Abstract
This study investigated how time from breast biopsy recommendation to biopsy procedure affected pre-biopsy anxiety (N = 140 women), and whether the relationship between wait time and anxiety was affected by psychosocial factors (chronic life stress, traumatic events, social support). Analyses showed a significant interaction between wait time and chronic life stress. Increased time from biopsy recommendation was associated with greater anxiety in women with low levels of life stress. Women with high levels of life stress experienced increased anxiety regardless of wait time. These results suggest that women may benefit from shorter wait times and receiving strategies for managing anxiety.
Introduction
Percutaneous imaging-guided cyst aspirations and core needle biopsies (CNB) are outpatient procedures performed by radiologists under ultrasound or stereotactic guidance to diagnose abnormalities identified during breast imaging. CNB has become the standard of care for diagnosing imaging-detected breast lesions and has many advantages over diagnostic surgical biopsy (e.g. minimally invasive, decreased cost) (Gutwein et al., 2011). The United States has witnessed an increase in CNB procedures over the last decade—approximately 70 percent of the 1.6 million annual breast biopsies are performed by CNB (Gutwein et al., 2011).
CNB is a stressful experience for many women, accompanied by insomnia, difficulty concentrating, and high levels of anxiety before and during CNB (Landercasper et al., 2010; Liao et al., 2008; Maxwell et al., 2000; Thorne et al., 1999). While 70–80 percent of diagnostic breast biopsies yield benign results, high levels of anxiety can persist for years in these patients (Andrykowski et al., 2002; Brett and Austoker, 2001; Deane and Degner, 1998; Liao et al., 2008; Lindfors et al., 2001; Maxwell et al., 2000). Elevated anxiety can interfere with patients’ adherence to follow-up screening recommendations (Andrykowski et al., 2001; Chang et al., 2005; Pisano et al., 1998; Sergentanis et al., 2009; Zografos et al., 2010), and negatively affect coping and quality of life (Roest et al., 2010; Stein et al., 2005). Patient anxiety can also impact efficiency of patient flow through radiology clinics (Flory and Lang, 2011) and has been cited as a potential harm of mammography screening, contributing to the US Preventive Services Task Force (2009) recommendation to reduce screening.
During the sometimes prolonged, multi-step process between receiving abnormal screening mammography results and receiving biopsy results, patients likely experience anxiety for a variety of reasons. Fear of pain during biopsy and uncertainty about biopsy results contribute to patient anxiety (Flory and Lang, 2011; Lang et al., 2009), and delays in performing the procedure may further exacerbate women’s emotional distress before biopsy (Lebel et al., 2003; Rosenberg et al., 2011). Breast biopsy facilities vary considerably in number of days that elapse between biopsy recommendation and definitive diagnosis after CNB (Rosenberg et al., 2011), but few studies have investigated the impact of biopsy waiting periods on anxiety. One retrospective study demonstrated that patients who waited 4–6 weeks for diagnostic surgical biopsies reported high levels of anxiety during the waiting period (Poole, 1997). In another study, women waiting an average of 40 days for stereotactic biopsies reported high levels of anxiety from the time of biopsy recommendation to 2 days before the procedure (Lebel et al., 2003). Most patients in that small sample (N = 25) stated that wait times were too long and described feeling increasingly anxious as the biopsy date approached (Lebel et al., 2003).
Psychosocial factors are also associated with women’s emotional distress before and during the biopsy (Drageset et al., 2012; Montgomery et al., 2003; Northouse et al., 1995; Poole, 1997). Research exploring the role of social support during breast biopsy found that patients perceiving higher levels of social support around biopsy procedures experience lower levels of emotional distress (Harding, 2014; Poole, 1997). Providing emotional support to patients during breast cancer screening has also resulted in decreased anxiety (Liao et al., 2010). Related studies exploring the negative impact of psychosocial variables on psychological functioning before biopsy found that concurrent stressors at the time of biopsy can lead to increased distress (Northouse et al., 1995; Poole, 1997). Research is needed to further explore the impact of psychosocial variables before and during breast biopsy.
This study aimed to (1) examine the relationship between anxiety and waiting time from biopsy recommendation to performance of the procedure, (2) investigate relationships between patient anxiety and psychosocial factors (i.e. social support, chronic life stress, traumatic life events), and (3) determine whether the relationship between waiting time and patient anxiety is affected by psychosocial factors.
Materials and methods
Between August 2010 and February 2011, 207 women undergoing CNB or diagnostic cyst aspirations were invited on the day of procedure to participate in this institutional review board–approved, Health Insurance Portability and Accountability Act–compliant study. Data presented in this article were collected as part of a larger 3-year longitudinal study of adherence to recommended care.
Women met the following inclusion criteria: (1) ⩾21 years old, (2) presented for percutaneous breast imaging-guided diagnostic procedure, (3) able to speak and read English, and (4) able to provide informed consent. Women having undergone CNB in the previous 6 months were excluded. Overall, 152 women provided informed consent (participation rate: 73%) and received a parking pass for participating. In all, 12 participants were excluded from the data analyses: procedures were canceled (n = 4), cognitive impairment interfered with questionnaire completion (n = 1), and incomplete study measures (n = 7). A total of 140 women comprise the study sample.
Procedures
Immediately before biopsy, in a private waiting room adjacent to the biopsy suite, all participants completed a self-report measure of state anxiety. A research team member was present to administer questionnaires; however, biopsy staff was not present, minimizing any influence on patient reports. Patients also completed self-report measures of chronic life stressors, exposure to traumatic life events, perceived social support, and socio-demographic (e.g. education, race) and medical characteristics (e.g. family breast cancer history) during the appointment. The date of biopsy recommendation, date of diagnostic procedure, whether CNB was recommended by a radiologist in our clinic versus an outside physician/provider, type of biopsy procedure, and histological outcome were recorded.
Measures
Anxiety
The State Anxiety Scale of the State-Trait Anxiety Inventory (STAI) was used to measure pre-biopsy anxiety (Spielberger et al., 1970). This 20-item scale measures feelings of anxiety that fluctuate in time in reaction to threatening stimuli (Novy et al., 1993). The 4-point response format assesses intensity of feelings; choices range from 1 (not at all) to 4 (very much). Items are summed, creating a total score (possible range: 20–80); higher scores indicated higher anxiety (Spielberger et al., 1970). Cronbach’s alpha in this sample was .91.
Chronic life stress
Chronic life stressors were measured using a 51-item questionnaire covering nine domains: general or ambient problems, financial issues, work, marriage and relationship issues, parental concerns, family, social life, residence, and health issues (e.g. “you want to change jobs or careers but don’t feel you can” and “your partner is not committed enough to your relationship”) (Turner et al., 1995). Responses include “not true” (0), “somewhat true” (1), and “very true” (2). Responses are summed to create a total score (potential range: 0–102) with higher scores indicating greater chronic life stress (Cronbach’s alpha = .91).
Traumatic life events
An 11-item traumatic life event scale measured exposure to traumatic life events (Turner et al., 1995). Items ask about major traumas occurring during the patient’s lifetime (e.g. “have you ever been in a major fire, flood, earthquake, or other natural disaster?”). Responses are “yes” (1) or “no” (0). Items are summed to create a total score (possible range: 0–11) with higher scores indicating exposure to more traumatic life events (Cronbach’s alpha = .66).
Perceived social support
The 19-item Medical Outcomes Study (MOS) Social Support Survey (Sherbourne and Stewart, 1991) measured social support. Participants rate items using a 5-point response scale ranging from 1 (none of the time) to 5 (all of the time). A total average social support score is computed, and a linear transformation is conducted so the lowest possible score is 0 and the highest possible score is 100. Higher scores indicate more perceived availability of social support. Internal consistency was high (Cronbach’s alpha = .96).
Biopsy wait time
The dates of biopsy recommendation and procedure were recorded. Wait time was computed as the number of days elapsing between receipt of biopsy recommendation and biopsy procedure.
Demographic and medical information
Participants completed questionnaires assessing demographic (i.e. age, race, education, and marital status) and medical (i.e. cancer history, family history of breast cancer, history of breast biopsy and/or surgery, and comorbid illnesses) characteristics. Biopsy procedure type, histological outcome, and whether biopsy was recommended by a radiologist in our clinic versus outside physician/provider were recorded.
Statistical analysis
Bivariate analyses (Pearson or point-biserial correlations) examined associations among study variables and participant characteristics. Multiple linear regression analyses tested whether wait time was associated with anxiety and whether the relationship between wait time and anxiety differed across levels of chronic life stress, traumatic life events, and social support. Each regression model included control variables (i.e. demographic characteristics and biopsy-related factors associated with anxiety in bivariate analyses, p < .05), biopsy wait time, psychosocial factor of interest (i.e. chronic life stress, traumatic events, or social support), and biopsy wait time × psychosocial factor interaction term. Variables were mean-centered and simple slope analyses were conducted to facilitate interpretation of significant interaction terms (Aiken and West, 1991).
Results
Sample description
Table 1 displays participant characteristics and descriptive statistics. The majority (77.9%) of women reported at least one health problem; common problems included hypertension (32.1%), back problems (15.0%), arthritis (14.3%), and headaches (14.3%). Women also reported history of anxiety or depression (22%), personal history of cancer (26.4%), previous CNB (46.4%), and previous breast surgery (35.0%). In total, 21 percent of women had first-degree relatives with breast cancer.
Sample characteristics (N = 140).
SD: standard deviation; STAI: State-Trait Anxiety Inventory.
Total adds to more than 100 percent because some women had more than one type of biopsy procedure.
Most women (92.1%) received biopsy recommendations from radiologists in our clinic. On average, women waited 6.15 (standard deviation (SD) = 7.25) days between biopsy recommendation and procedure. Women underwent ultrasound-guided CNB (66%), ultrasound-guided diagnostic aspirations (10.7%), and stereotactic-guided CNB (30%); 17.1 percent underwent more than one procedure. CNB histology was benign in 67.9 percent of women, malignant in 24.3 percent, and atypical in 7.9 percent (later surgical excision of atypia yielded malignancy in three patients). Average anxiety was 44.46 (SD = 12.52, range: 20–70). STAI State Anxiety scores of 40 or greater indicate clinically significant anxiety in women of this age group (Spielberger, 1983).
Associations among anxiety, wait time, and participant characteristics
Compared to non-White participants, White participants reported greater anxiety (r = .21, p = .01). On average, anxiety scores were 5.76 (standard error (SE) = 2.32) points higher for White participants compared to non-White participants. Receiving a biopsy recommendation from radiologists in our clinic was associated with shorter wait times (r = .36, p < .001). Women receiving biopsy recommendations from outside providers waited an average of 9.60 (SE = 2.13) days longer than women receiving recommendations in our clinic. Other demographic and medical variables were not associated (p > .05) with anxiety or wait time.
In bivariate analyses, anxiety was not associated with wait time, chronic life stress, traumatic life events, or perceived social support (r = −.06 to .14, p > .10). Women with more chronic life stress had longer wait times for biopsy (r = .26, p < .001). To further examine this association, we tested relationships between wait time and nine domains of chronic life stress assessed in this study. Marriage and relationship issues (r = .28, p = .001), health issues (r = .27, p = .001), residence-related concerns (r = .25, p = .003), financial issues (r = .21, p = .01), and general or ambient problems (r = .17, p = .05) were significantly associated with longer wait times. Chronic life stress was also associated with having experienced more traumatic life events (r = .27, p = .001) and lower social support (r = −.25, p = .003).
Multiple regression analyses
Table 2 displays results of multiple linear regression analyses. Unstandardized regression coefficients and SEs are provided (Aiken and West, 1991). The model for chronic life stress accounted for significant variance in anxiety (total R2 = .10, F(5, 134) = 3.00, p = .01). The interaction between wait time and chronic life stress was significant (B = −0.03, SE = 0.01, t = −2.12, p = .04) indicating that the relationship between wait time and anxiety differed across level of chronic life stress. Figure 1 displays relationships between wait time and anxiety across low (one SD below the mean), average (at the mean), and high (one SD above the mean) levels of chronic life stress.
Multiple regression analyses for anxiety (N = 140).
SE: standard error.
All variables included in interaction terms were mean-centered.
Race: 0 = Black/Asian/American Indian, 1 = White.
Recommendation received from outside physician/provider: 0 = biopsy recommendation received from radiologist in our clinic, 1 = biopsy recommendation received from a physician or provider at an outside facility or clinic.

Relationship between wait time and anxiety across levels of chronic life stress.
Among women with low levels of chronic life stress, increasing wait time was associated with increasing anxiety (slope: B = 0.65, SE = 0.24, t = 2.69, p = .008). There was no relationship between wait time and anxiety among women with high levels of chronic life stress (slope: B = −0.01, SE = 0.12, t = −0.09, p = .93). Examination of the region of significance for slopes indicated that increasing wait time was associated with greater anxiety for women with chronic life stress scores of 13 or lower (i.e. 2.81 points below the mean of chronic life stress).
The model for traumatic life events also accounted for significant variance in anxiety (total R2 = .08, F(5, 131) = 2.35, p = .05). There was a trend for the interaction between wait time and traumatic life events (B = −0.18, SE = 0.10, t = −1.84, p = .07); the pattern was similar to those for the interaction between wait time and chronic life stress. Among women reporting low exposure to traumatic life events, increasing wait time was associated with increasing anxiety (slope: B = 0.53, SE = 0.24, t = 2.15, p = .03). There was no relationship between wait time and anxiety among women reporting average or high levels of traumatic life events (p > .29). Examination of the region of significance for slopes indicated that a significant (p < .05) relationship between wait time and anxiety was present for women with traumatic life events score of 1.44 or lower (i.e. 1.12 points below the mean of traumatic life events).
The model for perceived social support failed to account for significant variance in anxiety (total R2 = .06, F(5, 131) = 1.78, p = .12). The effects for wait time, perceived social support, and the interaction between wait time and social support were not significant (p > .10).
Discussion
Given the clinically significant levels of anxiety that women experience prior to biopsy, (Bugbee et al., 2005; Poole, 1997), a better understanding of factors that contribute to anxiety and strategies to help women better manage anxiety is needed. This study examined relationships between anxiety and waiting times from breast biopsy recommendation to procedure, and whether psychosocial factors impact these relationships. We found clinically significant levels of anxiety prior to CNB, regardless of wait time, and greater anxiety was found among White women than non-White women. We also found an interaction between biopsy wait time and chronic life stress. Patients with low-to-average chronic life stress had higher anxiety as waiting time increased, while patients with high levels of chronic life stress had high levels of anxiety regardless of wait time. A similar trend was found for traumatic life events. Perceived social support was not related to pre-biopsy anxiety.
In the subgroup of women experiencing lower levels of chronic life stress who showed increased anxiety as wait times increased, we speculate that lack of exposure to stressors prior to the biopsy recommendation may account for lower anxiety soon after the recommendation was delivered. However, anxiety in this subgroup may have been higher for women experiencing longer waiting periods because of increasing uncertainty about biopsy results. Uncertainty about biopsy results is a known stressor (Lang et al., 2009); patients awaiting results after CNB have been shown to experience increasing physiologic distress over time, equivalent to distress in women who have received a malignant result (Lang et al., 2009). Similar distress patterns could occur in women as wait time increases prior to biopsy, possibly because greater delays allow patients more time to consider the meaning and impact of a cancer diagnosis. Uncertainty about the CNB procedure itself could also affect anxiety over time. With increasing delays, patients could be exposed to more negative or conflicting accounts about actual biopsy experiences (e.g. pain during the procedure) from others having undergone CNB. Further investigation is warranted to explore these issues.
Patients with high levels of chronic life stress reported high levels of anxiety, regardless of wait time; no increases in anxiety were noted among women in this group who waited longer for their procedure. It is possible that women who experience high levels of chronic life stress are more likely to experience clinically significant levels of anxiety in the context of an acute stressor such as a recommendation for biopsy. When faced with an acute stressor, chronically stressed individuals have been found to experience significantly greater psychological distress and delayed recovery than individuals with lower levels of chronic stress (Pike et al., 1997). Those with a history of exposure to traumatic life events are also more likely to experience significant psychological distress in response to new life stressors (Brewin et al., 2000; Ozer et al., 2003). In our study, similar trends were found among women with differing levels of traumatic life events. Women with low exposure to traumatic life events experienced increasing anxiety as wait times increased; however, women with exposure to high levels of traumatic life events showed no change in anxiety as wait times increased. It is also possible that our measure of anxiety was not sensitive enough to capture any increase in anxiety beyond the already elevated baseline measures in these patients.
The underlying factors that contributed to the interaction between wait times and chronic life stress could not be ascertained in this study. Delays in undergoing biopsy could have resulted from external factors (e.g. women’s inability to take time off work, scheduling delays related to the biopsy clinic), or could have been caused by patient anxiety about the procedure or outcome. We suspect that biopsy facility-related factors such as limited biopsy appointments caused delays for many women, given our anecdotal observations that many patients in our clinic request same-day biopsy appointments, yet the average wait time in our study was 6 days. Likewise, a previous study of women who experienced increasing anxiety as wait times increased also suggests that women prefer a shorter delay, and women in that study reported that wait times were too long (Lebel et al., 2003). Scheduling delays could also occur due to patient-related factors such as financial barriers, health issues, or family or work responsibilities. These domains of chronic life stress were found to be associated with biopsy delays in our study; therefore, it is likely that women with higher levels of chronic life stress were impacted by these types of delays. Patient anxiety could also cause delays in scheduling and might be a greater factor for women with greater chronic life stress. Further investigation is necessary to better understand the relationship between delays in undergoing breast biopsy and chronic life stress.
Psychosocial services are needed for patients prior to biopsy regardless of wait times. Our findings suggest that psychosocial interventions to manage the relationship, health, and financial domains of chronic life stress might be especially helpful. Future research should explore whether brief behavioral interventions delivered in mammography clinics could effectively provide patients with problem solving and communication tools, as well as health education and connection with financial resources, to better manage chronic life stressors during this time. Referrals to financial counselors, social workers, patient navigators, or psychologists could also be considered.
Surprisingly, perceived social support was not related to pre-biopsy anxiety. Study participants reported high levels of social support overall, which may have limited our ability to examine the relationship between social support and anxiety among those who experience a lack of support. Given that marital and relationship domains of chronic life stress were associated with longer biopsy wait times, these social factors may influence women’s experiences as they undergo CNB. Future studies are needed to explore how relationship stress and other social factors (e.g. feelings of social isolation) might impact the biopsy experience.
In contrast to the larger breast cancer screening literature, higher levels of anxiety were found among White women in our study than among non-White women. African American women in this setting have often reported greater distress than White women, with past studies identifying heightened breast cancer-related fear and negative beliefs such as fatalism among some African American women (Ashing-Giwa and Ganz, 1997; Phillips and Smith, 2001; Powe and Finnie, 2003). Several studies have investigated strategies for providing information and support to African American women undergoing breast biopsy (Bradley et al., 2006); however, our findings suggest White women also might need emotional and psychological support during CNB. Our findings could represent an artifact related to which women either present more frequently for screening or have resources for treatment at major medical centers; further study is needed to determine which factors influence anxiety at the time of CNB.
Findings from our study also underscore the need for shorter wait times before biopsy. Time from biopsy recommendation to procedure varies among breast imaging facilities (Rosenberg et al., 2011), and many facilities may be unable to shorten wait times (e.g. limited clinic space, limited number of radiologists). Rosenberg et al. (2011) demonstrated that timely biopsies were associated with larger facility procedure volumes rather than specific facility types or other facility-related characteristics. While small volume practices with few radiologists might have difficulty performing timely biopsies, radiology teams in larger medical centers could likely facilitate quicker biopsies for women. Some radiology groups have begun offering same-day biopsies to patients receiving abnormal mammography results; subsequent research shows higher patient satisfaction among women undergoing biopsy on the day of recommendation (Landercasper et al., 2010). Further research is needed to explore the effects of same-day biopsies for managing patient anxiety.
Because same-day biopsies may be unattainable in many settings, it may be especially important to have psychosocial support resources available to women awaiting biopsy. Past studies have demonstrated that psychosocial interventions (e.g. relaxation-based protocols, hypnosis) can reduce anxiety during biopsy and other breast cancer-related procedures (Bugbee et al., 2005; Lang et al., 2006; Montgomery et al., 2007). Future research could explore whether delivery of brief psychosocial interventions in mammography clinics could teach anxiety management strategies to patients awaiting their procedure (e.g. relaxation, mindfulness exercises).
This study had several limitations. First, the study included a relatively small sample and recruited women from one academic medical center clinic. Given the clinic setting, wait times between biopsy recommendation and procedure were typically shorter than wait times that might occur in smaller community-based clinics. Future studies are needed to determine whether results of this study generalize across different clinic settings. Second, patients obtaining treatment in academic medical centers may have more resources (e.g. education, financial resources) than patients treated in other clinic settings, suggesting the need for more research in diverse clinical settings. Third, due to the lack of longitudinal data, study results can only be interpreted in terms of associations, making it difficult to determine the direction of relationships between variables. For example, chronic life stress could impact wait time or longer wait times could influence women’s perceptions of life stress. Prospective studies could investigate whether longer wait times were due to patient anxiety and fear versus external factors. Finally, for some women, high levels of anxiety could have influenced their decision to decline participation in the study, which could impact study findings.
Conclusion
This study found that patients with low-to-average chronic life stress demonstrated higher anxiety as waiting time to CNB increased, while patients with high levels of chronic life stress reported high levels of anxiety regardless of wait time. These findings suggest that shortening biopsy wait time may reduce anxiety for women with low-to-average chronic life stress, but additional strategies are needed for women with high levels of life stress.
Footnotes
Declaration of conflicting interests
The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding
The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This research was supported in part by a pilot grant from The John Templeton Foundation (grant 12111) through the Center for Spirituality, Theology and Health at the Duke University Medical Center (Durham, North Carolina).
