Women's Reproductive Health in Transition

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WOMEN S REPRODUCTIVE HEALTH IN TRANS’ITION: THE OVERLAPPING CHALLENGE OF BREAST AND CERVICAL CANCER

FELICIA M KNAUL, HARVARD GLOBAL EQUITY INITIATIVE, BOSTON, MA, USA AND HARVARD MEDICAL SCHOOL, BOSTON, MA, USA; AFSAN BHADELIA , HARVARD GLOBAL EQUITY INITIATIVE, BOSTON, MA, USA AND HARVARD MEDICAL SCHOOL, BOSTON, MA, USA; HECTOR ARREOLA-ORNELAS , MEXICAN HEALTH FOUNDATION, MEXICO CITY, MEXICO; ISABEL DOS-SANTOS-SILVA , DEPARTMENT OF EPIDEMIOLOGY AND POPULATION HEALTH, LONDON SCHOOL OF HYGIENE & TROPICAL MEDICINE, LONDON, UK; DANIELLE RODIN , HARVARD GLOBAL EQUITY INITIATIVE, BOSTON, MA, USA AND DEPARTMENT OF RADIATION ONCOLOGY, UNIVERSITY OF TORONTO, TORONTO, ON, CANADA; RIFAT ATUN , HARVARD SCHOOL OF PUBLIC HEALTH, HARVARD UNIVERSITY, BOSTON, MA, USA; ANA LANGER , HARVARD SCHOOL OF PUBLIC HEALTH, HARVARD UNIVERSITY, BOSTON, MA, USA AND JULIO FRENK , HARVARD SCHOOL OF PUBLIC HEALTH, HARVARD UNIVERSITY, BOSTON, MA, USA

Substantial improvements have been achieved in reducing the mortality of women from infectious diseases and from complications of pregnancy and childbirth. The emerging disease burden, primarily associated with chronic and non-communicable diseases, requires a new approach that maintains an expanded focus on reproductive health. The evolution over time and across countries of the two leading causes of cancer death in women – cancer of the cervix and of the breast, both associated with maternal and reproductive health – poignantly illustrates how low- and middle-income countries are faced with the challenges of responding to a complex burden of disease that demands both prevention and treatment interventions and falls most heavily on the poor. This paper combines global, cross-country and historical time-series data from a selection of countries to describe the cancer transition for women. The equity issues are presented using sub-national, time series data for Mexico that illustrate the dual burden of women’s cancers in poorer states where women continue to face high rates of both cervical and breast cancer. The protracted and polarized nature of the women s cancer transition is emblematic of the equity imperative of meeting the challenge of cancer globally and’ closing divides between rich and poor. The findings highlight the need to develop integrated programmes and policies that consider both treatment and prevention, underpinned by a life cycle approach to effectively respond to the burden of cancer faced by women globally. Integration with maternal and reproductive health interventions is the effective strategy to meet the emerging challenges to women s health of chronic and non-communicable disease. ’

ubstantial improvements have been achieved in some 65% of all deaths globally are due to NCDs, many of reducing deaths among women from infectious which occur during childbearing age. 3 Sdiseases and from complications of pregnancy and The complexity of the health challenges that face girls and childbirth. Although maternal mortality levels and infection- women in resource-constrained settings provides a associated causes of death continue to be unacceptably high, compelling case – on health, equity and economic grounds – non-communicable (NCD) causes now dominate the burden for adopting a life cycle approach. Applying this approach of disease in low- and middle-income countries. 1,2 For women, implies taking advantage of the range of opportunities to

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invest in the health of a woman at each stage in her life through appropriate preventive, supportive, curative and 4,5 The response to the emerging palliative interventions. challenge of chronic disease and The emerging disease burden, primarily associated with NCDs in low- and middle-income chronic diseases and NCDs, requires a holistic approach to countries has been inadequate. women´s health that maintains a focus on reproductive and Cancer, and especially cancer in maternal components, while extending the reach of women, is a case in point programmes and policies beyond reproduction to encompass the health challenges that are faced by women over their lifespan. 4 The impressive gains in the life expectancy of women and recent improvements in maternal mortality rates 6,7 will be seriously undermined if emerging health issues countries are faced with the equity challenges of responding affecting women are not addressed. to both the preventable and treatable aspects of disease. 21 In line with the suggestions of the High-level Meeting of the Trends in women’s cancers also highlight the equity General Assembly on the Prevention and Control of Non- imperative of meeting the challenge of cancer globally and communicable Diseases, 8 much of the recent literature on closing divides between rich and poor. Further, the focus on NCDs in low- and middle-income countries has focused on these cancers recognizes the specific risks to women opportunities for risk factor reduction and primary associated with their role in reproduction, and highlights the prevention – arguing correctly that these represent key and need for dedicated actions, particularly because diseases cost-effective opportunities to prevent future disease. specific to women often receive delayed and lower quality However, there is an emerging discourse, some care and are neglected in other health agendas, especially in encompassed in the WHO Action Plan for the Prevention and low- and middle-income countries, where gender inequities Control of NCDs 2013–2020, 9 that argues for incorporating are most pronounced. 21 necessary and effective treatment interventions – with one This paper presents cross-country global data, historical of the key diseases of concern being breast cancer. 10-16 This data from specific countries and within-country data from broader approach takes advantage of the many instances Mexico to illustrate the cancer transition for women. The where treatment-related interventions are appropriate in analysis focuses on the equity imperative of meeting the the low- and middle-income country context. Many challenge of both diseases in the context of protecting and treatments for cancer, for example, are relatively inexpensive promoting the health of women over the life cycle. The first as they use off-patent medications for curative intent. part describes the cancer transition as part of the Further, the risk-factor-only focus has stifled efforts to epidemiological transition. The next section introduces the develop appropriate treatment guidelines in accord with the data used in the paper, followed by a discussion of the needs and financial capacity of each country and has thus empirical results. ignored the opportunities to reduce the costs of treatment by The findings highlight the need to develop integrated developing innovative approaches to deliver medicines and responses that consider and include both treatment and other life-saving care. 17-19 prevention interventions. They also indicate the importance The response to the emerging challenge of chronic disease of framing the challenges of the cancers of women within a and NCDs in low- and middle-income countries has been life cycle approach that considers the risks of disease at inadequate. Cancer, and especially cancer in women, is a case different stages of their lifetimes. in point. Recent studies have coined the term “cancer divide” to refer to the concentration of risk factors, incidence of Cancer transition preventable cancers, stigma, uncontrolled pain, and death The epidemiological transition was originally put forward by and disability from treatable cancers in low- and middle- Omran. 22 The decline in the incidence of communicable, income countries as well as amongst the poor in both low- reproductive and nutritional diseases and a rise in that due to and middle-income countries and in high-income countries. 20 NCDs and injury have been demonstrated empirically, most The evolution over time and across countries of the two recently by the 2010 Global Burden of Disease Study (GBD). 1 leading causes of cancer death in women – cancer of the The GBD shows a global decline in communicable, cervix and of the breast, both associated with reproductive maternal, neonatal and nutritional causes of death from health – poignantly illustrates how low- and middle-income 34.1% in 1990 to 24.9% of deaths in 2010. 1 By contrast,

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Figure 1: Trends in the incidence of breast and cervical cancer in selected populations: (a) Denmark, 1953 –2002; (b) Osaka, Japan, 1963 –2002; (c) Costa

Rica, 1980 –2002; (d) India (combined data from 2 population-based registries in Chennai and Mumbai, India), 1983 –2002

(a) Denmark (c) Costa Rica

100 100

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t 40 e t a a

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Data extracted from CI5plus (1)

deaths from NCDs rose sharply and consistently and now hepatocellular carcinoma which is increasing in high-income account for two out of every three deaths in the world. By countries such as the Unites States due in par t to a lcohol

2010, approximately 54% of all DALYs were due to NCDs, consumption and Hepatitis B infection. 25-27 Although t here is

compared to 35% from communicable, maternal, neonatal no specific relationship between the patterns acro ss ty pes of and nutritional disorders, and 11% due to injuries. 2 cancers or notion of competing risk – i.e. red uctions in the

These shifts in the burden of disease have been particularly burden of one type of cancer does do not necess arily leave

strong in low- and middle-income countries and the pattern large groups of populations at risk of other can cers –

of epidemiological transition facing these countries has been infection-associated cancers are emblematic of the overall characterized as polarized and protracted. 23 These countries decline in communicable, reproductive and nutrit ional causes

face the backlog of mortality and morbidity from infectious of death, while increases in incidence and death from other

diseases and conditions associated with poverty and cancers parallel the rise in NCDs. underdevelopment, together with an increasing burden of The cancer transition tends to be associated wi th the 23 chronic disease and NCDs and injury. socioeconomic development of popul ations bo th acro ss and A cancer transition has also been documented. Overall within countries and can also be characterized as po larized

3 cancer mortality has risen 38% and incidence is projected to and protracted. Analogous to the overall ep idemio logical rise at twice the rate estimated for high-income countries. 24 transition in low- and middle-income coun tries, s everal

The term “cancer transition” is used to describe a decline in cancers are increasingly only of the poor, but these are not the

wealthier parts of the world of many cancers of infectious only cancers faced by the poor. 20 etiology and a rise in cancers with no known connection Cancers of women are illustrative of this transition. to an infectious agent. 24 There are exceptions such as Cervical cancer, which is infectious in origin, is now and will

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ar Figure 2: Incidence of, and mortality from, breast and cervical cancers by World region, 2008

Breast cance r Cervical cance r

Eastern Africa Western Asia Middle Africa Australia/New Zealand Melanesia Northern America South-Central Asia Northern Africa Eastern Asia Western Europe Central America Southern Europe Less developed regions Northern Europe South-Eastern Asia More developed regions Mortality Incidence Mortality Incidence Western Africa Micronesia Western Asia Eastern Asia Northern Africa Central and Eastern Europe Southern Africa World World South-Eastern Asia Caribbean Polynesia South America Less developed regions Central and Eastern Europe Caribbean Micronesia Central America Polynesia Middle Africa More developed Regions Melanesia Southern Europe South America Northern America South-Central Asia Northern Europe Southern Africa Australia/New Zealand Western Africa Western Europe Eastern Africa

0 20 40 60 80 100 0 10 20 30 40

Data extracted from GLOBOCAN (4) International Agency for Research on Cancer. GLOBOCAN 2008. Cancer incidence, mortality and prevalence worldwide in 2008. Available from: http://globocan.iarc.fr/

continue to be even more so as coverage of the HPV vaccine transition for women by comparing mortality rates for progresses, a disease that kills women living in poverty. The cervical and breast cancer. burden of breast cancer, by contrast, falls on women at all The global cross-sectional data are age-adjusted (to the levels of income, yet the probability of death is greater if the world standard population) rates for the year 2008 extracted woman is poor. 20 As is evident from Figure 2, while the from GLOBOCAN (http://globocan.iarc.fr/). Historical incidence of breast cancer is several times higher in countries trend data for specific countries are age-adjusted (to the of high income, mortality rates are similar indicating that world population) rates extracted from CI5plus fatality is much higher in low- and middle-income countries. (http://ci5.iarc.fr/CI5plus/ci5plus.htm). Further, and particularly due to the relatively young age The analysis for Mexico uses official mortality data distributions of populations, a large group of young women published by the Ministry of Health. We use the sub-national face these cancers in low- and middle-income countries. series that spans 1979 to 2010 at the state level. 30 The state- Although the incidence of breast cancer typically increases level data aggregates over a wide range of municipalities, with age, as a fraction of all women within this age group, it is including both larger urban centres where access to health twice as common in women under age 50 – often the primary and other services tends to be better and levels of poverty custodians and caregivers of families including young less severe, and smaller, poorer municipalities with much children – in low- and middle-income countries as it is in high- less access. income countries. 5,28 A recent study comparing four Latin These data are aggregated according to the index of American countries to the United States and Canada found deprivation (marginalization) developed and maintained by similar results. 29 This generates a particular set of challenges the National Population Council. 31 Mexico’s five-category related to maternal health and reproduction. deprivation index differentiates the 32 states (federal entities) and municipalities according to the proportion of Data and methods the population with low levels of education, residence in We use data from several sources – global cross-sectional inadequate dwellings (without drainage, electricity or water, data, historical data from a sub-set of countries and sub- or characterized by overcrowding or earth flooring), low national data from Mexico – to demonstrate the cancer household monetary income and rural residence. The index,

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which is derived from classifying the Mexico’s approximately the mortality burden is also seen in less developed regions. 2,500 municipalities that vary greatly in population and Long-run trend data on cancer incidence are sparse, 35 but socioeconomic conditions, is closely aligned with the level of existing information clearly demonstrates a cervical-breast poverty. The most recent index was calculated in 2010, using cancer transition, which began in high income countries (i.e. in census data, and the data presented below apply this North America, Europe, Australia, New Zealand and Japan) categorization retrospectively to the entire time series of and is now evident in low- and middle-income countries (i.e. mortality data. Additional analysis was undertaken applying all other regions). For instance, in Denmark, the age-adjusted earlier indices by period with little change in the overall incidence of breast cancer surpassed that of cervical cancer results. prior to the 1950s, with the differential growing due to the Basic sensitivity analysis was also undertaken to take marked increase in breast cancer over the next five decades account of possible bias from misclassification of uterine (Figure 1a). The cross-over in the age-adjusted incidence cancer deaths. The trends over time are little affected by rates of these two cancers occurred much later in Asian and sensitivity analysis that reclassifies a proportion of deaths Latin American populations – e.g., only in the mid-1970s in listed as cervix. i Osaka, Japan (Figure 1b), during the 1980s in Costa Rica (Figure 1c), and in the early 1990s in urban India (Figure 1d). Equity aspects of the women´s cancers transition The cervical-breast cancer transition, and its Both incidence and death from cervical cancer, a disease that consequences, can now be clearly observed in Africa, where can be prevented, 33 is increasingly concentrated among poor breast cancer has recently surpassed cervical cancer to women. At the same time, the burden of breast cancer is become the most common female cancer in the continent. 36 rising in these same populations. Certain regions in Africa now have the added challenge of not A recent analysis of the global burden of cancer in relation only the highest incidence and the highest mortality rates to the Human Development Index (HDI), showed that breast from cervical cancer worldwide, but also the growing cancer incidence rates have been increasing in almost all challenge of breast cancer. Though breast cancer incidence regions in the world, irrespective of the level of economic rates are lower than in wealthier countries, mortality rates development. 25,34 By contrast, the incidence of cervical cancer are much higher due to late detection and lack of access to has been declining in most regions, including countries of treatment (Figure 2). both higher and lower income, with the exception of only the In the case of Mexico, the women´s cancers transition for very poorest countries. 6,25 As a result of these diverging women from the mortality data that span the period 1955 to trends, breast cancer has now surpassed cervical cancer to 2010 5,37 shows mortality from cervical cancer peaked at become the most common female cancer in the majority of almost 17 per 100,000 women in the late 1980s and countries with the exception of some of the poorest countries subsequently fell continuously, reaching a low of just close to where cervical cancer is still the most common cancer among 7.5 per 100,000 women in 2010. By contrast, breast cancer women. Consequently, regions made up predominantly of mortality rose steadily until the mid-1990s and has since low- and middle-income countries are facing a dual female remained stable at a rate of approximately 9.5 per 100,000 cancer burden – their historically high and persisting women. These rates converged between 2005 and 2006 and, incidence burden from cervical cancer as well as an emerging since that point in time, breast cancer has been the leading high incidence burden from breast cancer. As survival from cause of cancer death in women. both breast and cervical cancer are positively associated with The equity aspects of the women’s cancers transition in level of socioeconomic development, a greater proportion of Mexico is most clearly seen by analyzing within-country trends. The 32 states are classified into five categories

i according to their level of marginality (a composite index of There is some evidence of imprecise coding of uterine cancer deaths due to difficulties in identifying the origin of the cancer as cervix or corpus uteri. 32 poverty and access to basic services where high marginality is This could bias our results by underestimating the number of deaths associated with the greatest poverty). In the 1980s, the range attributable to cancer of the cervix. This bias could be associated with in marginalization-specific absolute differences in cervical poverty, as miscoding may be more likely where training and human versus breast cancer rates was relatively small. This is largely resources for health are lower. Thus, basic sensitivity analysis was also because cervical cancer mortality rates had not yet peaked in undertaken by reclassifying uterine cancer deaths in women below age 50 as the poorer states and because the middle-income states had cervical cancer, the rationale being that cancer originating in the uterus is very uncommon in younger women. The trends over time are little affected not passed far into the transition. By the late 1980s, the by this reclassification. overall pattern is quite clear: the absolute differences in the

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mortality rates between cervical and breast cancer increase steadily with marginalization. The states in the highest The challenge of the transition in marginalization category had the greatest difference in C-V women’s cancers is further rates. illustrated by analysing trends in The challenge of the transition in women’s cancers is mortality rates separately for further illustrated by analysing trends in mortality rates cervical and breast cancers within separately for cervical and breast cancers within Mexico at Mexico at the sub-regional level the sub-regional level. There is a clear progression in the cervical-breast cancer transition by category of state marginalization. In poorer states, cervical cancer continues to be the primary cause of cancer-related mortality for women, although the gap has narrowed significantly. In wealthier driven by persistently higher levels of cervical cancer parts of the country, breast cancer is the dominant cause of mortality in the poorer states. The women living in these death from cancer in women. In some states, this has been the states, the poorest in the country, continue to face a double case since the late 1980s (Figure 3). In states with the highest cancer burden. Yet, deaths from cervical cancer are levels of marginalization (represented by Oaxaca), cervical beginning to decline even in the poorer regions and the gap cancer mortality rates continue to be almost double those of between rich and poor states for cervical and breast cancer breast cancer, although the gap has closed substantially from mortality in Mexico will likely narrow further in the future. the fourfold difference of the early 1990s. Indeed, in Oaxaca Over time, and especially with the recent introduction of in the early 1990s, the difference between the cervical and national coverage of HPV vaccination to prevent cervical breast cancer mortality rate reached up to fivefold with a cancer, breast cancer will dominate both in incidence and high of close to 20 deaths per 100,000 women from cervical mortality. 38 cancer compared to rates of breast cancer mortality of less than 5. Conclusions and policy recommendations The smallest C-V (cervical-breast or C-V) differences The global cross-sections, historical data and within-country occurred in the wealthiest states where the rates were close trends clearly illustrate the transition in women´s cancers. to inverting. In these states, the twofold gap that was evident Low- and middle-income countries, and especially poorer in the early 1980s had closed by the early to mid-1990s. By women, face a double burden of cervical and breast cancer 2008, the inverse was true: breast cancer mortality was and strategies are required to meet the challenge of both approximately double that of cervical cancer with rates of diseases in the context of programmes that promote the over 13 per 100,000 for breast cancer compared to below 7 health of women. per 100,000 for cervical cancer. In the case of Nuevo León, Health systems must offer prevention, treatment and one of the wealthiest states of Mexico, the crossover in palliation responses that are appropriate to each disease. In mortality rates occurred prior to 1985. the absence of efforts in vaccination, screening and In the two decades spanning 1990 to 2010, the relative treatment of precancer lesions, cervical cancer mortality will levels of mortality for women’s cancers in Mexico were become a persistent burden restricted increasingly to the poorest countries and the poorest women. It is a moral and equity imperative to prevent cervical cancer through HPV Health systems must offer prevention, vaccination and screening for precancerous lesions, while treatment and palliation responses offering treatment to those women affected by cervical that are appropriate to each disease. cancer. In the absence of efforts in There is reason to hope that with increased community vaccination, screening and treatment health measures for detecting and managing precancerous of precancer lesions, cervical cancer lesions of the cervix, and expanded coverage of the HPV mortality will become a persistent vaccine, that cervical cancer mortality will continue to decline burden restricted increasingly to the globally. 39 The remaining challenge is one of equity, and the poorest countries and the poorest imperative will be to ensure that cervical cancer does not women become another neglected “tropical” disease of the poor. At the same time, breast cancer is likely to increase and

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Figure 3: Trends in the mortality rate from cervical and breast cancer in Mexico by category of state marginality, 1979 –2010

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combined with early detection and treatment to mount an systems program at the Johns Hopkins Bloomberg School of effective response to a cancer that is rapidly becoming a Public Health. Her research interests include promoting health leading cause of death in low- and middle-income countries. equity through chronic care management, women’s health and Resource stratified guidelines have been developed for palliative care. breast cancer that offer alternatives for countries to make evidence-based decisions in setting priorities and these need Hector Arreola-Ornelas is Economic Research Coordinator of to be applied and integrated into programmes for women´s the Health Competitiveness Program in the Mexican Health health. 44 Indeed, if countries ignore the emerging challenge of Foundation (FUNSALUD). He is also the Coordinator of the breast cancer because it is not associated with a quick, Health Observatory for Latin America. His areas of research preventive fix, we are likely to see the emergence of a gaping include financial protection, policy and health systems, labour cancer divide. If early detection and access to effective economics, economic evaluation and health and competitiveness. treatment are denied to poor women, mortality will decline only among the rich countries and the wealthy, while Dr Isabel dos-Santos-Silva is Professor of Epidemiology in the continuing to increase among poor women. Department of Epidemiology and Population Health at the For both cervical and breast cancer, there are important London School of Hygiene & Tropical Medicine. Her research opportunities to apply a diagonal approach that will focuses on the causes of cancer as a basis for the development of strengthen health systems and improve women’s health and appropriate prevention and control strategies, both in high and cancer care and control simultaneously. 5,18,41 This involves low resource settings. integrating key interventions on women´s cancers such as education and early detection, into maternal health, sexual Dr Danielle Rodin is a Resident in the Department of Radiation and reproductive health and anti-poverty programmes that Oncology at the University of Toronto and an MPH Candidate at focus on women. It also requires promoting policy dialogue, the Harvard School of Public Health. Her current research research and international action that cut across false interests are in the area of health equity in the treatment and boundaries and silos such as those that have separated palliation of cancer and in the role of radiotherapy. women on women’s health with that on NCDs. 45 Integrated approaches will help to meet the many facets of Dr Rifat Atun is Professor of Global Health Systems and Director women’s cancers that are related to motherhood, sexuality, of the Global Health Systems Cluster at the Harvard School of menopause, and to face the barriers associated broader Public Health. He previously led the Health Management Group issues of discrimination against women. These actions can at Imperial College London and was a member of the executive and should be effectively catalyzed through national and management team at The Global Fund to Fight AIDS, global strategies to curb not only the tide but also the swell of Tuberculosis and Malaria. women’s cancers as part of the larger, emerging challenge of chronic and non-communicable disease. l Dr Ana Langer is Professor of the Practice of Public Health and Director of the Dean's Special Initiative in Women and Health at Dr Felicia Marie Knaul is Associate Professor at Harvard the Harvard School of Public Health. Dr Langer is a reproductive Medical School and Director of the Harvard Global Equity health expert. She was previously the president and CEO of Initiative. Dr Knaul is also Senior Economist at the Mexican EngenderHealth. Health Foundation (FUNSALUD), Honorary Research Professor of Medical Sciences at the National Institute of Public Health of Dr Julio Frenk is Dean of the Faculty at the Harvard School of Mexico, and founder of Cáncer de Mama: Tómatelo a Pecho. Public Health and T & G Angelopoulos Professor of Public Health and International Development, a joint appointment Afsan Bhadelia is a Research Associate at the Harvard Global with the Harvard Kennedy School of Government. Dr Frenk is an Equity Initiative, where she previously served as Research eminent authority on global health who served as the Minister Director. Concurrently, she is a doctoral candidate in the health of Health of Mexico from 2000 to 2006.

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