in cancer incidence would shed additional light on the concerns and questions surrounding environmental and life-style aspects and cancer.