Cancer registration challenges in low- and middle-income countries-the case of the Pacific Islands

The burden of cancer is increasing worldwide due to ageing, growing populations and increased exposure to major risk factors, including unhealthy diet, sedentary lifestyle and for many populations, tobacco smoking (Global Burden of Disease Cancer Collaboration et al., 2015). This trend is part of a wider phenomenon of increasing burden of non-communicable diseases (NCDs) (World Health Organization, 2011). Deaths from NCDs are projected to increase from 38 million to 52 million between 2012 and 2030 (World Health Organization, 2014). The NCD burden is not evenly distributed, with more than 80% of all premature NCD deaths occurring in low- and middle-income countries (LMIC). The growing burden of cancer in developing countries is due to changes in lifestyle and reproductive factors, which complement a pre-existing high burden caused by infectious diseases (Bray, Jemal, Grey, Ferlay, & Forman, 2012; Kanavos, 2006). Much of the cancer burden in developing countries is preventable through lifestyle modification, tobacco control, screening and vaccination (Kanavos, 2006). As a result of overburdened, poorly developed and fragmented health care systems, the prevailing lack of prevention, early detection and treatment interventions contributes to a disproportionately higher cancer mortality in these countries. Given many competing priorities, governments and donor agencies lack the resources and strategic direction to address the scale of the NCD challenge (Reeler & Mellstedt, 2006). Underfinanced health care facilities are not able to offer complex and expensive cancer treatments (Global Burden of Disease Cancer Collaboration et al., 2015). Another important issue is the lack of appropriate data on cancer incidence, mortality and outcomes of services. These data are necessary to understand the extent of the cancer problem across the population, and to monitor status changes in incidence and mortality, including responses to cancer control initiatives, such as treatment and preventive programmes (Bray, Znaor, et al., 2015; Parkin, 2006). In this commentary, we provide an overview of cancer epidemiology and cancer registration challenges in LMIC, with a special focus on the Pacific Islands. There were an estimated 14.1 million new incident cancer cases and 8.2 million cancer deaths globally in 2012, with 57% of new cases and 65% of the cancer deaths occurring in the less developed countries (Ferlay et al., 2013). Large increase in global cancer burden is projected by 2025 (Bray, 2014). Increases in cancer incidence are projected to be proportionally greatest in LMIC (Bray et al., 2012). According to GLOBOCAN data, the overall age-standardised cancer incidence and cancer mortality rates in less developed regions were 147.7 and 98.4 per 100 000 people in 2012 (Ferlay et al., 2013). The most frequent cancer sites were lung, breast, stomach, liver and colon/rectum. By comparison, the corresponding cancer incidence and mortality rates in more developed regions were 267.2 and 108.5 per 100 000 respectively. The smaller elevation in mortality than incidence in more developed areas reflects both a difference in mix towards less lethal cancer types and better survival. The incidence gap is closing rapidly, however, as developing countries adopt "Western" lifestyle and health behaviours (Bray, 2014). In more developed areas, breast, prostate, lung and colorectal cancers comprise approximately half of all cancers, whereas in less developed areas, stomach, liver and cervical cancers play a more important role (Ferlay et al., 2015). Infectious agents play an important role in the genesis of these cancers highlighting the greater importance of infections as a cancer cause in developing countries. Infections are responsible for an estimated 25% of cancers in developing countries, whereas the corresponding proportion is about 10% in developed countries (Plummer et al., 2016). In recent decades, a cancer transition has taken place, however, with an increasing incidence of breast, colorectal and prostate cancers also taking place in less affluent populations which historically had a lower risk of these cancers (Bray et al., 2012). Changes in reproductive, dietary, metabolic, hormonal and behavioural factors are likely to be responsible for this transition. Pacific Islands countries and territories (PICTs) comprise 20 000–30 000 islands in the Pacific Ocean (World Health Organization Western Pacific Region, 2012). PICTs vary in stage of human development, size, culture and economic resources; however, they all face the triple burden of NCDs, communicable diseases and the impact of climate change (World Health Organization Western Pacific Region, 2012). PICTs have one of the highest NCD incidence rates in the world, comprising the leading cause of mortality. Relatively small populations, large physical areas with long distances, geographic isolation, reliance on overseas assistance and weak economies complicate the provision of the health care services that would be essential to address this increasing public health challenge. The cancer burden is thought to be increasing in the PICTs, although only limited quantitative evidence is available due to a paucity of cancer incidence and mortality data (Moore et al., 2010; Varghese, Carlos, & Shin, 2014). Eight of the 22 PICTs were included in the GLOBOCAN 2012 (Fiji, French Polynesia, Guam, New Caledonia, Papua New Guinea, Samoa, Solomon Islands and Vanuatu) (Ferlay et al., 2013). Most of these PICTs had national incidence data for some diagnostic time periods, but not Papua New Guinea and Solomon Islands, where all cancer rates or rates for neighbouring countries have been used to estimate cancer incidence. Meanwhile, mortality data were missing for Guam, Papua New Guinea, Samoa, Solomon Islands, and Vanuatu, where mortality estimates were derived from estimated national incidence rates and modelled survival. None of the PICTs were reflected in or contributed to the Cancer Incidence in Five Continents Volume X (CI5-X) publication (Forman et al., 2014), indicating their relatively low availability of high quality data. According to GLOBOCAN 2012, cancer incidence was estimated to be highest in New Caledonia (age-standardised rate (ASR) of 330.7 for men and 269.3 for women per 100 000) and in French Polynesia (ASR 287.4 for men and 227.3 for women per 100 000) (Ferlay et al., 2013). Similarly, age-standardised cancer mortality rates were estimated to be highest in French Polynesia (ASR 153.9 for men and 116.3 for women per 100 000) and New Caledonia (ASR 146.0 for men and 112.0 for women per 100 000). In all other countries, cancer incidence estimates were below the World average, with cancer incidence generally higher among women than men. The most common cancers among men were estimated to be prostate, lung, stomach, liver and lip/oral cavity cancers. For women, breast cancer was ranked as the most common cancer in all countries, except in Papua New Guinea where cervical cancer was most common. Notably Papua New Guinea accounts for over a third of the total Pacific population at over 6 million, thereby increasing the contribution of cervical cancer to the cancer burden in the Pacific region. A study examining cancer incidence in four PICTs (Fiji, Tonga, Cook Islands and Niue) reported that age-standardised cancer incidence was lower in these countries than among Pacific people living in New Zealand (Foliaki et al., 2011). Under-recording is likely to have contributed to these differences. Despite relatively low (reported) cancer incidence in many PICTs, cancer is one of the leading causes of death in the region (Carter et al., 2011, 2016; Pacific Regional Central Cancer Registry, 2015). There are distinguishing features of cancer epidemiology in the PICTs, such as very high thyroid cancer incidence in New Caledonia and French Polynesia (Ferlay et al., 2013), a high burden of cervical and uterine cancers, especially in Fiji and the Cook Islands (Foliaki et al., 2011; Law et al., 2013) and a high burden of oral cavity and pharyngeal cancers linked with betel nut chewing (Moore et al., 2010; Pacific Regional Central Cancer Registry, 2015). Nuclear tests conducted by France in French Polynesia and by the US in Marshall Islands have been linked to increased thyroid cancer and leukaemia rates (Bouchardy, Benhamou, de Vathaire, Schaffar, & Rapiti, 2011; Simon, Bouville, Land, & Beck, 2010). Data collected by population-based cancer registries (PBCR) are the gold standard for providing information on cancer incidence across geographic areas and for planning population-wide cancer control programmes (Bray, Znaor, et al., 2015). Full case ascertainment and unbiased information on cancer burden is optimally achieved where there is a well-functioning health care system. Availability as well as quality of cancer incidence and mortality data tends to increase with development and infrastructure levels, with many LMIC still without cancer registration systems in place or hospital- or pathology-based registration systems that are not population-based. In addition to cancer data, population denominator data are also needed in order to provide accurate information on cancer incidence rates. These data commonly come from censuses which may be rarely or irregularly conducted in developing countries (Valsecchi & Steliarova-Foucher, 2008). Population-based cancer registries systematically collect information on all cancers occurring in a defined population using multiple data sources, whereas hospital- and pathology-based registries collect information on cases treated/diagnosed in selected institutions or laboratories (Bray, Znaor, et al., 2015). While useful, such data may not be representative of the overall population experience and may contain important statistical biases from a population perspective. While data collected from hospital- or pathology-based registries may provide a misleading cancer profile for the general population, they still can be useful for hospital administration purposes, for reviewing clinical performance and for providing information about cancer profiles of people who obtain hospital/pathology services (Bray, Znaor, et al., 2015; Valsecchi & Steliarova-Foucher, 2008). There are many challenges with cancer registration in developing countries, including weak or non-existent health care infrastructures, lack of accurate death records and population data, complicating issues related to cultural norms and problems caused by political and economic instability, and mobile populations (Parkin & Sanghvi, 1991; Valsecchi & Steliarova-Foucher, 2008). In order to register all cases of cancer, data need to be collected from multiple sources, including hospitals, laboratories and death certificates (Bray, Znaor, et al., 2015). Lack of health care networks, poorly developed communications between different stakeholders as well as inability to uniquely identify individuals complicate the collection of these data (Valsecchi & Steliarova-Foucher, 2008). Underestimation of both cancer cases and deaths is commonplace where many people lack access to basic health care services and cancers and cancer deaths go unrecorded, as may apply in particular in the rural areas. People may die at home and be buried at home or otherwise locally without reporting to government authorities (Jedy-Agba et al., 2015). Poor transportation networks and phone connections, cultural and religious constraints, preference for traditional healing and taboos and stigmas relating to cancer contribute to an underestimation of numbers of cancer and a lack of follow-up for registered cases (Valsecchi & Steliarova-Foucher, 2008). In addition to these technical challenges, a lack of financial and material resources, trained personnel and support from governments, policymakers and health professionals further complicates cancer registration. As cancer registration involves considerable costs, regional registries collecting data on sub-national samples have been considered good options in some low-resource countries (Bray, Znaor, et al., 2015). When cancer data are collected, there may be issues with quality, such as low proportions of cases confirmed microscopically due to a lack of pathology services (Bray, Ferlay, et al., 2015). Cancer diagnoses may be based on clinical examination only, with greater uncertainty (Parkin & Sanghvi, 1991). Another important indicator of poorer data quality is a high percentage of cases registered from death certificates only (DCOs), reflecting incomplete case identification (Bray, Ferlay, et al., 2015). On the other hand, a total lack of DCOs may indicate failure to use death certificate information or to link death information to the cancer registry (Curado, Voti, & Sortino-Rachou, 2009). Accuracy of diagnostic information derived from death certificates is generally suboptimal. In addition, there may be specific problems in developing countries in relation to the quality of death certification, with information on causes of death often missing/erroneous and with certificates often completed by lay-people instead of medical doctors. In addition to cancer diagnosis and death data, other essential data may be missing or incomplete, including birth date, age and place of residence (Jedy-Agba et al., 2015). Lack of co-operation and difficulties in accessing data from several data sources may be caused by general distrust of government-related activities, lack of a culture of data collection and concerns about confidentiality (Jedy-Agba et al., 2015). Making cancer a registrable disease by government regulations can mitigate challenges in data collection and increase the authority of PBCR, although success is likely to depend on availability of resources and culture and politics of the country. Continuous monitoring and mentoring involving both local and international experts and sustainable funding models are often essential for ongoing, successful registration (Jedy-Agba et al., 2015). Commonly, low cancer data quality stems from overall weakness of health care system and, therefore, wide-ranging system-level improvements would materially improve registry quality. The first cancer registry in the PICTs was established in Papua New Guinea in 1958 (Foliaki et al., 2011). According to information from the World Health Organization, many PICTs have cancer registries nowadays (World Health Organization, 2016). In addition, most PICTs have collected census information in recent years (Secretariat of the Pacific Community, 2016). There are issues, however, with quality, coverage and completeness of cancer data (Dachs et al., 2008; Moore et al., 2010; Shin, Carlos, & Varghese, 2012). Many of the registration challenges mentioned earlier in this commentary are familiar to PICTs. Lack of infrastructure, coordination and funding, poorly developed health care systems, under-recording as well as poor quality of death certificates and diagnostic information complicate the collection of cancer data in many PICTs (Palafox et al., 2004). Along with vast distances between PICTs and degree of remoteness, the high proportions of foreign contract workers in some islands, and conversely the extent to which the birth population has migrated off-island impact the development of sustainable infrastructure. Different development agencies, including funders of new programmes, often request data in formats and using software modules that are not familiar to local data custodians complicating the meaningful collection and utilisation of data at the regional level. Many PICTs have close relationships with 'host' countries (the US, New Zealand and France) and are dependent on external aid, including health development. There is an opportunity to review health development assistance platforms with one of the major initiatives being health information and monitoring. Due to natural conditions, many PICTs are dependent on imported food (World Health Organization Western Pacific Region, 2012). Financial incentives, such as the Nuclear Claims Tribunal in the Marshall Islands, may facilitate the case finding of certain cancer types, but not others. Natural and other disasters have destroyed cancer registry databases in Nauru (Palafox et al., 2004), Niue (Foliaki et al., 2011) and American Samoa (Tsark, Cancer Council of the Pacific Islands, & Braun, 2007). Due to limited treatment options, people diagnosed with cancer may die off-island and, therefore, may not be registered. The Global Monitoring Framework of WHO, subsequent to the United Nations high-level meeting to "launch and all-out attack" on NCDs in 2011, specifically mentions the recording of cancer incidence by type of cancer per 100 000 population as an indicator to monitor 2025 targets; thereby placing an onus on countries to establish PBCR. The International Agency for Research on Cancer (IARC) in collaboration with major international and national partner organisations established the Global Initiative for Cancer Registry Development (GICR) in 2011 (International Agency for Research on Cancer, 2014, 2016). The aim of the GICR is to improve the coverage, quality and networking capacities of PBCR in LMIC. The GICR is organised around Regional Hubs for providing technical support and on-site training, assessing data quality and overall capacity for development, coordinating different activities and monitoring overall progress in the region. One of these is the emerging Pacific Islands Regional Hub which will focus on supporting cancer registries and improving data collection and data utilisation for cancer control in Fiji, New Caledonia, Papua New Guinea, Solomon Islands, Vanuatu, Guam, French Polynesia and Samoa. The Hub will be governed by an Advisory Board comprising regional experts from participating PICTs, along with Australia and New Zealand, and other local experts in the use of registry data to support local service delivery and research. The Pacific Islands Regional Hub will comprise a collaboration of registry experts, local public health practitioners and administrations. The registry experts will provide support and consultancy services for existing registries, such as ongoing training and assistance with registration, quality assurance, statistical analysis and research activities, whereas local PICT public health practitioners and administrators will give direction to the use of these data for local service delivery. There is no question that the Pacific Hub initiative should be tested, along with obligations to establish PBCR. It will be critical to continually monitor progress and reassess implementation in terms of strategic approaches, steps taken, and local involvement to ensure full participation and ownership of the initiative by Pacific countries, as well as sustainability and effectiveness of the Hub activities. The US-associated PICTs (American Samoa, Guam, the Commonwealth of the Northern Mariana Islands, the Federated States of Micronesia, the Republic of the Marshall Islands and the Republic of Belau) established the Cancer Council of the Pacific Islands and the Pacific Regional Central Cancer Registry in the early 2000s (Pacific Regional Central Cancer Registry, 2015; Tsark, Cancer Council of the Pacific Islands, & Braun, 2007). This collaboration has enabled the development of culturally appropriate cancer control strategies and activities for the US-associated PICTs, with publication of cancer incidence rates for 2007–2012. The key to the success has been culturally appropriate approaches, local capacity building and leadership, and funding support. The Pacific Islands Regional Hub seeks to build on this experience and through collaborative arrangements, provide complementary support services for other PICTs that are attuned to their needs. In order to strengthen cancer registration in the PICTs, improvements in health care systems and infrastructure are needed more generally and in quality of death certificates and diagnostic information systems. The key strategies for achieving these improvements include building governance structures which coordinate the responsibilities and actions of different stakeholders and using culturally appropriate methods in order to ensure strong local engagement and sustainability. The potential of the emerging Pacific Islands Regional Hub to serve a useful role in advancing and coordinating these activities will be tested. None to declare.