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Future Directions in Cancer Prevention REVIEWS Future directions in cancer prevention Asad Umar1, Barbara K. Dunn2 and Peter Greenwald 3 Abstract | Prevention of cancer remains the most promising strategy for reducing both its incidence and the mortality due to this disease. For more than four decades, findings from epidemiology, basic research and clinical trials have informed the development of lifestyle and medical approaches to cancer prevention. These include selective oestrogen receptor modulators and aromatase inhibitors for breast cancer, the 5‑α-reductase inhibitors finasteride and dutasteride for prostate cancer, and the development of vaccines for viruses that are associated with specific cancers. Future directions include genetic, proteomic and other molecular approaches for identifying pathways that are associated with cancer initiation and development, as well as refining the search for immunologically modifiable causes of cancer. Globally, cancer is the leading cause of death in devel- cancer, as can aspects of the immune response, such oped countries and the second leading cause of death as immunoediting7. in developing countries, where the cancer burden is The physiological goal of cancer prevention is to inter- rising. Estimates for 2008 pointed to 12.7 million can- cept these processes in order to inhibit progression to the cer cases and 7.6 million cancer deaths worldwide1,2. invasive stage (FIG. 2). An understanding of the accumu- Despite improvements in the treatment of various lating genetic and other molecular alterations that char- common cancers, a large cancer burden remains, pro- acterize progressively advanced, pre-malignant lesions 1National Cancer Institute, viding a growing incentive to address this problem by will offer targets for putative, preventive interventions. Division of Cancer Prevention, a preventive approach. Although eliminating exposure Protracted carcinogenic progression also lends itself to Gastrointestinal and Other to carcinogens, such as tobacco, is a well-established the screening of high-risk individuals without clinically Cancers Research Group, approach to prevention, active intervention with evident cancer (BOX 1). Screening identifies not only National Cancer Institute, agents that are expected to reduce the risk of cancer is early stage invasive cancers that are expected to be more Executive Plaza North 2142, 3,4 6130 Executive Boulevard, becoming increasingly accepted . amenable to cure, but also pre-malignancies that can be MSC 7317, Rockville, removed and thus prevented from progressing to inva- Maryland 20852–7371, USA. Carcinogenesis: opportunities for prevention sive lesions. Finally, precancerous lesions often spontane- 2National Cancer Institute, Common, adult, epithelial cancers represent the final ously regress, presumably in response to innate immune Division of Cancer Prevention, Chemopreventive Agent step in a multi-year progression from normal tissue, mechanisms. This endogenous behaviour suggests that Development Research Group, through increasingly abnormal-looking stages of pre- exogenously administered immunological interven- National Cancer Institute, malignancy to invasion of the basement membrane, tions should be effective in eliminating pre-cancers. Executive Plaza North 2056, which constitutes overt cancer. Once a histological In fact, prophylactic vaccines against cancer-causing 6130 Executive Boulevard, boundary has been penetrated, invasive cancer has the infectious agents are highly effective in eliminating the MSC 7317, Rockville, Maryland 20852–7371, USA. potential to metastasize, and metastases generally lead causative agent for cancer initiation. Other immune 3National Cancer Institute, to cancer-related mortality. response modulators might also have a role in cancer Associate Director for The evolution of these adult malignancies involves prevention. Prevention, Office of the the gradual accumulation of genetic and epigenetic The precancerous lesion itself is not the only mani- Director, National Cancer (FIG. 1) Institute, Building 31, Room cancer-promoting changes . The affected festation of the process of carcinogenesis. The micro­ B2B37, 31 Center Drive, genes, oncogenes, as well as tumour suppressor environment encasing and interspersed with a lesion MSC 2037, Bethesda, genes, are mutated in a manner that subverts their often undergoes changes that actively contribute to MD 20892-2037, USA. normal function, thereby contributing to the multi- carcinogenesis. Precancerous changes in the micro- Correspodence to A.U. ple processes that are considered to be the hallmarks environment can be included in the larger category e‑mail: [email protected] 5,6 8,9 doi:10.1038/nrc3397 of cancer . Additional modifications, such as epi- of field effects : those generalized tissue changes Published online genetic silencing of tumour suppressor genes also that provide a crucial backdrop against which a given 15 November 2012 contribute to the relentless progression to invasive lesion will develop. Therefore, relevant changes in the NATURE REVIEWS | CANCER VOLUME 12 | DECEMBER 2012 | 835 © 2012 Macmillan Publishers Limited. All rights reserved REVIEWS At a glance programmes in such countries have been successful in raising awareness of the dangers of tobacco use; • In the past three decades, the approach to cancer prevention has moved from however, initiatives will need to be adapted for imple- population and epidemiological studies to molecular targeting and immunological mentation in developing countries owing to differ- approaches and to identifying high-risk pre-cancerous lesions in individuals using ences in cultural and societal norms between different emerging early detection technologies. countries14. • Global implementation of these scientifically-sound lifestyle- and medical-based cancer prevention strategies has the potential to reduce worldwide cancer incidence, prevalence and mortality rates in the decades ahead. Nutrition and diet. Considerable progress has been • As more is learned about the mechanisms and pathways that are influenced by made in the past four decades regarding our under- 13,15,16 genetic and molecular changes that initiate cancer or encourage its progression, standing of the association between diet and cancer . targeted therapies are being developed to interrupt these processes. Additional The study of diet and cancer has been separated into strategies are specifically focused on interrupting the late-stage, but still studies investigating dietary patterns, specific foods and pre-malignant, processes that lead to in situ cancers, with the goal of averting biologically active food components (BFCs). Large popula- progression to actual invasive cancer. tion studies have revealed associations between certain • The success of vaccines for human papilloma virus (HPV)- and hepatitis B virus dietary patterns and cancer risk, thus setting the stage (HBV)-related cancers has led to an increased focus on immunologically based for nutritional intervention programmes that encourage research for many other cancers. Efforts are ongoing to develop immune response healthier diets and clinical trials that include cancer risk modulation strategies to augment the innate immunity and to develop vaccines reduction as an end point17,18. against oncogenic infectious agents, as well as tumour-associated and Going beyond studies of overall diets, laboratory- tumour-specific antigens. based investigations are progressively identifying • The groundwork for the future of cancer prevention is currently being developed through multidisciplinary initiatives that involve researchers from tradition specific cancer-preventive nutrients and the molecu- 19 biology-based laboratories, as well as collaborators from the fields of information lar mechanisms by which they exert this property . technology, imaging technologies, ‘-omics’ (such as genomics, proteomics and Among the BFCs that seem to be somewhat promis- metabolomics) and communication. Expertise in communication is essential to ing for cancer prevention are soy isoflavones for breast disseminate research findings to the communities that are likely to benefit from these cancer, lycopene (found in tomatoes) for prostate can- findings. Inherent to this future progress is a focus on precision (individualized) cer, as well as resveratrol (from grapes and red wine), medicine that will include identifying those who are at a high risk of developing cancer. omega‑3‑fatty acids (found in fish oil), pomegranate, curcumin and antioxidants such as selenium and vitamin E, for other cancers20 (TABLE 1). Several large microenvironment can be used as biomarkers for early Phase III trials that randomize participants to specific detection and treatment, as well as serving as targets nutrients that have been hypothesized to lower the risk for chemopreventive and immunopreventive interven- of specific cancers have been carried out. One such tions8,10. Examples of microenvironment modifications trial, the Selenium and Vitamin E Cancer Prevention that contribute to carcinogenesis include increased Trial (SELECT), indicated that neither selenium nor angiogenesis10, as well as inflammatory and immuno­ vitamin E supplementation, alone or in combination, logical changes. Notably, increased mammographic reduced the risk of prostate cancer compared with a density, a frequently cited risk factor for breast cancer, is placebo21. Indeed, dietary supplementation with vita- actually an imaging manifestation of microenvironment min E alone increased the risk of prostate
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