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Keywords:

  • prostate cancer;
  • androgen deprivation therapy;
  • osteoporosis;
  • knowledge;
  • health beliefs;
  • healthy bone behaviours;
  • bone mineral density

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Patients and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Conflict of Interest
  9. References

What's known on the subject? and What does the study add?

  • There is an increase in use and duration of androgen-deprivation therapy (ADT) in patients with prostate cancer. ADT can cause decreased bone mineral density and lean muscle loss, putting these patients at increased risk of fracture. Guidelines exist for the prevention and management of bone loss in this population; however, data suggests that most patients are not receiving proper screening, evaluation, or treatment for bone loss. Research to date suggests that patients on ADT are unaware of the risks and side-effects of ADT and that most are not engaging in important preventative behaviours, e.g. calcium and vitamin D intake.
  • To our knowledge, there are no studies in patients on ADT specifically assessing patients' osteoporosis (OP) knowledge, self-efficacy, and feelings of susceptibility towards OP and their relationships to engagement in recommended healthy bone behaviours. We think that these data will aid in the development of health promotion uptake strategies that are directly targeted to this patient population.

Objectives

  • To describe in patients with prostate cancer, receiving androgen-deprivation therapy (ADT): (i) knowledge, self-efficacy (SE), and health beliefs about osteoporosis (OP); (ii) current engagement in healthy bone behaviours (HBBs).
  • To explore the relationships between knowledge, SE, and health beliefs, and engagement in HBBs.

Patients and Methods

  • 175 patients receiving ADT by injection completed questionnaires assessing current HBBs, OP knowledge, SE, and health beliefs (motivation, perceived susceptibility, and seriousness).
  • Descriptive statistics and independent samples t-tests were used to assess relationships between knowledge, SE, health beliefs, and engagement in HBBs.

Results

  • Only 38% of patients had undergone a dual X-ray absorptiometry scan in the past 2 years. OP knowledge was low (mean [sd, range] 9.6 [4.4, 0–19]) and perceived SE moderate (84.7 [24.5, 0–120]). Health motivation was fairly high (23.6 [3.1, 6–30]), but perceived susceptibility (16.8 [4.3]) and seriousness (16.8 [4.2]) of OP were low.
  • Few patients met the recommendations for vitamin D intake (42%) and exercise (31%), and 15% were at risk of over-supplementation of calcium.
  • Patients taking calcium supplements (P = 0.04), and meeting guidelines for vitamin D (P = 0.008) and for exercise (P = 0.002) had significantly greater knowledge than those who did not.
  • Patients who were engaging in less than four of five HBBs had lower knowledge (P < 0.001) and health motivation (P = 0.01) than those who were engaging in four or all five HBBs.

Conclusions

  • Most patients who are receiving ADT are not receiving appropriate screening, lack basic information about bone health, and are not engaging in the appropriate HBBs.
  • These findings support the application of the Health Belief Model in this population: interventions that teach patients about the implications of bone loss, encourage proper uptake of HBBs, and promote feelings of SE could increase engagement in HBBs to prevent and manage bone loss.

Abbreviations
ADT

androgen-deprivation therapy

BMD

bone mineral density

DXA

dual X-ray absorptiometry

FRAX

Fracture Risk Assessment Tool

FOOQ

Facts on Osteoporosis Quiz-Revised

HBB

healthy bone behaviour

OHBS

Osteoporosis Health Belief Scale

OP

osteoporosis

PMH

Princess Margaret Hospital

SE

self-efficacy

Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Patients and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Conflict of Interest
  9. References

Prostate cancer is the most commonly diagnosed malignancy in North American men [1, 2]. Fortunately, due to earlier detection and advances in treatment, the mortality rate for prostate cancer has significantly decreased over the past two decades [3] and the overall 10-year disease-specific survival is >90% [4]. Consequently, quality of care for patients with prostate cancer must incorporate health and wellness promotion strategies that both minimise dysfunction and disability caused by prostate cancer and its treatments and maximise survivors' quality of life [5].

Prostate cancer is commonly and increasingly treated with androgen-deprivation therapy (ADT), involving either surgical castration (orchidectomy) or chemical castration using GnRH agonists [6]. Due to its use at earlier stages of disease, almost one in every two men diagnosed with prostate cancer are now expected to receive this treatment [7, 8]. While ADT has been shown to reduce tumour growth and disease-specific symptoms and extend survival [3, 7, 8], these therapies can induce several long-term side-effects [3, 6, 9-12], one of the most significant of which is bone loss [6, 9, 10, 13, 14].

Prostate cancer typically occurs at an age when serum testosterone levels are naturally decreasing in men. The initiation of ADT results in dramatic hypogonadism, which causes decreased bone mineral density (BMD) and muscle loss [6, 10-12, 15]. Men receiving ADT have been shown to have a 5- to 10-fold increased loss of BMD at multiple skeletal sites, with maximal loss occurring within the first year after ADT initiation [16, 17]. This bone loss and accompanying decrease in muscle mass increases the risk of osteoporosis (OP), falls, and fractures. The risk of fracture in men on ADT has been reported as high as 20% by 5 years of treatment [3, 14]; this is almost twice the risk of fractures in healthy controls or men with prostate cancer who are not on ADT [18]. Fractures secondary to OP can result in severe pain, fatigue, depression, functional impairment, and up to 20% mortality [13, 19, 20], and they are a significant cost to the healthcare system [21, 22].

There is widespread consensus that bone loss and its consequences are often preventable and prostate cancer specialists should prescribe ADT with this knowledge. Guidelines and consensus statements exist for the prevention and management of bone loss in the general population [21, 23], in men [24], and more specifically in those with cancer-treatment induced bone loss [11, 12, 25] including men on ADT therapy [26, 27]. The recommendations include screening for OP with dual-energy X-ray absorptiometry (DXA) scans, evaluation of fracture risk through the use of the WHO Fracture Risk Assessment Tool (FRAX), initiation and maintenance of healthy bone behaviours (HBBs), and guidelines for the cost-effective use of pharmacological therapy [28]. The FRAX tool provides a validated score upon which to base treatment recommendations based upon fracture risk. Low risk is defined as a 10-year risk estimation of <10%, moderate risk is a 10–20% risk of fracture, and high risk is defined as anybody with an overall risk of >20% or >3% risk of hip fracture [28].

Screening for men receiving ADT should be done through the use of baseline (at the initiation of ADT) and repeat (1–2 years) DXA, and the results should be used to evaluate fracture risk [11, 23, 26]. Recommended HBBs include smoking cessation, limiting alcohol consumption (<21 servings/week), daily intake of 1000–1200 mg calcium and 800–1000 IU vitamin D, and almost daily moderate-to-vigorous weight-bearing exercise [23, 26].

Prostate cancer specialists and primary healthcare providers play an essential role in screening, evaluation, and treatment of bone loss in men receiving ADT. In addition, uptake and proper implementation of HBBs by the affected man can play an important role in delaying or preventing the need for pharmacotherapy, and may also reduce muscle weakness, resulting in decreased risk of falls and fractures [29-31]. However, the factors related to a person's decision to engage in and maintain healthy behaviours are numerous and complex. Rosenstock's Health Belief Model, one of the most widely used theoretical frameworks that guides OP-related health behaviour research and practice, suggests that an individual's actions to prevent, screen for, and manage disease is dependent on several factors, including knowledge, perceived susceptibility and seriousness of the disease, and inherent self-efficacy (SE) [32-35].

Despite the high risk for accelerated bone loss, the consequences of fractures, and the existence of guidelines, preliminary data suggests that a minority (18%) of men on ADT in Ontario have a DXA test done ≤2 years of starting ADT [36] and that most men on ADT do not routinely receive information, evaluation, or treatment for bone loss [13, 37-40]. Research to date suggests that men in the general population are less aware and knowledgeable about OP and related preventive behaviours and feel less susceptible to OP than women [35, 41]. One study found that up to half of men on ADT are unaware of its significant potential side-effects including OP and increased fracture risk [42], and preliminary data suggest that most do not have adequate calcium and vitamin D intake [37].

To our knowledge, there are no studies in patients on ADT specifically assessing the relationship of the Health Belief Model, including OP knowledge, SE, and health beliefs, with receipt of DXA and engagement in HBBs. These data will aid in the development of health promotion uptake strategies that are directly targeted to this patient population.

Patients and Methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Patients and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Conflict of Interest
  9. References

Approval for this study was received from the University Health Network (UHN) Research Ethics Board. From June to December 2011, patients were recruited from the genitourinary cancer clinics during their regular follow-up appointments at Princess Margaret Hospital (PMH). PMH is an academic teaching hospital situated in downtown Toronto and the largest cancer centre in Canada. Over 1000 men with prostate cancer are treated at PMH each year. Eligible patients met the following study criteria: (i) currently receiving ADT by injection, (ii) able to speak and read in English, and (iii) able to provide informed consent. Patients were excluded if they were receiving concurrent chemotherapy or had symptomatic metastatic disease. Upon consent, patients were scheduled for BMD testing (DXA) if they had not received one in the past 18 months, with the exception of 10 patients who refused. Patients completed the questionnaire package in the clinic or sent it back by mail.

Measures

The questionnaire package comprised of four sections, including demographic information, clinical OP risk factors, HBB assessment, and validated measures for knowledge, SE, and health beliefs. Demographic variables and clinical OP risk factors were collected via the self-reported questionnaire and corroborated with the BMD radiology report. Based on current guidelines we classified patients as meeting current recommendations for HBBs based on the following criteria: (i) smoking (not smoking) [11], (ii) alcohol (<21 drinks/week) [11], (iii) calcium (1200–2000 mg) through diet and/or supplementation, (iv) vitamin D (≥800 IU) [23, 26], and (v) exercise (≥150 min of moderate-to-vigorous exercise per week) [43]. Smoking status and alcohol consumption were assessed via a yes/no response and quantified as necessary. Patients were asked directly (yes/no) about whether they took calcium and vitamin D supplementation and asked to quantify the daily dose.

Average daily dietary sources of calcium were measured using the validated 16-item Food Frequency Questionnaire [44] and this was then combined with the supplement amount to form total daily calcium intake. Exercise frequency and intensity was assessed with the Godin Leisure-Time Exercise Questionnaire (GLTEQ), a brief validated three-item questionnaire that asks respondents to report on their typical weekly exercise habits [45].

OP knowledge was assessed using a revised 19-item version of the Facts on Osteoporosis Quiz-Revised (FOOQ), which included the six-item Men's Osteoporosis Knowledge Questionnaire (MOKQ), designed to complement the FOOQ [46, 47]. SE was measured with the Osteoporosis Self-Efficacy Scale (OSES) that includes two six-item subscales to measure confidence in initiating and maintaining calcium intake and initiating and maintaining exercise habits [48]. Health beliefs about bone health and OP were assessed using the Osteoporosis Health Belief Scale (OHBS). Three six-item subscales of the OHBS were used to measure beliefs about OP susceptibility, OP seriousness, and general health motivation [32].

Descriptive statistics were calculated to provide summary information about the characteristics of patients. Independent samples t-tests were used to assess relationships between knowledge, SE, health-beliefs, and engagement in HBBs.

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Patients and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Conflict of Interest
  9. References

Of 330 eligible patients, 191 agreed to participate and provided written consent (58% response rate) and 175 completed the questionnaires (53% completion rate). The sample was primarily English speaking (91%), married or common-law (80%), and retired (68%). Half of the sample (51%) were born in Canada, and 66% had received college or university education. Patient demographics and clinical variables (175 patients) are given in Table 1. One-third of patients had started ADT therapy within the past year, 39% within 1–5 years, and 27% >5 years ago. The median (range) duration of ADT exposure was 30 (1–221) months. Most of the patients were overweight or obese (73%). Just over one-third (38%) of the patients had received a DXA scan within the previous 2 years. Based on DXA results, 81 (46%) patients had osteopenia and 10 (6%) patients had OP; based on the FRAX assessment 37 (21%) were at moderate and three (2%) were at high risk for fracture.

Table 1. Demographic and clinical variables of the 175 patients
VariableValue
Mean (sd, range; median) age, years72.6 (8.9, 51–90; 73)
N (%): 
English spoken at home160 (91)
Married/common-law140 (80)
Retired119 (68)
Prior treatments received: 
Androgen deprivation175 (100)
Radiation109 (62)
Surgery58 (33)
Chemotherapy8 (5)
Body mass index, kg/m2 
Underweight <18.52 (1)
Normal weight 18.5–24.945 (26)
Overweight 25.0–29.989 (51)
Obese ≥30.039 (22)
Mean (sd, range; median) duration of androgen deprivation, months47 (51, 1–221; 30)
N (%): 
Duration of androgen deprivation, years 
<158 (33)
1–341 (23)
3.1–528 (16)
>546 (28)
Previous fragility fracture21 (12)
Self-reported prior diagnosis of OP18 (10)
DXA category (based on femoral neck T score)74 (42)
Normal bone density81 (46)
Osteopenia11 (6)
OP10 (6)

In all, 18 (10%) patients reported having previously received a diagnosis of OP and nine of 18 (50%) reported that they were currently taking some form of OP medication. An additional 15 (9%) patients reported previous fragility fracture (non-traumatic fracture aged >50 years) and, of these, none reported taking medication. An additional eight (4.6%) patients who had not previously been diagnosed with OP scored <–2.5 on femoral hip DXA, and four of these eight patients reported taking OP medications.

Knowledge, SE and Health Beliefs

In this sample, overall OP knowledge was low (mean [sd, potential range] 9.6 [4.4], 0–19) and perceived SE was moderate (84.7 [24.5, 0–120]). Health motivation was relatively high (23.6 [3.1, 6–30]), but susceptibility towards (16.8 [4.3, 6–30]) and seriousness in regards to OP (16.8 [4.2, 6–30]) were low.

Patients with a college or university education had higher OP knowledge (10.3 vs 8.0, P < 0.001) and higher SE (78.6 vs 87.7, P = 0.024) than those with only high school education or less. We also found higher OP knowledge in patients who had received a prior DXA scan (within the past 2 years) (9.0 vs 10.5, P = 0.03) and patients who reported currently taking OP medication (9.3 vs 11.5, P = 0.033). There was a trend toward increased knowledge in patients with a previous diagnosis of OP (9.4 vs 11.4, P = 0.074). In addition, we found lower SE in patients who were overweight or obese according to BMI (81.8 vs 93.4, P = 0.009) and in patients with a previous fragility fracture (74.1 vs 86.0, P = 0.043). Feelings of susceptibility towards OP were higher in patients with a previous diagnosis of OP (16.3 vs 20.5, P = 0.002), as well as in patients taking OP medications (16.5 vs 19, P = 0.019), but not in patients who had received a DXA scan within the past 2 years. There were no differences in these outcomes between patients who started ADT within the past year (58 patients, 33%) vs those who started on ADT prior to that (117, 67%).

HBBs

There was wide variation in the proportion of patients engaging in each HBB based on current guidelines (Fig. 1) [23]. Most patients did not smoke and limited their alcohol consumption to levels that are considered low risk for bone health.

figure

Figure 1. Percentage engagement in HBB guidelines (based on self-report of 175 patients). Guidelines based on Papaioannou et al. [23] 2010 and Canadian Physical Activity Guidelines 2012.

Download figure to PowerPoint

About 35% of patients were meeting recommendations for safe intake of 1200–2000 mg of calcium per day, 28% were getting <1200 mg, and 37% were getting >2000 mg. In all, 60% of patients reported taking calcium supplements. Interestingly, more than half of the sample (56%) was getting >1200 mg of calcium through their diet alone and one-quarter of these patients were also taking a calcium supplement, placing them at risk for too much calcium.

Less than half of the cohort met appropriate guidelines in terms of vitamin D intake ≥800 IU (42%) and exercise frequency/intensity ≥150 min/week (31%) [43]. To calculate a total HBB score, patients were given 1 point for meeting defined recommendations for each of the five HBBs. A total of 45% (79) of patients achieved a score of 4 or 5.

OP knowledge, SE and health beliefs did not differ between those getting enough calcium (either by diet or supplement) vs those who were not. However, patients taking a calcium supplement had higher OP knowledge scores than those who were not taking a supplement (mean [sd] 8.7 [4.4] vs 10.2 [4.4], P = 0.035). Similarly, patients taking ≥800 IU of vitamin D daily had higher OP knowledge scores than those who were not meeting the recommendation (mean [sd] 8.8 [4.2] vs 10.6 [4.4], P = 0.008) (Table 2). For exercise, patients were who exercising ≥150 min/week had higher OP knowledge (8.9 [4.3] vs 11.1 [4.1], P = 0.002), SE (78.7 [24.7] vs 97.8 [18.7], P < 0.001), and health motivation (23.2 [3.1] vs 24.5 [2.8], P = 0.012) than those who were not meeting recommendations. Overall, patients who were engaging in less than four HBBs had lower knowledge (8.5 [4.3] vs 10.8 [4.2], P = 0.001) and health motivation (22.9 [3.3] vs 24.5 [2.7], P = 0.001) than men who were engaging in four or all five HBBs (Table 3).

Table 2. OP knowledge scores for patients meeting vs not meeting HBB guidelines
Guideline description (threshold required to ‘meet’ guideline)Knowledge in patients not meeting guidelines, mean (sd)Knowledge in patients meeting guidelines, mean (sd)P
Calcium supplementation (yes)8.7 (4.4)10.2 (4.4)0.035
Vitamin D supplementation (≥800 IU of vitamin D daily)8.8 (4.2)10.6 (4.4)0.008
Exercise (≥150 min/week)8.9 (4.3)11.1 (4.1)0.002
Table 3. Health Belief Model scores in patients engaging in one to three HBBS vs four to five HBBs
 Score in patients engaging in one to three HBBs, mean (sd)Score in patients engaging in four to five HBBs, mean (sd)P
Knowledge8.5 (4.3)10.8 (4.2)0.001
SE82.1 (24.5)87.8 (24.4)0.141
Health motivation22.9 (3.3)24.5 (2.7)0.001

Overall engagement in HBBs did not differ based on mean age, duration of ADT treatment, previous known OP diagnosis, receiving OP medication, fragility fracture, BMI classification, or having received a DXA in the past 2 years (data not shown).

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Patients and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Conflict of Interest
  9. References

To our knowledge, this is the first study to describe and explore the relationship between OP knowledge, SE, health beliefs and engagement in HBBs in patients with prostate cancer receiving ADT. We found that despite the increased risk of bone loss in this population, overall OP knowledge, feelings of susceptibility toward bone loss, and engagement in essential preventative behaviours were relatively low and similar to a population of healthy adult men [47, 49].

As found in other studies [9, 13, 37-39], even in an urban comprehensive academic cancer centre, most patients (62%) had not received a DXA scan in the previous 2 years from either their prostate cancer specialist or primary care physician. Screening is important not only because it helps identify those who are at increased risk, but also, based on the present results which showed higher OP knowledge in those recently screened, it could lead to either patients being pro-active in seeking further knowledge or present an entry point for discussion and education from a healthcare provider. In patients identified as having OP or receiving pharmacologic therapies, proper relay of the diagnosis could lead to increased feelings of susceptibility that could empower patients to seek information about OP.

For engagement in HBBs, encouragingly the large majority of patients were avoiding smoking and excess alcohol intake. In addition, almost three-quarters were getting at least 1200 mg of calcium. However, it is important to note that 37% of the patients were getting >2000 mg of calcium either by diet and/or supplementation, which may place them at risk for vascular calcification and cardiovascular events [50, 51]. In contrast, we found that only a minority of patients were achieving the recommendations for vitamin D (42%). It may be that the poor DXA screening rates as well as poor uptake of calcium and vitamin D recommendations are, in part, due to physician uncertainty about current guidelines and practices. Therefore, the information is not properly disseminated to the patient. Nevertheless, the present results suggest the need for active knowledge translation processes to encourage the uptake of OP guidelines in healthcare providers treating this population. The Canadian Quality Circle project has shown that implementation of a multifaceted educational intervention targeted to healthcare providers increased physicians' awareness of OP risk factors and appropriate BMD testing [52], as well as use of the appropriate OP medication [53]. If such a project expanded to incorporate a component about appropriate use of calcium and vitamin D, this may lead to increased knowledge of guidelines by healthcare providers and therefore increased dissemination and uptake of guidelines by patients. Within these interventions, it will also be important to pay attention to factors such as older age, rural setting, and not having a primary care physician, which may put patients at risk of not receiving a screening DXA [36]. Further, simple patient self-assessment tools to calculate total calcium intake through diet are available and could also be helpful [54].

For exercise, engagement in recommended levels of moderate aerobic exercise (>150 min/week) was also quite low in this population (31%). We found those that were not meeting this recommendation had lower knowledge about OP and lower health motivation. As more research is done to investigate the optimal type of exercise for prevention/management of OP, brief sustainable interventions that are based on behaviour change theory and focus on increasing intrinstic motivation should be developed and implemented in this high-risk group.

Overall, patients with high OP knowledge were more likely to be taking calcium and vitamin D supplements. In addition, patients who were engaging in more total HBBs (four or five in total) had higher OP knowledge, SE and health motivation. This lends support to the applicability of the Health Belief Model and its use as a theory for the development of interventions in this population. In other groups at risk for OP, knowledge-based interventional studies have been shown to increase patients' knowledge about OP without changing behaviour [55-59], whereas interventions which have offered multiple educational sessions or targeted feelings of susceptibility through provision of DXA results have shown increased feeling of susceptibility, increased OP knowledge, increased calcium intake, and increased uptake/adherence to OP medications [59-63]. These findings suggest that providing patient personalised DXA results or risk information as well as accurate, specific, and clear evidence-based patient education may be an effective strategy to influence the uptake of HBBs in this population [35].

Since the completion of the present study, a more recent guideline on OP in men has been published by the Endocrine Society [24]. This new guideline recommends similar frequency of DXA monitoring but has also added that DXA evaluation of patients on ADT therapy should include screening at the forearm (33% radius) as bone loss occurs more rapidly in this site in this population [24]. Unfortunately, this guideline was published after the study was completed, and forearm BMD testing is not yet covered by the government health insurance plan in Ontario unless hip or lumbar spine cannot be done. For the five preventative behaviours or HBBs discussed, recommendations around smoking cessation and limiting alcohol consumption are unchanged and those surrounding calcium and vitamin D had only very minor modifications. We used 800 IU as the threshold for vitamin D, which is supported by the Endocrine Society Guidelines [64]. A more concrete recommendation for exercise is provided in the new guideline, which recommends weight-bearing activities for 30–40 min/session, three to four sessions per week for men at risk of OP [24]. This new guideline will be useful to use as a standard to compare against in future studies.

The limitations of the present study include a modest completion rate (53%) and that this study was undertaken in a single comprehensive academic, downtown setting and with a group of highly educated patients. These factors could have resulted in an under or over estimation of our outcomes. For example, it may be that those patients who responded and completed the study measures are more oriented to bone health and as a result knowledgeable about OP resulting in an overestimation of our outcomes.

In summary, the present results suggest that most patients who are receiving ADT are not receiving appropriate DXA screening, lack basic information about bone health, and are not engaging in the appropriate HBBs. Further, the present findings provide support for the application of the Health Belief Model in this population: they support the need for interventions that increase feelings of susceptibility toward bone loss, provide accurate and clear information to increase knowledge of HBBs, and promote feelings of SE to increase effective engagement in HBBs. This, in turn, has the potential to prevent and manage bone loss, falls, and fractures in this population.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Introduction
  4. Patients and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Conflict of Interest
  9. References

We would like to thank the following individuals for their support and assistance throughout this study: Mihaela Dirlea, Alison Ross, and Mike Wang.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Patients and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Conflict of Interest
  9. References