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��ࡱ�>��	������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������	��bjbj�W�W	4�=�=�{�
���������%999����MMM8��a\M�9���w#w#w#w#R$R$R$a8c8c8c8c8c8c8$p;�>��8�9])R$R$])])�899w#w#�D9�0�0�0])<9w#9w#a8�0])a8�0�0�2#3w#���� �|���M�-��2M8Z90�9�2,�?5/��?#3#3�?9A5R$H�%��0�&�@'R$R$R$�8�8�/�R$R$R$�9])])])])���������������������������������������������������������������������?R$R$R$R$R$R$R$R$R$�	�:	 The value of the Hospital Anxiety and Depression Scale to assess the effects of treatment toxicity in the follow-up of gynaecological cancer patients 

CL Barker*,, JA Routledge, DJJ Farnell2, R Swindell, SE Davidson1,2

Running title: HADS and treatment toxicity in gynaecological cancer


Keywords: radiotherapy; late toxicity; depression; anxiety; gynaecological cancer; longitudinal study
Abstract

The aims of this study were to investigate psychological morbidity in women undergoing curative radiotherapy for gynaecological cancer (before and after treatment up to 3 years) and to analyse the relationship between treatment toxicity and both anxiety and depression. This was a prospective study involving 224 gynaecological cancer patients. Patients completed the Hospital Anxiety Depression Scale (HADS) and Late Effects on Normal Tissue Subjective Objective Management Analytic scales (LENT SOMA) questionnaires both before and after treatment (immediately post-radiotherapy, 6 weeks, 12, 24 and 36 months). At least 48.2% of the patients experienced anxiety and 48.4% experienced depression from diagnosis to 3 years following radiotherapy treatment. Levels of anxiety were highest pre-treatment, whereas depressive symptoms peaked immediately following the end of radiotherapy. There was also a strong negative correlation between treatment toxicity and both anxiety and depression. 
This is the first study to analyse the relationship between psychological morbidity and treatment toxicity in gynaecological cancer patients. It supports the use of HADS and toxicity questionnaires in routine clinical practice for the detection of psychological morbidity. Furthermore, it highlights the need to establish effective management strategies to reduce the symptoms of late treatment effects and therefore improve patients� psychological health after treatment for gynaecological cancer. 


Introduction

Continuing advances in the treatment of cancer, combined with an ageing population, have resulted in an increasing number of people surviving longer following a diagnosis of cancer. Five year survival rates for cervical and endometrial cancer are now 67% and 77% respectively [1]. Early side effects of radiotherapy used to treat gynaecological disease are well known and often reversible; these include fatigue, bowel and bladder irritation[2]. However, late toxicity of pelvic radiotherapy, especially with concurrent chemotherapy, can cause bladder and bowel frequency, urgency, incontinence and fistula formation. Combined with the distress of infertility and early menopause following therapy, these late treatment effects can have devastating consequences for patients. 

There is currently a rising incidence of late treatment effects seen within the pelvis, especially following multimodal treatment regimes employed to treat gynaecological malignancy[3]. This is known to have a negative impact on patients� quality of life[4].  Despite this, psychological morbidity in gynaecological cancer patients has received relatively little attention. Studies assessing the prevalence of psychological distress report rates of 15-34% for anxiety and 6-40% for depression[5-9]. Longitudinal studies investigating psychological morbidity from diagnosis to follow-up are lacking, particularly in the UK. Table 1 summarizes studies that have addressed psychological morbidity in gynaecological cancer patients.

Psychological morbidity is a significant problem in  cancer patients and can occur at any point over the course of diagnosis and treatment and be aggravated by a multitude of factors including physical pain, relationship difficulties and symptoms related to therapy. A recent study of over 3000 cancer patients attending outpatient clinics in the United Kingdom reported 22% experienced significant emotional distress in the form of anxiety or depression[10]. Furthermore, psychological morbidity has been associated with reduced quality of life, increased impairment to immune response[11] and decreased survival rates in cancer patients[12]. Therefore detection and treatment of psychological morbidity in cancer patients helps to alleviate emotional distress and also reduces additional costs to the health service in general. Despite this, psychological problems are frequently unrecognised by oncology professionals[13] and therefore not addressed by cancer services. 

There were two main objectives of this prospective study. The first was to examine psychological morbidity in women undergoing radiotherapy for gynaecological cancer treatment (before and after treatment up to 3 years using the hospital anxiety and depression (HADS) scale).  The second aim was analyse the relationship between HADS score and treatment toxicity (using the Late Effects Normal Tissue (LENT) � Subjective Objective Management Analysis (SOMA) questionnaire) in addition to the association with cancer site, stage, age and treatment modality.
Materials and Methods

Patients
Ethical approval for this study was obtained from the South Manchester Research Ethics Committee. This was a prospective observational study in gynaecological cancer patients recruited between 1998 and 2006. All patients attended the Christie Hospital to receive radical radiotherapy treatment.  Patients who developed disease recurrence or had disease progression were excluded from this study.

Measures
Anxiety and depression were measured using the HADS questionnaire. The hospital anxiety and depression scale (HADS) was originally developed in 1983 and is a widely used self-assessment tool designed to identify patients experiencing levels of anxiety and depression[14]. It consists of 14 questions each scoring 0-3, resulting in a score out of 21 for 2 subscales; anxiety (HADS-A) and depression (HADS-D). It has been extensively validated and found to be a valuable tool in recognizing and screening for psychological morbidity[15]. Different cut-off scores were applied to each subscale to identify patients with possible clinical cases of anxiety or depression.

Late treatment effects were measured using the LENT SOMA scales. These were originally published in 1995 and a 37-item questionnaire was produced to contain the LENT subjective scales[16]. The latest version of this pelvic questionnaire can be found at the Christie Hospital website ( HYPERLINK "http://www.christie.nhs.uk/the-foundation-trust/treatments-and-clinical-services/clinical-oncology-scoring-treatment-effects/ctcaelent-soma-questionnaires.aspx" http://www.christie.nhs.uk/the-foundation-trust/treatments-and-clinical-services/clinical-oncology-scoring-treatment-effects/ctcaelent-soma-questionnaires.aspx). High scores on the subscales of the LENT SOMA indicate high levels of symptom experience from treatment-related toxicity

By using SPSS V16.0, a score was formed from the LENT SOMA scales according to the criteria proposed in the 1995 published tables. The questionnaires were divided up into six subsites: uterus/cervix, ovary/reproductive, rectum/bowel, bladder/urethra, ureter/kidney and vagina (including sexual function). An overall LENT SOMA score was also formed for all the questions in the questionnaire. Further details have been described in a previous paper[4].




Timing of the questionnaires
The first questionnaire was completed before the start or within the first week of radiotherapy and served as a baseline assessment. Timings post-treatment were measured from the last day of treatment. Post-radiotherapy questionnaires were completed after treatment (-1 week to +2 weeks), at 6 weeks following radiotherapy (� 2 weeks), 12 months (� 4 weeks), 24 months (� 4 weeks) and 36 months (� 4 weeks). Questionnaires completed outside the designated range were not included in the statistical analysis.

Statistical Analysis
As data was not normally distributed non-parametric statistics were used. Friedman�s two-way analysis of variance was not utilised to examine the changes in scores with time, as the sample size was small at 36 months after treatment. Instead the Wilcoxon matched pairs signed rank test was used and a Bonferroni correction applied. Therefore, all changes in scores with time (e.g., from baseline assessment to 6 weeks after treatment) are reported at a reduced level of 0.01 significance (0.05 per number of tests). The relationship between HADS scores and overall LENT SOMA score was assessed using Spearman�s rank correlation. The relationship between HADS score and age, stage or treatment type (radiotherapy and/or chemotherapy and surgery) was determined using Mann-Whitney U and Kruskal-Wallis tests.
Results
Compliance
In total 224 patients took part in the study. Their disease and treatment characteristics are given in Table 2. From this consecutive series of 224 patients, 196 patients returned completed questionnaires at the pre-treatment assessment. As the study was prospective there were a decreasing number of patients completing questionnaires at each subsequent time point. Additionally 9 patients wished to stop the study, 39 patients did not return the questionnaires, 35 patients developed disease recurrence and 14 patients died during the 3 year period and therefore these were withdrawn from the study. 

This gave a total of 176 patients who had either completed or withdrawn from this prospective study, with 49 patients still at various time points post-treatment. Out of these 176 patients, 39 stopped returning questionnaires and therefore the overall level of compliance was determined to be 72.7%. 

Table 3 shows the number of patients who completed the questionnaires at each time point. 

Longitudinal results
Table 4 shows the mean HADS scores over time and the prevalence of anxiety and depression using various cut-off scores from past literature.  Taking the lowest value for the cut-off score (HADS-A e" 7, HADS-D e" 5) the results indicate that 48.2% of the patients experienced anxiety and 48.4% experienced depression from diagnosis to 3 years following radiotherapy treatment. In addition, 45.4% of patients scored e" 13 on the total HADS scale during this time.

The proportion of patients with a HADS-A score exceeding the lowest cut-off value (HADS-A e" 7) was highest at pre-treatment assessment, whereas the proportion of patients with a HADS-A score above the highest cut-off value (HADS-A e" 11) was largest 6 weeks after the end of treatment. Additionally, the proportion of patients with a HADS-D score exceeding the lowest cut-off value (HADS-D e" 5) was highest immediately following radiotherapy treatment, whereas the proportion of patients with a HADS-D score above the highest cut-off value (HADS-De" 11) was again largest 6 weeks after the end of treatment.
Table 5 shows the HADS subscale scores (mean and median) throughout the course of treatment for gynaecological cancer and 3-year follow-up. Mean anxiety scores exceed mean depression scores at all time-points. Baseline results provided by assessments completed before the start of radiotherapy were compared with subsequent HADS scores. There was a significant decrease in the mean HADS-A score from pre-treatment to immediately following radiotherapy. Conversely, there is a significant increase in mean HADS-D score also from pre-treatment to immediately after radiotherapy. Apart from these time points there are no significant changes between scores taken from pre-treatment assessment and subsequent points in the 3 year follow-up. Figure 1 also provides an illustration of HADS anxiety and depression scores over time.

Relationship between HADS and late treatment effects
Scores for the overall LENT SOMA subscale and HADS questionnaires were compared using Spearman�s rank correlation. The results are shown in Table 6 and demonstrate that the overall LENT SOMA score was strongly correlated with both HADS-A and HADS-D scores at all time points. The correlation coefficients ranged from .256 to .598 for HADS-A, and from .346 to .563 for HADS-D (all p values <.05, except HADS-A at 36 months). This revealed a strong positive relationship between late treatment effects and levels of anxiety and depression. In general, the correlation coefficients for the HADS-D were higher than those for HADS-A and they also increased with time. The strongest correlation with the overall LENT SOMA score was at 24 months for HADS-A and 36 months for HADS-D.

Relationship between HADS and cancer site, age, stage and treatment type
To analyse the relationship between cancer site and both anxiety and depression, the sample was split into two groups. One group included patients with cervix cancer and the other contained those patients with cancer of the uterus (the individual with vaginal cancer was omitted). At pre-treatment assessment there were statistically significant differences in HADS-A, HADS-D and HADS-T scores between the two groups. Specifically, those patients with cervical cancer had higher levels of anxiety and depression than those with uterine cancer (all P values <0.05).
There was no significant association between age and HADS-A, HADS-D or HADS-T scores at pre-treatment assessment.

Additionally the number of different treatments each patient received was compared with the change in HADS-A and HADS-D scores from baseline assessment to immediately following radiotherapy. Surgery, chemotherapy, brachytherapy and radiotherapy were counted as distinct treatments. There were no statistically significant differences in anxiety and depression scores for the number of treatment modalities received.
Furthermore there was no statistically significant difference between the cancer stage (I, II, III or IV) and mean HADS-A and HADS-D scores. 
Discussion

Main findings
The results from this study suggest that up to 45.3% of gynaecological cancer patients experience significant psychological distress from diagnosis to 3 years following treatment (using a total HADS score e"13). It also demonstrates that symptoms from treatment-related toxicity are associated with higher levels of depression and anxiety.

Comparison with previous literature
There are only a small number of studies that have investigated psychological morbidity specifically in gynaecological cancer patients. Longitudinal studies are lacking, particularly in the UK, and a variety of measures have been used to assess psychological distress; therefore making direct comparison of research difficult. 

Considering this, the results from this study show that levels of anxiety are highest pre-treatment (48.2%). The elevated symptoms of anxiety prior to treatment are consistent with previous longitudinal research in gynaecological cancer patients[7] and other solid tumours treated with radical radiotherapy[17-18]. Additionally, results from this study show that the levels of depression are highest immediately following the end of radiotherapy treatment (48.4%). Depression is known to be a common disorder in the acute phase of cancer following diagnosis and treatment[19] and these findings are consistent with previous research.

Throughout this study the overall LENT SOMA score was strongly correlated with both mean HADS-A and HADS-D scores. This demonstrates a strong positive relationship between late treatment effects and levels of anxiety and depression. This is in agreement with previous research showing that symptom severity even 11 years following radiotherapy treatment is still significantly associated with poorer overall quality of life and higher levels of�depression[20]. 

Furthermore, a previous study showed that symptoms related to the rectum/bowel subscale within the LENT SOMA questionnaire contributed the most to the overall LENT SOMA score[4]. These late treatment effects include diarrhoea, tenesmus and urgency. It can be therefore argued that these symptoms have the largest impact on anxiety and depression. 

This study suggests that patients with cervical cancer have higher levels of anxiety and depression than those with uterine cancer. There was no association between either treatment modality or stage and mean HADS-A and HADS-D scores. Although there was a significant difference in average age between the cervix and uterus cancer patient groups (cervix group 51; uterus group 62.5); age did not correlate significantly with either HADS-A or HADS-D scores, suggesting that is not responsible for the higher levels of anxiety found in patients with cervical cancer.

There is some controversy about the recommended cut-off scores in the HADS questionnaire for detecting psychological distress in cancer patients. Initially a cut-off score of e" 8 represented a borderline disorder and e" 11 was considered indicative of a clinical case of anxiety or depression[14]. However, subsequent research suggested these thresholds might be too high for cancer patients[21]. Recently a cut-off score of e" 7 for anxiety and e" 5 for depression has been proposed as the optimum threshold for identifying patients with psychological morbidity and the best trade between sensitivity and specificity[22]. In addition, it was suggested that a total HADS score could be used to identify a psychiatric disorder (cut-off score e" 13 identified 76% of cases) and this would be easier to employ in a routine clinical setting.

Conclusions
This research further supports the use of the HADS scale in routine oncology practice. It is a straightforward, simple screening which identified a high proportion of patients undergoing gynaecological cancer treatment experienced anxiety and depression   This study has also demonstrated the association between symptoms from treatment-related toxicity and psychological distress. 
This study did not demonstrate an individual time point that the HADS questionnaire should be completed as a screening instrument for psychological distress. As 45.3% of patients had a HADS-T score e" 13 during the 3 year follow-up, it is felt that the questionnaire should be completed repeatedly at different time points after diagnosis and during treatment. 
Although different cut-off scores are applied to the results from this study, we feel that the lower thresholds proposed by Singer et al are more appropriate to use. It is preferable to overestimate cases than allow patients with psychological distress to go undetected. Moreover, a total HADS score is simpler to use compared to both scales of HADS-A and HADS-D and therefore we recommend that all patients with HADS-T e" 13 should be referred for psychological intervention.
Role of the Funding Source

CRUK funded salaries of Damian Farnell and Jacki Routledge

Conflict of Interest

There is no conflict of interest declared


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 Department of Clinical Oncology, The Christie NHS Foundation Trust, Manchester, UK
 Academic Department of Radiation Oncology, University of Manchester The Christie NHS Foundation Trust, Manchester, UK
 Department of Statistics, The Christie NHS Foundation Trust, Manchester, UK





























* Correspondence: Dr CL Barker, Department of Clinical Oncology, The Christie NHS Foundation Trust, Wilmslow Road, Manchester, M20 4BX, United Kingdom. E-mail: claire.barker@doctors.org.uk











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