A Glimpse into the Epidemiology of Geriatric Cancers in India: Report from the Indian Population Based Cancer Registries

Introduction: Indian population is aging and the cancer rates are rising. Older adults (OAs)(≥60 years) with cancer require specialized care. However, data on geriatric cancer epidemiology is scarce. Methods: The study compiled the geriatric cancer data from the published reports(2012-2014) of Indian population-based cancer registries(PBCRs). Results: Of the 1,61,363 cancers registered in the Indian PBCRs, 72,446(44.9%) occur in OAs, with 21,805(30.1%), 18,349(25.3%), 14,645(20.2%), and 17,647(24.4%) occurring in 60-64, 65-69, 70-74, and ≥75year age groups. The truncated incidence rates for OAs are 555.9,404.5, and 481.9 for males, females, and OA populations respectively. The common cancers are lung, prostate, and esophagus cancers in males, breast, cervix, and lung in females. The overall common cancers are lung, prostate, and breast. While >50% of the incident cases of prostate, and bladder cancers occurred in OAs, <20% of Hodgkin lymphoma and thyroid cancers occurred in OAs. OA cancer epidemiology has a regional variation, highest in South India and lowest in Western India. Conclusion: The current study quantifies the cancer burden in the Indian geriatric population. Understanding the epidemiology of geriatric cancers is vital to health program planning and implementation. Increased awareness, focused resource allocation, research, and national policies for streamlining care will all help to improve geriatric cancer outcomes.


Introduction
India is now the most populous country in the world [1].Combined with the increase of life expectancy by nearly one decade, from the 1980s to the 2020s, the proportion of older adults(OA) (≥ 60 years of age) is also increasing in India [2].The number of OAs is 149 million, around 10.5% of the Indian population.Also, the cancer incidence in India is increasing, termed a cancer tsunami or epidemic [3,4].Thus, there is an increasing incidence of cancers in OAs [5,6].There is also a global predicted increase in geriatric cancers [7].Though the United Nations defines 'older persons' as those aged over 60 years, different organizations and geriatric societies have used different age cutoff for OAs; the International Society of Geriatric oncology (SIOG) uses 70 years while American Society of Clinical Oncology(ASCO) uses 65 years [8,9].In India, most geriatric cancer reports include

RESEARCH ARTICLE
A Glimpse into the Epidemiology of Geriatric Cancers in India: Report from the Indian Population Based Cancer Registries patients ≥ 60 years of age due to the retirement age, the age cut-off for governmental schemes, and the average life expectancy [10][11][12].
Geriatric cancers may have a distinct biology; however, it is undisputed that OAs with cancer require special care from both disease and psychosocial perspectives [13][14][15].A comprehensive geriatric assessment(GA) changes the management of the patients, emphasizing the need for such evaluations in day-to-day oncologic practice [16] Despite the need for GA, many oncology facilities do not have access to a specialized geriatric clinic facility for the performance of GA.Oncologists have to resort to 'intuitive' assessments with basic laboratory reports for assessing the fitness of geriatric patients, which may not be ideal [16,17].There are several challenges in geriatric oncology practice in India, with a shortage of trained doctors and an uneven distribution of tertiary cancer care centers in India [18][19][20].There are very few centers with provision for specialty-based oncology practice [19,20].Fewer geriatric training programs also lead to a lack of specially trained physicians.There are only 69 seats for specialty training in geriatrics in India, as opposed to 448 emergency medicine and 5,179 general medicine seats [21].Cancer registration and population based cancer registries (PBCRs) were established in India since the 1960s, with addition of increasing network of registries over the past few decades.Though it covers only around 10% of the population, the wide distribution and the meticulous quality assurance protocols makes the PBCRs an immense data source, for compiling epidemiological data and guiding cancer care policies and health planning [22][23][24].
Understanding the burden of geriatric cancers in India and the detailed epidemiology may help to improve awareness among all the stakeholders.The healthcare systems need immense support with infrastructure and the workforce to meet the overwhelming needs of the OA population [6,25].Though there are reports of cancer epidemiology in OAs, Indian epidemiologic data is scarce, mostly from single centers/areas [1,7,[25][26][27].The current study attempts to trace the Indian geriatric cancer epidemiology comprehensively from the PBCR data.

Data sources
For mapping the epidemiology of geriatric cancers at the national level, the study accessed the reports of  [11].The Indian PBCRs are mostly urban, urban and rural or only rural [2,23].The Indian Council of Medical Research(ICMR) publishes the reports as a part of the National Cancer Registry Programme and are available at https://www.ncdirindia.org/All_Reports/Report_2020/default.aspx.

Quality of the included PBCRs
The PBCRs in India follow the standard quality norms and undergo rigorous quality checks at multiple levels.The procedure of data collection and the quality of PBCR data has been reported by prior studies [28,29].In brief, the PBCRs collect data from a prespecified geographic region.The method of cancer case detection is active, with data collected from hospitals, diagnostic centers and death certificates.The cancer cases are coded with International Classification of Diseases for Oncology (ICD-O) and entered.The cancer registries follow the international norms for quality control, and undergo multistage quality assurance checkpoints under the Indian Council of Medical Research (ICMR) [23].The percentage of deathcertificate-only, microscopically verified cases and the percentage of 'other and unknown' cancer sites are also at acceptable levels, as previously reported [30].

Calculation of the geriatric cancer rates
The data on geriatric cancers were extracted from all the reports.This study summed up the total number of cases of each cancer type as per the ICD classification (International Classification of Diseases ICD nomenclature ) among men, women, and the total population at risk (above 60) from each PBCR.The PBCR reports consist of a population pyramid providing the total population covered and the constitution of the population, in terms of age groups.

Statistical analysis
The crude rates(CR) were calculated by dividing the total number of cases by the total population; multiplied by 100,000.The age-specific incidence rates for each cancer type was calculated for this study by dividing the total number of cases of all the cancers in persons ≥60 years by the total population at risk (the sum of the population ≥60 years of age in the included PBCRs).The age-adjusted rates were calculated by multiplying each of the age-specific rates with the weight of the population of the corresponding age-group, as per the World standard population [31].The standard error was calculated as the square root of the calculated variance, as per standard method.The limits of the 95% confidence interval were calculated with the formula, x± 1.96 s/√n (x= mean, s=standard error, n=sample size.The percentage of geriatric cases among each cancer type, age distribution, and the common cancers in the geriatric age group were analysed.For each PBCR, truncated incidence rates and age-standardized rates were calculated for comparison.Further, regional data was summarized for comparison of data from different parts of India (North and Central India, East and NE India, South India, and West India).The study was reported in line with the recommended REPCAN guidelines [32].

Ethical concerns
The data was collected from the published reports of the PBCRs available on a public database.Moreover, only depersonalized data was available in PBCRs.Hence ethical clearance was not required.

Results
In the reported period, there were  [33].The common cancers in OAs reported in the international study were prostate, lung, colorectal, liver and stomach cancers [7].Though prostate cancer is a disease of the OAs, [34] lung cancer seems to have a higher incidence than prostate cancer in Indian OAs.However, there is no robust screening program for prostate cancers in India, as compared to globally, hence the detection rates may be lower [35,36].
Comparing to the common cancers and their estimated crude incidence rates in persons between 30-59 years; breast (CR 45.2), cervical (CR 31.5),ovarian (CR 10.4), oral cavity (CR 7) and esophageal cancers(CR 4.6) are common in women; and oral cavity (CR 22.8), esophagus(CR 8.4), lung(CR 7.2), colorectal (CR 6.6) and stomach (CR 6.6) cancers are common in men [37] (Table 2).Mathur et al have detailed the Adolescent and Young adult (AYA) cancer epidemiology in India, reporting highest incidence rates of breast, thyroid, mouth and brain/nervous system cancer [29].The geriatric cancer incidence rates of 556 and 405 per 100,000 men and women are more than ten times the rates reported in the AYA population (22.2 and 29.2 respectively among men and women) [29].The cancer rates in the 30-59 years of age are also much lower, 130.7 and 123.5 respectively among men and women [37].As expected the cancer occurrence patterns are different in the different age groups.The cancers with a genetic basis of causation are found at an earlier age, while cancers with a predominant causation due to environmental exposure are seen at later ages.Also, there are some cancers which are seen in OAs, like prostate cancer and plasma cell neoplasms, leading to an increased proportion of such cancers in the OA age group, compared to lymphoid leukemias, Hodgkin lymphoma and thyroid malignancies which are seen in younger patients.
Cervical cancer is also among the common cancers among the Indian OAs, as the median age of occurrence of cervical cancer in India is 56 years and nearly one-third of the cervical cancer cases occur in the 50-59 year age group [38,39].The OAs with cervical cancer form only around 35% of the total numbers, with the age groups of 60-64, 65-69, 70-74 and 75+ years contributing 13%, 10%, 6% and 7% each.Though the rates of cervical cancer are decreasing, cervical cancer is still the second most common cancer among women in India [33].In India, breast cancer on an average has a lower age of onset, compared to global breast cancer epidemiology, probably explaining the lower incidence of breast cancer among OAs when compared to the overall numbers [40][41][42].Though the burden of head and neck cancers is high among the OAs, the current study analyzed the subsites of mouth (ICD C03-06) and tongue (C01-02) separately as per the PBCR data (Table 2).Prostate and esophageal cancers among men and breast and cervical cancers among women are also common among the OA population in Sub-Saharan Africa, according to another PBCR-based study.However, cancers in OAs represented only 34% of the incident cancers in the report, compared to nearly 50% in India [43].
groups respectively which constituted 13.5%, 11.4%, 9.1%, and 11% of the total number of cases reported in the PBCRs.The age-specific incidence rates for ≥ 60 years were 555.9 per 100,000 males and 404.5 per 100,000 women (Table 1).
Among men, the most common cancer sites in the OAs were lung, prostate, esophagus, stomach and mouth cancers.In contrast, the corresponding sites among OA women were breast, cervix, lung, ovary and esophagus.The most common sites overall in the geriatric population were lung, prostate, breast, cervix and esophageal cancers.(Table 2) The incidence difference between male and female cancers was most apparent for lung, larynx, stomach, esophageal, hypopharynx, bladder liver, tongue, mouth, colorectal, kidney malignancies (male >female) while gallbladder cancers were more common in women OAs (Supplementary Tables 1 and 2).
On analyzing the proportion of cases occurring in OAs, 88.8% of prostate cancer occurred in OAs.OAs with cancer formed more than 50% of the incident cancers in sites like bladder, ureter, lung, multiple myeloma and larynx and <20% of Hodgkin lymphoma, thyroid, lymphoid leukemias, adrenal and testicular malignancies.(Supplementary Table 3) Further, exploring the geriatric cancer rates in each registry, the rates were higher in Kamrup, Mizoram, Delhi, and Mumbai registries while lowest in Barshi, Wardha, Aurangabad, and Tripura.(Table 3) To understand the regional variations better, the PBCRs were grouped into four regions -North and Central, West, East and NE, and South, including five, six, twelve, and four registries in each area.(Supplementary table 4) The ASR was highest in South India (556.9) and lowest in the West (410.4).The proportion of geriatric cancers was also lowest in North/Central registries, where only 40.6% of all cancers occurred in OAs.

Discussion
The current study systematically explores the cancer burden, incidence rates and the regional variations of geriatric cancers in India from the consolidated actuarial data of the Indian PBCRs.The study reports that 44.9% of the total incident cancers occur in OAs in India, though the truncated incidence rates of geriatric cancers are lower, nearly half of the world rates [7].The geriatric cancer rates also vary markedly across the nation, with the highest rates in South India and the lowest rates in West India.
The lower geriatric cancer rates in India may reflect the overall lower cancer incidence rates in India [3,5].The international report on geriatric cancer epidemiology has looked into the estimated cancer cases in persons older than 80 years rather than the actual numbers [26].The rates of cancers varied from 550 (India), 745 (south Central Asia excluding India),967 (Africa) and 1613 (World), revealing that the cancer rates are lower in India, even among the OAs, though comparable with Africa and some other parts of Asia [26].However, the changes between the top cancers in the international and national lists reflect the differences in cancer epidemiology overall, as cervical, oral cavity and esophageal cancers are    Table 2. A) Lists the top ten cancers and their incidence rates in the overall geriatric, men and women in India from the derived cancer incidence rates from the PBCR data (2012-2014); B) Lists the common cancers in the 30-59 years age group * *The cancer incidence rates in the 30-59 years are estimated from the GLOBOCAN projections [37].
Similar to the overall cancer epidemiology, OA males have a higher incidence of lung, head and neck and bladder cancers while thyroid and gall bladder malignancies are more common in older women [44].In a prior geriatric cancer epidemiology study from the Mumbai PBCR(2002-04), Yeole et al. [10] reported that lung, prostatic and breast and cervical cancers are the common cancers in OAs, similar to the current study.The current geriatric cancer rates of 555.9 and 404.5 per 100000 male and female OAs seem comparable with the older report from Mumbai.However, the lung cancer incidence seems higher in OA women and liver cancer incidence lower in OA men in the current study.However, the prior report explored the cancer incidence of only a single urban registry.
India is one of the most populous nations in the world, with a diverse population.The cancer epidemiology is distinct and varies between the different regions in India [45].The country has a 'nation with nation' pattern of cancer incidence with vast variations in cancer incidence and distribution among the different states of India [45,46].Since each portion of India has distinct sociocultural, genetic and environmental profiles, the differences in cancer incidence may merely reflect such disparities.Even carcinogen exposures like arecanut have a wide regional disparity between states; there are also known genetic polymorphisms which may affect the carcinogenicity of the same [47][48][49].Some cancers in India are known to have geographical clustering due to various putative factors, like gallbladder cancer in the Northern part of India.Infection associated cancers like hepatitis B related hepatocellular cancer and human papilloma virus(HPV) associated cancers also show geographic variations in India [50,51].Keeping with the unique epidemiology and population structures, the distribution of geriatric cancers varies across India.The study noted the highest geriatric age-standardized rates from Kamrup (Assam), Mizoram, Delhi and Mumbai and the lowest rates from the rural registry of Barshi and Wardha in Madhya Pradesh.The overall rates of cancer are highest in Aizawl (269.4),Kamrup, Mizoram and Delhi also with relatively higher rates compared to the rest of the country [29].The North Eastern(NE) part of India consists of an ethnically and culturally distinct population, with a distinct genetic profile [52][53][54].The tobacco use in the NE is among the highest in India, with a relatively high proportion of tobacco associated cancers, contributing to the major cancer burden [55,28].In addition to the increased cancer burden, NE region is also plagued with limited infrastructural and manpower resources and other logisitic isuses in access to quality cancer care, leading to DOI:10.31557/APJCP.2024.25 [56,57].Further analyzing the consolidated regional incidence rates, South India has higher age-standardized rates than the other parts of India, an expected finding, as two of the four included Southern PBCRs are in Kerala and the other two are major cities in India.As a state, Kerala boasts higher life expectancy, the highest health index and an increased proportion of OAs (13%) [58,59].With the increasing availability of healthcare facilities and rising life expectancy, bigger metropolitan cities like Chennai, Mumbai, Delhi and Bengaluru have higher geriatric cancer rates, as seen in the current study.Though the PBCRs are scattered across India, most of them cover predominatly urban areas, with resultant heterogeneity in the data obtained [22].Information on the OA cancer trends in different parts of India will help in planning national and state policies appropriately for OAs with cancer.
The current study looks at the population-based data while the hospital based data may give a different perspective on the geriatric cancer burden.In a hospitalbased study from India, 28% of the total new cancer cases in a hospital occurred in OAs, with a predominance of cervical, gallbladder, laryngeal and urinary bladder cancers [60].A report from a rural hospital registry in South India reported the common cancer sites as head and neck, lung, breast and gastrointestinal [61].The separate analysis of each head and neck cancer subsite as per the ICD classification may also explain the lower representation of head and neck cancers in our geriatric cancer list.In a ten-year analysis from Nigeria, authors reported 33.7% geriatric cancers among the incident cancers.The common cancers were prostate, cervical, breast, colorectal and gastric cancers [62].
The PBCRs in India cover only around 10% of the total population of India, which is a significant limitation of this study [23,30].However, many registries are over three decades old and contribute to the international epidemiological databases.There are also strict quality assurance checkpoints to ensure adherence to the international norms for cancer registries.Without national electronic medical records, PBCR may be the richest source of information about cancer epidemiology.Also, the reported incidence rates are close to the estimated rates reported in the international study on cancers in OAs [7].
Studies on the epidemiology of geriatric cancers are essential for improving outcomes of OAs with cancer.Improvement in outcomes requires interventions at different levels.At the institute/tertiary care center levels, provision for specialized geriatric oncology clinics or at least prioritization of geriatric patients given their particular needs and mandatory inclusion of geriatric assessment reports in multidisciplinary tumor board discussions may help to improve care for OAs.Academic research institutes require allocated research funds for conducting research in OAs, a population subgroup usually excluded from most clinical trials.International and national organizations are trying to enhance knowledge and expertise among oncologists by conducting training programs and geriatric cancer workshops in conferences.Including geriatric oncology as a separate subspecialty in the curriculum of all oncology training programs may increase awareness about the needs of OA cancer patients.
There is also an unmet need for development of a framework for geriatric palliative care pathways as a significant proportion of the OA patients with cancer may have advanced disease [63].The presence of disabling comorbidities may also preclude the patients with limitedstage cancers from curative treatment.Hence early integration of palliative care with clear documentation of goals of care and advanced care directives may help in maintenance of good quality of life and 'death with dignity' in this subset of vulnerable patients [64,4].The data from this study may help in planning and implementation of specialized geriatric palliative care packages, appropriate for the LMIC context, as has been developed for some specific cancers [65].At the health policy level, creating regional geriatric centers and national centers of aging under governmental schemes like the National Policy for Senior Citizens (2011) and National Programme for Health Care of the Elderly are reasonable steps towards streamlining care for OAs [66].
Provision of special insurance schemes for OAs with coverage for appropriate cancer treatment, improved access to cancer care with outreach centers for supportive and palliative care, subsidized care for OAs and community support programs may go a long way to help the OA cancer patients.However, there is a deficiency of trained oncologists and geriatricians in India; hence, many tertiary cancer centers may not have the workforce to run a separate geriatric oncology clinic But, given that nearly 50% of the incident cancers occur in OAs, there is an urgent unmet need for expansion the cancer care of the OAs in the country.The data on geriatric cancer epidemiology will also help in national health policy planning and resource allocation for OAs, not only in India, but also other countries facing similar health care challenges like LMICs.Detailed PBCR data may not be available in other smaller countries; hence, extrapolating Indian data may help policymakers anticipate the needs of their OAs.All the stakeholders involved in geriatric cancer care need to unite and move forward to face the 'cancer tsunami' in OAs.

Table 1 .
Summary of the Geriatric Cancer Disposition in India, with the Cancer Incidence Rates in Persons >60 Years of Age (2012-2014) * Other and unspecified malignant neoplasms of lymphoid, hematopoietic and related tissue; ASR, Age standardised rates, TR truncated rates; SE, standard error; CI, confidence interval; Malig Imn.Prol D Malignant immunoproliferative disease; O & U, Other and Unspecified, Oth Other, uns unspecified,uri urinary, NHL non-Hodgkins lymphoma, leuk leukemia, MGO male genital organs, FGO female genital organs, KS Kaposi sarcoma, Conn and STconnective and soft tissue, Ns nervous system

Table 1 .
Continued* Other and unspecified malignant neoplasms of lymphoid, hematopoietic and related tissue; ASR, Age standardised rates, TR truncated rates; SE, standard error; CI, confidence interval; Malig Imn.Prol D Malignant immunoproliferative disease; O & U, Other and Unspecified, Oth Other, uns unspecified,uri urinary, NHL non-Hodgkins lymphoma, leuk leukemia, MGO male genital organs, FGO female genital organs, KS Kaposi sarcoma, Conn and STconnective and soft tissue, Ns nervous system A) Common Cancers in Persons Older Than 60 Years

Table 3 .
Geriatric cancer rates in India from each PBCR*

Table 3 .
Continued inferior treatment outcomes