Worry about prostate cancer and risk perception among middle-aged men: results from the PROBASE trial

Prostate cancer (PCa) is the second most common cancer in men worldwide (Bray et al., 2018) and most often diagnosed following an elevated prostate-specific antigen (PSA) level (Cooperberg et al., 2005). However, there is uncertainty about the benefits of PCa screening due to an elevated risk of overdiagnosis (Brawley, 2012). Patients and their health care providers must weigh benefits, uncertainties, and risks of PCa screening resulting in a complex decision-making. Additionally, conflicting recommendations across various health authorities (Grossman et al., 2018; Mottet et al., 2017) increase this complexity and men with a family history of PCa must be aware of their elevated risk in their decision-making process. For instance, risk perceptions play an important role in many theories on health behavior including the Protection Motivation Theory (Rogers, 1975) and the Health Belief Model (Rosenstock et al., 1988) where higher perceived risk leads to more preventive health behavior.

Personal risk estimates vary significantly depending on whether individuals are rating their subjective risk alone (absolute risk perception) or relative to a standard (comparative risk perception), such as the risk of other individuals. Absolute and comparative risk perception of cancer appear to be relatively independent constructs, as suggested by their modest correlations. Moreover, absolute and comparative risk perceptions explained a different portion of the variance in cancer worry (Lipkus et al., 2000). For instance, comparative risk perception is related to affect, behavior, and health information processing even when controlling for absolute risk perceptions (Lipkus et al., 2005; Radcliffe & Klein, 2002). Among participants in a national survey reporting risk perceptions and cancer worry analyses showed that absolute and comparative risk perceptions were independent predictors of worry across all cancer sites (i.e., breast, colon, and prostate). However, absolute risk perceptions were more predictive than comparative risk perceptions of worry for women, but not for men (Zajac et al., 2006), emphasizing significant differences in these two constructs.

Similarly, other key factors in health behaviors and attitudes toward preventive health care are affective or experiential perceptions of vulnerability (e.g., cancer worry), even when controlling for cognitive perceptions (Jensen et al., 2010; Moser et al., 2007). The relationship between worry and behavior seems logical since affective appeals have been shown to motivate health behavior (Witte, 1998). Affective perceptions may either influence or be influenced by cognitive perceptions. If this is indeed the case, it has significant implications for the development of effective communication strategies aimed at promoting health-enhancing behaviors. For example, an association between perceived risk of PCa and worry about PCa has been described in a large sample of participants undergoing PCa screening (Cohen et al., 2003). Furthermore, in individuals with a positive family history of PCa higher perceived risk of PCa was associated with a higher likelihood of cancer-related worries affecting daily life (Bratt et al., 2000). While the evidence clearly indicates an association between risk perception of PCa and worry about the disease, the causal direction remains unclear. Some researchers conceptualized risk perception as antecedent of cancer worry (Schnur et al., 2006; Zajac et al., 2006), which has been shown in the context of other illnesses (DiLorenzo et al., 2006). However, the opposite causal direction has also been demonstrated by conceptual frameworks and empirical evidence, suggesting worry as a predictor of perceived risk for developing cancer (Hay et al., 2006; Slovic et al., 2004). The Tripartite Model of Risk Perception (TRIRISK) distinguishes among deliberative, experiential, and affective components of risk perception. In this framework cancer worry represents an aspect of risk perceptions, not a distinct model component (Ferrer et al., 2016). Nevertheless, both risk perception and cancer worry are well investigated as predictors of preventive health behavior such as PCa screening (Beebe-Dimmer et al., 2004; McDowell et al., 2009; Vadaparampil et al., 2004), and younger age, decreased subjective health, presence of physical symptoms, and a positive family history of cancer emerged most consistently as factors associated with higher cancer worry and risk perception (Hay et al., 2006; Hidalgo et al., 2015; Konings et al., 2017; Montgomery et al., 2003; Robb et al., 2004).

With regard to PCa, a British registry-based study examined worry about PCa in a sample of first-degree relatives of PCa patients. Higher health anxiety, higher subjective stress, and higher perceived risk reliably predicted higher worry about PCa (Sweetman et al., 2006), and the number of relatives deceased due to PCa is associated with worry about PCa among men in families with hereditary PCa (Bratt et al., 2000). With regard to risk perception, previous studies have found greater risk perceptions in men with a positive family history of PCa, whereas increasing age, which is a major risk factor for PCa, was associated with decreasing risk perceptions (McDowell et al., 2013; Schnur et al., 2006).

Taken together, despite the large number of studies investigating factors associated with preventive health behavior such as cancer worry and risk perceptions, available research concerning factors associated with cancer worry and risk perception, especially in PCa, is quite outdated and mainly limited to samples with a positive family history. Furthermore, recent research on this topic as well as studies investigating large community-based samples are lacking, while they are available for other cancers such as breast, colon and lung cancer (Hay et al., 2006; Lebrett et al., 2022; Zajac et al., 2006). Hence, the objective of this study was to investigate factors associated with worry about PCa and risk perception in a community-based sample of more than 30,000 45-year-old men who participated in a prospective risk-adapted PCa screening trial. Additionally, due to the large sample size and comprehensive data collection, it was possible to control for a broad set of sociodemographic, lifestyle, clinical, and psychological factors as well as family history.

The aim of the current study was to assess prevalence and factors associated with worry about PCa and risk perception in a large, community-based sample of middle-aged men Multivariable logistic regression analyses revealed that important factors of worry about PCa were LUTS, a positive family history of PCa, and high perceived severity about developing PCa. Important factors of absolute risk perception were also a positive family history of PCa and LUTS, and additionally previous PSA testing. Important factors of comparative risk perception were again a positive family history of PCa and LUTS, but also a positive history of own urological cancers and previous PSA testing.

In general, worry about PCa and risk perception were lower among the middle-aged men of this study compared to available research in population-based studies (Shavers et al., 2009; Wallner et al., 2008). As such, prevalence of worry about PCa was slightly lower in this study compared to a randomly selected cohort of American men of the Olmsted County Study (7.3% vs. 10.3%) (Wallner et al., 2008). However, the American sample had a median age of 51.9 years, which might be one reason for the higher prevalence, since the risk of PCa increases with higher age. Only 3.7% of men surveyed in the PROBASE trial perceived their future risk of developing PCa as somewhat or very high compared to 14.5% in a nationally representative sample of American men of the Health Information National Trends Survey (Shavers et al., 2009). Regarding comparative risk perception, 9.9% of men surveyed in the PROBASE trial perceived their comparative risk as somewhat or much higher as the average men of their age. Similarly, the Health Information National Trends Survey reported higher numbers of comparative risk perception (12.9%) (Shavers et al., 2009). While both aforementioned studies, i.e., the Olmsted County Study and the Health Information National Trends Survey (Shavers et al., 2009; Wallner et al., 2008), utilized large population-based cohorts either through a telephone or an in-home interview, the sample of the PROBASE trial consisted of men taking part in a randomized PCa screening trial. There is ample evidence that risk perception and health behavior are strongly associated (Beebe-Dimmer et al., 2004; Brewer et al., 2004; McDowell et al., 2009; Vadaparampil et al., 2004). According to the Risk Reappraisal Hypothesis (Brewer et al., 2004) performance of a health protective behavior, i.e. PCa screening, results in a lowering of risk perceptions. Another explanation for lower risk perceptions among participants of a PCa screening trial relates to research on insurance and risk perceptions. In a comparative study, men who were insured (e.g., health, travel, car) felt they were less likely to suffer problems in the future compared to their counterparts (Tykocinski, 2008). Taken together, taking part in a PCa screening trial might equally lead to lower risk perceptions and cancer worry resulting in a healthy screenee bias.

The main results of the current study showed that a positive family history of PCa was an important factor of worry about PCa and was associated with a 15- and 10-fold increase in the odds of absolute and comparative risk perception, respectively. These results are in line with previous research (Bratt et al., 2000; McDowell et al., 2013; Miller et al., 2001; Sweetman et al., 2006). Interestingly, a positive family history of PCa as well as of other cancers showed significant results for worry about PCa and absolute risk perception compared to a personal history of either urologic cancers or non-urologic cancers, which is consistent with results found in previous studies in colon cancer research (Hay et al., 2006). Witnessing a close relative going through treatment for cancer might lead to feeling vulnerable through a process of vicarious learning (Schwarzer, 1994). Another explanation is that people may believe they are genetically predisposed if a close relative has had PCa. Since a positive family history of PCa, in addition to age and African ancestry, is an objective risk factor for the disease, these results are hardly surprising. Rather, the absolute number of men experiencing worry about PCa (7.3%) or perceiving their absolute risk as somewhat high to very high (3.7%) or perceiving their comparative risk as somewhat higher to much higher (9.9%) seems low compared to the number of men with a positive family history (18.8%) in this sample. Such inconsistencies between the actual and perceived risk have been likewise reported relating to African Americans (Shavers et al., 2009) as well as older men with a PCa family history (McDowell et al., 2013) who are both often not aware of their increased risk of developing PCa. Therefore, there is a crucial need in risk communication to address this underestimation of risk.

LUTS was an important factor in association with worry about PCa and both absolute and comparative risk perception. Although several studies have shown that men with LUTS are at no greater risk of PCa than asymptomatic men of the same age (Young et al., 2000), many men express fears about PCa in relation to their LUTS (Brown et al., 2003). Interestingly, in a population-based sample of US American men, bowel symptoms were also strongly associated with higher perceived risk of colorectal cancer (Robb et al., 2004). These findings are of some concern, given the fact that PCa as well as colorectal cancer are often asymptomatic until an advanced stage and early detection plays an important role in the curative treatment of these cancers. These misperceptions surrounding the effect of LUTS on perceived risk need to be addressed in risk communication.

Previous PSA testing before the study enrollment at the age of 45 was associated with both higher absolute and comparative risk perception, whereas previous digital rectal examination showed no association. Both results are in line with previous results in African American men (Bloom et al., 2006). Apparently, the higher risk perception of developing PCa is a significant reason that affected men undergo PSA testing, even before the age of 45, which is not recommended for men without elevated risk by any guideline. Interestingly, an abnormal fear of cancer seems not to be the reason, since worry about PCa was not associated with previous PSA testing.

Of the psychological factors, high perceived severity of developing PCa was associated with a 2-fold increase in the odds of being worried about PCa. To our knowledge, this is the first time this factor is being investigated as a predictor of worry about PCa. However, it seems plausible that men fear a potential disease which is described by themselves as one of the worst things that could happen. However, risk perceptions were not associated with high perceived severity showing that these men do not have inadequately high levels of risk perception, since they are not at increased risk in general. The fact that perceived severity was associated with worry but not with risk perceptions is supported by previous findings in the literature. For instance, in participants receiving information about a genetic test of lifetime risks for various diseases (e.g., diabetes, heart disease, colon cancer) worry was correlated with perceived severity and likelihood of these diseases (Cameron et al., 2009). Analysis of further psychological factors revealed that higher perceived ambiguity about PCa prevention recommendations was associated with higher worry about PCa, but showed no association with absolute and comparative risk perceptions. Ambiguity, defined as uncertainty about the reliability and credibility of information about risks and potential decision outcomes, has been shown to trigger specific psychological and behavioral effects. Notably, it prompts people to view risks and possible outcomes more pessimistically and to steer away from decision making (Ellsberg, 1961). For instance, perceived ambiguity about other cancer types such as lung, colon, and skin cancer is inversely associated with perceptions of the preventability and with cancer-specific risk-modifying behaviors including cancer screening (e.g., smoking abstinence, sigmoidoscopy–colonoscopy testing, sunscreen use). However, for lung cancer only, perceived ambiguity has been shown to be associated with absolute risk perception and cancer worry. Colon and skin cancer showed no relationship between perceived ambiguity and risk perceptions and cancer worry, respectively (Han et al., 2007). These cancer-specific differences underline the importance of understanding how ambiguity perceptions may influence people’s behaviors and cognitions such as perceptions regarding the risk and controllability of a disease, and the risks of both choosing or avoiding a disease-protective intervention (Han et al., 2007; Leventhal et al., 2016). In PCa, it seems that the large number of existing prevention recommendations lead to increased cancer worry, while risk perceptions may not influenced. However, higher perceived preventability was associated with higher absolute risk perceptions, but not with cancer worry. This is in line with previous results in first-degree-relatives of colorectal cancer patients showing that a higher perceived risk was associated with believing that colorectal cancer cannot be prevented. Since most of them overestimated their actual cancer risk, perceived risk changed after counselling (Codori et al., 2005). In this context, adequate counselling and risk communication with patients is crucial to avoid misperceptions regarding the true risk.

From the sociodemographic variables, a higher level of education was associated with less worry about PCa. This result seems somewhat plausible since the prevalence of PCa in 45-year-old men is in general low and educated people might be aware of this. Further, previous research supports this inverse association in more than 2,000 men and women ≥ 50 years old with no history of cancers regarding breast, prostate, and colon cancer worry (McQueen et al., 2008). In the current study, absolute risk perception was not related to level of education, which is in line with other population-based studies (McQueen et al., 2008; Shavers et al., 2009). However, the fact that higher comparative risk perception was associated with a high level of education among participants of the current study remains unclear. Compared to the literature, divergent results can be found. Conversely, one study found that men with a low level of education had even higher comparative risk perceptions (Shavers et al., 2009). Previous research on comparative risk perception showed that it is more likely to be associated with worry and knowledge than absolute risk perception (Dillard et al., 2011; McCaul et al., 2003). However, since different assessments of the factor educational level were used, comparisons are difficult and valid conclusions can hardly be drawn. The other sociodemographic factors such as partnership and subjective economic situation showed likewise to the literature no significant results (Beebe-Dimmer et al., 2004; McQueen et al., 2008; Shavers et al., 2009).

The assessment of lifestyle factors showed that all risk factors (i.e., higher body mass index, higher waist circumference, high alcohol consumption, active smoking, and no physical activity) were associated with higher comparative risk perception. Interestingly, only higher waist circumference was associated with additionally both a higher absolute risk perception and worry about PCa, and active smoking was only associated with worry about PCa. This fact is somewhat disturbing, since all of these risk factors are related to a higher risk of PCa (Freedland & Aronson, 2004; Huncharek et al., 2010; Macke & Petrosyan, 2022; Shephard, 2017). Obviously, affected men are aware of their increased comparative risk, however, they do not perceive a higher absolute risk and also no or little worry about PCa, which highlights the need for more awareness in preventive measures.

To date, the current study is the largest community-based investigation on a broad set of sociodemographic, lifestyle, psychological, and clinical factors as well as family history in relation to worry about PCa and risk perceptions. Comparable data are only available for other cancers such as colon, breast or lung cancer (Hay et al., 2006; Lebrett et al., 2022; Zajac et al., 2006). The large, community-based sample provides a good generalizability and important insights into the predictors of health behavior of middle-aged men at the beginning of PCa screening. However, there are limitations to this study that need to be considered in interpreting the results. First, due to missing information in further variables assessed, 12,249 out of 33,476 men were not included in the regression analyses. However, the dropout analysis revealed only marginal differences (all < 8%) between the two groups. Notably, all lifestyle, clinical, and especially psychological factors as well as family history showed no to only marginal differences (< 3.5%) between the two groups. Second, the cross-sectional design does not allow to draw causal conclusions. Third, since the PROBASE trial is a PCa screening trial health-concerned men might be overrepresented, as well as men who might be suffering from prostate symptoms resulting in a recruitment bias. Further, since recruitment criteria of the PROBASE trial included 45-year-old men results of the current study are limited to middle-aged men and cannot be generalized to men of other ages or women; however, this rigorous participant selection allows excellent comparability and precise factor evaluation. Fourth, due to the low number of study participants with an even lower response rate, we had to exclude men with African and Asian ancestry, which is a notable limitation, since men with African ancestry are at increased risk of PCa. Therefore, our results are limited to White men.

This study is the first to explore important factors associated with worry about PCa and risk perceptions in a large community-based sample of middle-aged men using a multivariable approach to investigate a broad range of demographic, lifestyle, clinical, and psychological factors as well as family history. A positive family history of PCa, which is a well-known risk factor for PCa, strongly influenced risk perception. Since the absolute number of men affected by a positive family history was in total much higher than the absolute number of men with worry about PCa or higher risk perceptions, there is a crucial need to improve risk communication, addressing this underestimation of risk. Furthermore, although PCa is often asymptomatic until an advanced stage and men with LUTS are at no greater risk of PCa than asymptomatic men of the same age, LUTS was likewise an important factor associated with worry about PCa and risk perception. These misperceptions need to be addressed in risk communication with patients.