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Keywords:

  • distress;
  • depression;
  • screening;
  • satisfaction;
  • implementation;
  • cancer;
  • diagnosis

Abstract

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgements
  8. FUNDING SOURCES
  9. REFERENCES

BACKGROUND:

There is considerable uncertainty regarding the acceptability of routine distress screening.

METHODS:

In an unfunded implementation study, the authors asked 50 clinicians (chemotherapy nurses and treatment radiographers/radiation technologists) to implement a screening program for distress as part of routine care and to record their feedback after each clinical encounter. In total, 379 patients were screened using a simple paper-and-pencil versions of distress thermometer and the emotion thermometer (ET).

RESULTS:

Across all screening applications, clinicians believed that screening was useful during 43% of assessments and was not useful during 35.9% of assessments, and they were unsure or neutral in 21.1% of assessments. The application of the screening program assisted staff in changing their clinical opinion after 41.9% of assessments, and clinicians believed that the screening program helped with communication in >50% of assessments. However, 37.5% believed that screening was impractical for routine use, and more chemotherapy nurses than radiographers rated the screening program as “not useful.” On multivariate analysis, 3 variables were associated with high staff satisfaction with screening, namely, receipt of prior training, talking with the patient about psychosocial issues, and improved detection of psychological problems. A favorable perception of screening also was linked to a change in clinical opinion.

CONCLUSIONS:

Opinions of cancer clinicians regarding routine distress screening were mixed: Approximately 33% considered screening not useful/impractical, whereas >50%n believed promoted good communication and/or helped with recognition. Clinicians who were more positive about screening gained greater benefits from screening in terms of communication and recognition. Cancer 2012. © 2012 American Cancer Society.


INTRODUCTION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgements
  8. FUNDING SOURCES
  9. REFERENCES

Distress is a common complication of cancer, occurring in approximately 4 in 10 cancer patients who undergo cross-sectional assessment.1-3 Depression with or without adjustment disorder occurs in approximately 3 of 10 patients.4 Distress, depression, and anxiety are important not just for mental health professionals but also for cancer clinicians. The presence of distress is linked with reduced health-related quality of life,5 poor satisfaction with medical care,6 and possibly reduced survival.7 Although distress is poorly operationalized, a working definition has been offered by the National Comprehensive Cancer Network (NCCN).8 Distress should be considered a treatable complication of cancer that can present at any stage in the cancer pathway.9 Previously, several groups reported that the ability of cancer clinicians to detect patient-rated distress is modest to low when unaided.9-13 Indeed, only a minority of clinicians ask about emotional problems systematically, many preferring to rely on patients mentioning a problem first.14 Less than 15% use a screening instrument, and most prefer their own clinical judgement.14, 15 Observed interview studies confirm that emotional issues are discussed in approximately 15% to 40% of consultations.16-18 It is noteworthy that patients, not clinicians, initiate these discussions in most instances.18, 19 The main barriers to a thorough psychosocial assessment appear to be perceived lack of time, lack of training and low personal skills or confidence about diagnosis and availability of mental health services,14, 20 and, in some cases, over confidence about personal skills.21, 22

Given this context, several national guidelines recommend screening to enhance the ability of clinicians to detect emotional problems.23-25 Provisional evidence appears to provide some support for screening programmes regarding added value to clinicians.26-28 Yet, in clinical practice, the uptake of screening often is suboptimal, and this can be perceived as a marker for difficulties patients and clinicians have with any particular screening approach.29-31 The success of screening will be limited if uptake is insufficient. To date, randomized trials of screening have provided only mixed support for improved recognition of patients' emotional problems, and data on long-term patient reported benefits are lacking. In contrast, a positive impact on communication between patients and their medical teams has been observed.31-33 Against this, the potential hazards of screening have recently been acknowledged.34 The main issues are that it may be inappropriate to reveal unmet needs without a clear therapeutic strategy, there is a potential issue of making a diagnosis where none exists (false-positive), and there also is a question of whether frontline cancer clinicians can use systematic screening as part of routine care.35

The potential for screening to be adopted and to change practice can be measured by patient-reported outcomes, such as change in newly initiated treatment and referrals.36 Another simple method is to survey clinicians and or patients about its merits. This can be done hypothetically, asking about screening in general or prospectively by eliciting feedback about a particular screening program. In 1 example of the former strategy, Mitchell et al14 surveyed 226 United Kingdom cancer health professionals and observed that only 6% screened using a formal questionnaire, the majority preferring their own clinical judgment. Pirl et al15 also surveyed 448 oncologists about distress screening. Two-thirds reported screening patients for distress routinely, but only 14.3% used a screening instrument. Predictors of screening patients for distress included availability of mental health services, knowledge of NCCN guidelines, experience, lack of time, uncertainty about identifying distress, and being a women practitioner. Recently, Absolom et al37 interviewed 23 United Kingdom health professionals and reported that experience with screening tools was limited and that the respondents expressed several reservations about routine implementation. A significant weakness of these surveys is that they ask about theoretical, self-reported practice. This method tends to overestimate actual performance.38, 39 We suggest that feedback on the views of health care professionals currently participating in screening programs would be valuable. In oncology, we were able to identify only 4 studies that reported clinicians' opinions or feedback concerning the value of screening.40-43 Two studies reported effects on communication. A study by Lynch et al indicated that outpatient clinic staff believed screening helped them talk to patients about their concerns before their consultation with the physician.42 Recently, Dinkel et al reported that 36% of cancer clinicians believed screening helped them become more attentive to emotional concerns.43 Although there is a paucity of studies in cancer settings, staff surveys from other areas are informative. In the context of postnatal depression and primary care depression screening, clinicians generally supported screening and believed that screening enhanced detection.44-46 However, staff also can report that screening is burdensome and time-consuming.47, 48 In a cardiovascular setting, Sowden et al49 screened 3504 patients with the 2-item Patient Health Questionnaire (PHQ-2) followed by the PHQ-9 administered by a social worker. Nurses reported high satisfaction with the screening process, and they believed that screening was a useful addition to patient care and that it helped the patient receive better treatment of depression. In primary care, Bermejo et al investigated at attitudes to screening with the PHQ-9.50 Patients rated the usefulness of the instrument more positively than general practitioners (GPs): Indeed, 62.5% of the GPs believed that the questionnaire was too long, and 75% thought it was impractical compared with only 25% of patients.

In 2009, we introduced a screening program into routine oncology practice involving chemotherapy and radiotherapy departments (see Fig. 1). Chemotherapy nurses routinely explain complex treatments (including possible side effects), administer chemotherapy, give information, and deliver face-to-face support. Similarly, radiographers routinely undertake treatment planning, administer treatment, give information, and also deliver face-to-face support. They are key nonmedical, frontline cancer clinicians who regularly see patients many times during the course of treatment. Our objective was to examine clinician satisfaction regarding the benefits of routine screening during routine implementation in a clinical setting. Our secondary objective was to examine clinician opinion on the merits of screening their communication with patients and distress management.

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Figure 1. Leicester screening tool for the radiotherapy setting. UHL indicates University Hospitals of Leicester.

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MATERIALS AND METHODS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgements
  8. FUNDING SOURCES
  9. REFERENCES

Setting

We approached all local nurses and treatment radiographers/radiation technologists working in the chemotherapy suite and radiotherapy department at the Cancer Center of Leicester Royal Infirmary, a busy United Kingdom teaching hospital. Fifty clinicians agreed to participate and were involved in the implementation of paper-and-pencil based screening. The Cancer Center has approximately 3500 new cases per year. Our study involved front-line cancer clinicians, comprising 20 chemotherapy nurses and 30 treatment radiographers, all of whom volunteered to take part in the study, although 66% of screening was undertaken by the chemotherapy nurses. The mean age of chemotherapy nurses was 45.5 years, and the mean age of treatment radiographers was 52.3 years (age range, 22-63 years). Forty-seven clinicians were women, and 3 were men.

Screening Program

All clinicians used the distress thermometer and/or the emotion thermometers screeners, which were integrated into a screening program that included assessment of unmet needs and clinician therapeutic response (see Fig. 1). Screening was implemented as part of routine clinical care starting in April 2009 for 9 months in the chemotherapy suite and in September 2010 for 6 months at the radiotherapy assessment center. The original screener took approximately 4 minutes to complete but this was streamlined after clinician feedback to a version that took about 3 minutes. All staff members were offered 1-hour induction training with the recommendation to attend up to 4 additional hourly sessions of support during the implementation phase. Training covered common emotional complications, how to screen, and the management of distress and related emotional issues. Communication training was available separately. Uptake of the training package was incomplete, with less than 25% of clinicians taking up training opportunities. During this pilot phase, clinicians had access to usual care, which included expert psycho-oncology referral. Even in the context of systematic screening, clinicians were permitted to use their own clinical judgment about the appropriateness of screening on a case-by-case basis, for example, by not screening when patients were too unwell or uncooperative. The project was ethically approved by the University Hospitals of Leicester Department of Cancer Studies as an audit of clinical practice.

All clinicians were invited to use the screener as part of routine care. Clinicians themselves used the screen on each clinical contact without automated help and without assistance from administrative staff. Clinicians were asked to screen all consecutive patients unless there was a clinical reason to avoid screening. Reasons for noncompletion included the patient being unable or unwilling to complete the screen. Clinicians themselves administered the screener during their own clinical assessments, typically during initial assessment (treatment planning) or during the early stages of treatment. Clinicians were encouraged to screen at least once per patient, with the maximum frequency dictated by clinical judgment. Screening was conducted regardless of patient sex, ethnicity, or disease stage using informal verbal translation if required (because many of our Gujarti speakers cannot read printed Gujarti). Clinicians decided on the benefits of screening while they were with the patient (Fig. 2) at the time of the index assessment.

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Figure 2. Leicester screening tool feedback and evaluation section. UHL indicates University Hospitals of Leicester; N/A, not applicable; FAO, for attention of.

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Outcome Measurement

We rated clinician satisfaction with several short quantitative and qualitative questions regarding the success of screening and the burden of screening that were applied prospectively after each consultation (for the screening procedure, see below). Therefore, clinicians could evaluate their opinion regarding appropriateness of the tool across all types of clinical encounters. We measured several variables that could influence the success (or otherwise) of screening. These included the following clinician baseline measures: clinical rating of practicality of the screening program, clinician self-rated confidence, and clinician receipt of psychosocial training. We also asked about the following clinician-reported outcome measures: perception of improved clinician-patient communication, improved detection of psychosocial problems, propensity of the clinician to act therapeutically (help offered), and change in clinical opinion after screening (Fig. 2). We also measured several patient-reported measures: distress as well as anger, depression, anxiety, and desire for help. We examined rates of global satisfaction and predictions of satisfaction with screening using logistic regression. Finally, we collected feedback using free text boxes on the screening form and asked a random split-half subset of 25 clinicians about their experiences with screening in more detail, namely, the effect on communication, recognition of emotional problems, and practicality of the screen.

Analysis

We used univariate logistic regression, multivariate regression and chi-squared test in StatsDirect 2.7.7 (StatsDirect Ltd., Cheshire, United Kingdom). StatsDirect calculates the probability associated with a chi-square random variable with n degrees of freedom.

RESULTS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgements
  8. FUNDING SOURCES
  9. REFERENCES

Cancer clinicians screened 379 unique patients with at least 1 screening application and provided detailed feedback after 267 screening applications. Demographics of the screened sample are provided in Table 1.

Table 1. Patient Demographics
CharacteristicPercentage of Patients (n = 379)
  1. Abbreviation: DT, distress thermometer.

Palliative stage, %15.5
Women, %74.7
Age, y 
 Mean63.3
 Range33.0-83.9
Chemotherapy setting65.7
 Breast cancer46.9
 Lung cancer6.7
 Prostate cancer7.2
 Colorectal cancer12.4
 Bladder cancer1.4
High distress, DT ≥331.4
Table 2. Clinician Predictors of High Satisfaction with Screening
VariableT StatisticP (Significance of T Statistic)
Receipt of training2.56.0110
Improved communication31.0.00001
Improved detection7.02.00001

Clinician Rating of Global Satisfaction

Across all 379 screening applications, clinicians believed that screening was useful in 43% of assessments but not useful in 35.9% of assessments, and they were unsure or neutral in 21.1% of assessments. The application of the screening program assisted staff in changing their clinical opinion in 41.9% of assessments. Most commonly, this was clarification of baseline uncertainty (50.9%), but it also included revaluation of an initially null assessment (ie, the patient appears nondistressed; 26%) or revaluation of a positive assessment (23.1%; ie, the patient appears distressed).

Clinician Rating of Clinical Benefits

From the sample of 267 assessments with more complete data, in 51% of assessments, clinicians believed that the screening program helped improve clinical communication. In 40.6% of assessments, clinicians believed that the screening program helped with recognition of distress, anxiety, or depression (in 18.9%, they expressed no opinion). Clinicians believed that the simple paper-and-pencil screening program was practical for routine use in 45.3% of applications but impractical in 37.5% (in 17.2% of assessments, staff expressed no opinion).

Chemotherapy Versus Radiographers Feedback

Chemotherapy nurses rated the value of the tool after 249 nurse-patient interactions. They rated the screener useful in 42.9% of assessments and not useful in 43.4% of assessments, and they were uncertain or had no opinion in the remaining 13.7% of assessments. Radiographers rated the value of the tool after 130 clinician-patient interactions. They believed that the screening program was useful in 56 of 130 assessments (43%) and not useful in 21.5% of assessments, and they were unsure about 35.4% of assessments. Although ratings of chemotherapy nurses and radiographers were similar, the difference in those who rated assessments “not useful” was significant (chi-square statistic, 7.35; P < .0001). Chemotherapy nurses appeared to have more difficulty accommodating screening into busy initial assessments, although both groups reported that screening was a challenge when patient turnover was high.

Predictors of Favorable Staff Perceptions of Screening

On univariate logistic regression, the following variables were associated significantly with a favorable staff perception: clinicians rating the instrument as practical (P < .0001), low clinician confidence (P < .001), and high patient-rated anxiety (P = .02). Two outcome variables were linked with staff satisfaction with screening: talking with the patient about psychosocial issues (P < .0001) and a change in clinical opinion (P < .0001). On multivariate analysis, 3 variables were associated with high staff satisfaction with screening, namely, receipt of training (P < .0001); talking with the patient about psychosocial issues (P < .0001); and improved detection of psychological problems, such as depression/anxiety (P < .0001). On univariate chi-square analysis, clinicians who rated the program useful were twice as likely to change their clinical opinion after screening (chi-square statistic, 15.9; P < .0001; odds ratio, 2.5) (Table 2).

Narrative Feedback

We received narrative feedback comments, which we divided post hoc into concerns about completion bias, completion difficulties, outcome feedback, tool design comments, and tool application comments. These are listed in Table 3.

Table 3. Staff Narrative Feedback Results
Concerns about completion bias
 Wife interfered and biased results
 Patient known to suffer from paranoid schizophrenia; this caused difficulty in assessing the patient
 Patient was not confident in filling form, therefore needed guidance; this may have biased the results
 This patient's anger relates to the length of time it has taken from diagnosis to treatment
 Patient's concerns are more related to having a disabled daughter to care for rather than diagnosis itself
 Although patient scored high last week, this is because of recent admission to hospital, and patient stated that this was not an accurate measurement of her “normal”
Completion difficulties
 Need more time for new cases to complete this
 Patient found it difficult to rate her feelings, as she is able to cope with family support
 Patient unable to read, as did not have reading glasses
Outcome feedback
 Referral to Macmillan nurses in view of palliative chemotherapy
 Macmilllan nurse involvement was decided by the patient at this stage
 Discussed coping with cancer and Macmillan nurses
 Patient currently okay with family support; wants to get better and start treatment
 Wig referral and appointment made for today to decrease patient's anxiety
 Patient declined help, as she felt her emotions were “normal” given current events
 Discussed thermometer with patient; he is very anxious to commence treatment
 Patient already has Macmillan nurse, feels well supported at home
 Full discussion with consultant has meant that the patient is not as confused
Tool design comments
 The form could use a small space for written comments
 There should be a section for those with a known history of mental illness
 A section to explain why no action needed
Tool application comments
 Need to be given to patient before having case talk

DISCUSSION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgements
  8. FUNDING SOURCES
  9. REFERENCES

We collected data after 379 screening applications conducted by front-line chemotherapy nurses and treatment radiographers (radiation technologists). The opinion of clinicians regarding the value and feasibility of screening was mixed. A substantial minority believed that screening was not helpful, and this was greater among nurses than among radiographers (43.4% vs 21.5%; P < .001). In 37.5% of assessments, clinicians believed that our streamlined screening program was impractical for routine use. Nevertheless, it should be noted that clinicians generally were willing to persist with screening, provided they were supported in this. Yet the narrative comment, “Need more time for new cases to complete this,” was the most common type of comment received. At the same time, clinicians also believed that screening was useful during 43% of assessments, and they were unsure or neutral in 21.1% of assessments. Indeed, the screening program assisted staff in changing their clinical opinion after 41.9% of assessments, most commonly by helping them clarify an uncertain initial judgment. This is the first study that we know of to systematically collect front-line cancer clinicians' opinions on the value of routine screening for distress. The study was unfunded and, thus, may provide better insight into the real-world feasibility of screening without the availability of dedicated screening researchers or administrators. Another strength of this study is that we collected data prospectively based on the actual implementation of a rapid paper-and-pencil–based screening program. Paper-and-pencil–based testing was favored over computerized methods mainly because of a lack of resources. Data were gathered at each clinician-patients interaction rather than by hypothetical survey. Thus, an individual clinician could report satisfaction with screening in some cases but dissatisfaction in others. We believe this is stronger methodologically than grouping clinicians' feedback into 1 category. One limitation, however, is that we did not collect patient opinions on the acceptability of screening. A second limitation is that we did not study the uptake of screening, although we previously reported that uptake was 78.3% in the chemotherapy setting studied alone.51 A third limitation is that we did not validate the screener using a semistructured interview.

These data demonstrate that a screening program can be both useful and burdensome, depending on the clinical context. For settings in which patients obviously are unwell, clinical opinion may not be significantly worse than screening performance, because the sensitivity of unassisted detection is approximately 75% when searching for severe distress.51 These results should be extrapolated only to screening that is applied by cancer clinicians themselves. The extent to which screening by cancer clinicians brings tangible benefits it is not certain, but this is an active area of research, as mentioned above. Screening using automated methods (touch screen) or using front-desk clinic staff may overcome some barriers cited here, but at additional initial cost. Nevertheless, screening may be most useful in cases of clinical uncertainty; and, in such situations, clinicians may be more likely to revise their clinical opinion on the basis of the screening result. We observed that, in approximately 25% of assessments in which the clinician reconsidered their clinical opinion, the clinician revised their judgment that the patient was well; and, in approximately 25% of assessments in which the opinion was reconsidered, the clinician revised their judgment that the patient was unwell. Clinicians rated the screening program as most useful in helping with communication in 50% of assessments, but they also believed that screening helped with recognition in approximately 2 of 5 assessments. The focus on communication rather than detection has been recognized previously, because nurses often want a therapeutic structure within which they can help patients to explore feelings, whereas physicians may want a formal method for diagnosis and rating symptoms.47

We also examined predictors of clinician satisfaction with screening. Clinicians who rated the instrument as practical, clinicians with low confidence, and clinicians assessing patients with more anxiety were more likely to believe that screening had value. This suggests that clinicians with high confidence may perceive that screening has little to offer; but, paradoxically, clinicians with low confidence may fail to take up screening or training opportunities.52 The relation between screening satisfaction and patient severity may produce a U-shaped curve. Screening patients with very high and very low distress may be perceived as bringing little added value to normal, unassisted judgment, as mentioned above. A favorable perception of screening also was linked with positive outcomes, namely, an increase in talking with the patient about psychosocial issues (P < .0001) and a change in clinical opinion (P < .0001). Thus, clinicians who favor screening are more likely to use it to their advantage, informing their clinical opinion and improving communication. It is worth noting that, even in instances in which clinicians did not rate the screening as useful, they nevertheless still changed their clinical opinion after screening in 19.4% of assessments. Assuming that a change in clinical opinion is a proxy for a worthwhile screening application, this suggests that screening still can be effective when clinicians use it reluctantly. On multivariate analysis, 2 additional variables—receipt of training (P < .0001) and improved detection of psychological problems—also were significant. This is concordant with the opinion that offering training in support of a screening program is likely to influence its success53 by improving motivation to screen (for which satisfaction with screening is a proxy) and by improving quality of application and interpretation: that is, assessment skills.

Few previous studies have measured satisfaction with distress screening in a cancer setting. In a survey of attitudes, Mitchell et al14 observed that 37% of United Kingdom clinicians did not regularly assess for emotional complications, only 5.9% did so using a formal questionnaire, and the majority (62.2%) relied on their own clinical judgment. The main barrier to successful screening was lack of time (cited by almost 60%), but insufficient training and low confidence also were influential. Lee et al41 reported that 56% of nursing and allied health staff indicated that routine distress thermometer-based screening was “very” helpful for them in thinking about how to work with patients. Although that study was based on group clinician responses, it was not dissimilar to our finding that screening was helpful in 43% of assessments. In a pilot study of quality-of-life and distress screening using the Hospital Anxiety and Depression Scale (HADS), oncologists in the United Kingdom rated screening as useful in 87% of 28 consultations but believed that it contributed to patient management in only 54% of consultations using a touch screen.54 In a larger follow-up randomized trial of that automated screening, only 68% of oncologists were willing to use screen-generated data routinely after cessation of a funded trial.55 That said, 1 qualitative United Kingdom study suggested that, despite initial reservations, clinicians generally believe that screening can help talk to patients about their concerns before their consultation with the physician.42 In our study, clinicians also stated that screening helped most with communication (in 51% of applications), but they also said it helped with recognition (40.6%). Indeed, by examining their clinical judgment before and after screening, we observed that screening assisted staff in revising their clinical opinion after 41.9% of assessments. Most commonly, this was clarification of baseline uncertainty, but it also included revaluation of an initial clinical opinion. We identified only 1 study to date that examined screening for distress in a radiotherapy setting. In 2010, Dinkel et al reported that 18.5% of radiographers believed that paper-based distress screening was too long. We also observed a higher than expected rate of clinician-reported barriers.43 On 37.5% of occasions, clinicians believed that our screening program was impractical for routine use, and more chemotherapy nurses than radiographers rated the screening program as “not useful” (43.4% vs 21.5% of occasions; P < .001). It should be noted that we attempted to implement a rapid screening program that would have least burden to staff and patients (Fig. 1) and simplified it in response to clinician feedback. Nevertheless, our screener was completed by clinicians themselves (not by waiting room or reception staff), and it is clear that even rapid, clinician-led screening, at least in a paper-and-pencil format, although acceptable to the majority, is not universally favored by front-line clinicians.

In conclusion, screening for distress in routine cancer care is relatively difficult to implement. Screening can be perceived as an unnecessary burden by many front-line clinicians, yet screening also is perceived as beneficial when applied to more vulnerable, high-risk patients and when the screening program is supported by ongoing training or supervision. Once screening is implemented, many clinicians do perceive real benefits. Clinicians who are willing to apply screening often perceive an improvement in communication as well as an improvement in the detection and diagnosis of psychological problems, particularly in cases of initial clinical uncertainty. When setting up screening programs, organizations should be attentive to the needs of both motivated and unmotivated clinicians. Several worthwhile strategies have been proposed.22, 53 The burden of screening should be minimized, results should be fed back to clinicians in a meaningful way, and clinicians should be encouraged to make local improvements and should be offered support and training in screening as well as in the subsequent management of distress and related concerns. Attendance at training sessions should be monitored. Those designing screening programs to be delivered by front-line clinicians should take into account burden of delivery, scoring, and interpretation. Clinicians should be involved in the implementation process and generally should be allowed to use their clinical judgment in situations in which they suspect screening errors (false-positive and false-negative results).

Acknowledgements

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgements
  8. FUNDING SOURCES
  9. REFERENCES

We thank the staff and patients of University Hospitals of Leicester who took part in this study.

FUNDING SOURCES

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgements
  8. FUNDING SOURCES
  9. REFERENCES

No specific funding was disclosed.

CONFLICT OF INTEREST DISCLOSURES

The authors made no disclosures.

REFERENCES

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgements
  8. FUNDING SOURCES
  9. REFERENCES
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