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RESEARCH

Commentary

Evidence-Based Nutrition Guidelines for Cancer Survivors:Current Guidelines,Knowledge Gaps,and Future Research Directions

KIM ROBIEN,PhD,RD,CSO,FADA;WENDY DEMARK-WAHNEFRIED,PhD,RD;CHERYL L.ROCK,PhD,RD C

ancer is one of the most prevalent chronic diseases in the United States and is the second leading cause of death (1).Approximately 1.48million Americans were diagnosed with cancer in 2009,with prostate,lung,breast,and colorectal cancers being most common (2).Although only 3million cancer survivors existed in the United States at the time of the National Cancer Act of 1971(3,4),there are now nearly 12million survivors (approximately 4%of the population),primarily due to increasing numbers of older Americans and advances in early cancer detection and treatment (5-8).The survivor population is comprised largely of individuals who have been diagnosed and treated for breast,prostate,and colo-rectal cancer because these are common cancers and have the best 5-year survival (9).Because cancer is a disease associated with aging,60%of cancer survivors are age 65or older (4).

Although survivorship should be celebrated,the impact of cancer is associated with several long-term health and psychosocial https://www.sodocs.net/doc/c27340423.html,mon late effects of cancer and its treatments include cardiovascular disease (CVD)(10),diabetes (11)and other endocrine disorders,and osteope-nia/osteoporosis (12,13),some of which could be pre-vented or managed by nutrition interventions (14-20).However,our ability to develop evidence-based nutrition recommendations for cancer survivors is limited by the dearth of research in this area.This commentary reviews

the current evidence-based diet and physical activity guidelines for cancer survivors,identi?es current knowl-edge gaps,and describes the research needed to ?ll those gaps.

POTENTIAL IMPACT OF NUTRITION INTERVENTIONS AMONG CANCER SURVIVORS

Compared with the general population,cancer survivors die of noncancer causes at signi?cantly higher rates,with almost one half of the deaths due to CVD (21-34).Cancer survivors have a twofold increased risk of functional lim-itations that may threaten their ability to live and work independently (35-47).In 2008,the US economic burden of cancer totaled more than $228billion.Although 41%of these costs involved direct cancer care,the majority of expenses were attributed to increased morbidity,lost pro-ductivity,and premature mortality (48).The vulnerabil-ity of cancer survivors and their unmet needs for ade-quate health care led to a 2005Institute of Medicine report (49),which called for increased efforts in survivor-ship,including a need to improve nutritional status and lifestyle factors (eg,diet and physical activity).

Data on cancer survivors’lifestyle behaviors have been accumulating over the past 2decades.Initial reports on select patient populations suggest that cancer survivors improve their lifestyle behaviors after diagnosis (50).However,data from larger subsequent population-based surveys with longer follow-up indicate that few health behavior differences may exist between cancer survivors and the general population (51-53).Given higher rates of comorbidity among survivors and the importance of diet and exercise for promoting overall health,these data support a need for lifestyle interventions that target this vulnerable population.

CURRENT RECOMMENDATIONS FOR CANCER SURVIVORS

In 1991,the American Cancer Society (ACS)?rst pub-lished nutrition and physical activity guidelines to reduce cancer risk,and in 2003guidelines were issued speci?-cally for cancer survivors.Both reports were updated in 2006and are scheduled for reassessment this year (54-57).In developing these reports,the ACS assembles pan-els of experts who systematically review the available

Audio Podcast available online at https://www.sodocs.net/doc/c27340423.html,

K.Robien is an assistant professor,Division of Epidemi-ology and Community Health,and a member,Cancer Outcomes and Survivorship Program,Masonic Cancer Center,University of Minnesota,Minneapolis.W.De-mark-Wahnefried is a professor and Webb Endowed Chair of Nutrition Sciences,University of Alabama–Bir-mingham (UAB),and associate director,UAB Compre-hensive Cancer Center,Birmingham.C.L.Rock is a professor,Department of Family and Preventive Medi-cine,University of California,San Diego,Moores UCSD Cancer Center,La Jolla.

Address correspondence to:Kim Robien,PhD,RD,CSO,FADA,Division of Epidemiology and Community Health,University of Minnesota,1300S Second St,Suite 300,Minneapolis,MN 55414.E-mail:robie004@https://www.sodocs.net/doc/c27340423.html,

Manuscript accepted:September 24,2010.Copyright ?2011by the American Dietetic Association.

0002-8223/$36.00

doi:10.1016/

j.jada.2010.11.014

368Journal of the AMERICAN DIETETIC ASSOCIATION ?2011by the American Dietetic Association

scienti?c evidence on diet and physical activity in relation to cancer risk reduction or for improving outcomes in cancer survivors.

Similarly,in1997the World Cancer Research Fund (WCRF)/American Institute for Cancer Research(AICR) produced an extensive systematic review of the evidence linking foods,nutrition,and related factors to cancer(58). The updated2007report also addressed cancer survivors and concluded that the lack of suf?cient research specif-ically among survivors precluded the development of ev-idence-based nutrition recommendations at this time (59).Thus,cancer survivors are encouraged to follow the recommendations for primary cancer prevention,which is consistent with the ACS recommendations.

The ACS and WCRF/AICR cancer prevention recommen-dations(Figure1)both emphasize achieving and maintain-ing a healthy weight;encouraging regular physical activity; eating a diet rich in vegetables,fruit,and whole grains;and limiting meat and alcohol consumption.Furthermore,both sets of recommendations advocate food,rather than supple-ments,as the source of nutrients.

WEIGHT CONTROL AND REGULAR PHYSICAL ACTIVITY

Excess body weight is a well-recognized risk factor for several types of cancers(59)and has been associated with higher mortality from all cancers combined,speci?cally for cancers of the breast,esophagus,colon and rectum, liver,gallbladder,prostate,and pancreas(60).Multiple biologic mechanisms may explain the association be-tween excess body weight and cancer risk,including in-creased low-grade chronic in?ammation,elevated levels of hormones and growth factors(for example,insulin, insulin-like growth factor-1,estrogens,and androgens), insulin resistance,adipokines(leptin,adiponectin),and signaling factors(phosphoinositol-3kinase[PI3K],mam-malian target of rapamycin[mTOR])(59).Weight gain after diagnosis is associated with higher cancer-speci?c and/or all-cause mortality in women who have been diag-nosed with breast cancer(61,62).A study of women with breast cancer found that women with normal body mass index(BMI;calculated as kg/m2)of24.9or less had sig-ni?cantly higher overall survival when compared with overweight(BMI25.0to29.9)or obese(BMI?30)women (63).In another trial,women with BMI of30or more had higher all-cause mortality and higher risk for contralat-eral breast cancer and other primary cancers(64).Al-though the observational evidence is largely consistent, there has never been a clinical trial to determine whether weight loss and maintenance of that loss reduces recur-rence risk or improves survival post-diagnosis.For colo-rectal and prostate cancer,available evidence suggests an unfavorable effect of increased adiposity on survival,al-though some inconsistencies exist(65).

Regular physical activity is a crucial determinant of weight control,and increasing evidence suggests that it exerts an important independent effect on survival af-ter a breast or colorectal cancer diagnosis(66-69).The level of physical activity necessary to have bene?cial effects on prognosis is still unclear.No clinical trials have yet reported the effect of physical activity on cancer recurrence or survival,though the Colon Health and Life-Long Exercise Change(CHALLENGE)trial is currently in progress(70).Several short-term studies have demonstrated improvements in physical function-ing and psychosocial factors with exercise(69).The American College of Sports Medicine has recently re-leased consensus guidelines on exercise for cancer sur-vivors(71),and now offers Certi?ed Cancer Exercise Trainer(CET)certi?cation(72).

DIET COMPOSITION

Few observational studies have reported associations be-tween diet composition and cancer survival.These stud-ies have been conducted largely in breast cancer survi-vors,although a few involve survivors of other types of cancer.

For breast cancer,evidence from observational cohort studies is mixed.Inverse associations have been found between fat intake and recurrence and/or survival,al-though these associations typically disappear with ener-gy-adjustment(73-76).A U-shaped relationship between dietary fat intake and survival following the diagnosis of breast cancer was identi?ed in one observational study (77),suggesting that extremes in fat intake may be asso-ciated with poorer outcomes.Intakes of vegetables,fruit, and related nutrients have been examined in relation to breast cancer recurrence and/or survival in11observa-tional studies,with signi?cant protective effects observed in four studies and suggestive?ndings in two others (73-75,78).Mixed?ndings from observational studies have been reported for?ber and meat.

Kroenke and colleagues(79)found that a prudent di-etary pattern(high in fruits,vegetables,whole grains, legumes,poultry,and?sh)was associated with a15% reduction in relative risk of overall mortality,and death from causes other than breast cancer,when compared with a Western dietary pattern(characterized by re?ned grains,processed and red meats,desserts,high-fat dairy products,and french fries).In another cohort of breast cancer survivors,consumption of at least?ve servings per day of fruits and vegetables plus a level of physical activ-ity equivalent to walking30minutes6days per week was associated with a50%reduction in mortality over a 7-year follow-up(78),although neither of these factors was signi?cantly protective alone.A study of1,009colon cancer survivors found that higher intake of a Western dietary pattern was associated with signi?cantly higher risk of recurrence and mortality(80).

Two large randomized controlled trials(RCTs)have tested whether diet modi?cation after the diagnosis of early-stage breast cancer affects cancer outcomes.The Women’s Intervention Nutrition Study(WINS)tested a low-fat diet (?15%of energy)in2,437postmenopausal women with early-stage breast cancer(81).Although on average the women in the intervention arm only decreased fat intake to 20%of energy at year1,the intervention resulted in a24% reduction in new breast cancer events.A stronger protective effect(42%reduction)was observed among women with estrogen receptor–negative tumors.Of note,women as-signed to the low-fat diet arm lost an average of6pounds over the course of the study,thus confounding whether the reduction in breast cancer events was due to dietary fat restriction or lower body weight.

The Women’s Healthy Eating and Living(WHEL) Study tested the effect of a diet very high in vegetables, fruit,and?ber and low in fat(20%of energy intake)on March2011●Journal of the AMERICAN DIETETIC ASSOCIATION369

cancer outcomes in3,088pre-and postmenopausal breast cancer survivors who were followed up for an average of 7.3years(82).At baseline,study participants reported a high average intake of vegetables and fruit(7.3servings/ day).At6years,the intervention group had increased to an average of9.2servings per day,whereas the control group averaged6.2servings per day.Recurrence-free sur-vival did not differ between the two study arms(83).However,serum estrogens at baseline were indepen-dently associated with poor prognosis,and a protective effect of the diet was observed in the subgroup of women who did not report hot?ashes at enrollment(84).These ?ndings suggest that reproductive hormonal status may determine whether a high-vegetable,fruit,and?ber diet affects prognosis.In addition,longitudinal exposure to carotenoids was associated with breast cancer–free sur-

Figure1.American Cancer Society2006Guidelines on Nutrition and Physical Activity for Cancer Prevention(57)and the World Cancer Research Fund/American Institute for Cancer Research Recommendations for the Prevention of Cancer,2007(59).

370March2011Volume111Number3

vival regardless of study group assignment(85).Thus, diet before the diagnosis of cancer and over the long-term may be more important than short-term dietary change post-diagnosis.

For prostate cancer,dietary factors associated with reduced risk for recurrence include?sh,tomato sauce, and monounsaturated fat intakes(86,87),whereas worse outcomes are observed with high levels of saturated fat (but not total fat)(88).In the single study that examined diet and survival after the diagnosis of ovarian cancer, increased consumption of vegetables,especially crucifer-ous,was associated with longer survival(89).No clinical trials of diet modi?cation with suf?cient follow-up have been reported for other cancer types.

Epidemiologic evidence has consistently linked alcohol intake to risk for several speci?c cancers,supporting the recommendation to limit alcohol intake for primary can-cer prevention(56).However,only a limited number of studies have evaluated the association between alcohol use after a cancer diagnosis and survival or disease re-currence.Observational evidence suggests worse progno-sis for individuals with head and neck cancer who report higher(vs lower)alcohol consumption after diagnosis (90,91).In contrast to the consistent positive association between alcohol intake and risk for primary breast can-cer,?ndings con?ict regarding alcohol intake and breast cancer recurrence(73,92,93).Small sample sizes,differ-ences in study design and data collection,and correla-tions between alcohol intake and other lifestyle factors (eg,smoking)or comorbid conditions may be responsi-ble for the con?icting results reported thus far.Recog-nizing the potential cardioprotective effects of alcohol on overall survival(94),the ACS report advises tai-lored guidance that considers other risk factors and comorbid conditions(57).

Micronutrients may play different roles in different stages of the cancer continuum,as is commonly demon-strated with the case of folate.Data from prospective observational cohort studies suggest that folate status is inversely associated with cancer initiation,due to its role in maintaining DNA stability and integrity(95).How-ever,once cancer is initiated,folate may enhance cancer proliferation(96).Mason and colleagues(97)hypothe-sized that the increased rates of colorectal cancers ob-served around the time of mandatory folate forti?cation of enriched grain products in the United States may be due to increased folate exposure promoting the growth of undetected cancers.Similarly,pharmacologic doses of mi-cronutrients may enhance progression of clinically unde-tectable cancers,including those remaining after cancer treatments,increasing the risk of relapse(98). DIETARY SUPPLEMENTS

Dietary supplement use is reported by52%of US adults (99),and studies report ranges between64%and81% among cancer survivors(100,101).A recent systematic review indicates that14%to32%of cancer survivors initiate supplement use after their diagnosis(100). Breast cancer survivors report the highest prevalence of supplement use,whereas prostate cancer survivors re-port the lowest(100).

However,evidence from both observational studies and clinical trials suggests that dietary supplements are not likely to improve prognosis or overall survival after the diagnosis of cancer,and may actually increase mortality. A2006meta-analysis found no association between anti-oxidant or retinol supplementation and all-cause mortal-ity among cancer patients,although the authors noted that this report was limited by the small number of trials, particularly those of high-quality(102).The use of mul-tivitamins or vitamins E or C were not associated with protection from cancer death in a cohort of77,719Wash-ington state residents followed up over a10-year period (103).A randomized clinical trial of540head and neck cancer patients receiving radiotherapy,in which partici-pants were randomly assigned to either400IU/day vita-min E or placebo,found that supplement use was associ-ated with signi?cantly higher cause-speci?c and all-cause mortality(104).

Both the ACS and the WCRF/AICR advise cancer sur-vivors to meet nutrient needs through food,although the ACS endorses the use of standard multivitamin/mineral supplements during and after cancer treatment for those who are unable to meet their needs through diet alone or who demonstrate speci?c de?ciencies(57). KNOWLEDGE GAPS TO BE ADDRESSED

Although results from research on the nutritional needs of cancer survivors is beginning to accumulate,several gaps in the knowledge base need to be addressed before evidence-based recommendations can be formulated speci?cally for cancer survivors.The focus of nutrition-related cancer sur-vivorship research to date has largely focused on interven-tions to decrease risk of cancer recurrence;however,data are also needed on the ability of nutrition interventions to address non-cancer endpoints and healthcare costs.In ad-dition,optimal timing and methodology of nutrition inter-ventions need to be identi?ed.

Need to Address Both Cancer and Noncancer Endpoints Cancer survivorship research commonly focuses on sur-vival and cancer recurrence as the primary outcomes of interest.However,data indicate that60%to75%of can-cer patients have at least one comorbid condition (105,106)and are signi?cantly more likely to die of non-cancer causes than the general population(21-34).There-fore,nutrition interventions aimed at prevention or man-agement of comorbidities and functional impairment,and at improving quality of life,may be as important as length of life to the individual survivor.In addition,re-search is needed to determine whether nutrition inter-ventions can decrease health care costs among cancer survivors.

Need for Risk-Based Nutrition Recommendations

Although all cancers share the characteristic of uncon-trolled growth and proliferation,there are more than100 different types of cancer,each with different etiology, rates of progression,recommended treatment regimens, response to treatment,and prognosis.Substantial heter-ogeneity in treatment regimens used to treat different cancer types contribute to the heterogeneity in health status and health concerns among cancer survivors.Bet-ter information about the relative effectiveness of speci?c March2011●Journal of the AMERICAN DIETETIC ASSOCIATION371

nutrition interventions in managing these cancer-and treatment-speci?c effects will allow nutrition services and resources to be better allocated.Risk-based,treat-ment-speci?c monitoring guidelines have been developed for pediatric cancer survivors(107),but these guidelines do not include nutrition recommendations,and similar guidelines for adults do not yet exist.

Need to Identify Optimal Timing and Method for Promoting Health Behavior Change

Despite efforts by the ACS and WCRF/AICR to encourage cancer survivors to follow diet and lifestyle recommenda-tions for cancer prevention,evidence suggests that few cancer survivors are doing so(108,109).Further research is needed to determine the optimal method and timing of interventions to promote healthy lifestyle behaviors among cancer survivors.

Figure2summarizes the stages of cancer survivorship, common nutrition issues,and challenges.For many pa-tients,the treatment period is overwhelming as patients cope with their treatment,treatment-related side effects, and other life demands.Patients also may be approached to participate in competing research studies that may prohibit participation in nutrition-related trials.Nutri-tion interventions during this stage need to be highly individualized and symptom-focused.Research to date has largely focused on the effect of medical nutrition therapy on short-term outcomes,such as ability to main-tain lean body mass,minimize weight loss,or improve quality of life(110-113).Until recently,the lack of stan-dardization in oncology nutrition training and the lack of controlled studies have complicated efforts to compare ?ndings across studies during treatment(114). Readiness to adopt long-term health behaviors may be enhanced after the completion of treatment.However, transition of health care to providers outside the cancer care facility may complicate recruitment for nutrition intervention studies,especially for individuals who are years beyond treatment.Outside of large urban areas, low population density and barriers involving travel and time also can be a challenge in recruiting suf?cient num-bers of participants.Alternatives to traditional face-to-face nutrition interventions,such as telephone counsel-ing and written materials,have been successful in achieving dietary behavior change among broad-based groups of cancer survivors(115,116).

CONCLUSION

Cancer survivorship research is still in its infancy,and the scienti?c evidence supporting nutrition recommendations for cancer survivors is currently limited.However,the in-creasing number of cancer survivors augments the impor-

Figure2.Stages of cancer survivorship and the corresponding nutrition and research issues. 372March2011Volume111Number3

tance of identifying appropriate nutrition interventions to improve outcomes,prevent or manage chronic health is-sues,improve quality of life,and decrease health care costs. Further research is needed to support the development of evidence-based nutrition guidelines for cancer survivors. STATEMENT OF POTENTIAL CONFLICT OF INTEREST: No potential con?ict of interest was reported by the au-thors.

FUNDING/SUPPORT:The authors certify that they have no af?liations or?nancial involvement with any organization or entity with a?nancial interest in or?-nancial con?ict with the subject matter or materials dis-cussed in this article.

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