Abstract
Less-developed-region countries (LDCs) are seeing a rapid rise in cancer incidence owing to changing lifestyles, infections, environmental carcinogens and increasing longevity. LDCs have poor resources to deal with cancers, leading to high mortality rates. Investment in nationally implementable and sustainable cancer prevention and screening strategies would be more appropriate for LDCs. This Science and Society article outlines the burden of preventable cancers in selected LDCs and discusses evidence on cost-effective and widely implementable prevention and screening strategies.
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References
Ferlay, J. et al. GLOBOCAN 2012 v1.0, Cancer Incidence and Mortality Worldwide: IARC CancerBase No. 11. International Agency for Research on Cancer [Online] (2013).
Morrell, S., Taylor, R., Roder, D. & Dobson, A. Mammography screening and breast cancer mortality in Australia: an aggregate cohort study. J. Med. Screen 19, 26–34 (2012).
Wilkinson, J. E. Effect of mammography on breast cancer mortality. Am. Fam. Physician 84, 1225–1227 (2011).
Magnus, M. C., Ping, M., Shen, M. M., Bourgeois, J. & Magnus, J. H. Effectiveness of mammography screening in reducing breast cancer mortality in women aged 39–49 years: a meta-analysis. J. Womens Health 20, 845–852 (2011).
Tabar, L. et al. Mammography service screening and mortality in breast cancer patients: 20-year follow-up before and after introduction of screening. Lancet 361, 1405–1410 (2003).
Nygard, M. Screening for cervical cancer: when theory meets reality. BMC Cancer 11, 240 (2011).
Sasieni, P., Castanon, A. & Cuzick, J. Effectiveness of cervical screening with age: population based case-control study of prospectively recorded data. BMJ 339, b2968 (2009).
Adegoke, O., Kulasingam, S. & Virnig, B. Cervical cancer trends in the United States: a 35-year population-based analysis. Journal of women's health 21, 1031–1037 (2012).
Shastri, S. S. et al. Effect of VIA screening by primary health workers: randomized controlled study in Mumbai, India. J. Natl Cancer Inst. 106, dju009 (2014).
Teguete, I. et al. Can visual cervical screening be sustained in routine health services? Experience from Mali, Africa. BJOG 119, 220–226 (2012).
Sankaranarayanan, R. et al. Accuracy of visual screening for cervical neoplasia: Results from an IARC multicentre study in India and Africa. Int. J. Cancer 110, 907–913 (2004).
Lazcano-Ponce, E. C., Moss, S., Alonso de Ruiz, P., Salmeron Castro, J. & Hernandez Avila, M. Cervical cancer screening in developing countries: why is it ineffective? The case of Mexico. Arch. Med. Res. 30, 240–250 (1999).
Othman, N. H. & Rebolj, M. Challenges to cervical screening in a developing country: The case of Malaysia. Asian Pac. J. Cancer Prev. 10, 747–752 (2009).
Goss, P. E. et al. Challenges to effective cancer control in China, India, and Russia. Lancet Oncol. 15, 489–538 (2014).
Wynder, E. L. & Stellman, S. D. Comparative epidemiology of tobacco-related cancers. Cancer Res. 37, 4608–4622 (1977).
Moulin, J. J., Mur, J. M. & Cavelier, C. Comparative epidemiology, in Europe, of cancers related to tobacco (lung, larynx, pharynx, oral cavity). Bull. Cancer 72, 155–158 (1985).
Restrepo, H. E., Correa, P., Haenszel, W., Brinton, L. A. & Franco, A. A case-control study of tobacco-related cancers in Colombia. Bull. Pan Am. Health Organ. 23, 405–413 (1989).
Benhamou, S. Cancers related to tobacco smoking. Rev. Prat 43, 1214–1217 (1993).
Gajalakshmi, C. K., Ravichandran, K. & Shanta, V. Tobacco-related cancers in Madras, India. Eur. J. Cancer Prev. 5, 63–68 (1996).
World Health Organisation. GATS (Global Adult Tobacco Survey). WHO [online] (2014).
Dikshit, R. et al. Cancer mortality in India: a nationally representative survey. Lancet 379, 1807–1816 (2012).
Borzekowski, D. L. & Cohen, J. E. International reach of tobacco marketing among young children. Pediatrics 132, e825–831 (2013).
Holford, T. R. et al. Tobacco control and the reduction in smoking-related premature deaths in the United States, 1964–2012. JAMA 311, 164–171 (2014).
Chaloupka, F. J., Yurekli, A. & Fong, G. T. Tobacco taxes as a tobacco control strategy. Tobacco Control 21, 172–180 (2012).
Hargreaves, K. et al. The social context of change in tobacco consumption following the introduction of 'smokefree' England legislation: a qualitative, longitudinal study. Social Sci. Med. 71, 459–466 (2010).
International Agency for Research on Cancer (IARC). IARC Handbooks of Cancer Prevention, Tobacco Control, Volume 13: Evaluating the Effectiveness of Smoke-Free Policies. (WHO, 2009).
Stallings-Smith, S., Zeka, A., Goodman, P., Kabir, Z. & Clancy, L. Reductions in cardiovascular, cerebrovascular, and respiratory mortality following the national irish smoking ban: interrupted time-series analysis. PLoS ONE 8, e62063 (2013).
Thavorn, K. & Chaiyakunapruk, N. A cost-effectiveness analysis of a community pharmacist-based smoking cessation programme in Thailand. Tobacco Control 17, 177–182 (2008).
World Health Organisation. WHO Framework Convention on Tobacco Control. WHO [online] (2014).
World Health Organisation. Parties to the WHO Framework Convention on Tobacco Control. WHO [online] (2014).
Jemal, A. et al. Global cancer statistics. CA Cancer J. Clin. 61, 69–90 (2011).
Kamangar, F., Dores, G. M. & Anderson, W. F. Patterns of cancer incidence, mortality, and prevalence across five continents: defining priorities to reduce cancer disparities in different geographic regions of the world. J. Clin. Oncol. 24, 2137–2150 (2006).
Yankaskas, B. C. et al. Performance of first mammography examination in women younger than 40 years. J. Natl Cancer Inst. 102, 692–701 (2010).
Haukka, J., Byrnes, G., Boniol, M. & Autier, P. Trends in breast cancer mortality in Sweden before and after implementation of mammography screening. PLoS ONE 6, e22422 (2011).
Gotzsche, P. C. Relation between breast cancer mortality and screening effectiveness: systematic review of the mammography trials. Dan Med. Bull. 58, A4246 (2011).
Biller-Andorno, N. & Juni, P. Abolishing mammography screening programs? A view from the Swiss Medical Board. N. Engl. J. Med. 370, 1965–1967 (2014).
Kapp, J. M., Walker, R., Haneuse, S., Buist, D. S. & Yankaskas, B. C. Are there racial/ethnic disparities among women younger than 40 undergoing mammography? Breast Cancer Res. Treat. 124, 213–222 (2010).
Harford, J. B. Breast-cancer early detection in low-income and middle-income countries: do what you can versus one size fits all. Lancet Oncol. 12, 306–312 (2011).
Semiglazov, V. F. et al. Results of a prospective randomized investigation [Russia (St. Petersburg)/WHO] to evaluate the significance of self-examination for the early detection of breast cancer. Vopr Onkol 49, 434–441 (2003).
Thomas, D. B. et al. Randomized trial of breast self-examination in Shanghai: final results. J. Natl Cancer Inst. 94, 1445–1457 (2002).
Miller, A. B. et al. Twenty five year follow-up for breast cancer incidence and mortality of the Canadian National Breast Screening Study: randomised screening trial. BMJ 348, g366 (2014).
Pisani, P. et al. Outcome of screening by clinical examination of the breast in a trial in the Philippines. Int. J. Cancer 118, 149–154 (2006).
Dinshaw, K. et al. Determinants of compliance in a cluster randomised controlled trial on screening of breast and cervix cancer in Mumbai, India. 1. Compliance to screening. Oncology 73, 145–153 (2007).
Grosse Frie, K. et al. Determinants of participation in a breast cancer screening trial in Trivandrum district, India. Asian Pac. J. Cancer Prev. 14, 7301–7307 (2013).
Mittra, I. et al. A cluster randomized, controlled trial of breast and cervix cancer screening in Mumbai, India: methodology and interim results after three rounds of screening. International journal of cancer. J. Int. Cancer 126, 976–984 (2010).
Sankaranarayanan, R. et al. Clinical breast examination: preliminary results from a cluster randomized controlled trial in India. J. Natl Cancer Institute 103, 1476–1480 (2011).
Denewer, A. et al. Cost-effectiveness of clinical breast assessment-based screening in rural Egypt. World J. Surg. 34, 2204–2210 (2010).
Okonkwo, Q. L., Draisma, G., der Kinderen, A., Brown, M. L. & de Koning, H. J. Breast cancer screening policies in developing countries: a cost-effectiveness analysis for India. J. Natl Cancer Inst. 100, 1290–1300 (2008).
de Sanjose, S. et al. Worldwide prevalence and genotype distribution of cervical human papillomavirus DNA in women with normal cytology: a meta-analysis. Lancet Infect. Dis. 7, 453–459 (2007).
Flores, Y. et al. Improving cervical cancer screening in Mexico: results from the Morelos HPV Study. Salud Publ. Mexico 45, S388–S398 (2003).
Markowitz, L. E. et al. Human papillomavirus vaccine introduction—the first five years. Vaccine 30 (Suppl. 5), F139–148 (2012).
Sankaranarayanan, R. et al. HPV screening for cervical cancer in rural India. N. Engl. J. Med. 360, 1385–1394 (2009).
Akamatsu, S., Kodama, S., Himeji, Y., Ikuta, N. & Shimagaki, N. A comparison of liquid-based cytology with conventional cytology in cervical cancer screening. Acta Cytol. 56, 370–374 (2012).
Siebers, A. G. et al. Comparison of liquid-based cytology with conventional cytology for detection of cervical cancer precursors: a randomized controlled trial. JAMA 302, 1757–1764 (2009).
Tsonev, A., Ivanov, S. & Kovachev, E. Comparison of conventional PAP smear with liquid based cytology method (LBC). Akusherstvo i ginekologiia 51, 20–24 (2012).
Laiwejpithaya, S. et al. Comparison between Siriraj liquid-based and conventional cytology for detection of abnormal cervicovaginal smears: a split-sample study. Asian Pac. J. Cancer Prev. 9, 575–580 (2008).
Sankaranarayanan, R. et al. Effect of visual screening on cervical cancer incidence and mortality in Tamil Nadu, India: a cluster-randomised trial. Lancet 370, 398–406 (2007).
Tamil Nadu Health Systems Project. Screening for Cervical Cancer and Breast Cancer. TNHSP [online] (2014).
Nessa, A. et al. Role of print and audiovisual media in cervical cancer prevention in Bangladesh. Asian Pac. J. Cancer Prev. 14, 3131–3137 (2013).
Untiet, S. et al. HPV self-sampling as primary screening test in sub-Saharan Africa: Implication for a triaging strategy. Int. J. Cancer 135, 1911–1917 (2014).
[no authors listed] HPV Test Recommended as Primary Screening Tool. Cancer Discovery 4, OF6 (2014).
Huang, J. et al. MGB-based one-step multiplex real-time PCR method for rapid detection of HPV. Cancer Biomark. 12, 107–113 (2012).
Zhao, J. et al. Clinical performance characteristics of the Cervista HPV HR test kit in cervical cancer screening in China. J. Lower Genital Tract Dis. 16, 358–363 (2012).
Ogilvie, G. S. et al. Primary cervical cancer screening with HPV testing compared with liquid-based cytology: results of round 1 of a randomised controlled trial — the HPV FOCAL Study. Br. J. Cancer 107, 1917–1924 (2012).
Arbyn, M., Walker, A. & Meijer, C. J. HPV-based cervical-cancer screening in China. Lancet Oncol. 11, 1112–1113 (2010).
Qiao, Y. L. et al. A new HPV-DNA test for cervical-cancer screening in developing regions: a cross-sectional study of clinical accuracy in rural China. Lancet Oncol. 9, 929–936 (2008).
Hopkins, T. G. & Wood, N. Female human papillomavirus (HPV) vaccination: global uptake and the impact of attitudes. Vaccine 31, 1673–1679 (2013).
Tracy, J. K., Schluterman, N. H., Greene, C., Sow, S. O. & Gaff, H. D. Planning for human papillomavirus (HPV) vaccination in sub-Saharan Africa: A modeling-based approach. Vaccine 32, 3316–3322 (2014).
Levin, A., Wang, S. A., Levin, C., Tsu, V. & Hutubessy, R. Costs of introducing and delivering H.P.V. vaccines in low and lower middle income countries: inputs for GAVI policy on introduction grant support to countries. PloS one 9, e101114 (2014).
Gavi. Human papillomavirus vaccine support. [online] (2014).
Pandhi, D. & Sonthalia, S. Human papilloma virus vaccines: Current scenario. Indian J. Sexually Transmitted Diseases 32, 75–85 (2011).
Gupta, S., Kerkar, R. A., Dikshit, R. & Badwe, R. A. Is human papillomavirus vaccination likely to be a useful strategy in India? South Asian J. Cancer 2, 193–197 (2013).
Naud, P. S. et al. Sustained efficacy, immunogenicity, and safety of the HPV-16/18 AS04-adjuvanted vaccine: Final analysis of a long-term follow-up study up to 9.4 years post-vaccination. Hum. Vaccin. Immunother. http://dx.doi.org/10.4161/hv.29532 (2014).
Konno, R. et al. Efficacy of the human papillomavirus (HPV)-16/18 AS04-adjuvanted vaccine against cervical intraepithelial neoplasia and cervical infection in young Japanese women: Open follow-up of a randomized clinical trial up to 4 years post-vaccination. Hum. Vaccin. Immunother. 10, 1781–1794 (2014).
Descamps, D. et al. Safety of human papillomavirus (HPV)-16/18 AS04-adjuvanted vaccine for cervical cancer prevention: a pooled analysis of 11 clinical trials. Hum. Vaccin 5, 332–340 (2009).
Chao, C. et al. Surveillance of autoimmune conditions following routine use of quadrivalent human papillomavirus vaccine. J. Intern. Med. 271, 193–203 (2012).
Arnheim-Dahlstrom, L., Pasternak, B., Svanstrom, H., Sparen, P. & Hviid, A. Autoimmune, neurological, and venous thromboembolic adverse events after immunisation of adolescent girls with quadrivalent human papillomavirus vaccine in Denmark and Sweden: cohort study. BMJ 347, f5906 (2013).
Dobson, S. R. et al. Immunogenicity of 2 doses of HPV vaccine in younger adolescents versus 3 doses in young women: a randomized clinical trial. JAMA 309, 1793–1802 (2013).
Romanowski, B. et al. Immune response to the HPV-16/18 AS04-adjuvanted vaccine administered as a 2-dose or 3-dose schedule up to 4 years after vaccination: Results from a randomized study. Hum. vaccin. immunother. 10, 1155–1165 (2014).
[no authors listed] World policy-makers cite UBC-CFRI research in approving fewer HPV vaccine doses. University of British Columbia [online] (2014).
Spencer, A. M., Roberts, S. A., Brabin, L., Patnick, J. & Verma, A. Sociodemographic factors predicting mother's cervical screening and daughter's HPV vaccination uptake. J. Epidemiol. Commun. Health 68, 571–577 (2014).
Parikh, S. & Hyman, D. Hepatocellular cancer: a guide for the internist. Am. J. Med. 120, 194–202 (2007).
Venook, A. P., Papandreou, C., Furuse, J. & de Guevara, L. L. The incidence and epidemiology of hepatocellular carcinoma: a global and regional perspective. Oncologist 15 (Suppl. 4), 5–13 (2010).
Nordenstedt, H., White, D. L. & El-Serag, H. B. The changing pattern of epidemiology in hepatocellular carcinoma. Dig. Liver Dis. 42 (Suppl. 3), S206–214 (2010).
Zhang, B. H., Yang, B. H. & Tang, Z. Y. Randomized controlled trial of screening for hepatocellular carcinoma. J. Cancer Res. Clin. Oncol. 130, 417–422 (2004).
Chen, J. G. et al. Screening for liver cancer: results of a randomised controlled trial in Qidong, China. J. Med. Screen 10, 204–209 (2003).
Sherman, M., Bruix, J., Porayko, M. & Tran, T. Screening for hepatocellular carcinoma: the rationale for the American Association for the Study of Liver Diseases recommendations. Hepatology 56, 793–796 (2012).
Ferenci, P. et al. World Gastroenterology Organisation Guideline. Hepatocellular carcinoma (HCC): a global perspective. J. Gastrointestin Liver Dis. 19, 311–317 (2010).
Omata, M. et al. Asian Pacific Association for the Study of the Liver consensus recommendations on hepatocellular carcinoma. Hepatol Int. 4, 439–474 (2010).
Lederle, F. A. & Pocha, C. Screening for liver cancer: the rush to judgment. Ann. Intern. Med. 156, 387–389 (2012).
Franco, E. et al. Hepatitis B: Epidemiology and prevention in developing countries. World J. Hepatol. 4, 74–80 (2012).
Goldstein, S. Global routine vaccination coverage, 2010. MMWR 60, 1520–1522 (2011).
Chen, C. J., You, S. L., Lin, L. H., Hsu, W. L. & Yang, Y. W. Cancer epidemiology and control in Taiwan: a brief review. Jpn J. Clin. Oncol. 32, S66–S81 (2002).
Lee, C. L., Hsieh, K. S. & Ko, Y. C. Trends in the incidence of hepatocellular carcinoma in boys and girls in Taiwan after large-scale hepatitis B vaccination. Cancer Epidemiol. Biomarkers Prev. 12, 57–59 (2003).
Kirk, G. D., Bah, E. & Montesano, R. Molecular epidemiology of human liver cancer: insights into etiology, pathogenesis and prevention from The Gambia, West Africa. Carcinogenesis 27, 2070–2082 (2006).
The General Assembly. Political Declaration of the High-level Meeting of the General Assembly on the Prevention and Control of Non-communicable Diseases. [online] WHO (2014).
Mahal, A., Karan, A., Fan, V. Y. & Engelgau, M. The economic burden of cancers on Indian households. PloS one 8, e71853 (2013).
McMahon, P. M. et al. Comparing benefits from many possible computed tomography lung cancer screening programs: extrapolating from the national lung screening trial using comparative modeling. PLoS ONE 9, e99978 (2014).
Patz, E. F. Jr et al. Overdiagnosis in low-dose computed tomography screening for lung cancer. JAMA Intern. Med. 174, 269–274 (2014).
Mizoue, T. et al. Prospective study of screening for stomach cancer in Japan. Int. J. Cancer 106, 103–107 (2003).
Leung, W. K. et al. Screening for gastric cancer in Asia: current evidence and practice. Lancet Oncol. 9, 279–287 (2008).
Choi, Y. S. et al. Colonoscopy screening for individuals aged 40–49 years with a family history of stomach cancer in Korea. Int. J. Colorectal Dis. 25, 443–447 (2010).
Sankaranarayanan, R., Gaffikin, L., Jacob, M., Sellors, J. & Robles, S. A critical assessment of screening methods for cervical neoplasia. Int. J. Gynaecol. Obstet. 89 (Suppl. 2), S4–S12 (2005).
Ying, H., Jing, F., Fanghui, Z., Youlin, Q. & Yali, H. High-risk HPV nucleic acid detection kit-the careHPV test -a new detection method for screening. Sci. Rep. 4, 4704 (2014).
Bansil, P. et al. Acceptability of self-collection sampling for HPV-DNA testing in low-resource settings: a mixed methods approach. BMC Public Health 14, 596 (2014).
Cervical screening. NHS [online] (2014).
Segi, M. Cancer mortality for selected sites in 24 countries (1950-57). (Tohoku University of Medicine, 1960).
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Glossary
- α-fetoprotein
-
(AFP). AFP is a protein found in the blood. It is produced by the liver of the fetus and its level steadily decreases after birth. Raised AFP levels in the blood are indicators of the presence of several diseases, including hepatocellular carcinoma.
- Breast self-examination
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(BSE). Both breasts are periodically (usually monthly) examined by the subject herself in a systematic manner.
- Global Alliance for Vaccines and Immunization
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(GAVI). A public–private global health partnership that is committed to increasing access to immunization in poor countries. GAVI has been negotiating with human papillomavirus (HPV) vaccine manufacturers to provide the vaccine to less-developed-region countries (LDCs) at very low costs.
- Less-developed-region countries
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(LDCs; as defined by the United Nations Population Division, Department of Economic and Social Affairs definition, 2012 revision). All regions of Africa, Asia (excluding Japan), Latin America and the Caribbean, Melanesia, Micronesia and Polynesia.
- Level-1 evidence of efficacy
-
Level-1 A evidence is derived from meta-analysis of randomized controlled trials, and Level-1 B evidence is derived from at least one randomized controlled trial. Grade A recommendations for medical practice are all based on Level 1 evidence.
- More-developed-region countries
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(MDCs; as defined by the United Nations Population Division, Department of Economic and Social Affairs definition, 2012 revision). All regions of Europe, North America, Australia, New Zealand and Japan.
- Opportunistic screening
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Also known as case-finding, this is a form of screening that is restricted to patients who consult a health practitioner for some other purpose.
- Physical breast examination
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(PBE). Both breasts and axillae are thoroughly examined in a systematic manner by a trained health care provider.
- Prevalence
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The number of persons in a defined population who have been diagnosed with the disease and who are still alive at the end of a given year.
- Primary health workers
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(PHWs). In LDCs, PHWs are usually state health services employees with some high school education and training in basic management of maternal and child health services and simple interventions for commonly occurring diseases in the community.
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Shastri, A., Shastri, S. Cancer screening and prevention in low-resource settings. Nat Rev Cancer 14, 822–829 (2014). https://doi.org/10.1038/nrc3859
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DOI: https://doi.org/10.1038/nrc3859
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