Influence of physician’s lifestyle on the prescription of healthy habits to breast cancer patients (LACOG 1218)

Healthy lifestyle is capable of positively modifying the survival of breast cancer (BC) patients. We aimed to evaluate how physician’s lifestyle influences on the prescription of healthy habits to BC patients. An online questionnaire to evaluate physician lifestyle and prescription of healthy habits to BC patients was developed and circulated by e-mail to physicians dedicated to treat BC patients. A multivariate Poisson regression analysis assessed which factors of physician lifestyle could influence on prescription of healthy habits. A total of 267 physicians answered the questionnaire from October to November 2018. In terms of physician lifestyle, 228 (85.4%) had healthy eating habits and 236 (88.4%) practiced physical activity. Overall, 84.3% of the physicians advised their BC patients on the importance of lifestyle modification. Physicians who did not exercise regularly have a higher probability of not advising for health lifestyle (RR 2.48; p = 0.0265) as opposite to physicians ≥ 50 years-old (RR 0.37; p = 0.0118). Obesity treatment and management was performed by 45.3% of physicians. Being a breast surgeon (RR 1.29; p = 0.0025) or radiation oncologists (RR 1.82; p = 0.0025) were associated with not performing obesity treatment and management. About 53.4% of physicians referred overweight or obese patients to a dietitian and/or endocrinologist. Male gender (RR 1.35; p = 0.0296), breast surgeons (RR 1.99; p = 0.0001), and clinical practice in public health system (RR 1.53; p = 0.0012) were associated with not referring as opposed to physicians ≥ 50 years-old (RR 0.46; p = 0.0005). Our survey showed some influence of physician’s lifestyle on the prescription of healthy habits to BC patients. Physicians who practice physical activity regularly had a higher probability of advising lifestyle modification and about half of physicians did some type of overweight and obese management.


Introduction
Breast cancer (BC) is the most frequent cancer diagnosed in women worldwide. In 2018, 2,088,849 new cases and 626,679 deaths due to BC were expected [1]. In addition to the advances in pharmacological therapies that Novelty and impact statements A healthy lifestyle has been shown to have a positive impact on the quality of life, risk of recurrence, and overall survival in breast cancer. Physicians play an important role in encouraging their patients to lifestyle modification. LACOG 1218 survey identified that physician's lifestyle influences on the prescription of healthy habits to BC patients. Thus, strategies to engage physicians in healthier behaviors should be developed. have improved overall survival (OS) in the last decades, a healthy lifestyle has also been shown to have a potential positive impact on both quality of life and OS in breast cancer patients [2,3].
The World Health Organization (WHO) defines a healthy lifestyle as a combination of healthy eating, regular physical activity, and avoidance of tobacco and harmful alcohol consumption [4]. Clinical benefits, including lower recurrence rates, mortality rates, and better quality of life, among BC patients who follow a healthy lifestyle have been observed in epidemiological studies [3,5]. However, in prospective randomized clinical trials, these findings are still controversial [6].
According to the Women's Intervention Nutrition Study, dietary fat reduction compared to usual diet may improve relapse-free survival of BC patients (hazard ratio [HR] 0.76, 95% CI 0.60-0.98) [7]. However, in longterm follow-up, there was no benefit on OS, except in an exploratory analysis in the hormone receptor negative BC subgroup (risk relative [RR] 0.41 for mortality, p = 0.003 for patients who followed fat reduction diet) [8]. A subsequent randomized clinical trial from the Women's Health Initiative assessed reduction on fat intake to 20% and increase fruit, vegetable, and grain intake versus usual diet in 48,835 postmenopausal women with no previous BC. Among patients who developed BC during the trial, those allocated to dietary intervention group had improvement in OS (HR 0.78, 95% CI, 0.65-0.94) [9]. A recent metanalysis of dietary intervention on early BC did not find difference in mortality and disease-free survival [6]. Regarding the regular practice of physical activity, defined as at least 150 min of moderate-intensity, or 75 min of vigorous-intensity, aerobic physical activity per week [10], findings have shown that physical activity does not only helped to maintain adequate weight, but also reduced overall mortality (46%) and BC mortality (33%) among BC survivors [9,10]. A meta-analysis evaluating the association of physical activity with mortality in BC survivors found a reduction of 48% in overall and 28% in BC-specific mortality among those more active versus those less active [11].
Physicians play a critical role in encouraging their patients to change their habits. Further, recent data suggest that the success in promoting healthy lifestyle in patients is strongly correlated to the physician's own habits [12]. Physicians with less healthy habits tend to be less proactive in giving advice or motivating practices that they themselves do not follow [11][12][13]. However, this relation has not been established among physicians caring for BC patients.
Therefore, we developed a survey to evaluate physician's lifestyle and its influence on the prescription of healthy habits to BC patients.

Materials and methods
An online questionnaire composed by 14 objective questions was developed with the goal to evaluate physician lifestyle and prescription of healthy practices to BC patients. The first questions addressed the following domains of physician lifestyle: diet, physical activity, smoking, weight, amount of sleep, and alcohol consumption (using the modified version of quantity-frequency index). Other questions addressed the prescription of healthy habits to patients, the management of obesity, and the frequency of referral to an endocrinologist or dietitian in case of overweight or obesity. The estimated time to answer the questionnaire was 5 min. The full questionnaire is presented in Supplementary Material Table S1.
A brief explanation of the study proposal containing the survey link was sent by e-mail to 400 members of the Brazilian Society of Clinical Oncology (SBOC) and Latin American Cooperative Oncology Group (LACOG). The study population consisted of clinical oncologists, breast surgeons, and radiation oncologists involved in the treatment of BC patients. No financial incentive was offered to encourage completion of the survey. The definition of healthy lifestyle follows the WHO recommendations: healthy diet (eating lots of fruits and vegetables, reducing fat, sugar, and salt intake), physical activity (at least 150 min of moderate-intensity, or 75 min of vigorousintensity, aerobic physical activity, per week), no smoking, and BMI between 18.5 and 24.9 kg/m 2 .
The primary outcome was to evaluate the correlation between the physician's lifestyle and the prescription of healthy habits to BC patients. We describe the demographic characteristics and lifestyle of these physicians and identify characteristics that could influence prescription of healthy habits and patient weight management, including referral to a dietitian and/or endocrinologist for management of overweight or obese patients.

Statistical analysis
Answers to the 14 items of the questionnaire were summarized by absolute and relative frequencies. A multivariate Poisson regression analysis with robust variance was adjusted to assess which factors of physician lifestyle could influence prescription [14]. All analyses were performed using SAS statistical software (version 9.4; SAS Institute, Inc. Cary, NC). A significance level of 5% was considered.
Descriptive analysis of physicians' lifestyle is shown in Table 1. A total of 228 (85.4%) physicians followed the guidelines on diet most of the time, whereas 236 (88.4%) practice physical activity. Alcohol consumption was moderate among physicians and only 8 (3%) of them were current smoker. Overweight and obesity were found in 93 (34.9%) of the interviewees and 163 (61.1%) had BMI between the recommended level of 18.5-24.9. Most of the physicians (79.4%) sleep between 5 and 7 h per day, and 44 (16.5%) sleep more than 7 h per day. Of all participants only 23 (8.6%) physicians followed all the evaluated lifestyle recommendations on diet, physical activity, smoke habits, alcohol consumption, and amount of sleep and had an ideal BMI.
Overall, 84.3% of the physicians advised their BC patients on the importance of lifestyle modification. In a multivariate analysis, physicians who did not exercise regularly have a higher risk of not advising healthy lifestyle (relative risk (RR) 2.48; 95% CI 1.28 to 4.82, p = 0.0265). In turn, being older than 49 years reduced the risk of not advising healthy lifestyle (RR 0.37; CI 95% 0.15-0.92; p = 0.0118) ( Table 2).
Regarding obesity management, 121 (45.3%) physicians did some type of obesity management, 120 (44.9%) did not manage obesity because they did not feel properly trained to do that, and 26 (9.8%) did not manage obesity for other reasons. In multivariate analysis, physicians who did not follow healthy eating habits most of the time (all the time, only occasional deviation, and on weekdays) did not have an increasing in the risk of not manage obesity (RR 1.28; 95% CI 0.98 to 1.67, p = 0.0884). Medical specialty influenced obesity management (p = 0.0025): clinical oncologists more frequently manage obesity, while breast surgeons (RR 1.29; 95% CI 1.02 to 1.63) and radiation oncologists not (RR 1.82; 95% CI 1.43 to 2.31) ( Table 3).
Considering the referral to a dietitian and/or endocrinologist as an additional management measure of overweight or obese patients, only 53.4% of physicians informed referral to a dietitian and/or endocrinologist (Table 4). After multivariate analysis, the following independent factors were associated with not referring patients to a dietitian and/or endocrinologist: male sex (RR 1.35; CI 95% 1.03 to 1.76; p = 0.0296), breast surgeons (RR 1.99; CI 95% 1.50 to 2.64; p < 0.0001), and clinical practice exclusively or most of the time in public health care system (RR 1.53; CI 95% 1.20 to 1.96; p = 0.0012). In contrary, physicians older than 49 years had lower risk of not referring overweight or obese patients to a dietitian and/or endocrinologist (RR 0.46; CI 95% 0.28 to 0.75; p = 0.0005).  5 Yes, I drink less than once a month and do not consume 5 or more doses. Yes, I drink 1 or 3 times a month, and may or may not consume 5 or more doses on this occasion(s). I consume 5 or more doses at least once a year and may or may not reach this consumption once a week. Yes, I consume 5 or more doses of alcohol 1 or more times per week

Discussion
Adherence to healthy lifestyle guidelines is important for BC patients to reduce their risk of recurrence, to improve quality of life and overall survival [3]. Increasing adherence of breast cancer survivors to a healthier lifestyle, including a balanced diet and regular physical activity, can increase their survival by up to 40% [15]. Physicians have a critical role in assisting BC patients to adapt healthy lifestyle. In our study, we found that 85.4% of physicians followed the guidelines on diet most of the time and 88.4% practice physical activity, while 84.3% of them advised their BC patients on the importance of lifestyle modification. Our results are aligned with previous studies which have shown that, when health professionals engage in healthy behaviors, they are more likely to provide preventive counseling to their patients [12,14,16,17]. When we evaluated the correlations among physician's lifestyle and its influence on the prescription of healthy habits to BC patients, we found that physicians who practiced physical activity regularly had more chance to advise lifestyle changes for BC patients. A similar correlation was previously demonstrated in a survey with North American physicians which showed that physicians who practiced aerobic exercise regularly were more likely to advise their patients on the benefits of exercise (OR 5.72; 95% CI 2.41-13.54; p < 0.0005) [17]. However, the rates of advising physical activity remains suboptimal. Studies have demonstrated that only 28% of patients receive any advice about physical activity, and 40% of them receive some assistance in planning an exercise routine. Physicians mention the need for exercise but do not specify or discuss the types of exercise or their frequency [18]. Stimulating physical activity is essential for cancer survivors, since there is strong evidence that moderate to intense aerobic activity 3 × per week combined with resistance exercise training not only can reduce anxiety, depressive symptoms, and fatigue, but also can improve overall quality of life [18,19].
Regarding the importance of weight management, it is well known that women with BC who gain weight during or after treatment have been shown to have a worse prognosis [5,20], especially those who gained more than 10% weight after diagnosis (HR 2.67; 95% CI, 1.37-5.05) [21]. In addition, breast cancer survivors who had a diet rich in saturated fats, especially dairy products, had an increase in mortality [22,23]. In our study, we found that only 45.3% of physicians did some type of obesity management and 53.4% of the overweight or obese patients were referred to a dietitian and/or endocrinologist as an additional management measure for overweight and obesity. Being a breast surgeon or radiation oncologist were factors associated with not performing obesity treatment and management. Additionally, physicians with clinical practice exclusively or mostly in the public health care system had an increased risk of not referring overweight and obese patients to a dietitian or endocrinologist. These findings might be explained by an overload both in terms of the physician's time and the back log of specialized consultations in the public health care system. Conversely, physicians older than 49 years had lower risk of not referring overweight or obese patients to a dietitian and/or endocrinologist. Other physician habits also seemed to correlate with advice and prescriptions; however, these findings were not statistically significant, possibly because of the sample size.
Motivating cancer patients to change their diet, exercise, and adopt healthy lifestyle has always been challenging, since patients may feel it more difficult to exercise after diagnosis and treatment. In the past, clinicians used to advise cancer patients to rest and to avoid physical activity, but research done in the 1990s and 2000s has questioned this concept, leading to a change in practice guidelines [24]. Exercise is not only safe and possible during cancer treatment, but it can improve physical function and quality of life. Currently, the recommendation is that physicians, including oncologists, counsel cancer survivors to adopt healthy lifestyles [25]. Despite the mentioned benefits and recommendations of healthy lifestyle for BC patients, there are several barriers to medical advice on healthy lifestyle, including insufficient training and lack of confidence to advise healthy diet and exercise [26]. An online questionnaire that assessed 971 oncology providers practice patterns and perceptions of obesity and weight management during and after cancer treatment showed that although the majority reported advising patients to maintain a healthy weight, increase physical activity, and eat healthy, only 42% of them refer patients to dietitian. The main barriers identified were lack of education, lack of time, lack of adequate programs to make referrals, and resistance of patients to change lifestyle [27]. These findings reinforce that training related to lifestyle modification should be incorporated into the medical school curriculum, fellowship programs, and continuing medical education to enhance physicians' knowledge and competence, including lifestyle management and behavioral change skills.
The present study has limitations that need to be addressed. First, the self-report nature (thus information about socially undesirable behaviors such as smoking and alcohol use may be underreported). Second, this sample of physicians was self-selected and thus may not be a representative sample of physicians under investigation. Third, the population studied includes only LACOG and SBOC members, which already selects professionals with an academic profile, causing a selection bias, which may impact the generalization of the information obtained. Lastly, respondents may represent a population that is specifically interested in the topic.
There is extremely limited information on Latin American physician lifestyle and its impact on the prescription of healthy habits to BC patients. Our study results may increase awareness and help design interventions to improve health professionals' own habits and health-promoting behaviors.

Conclusion
In conclusion, our survey showed some influence of physician's lifestyle on the prescription of healthy habits to BC patients. Physicians who practice physical activity regularly or that are older than 50 years had higher probability of advising lifestyle modification. Only half of BC patients' physicians treat obesity or refer these patients to specialist which in this case may impact BC patient's outcome. Thus, strategies to engage physicians in healthy habits, as well as educational initiatives, should be stimulated for physicians treating patients with breast cancer.