Journal of P,s)rhosomaric Prmled nn Great Britain

Research,

Vol.

34, No

2, pp. 129-140.

1990.

0022-3999/90 53.00 + .oO Pergamon Press plc

INVITED REVIEW: PSYCHOLOGICAL ASPECTS OF CANCER AND CHEMOTHERAPY ANN CULL*

RAPID advance in the investigation of cancer at the cellular level and in the development of more effective cytotoxic therapies seemed for a time to eclipse psychological considerations in oncology. More recently interest in psychosocial issues has gathered momentum and the wide ranging and rapidly growing literature in ‘psychosocial oncology’ defies review in a single article. Substantive progress has been hampered by a lack of theoretical framework, imprecise research questions, formidable methodological difficulties and fragmented effort, at times as negligent of biological variables as earlier scientific work was of the psychological. Progress in two broad areas will be reviewed. Firstly, the role of psychological factors, particularly stress in promoting the development of cancer which is attracting much current research effort. The development of this work requires rigorous assessment of the relevant variables and further collaborative psychobiological effort. It raises the question of the value of psychological indices as prognostic indicators with potential implications for psychological intervention. Secondly, the benefits of chemotherapy are achieved at a cost in terms of toxicity. Recognition of the true extent of morbidity allows preventative and palliative efforts to be mobilized and evaluated. Psychological factors are a vital component in the accurate cost-benefit analysis which is central to clinical decision-making and to assessment of the worth of chemotherapy.

PSYCHOLOGICAL ANTECEDENTS OF CANCER Aspects of human behaviour such as smoking or compliance with health education advice may be crucial to cancer prevention, screening and early detection but are only indirectly related to the factors of mood, stress and personality to be reviewed here. Depression The Roman physician Galen reputedly noted ‘melancholic’ women to be at greater risk of cancer than more ‘sanguine’ women [l] and there have been numerous clinical observations of depression preceding the diagnosis of cancer [2]. The date of onset of cancer cannot be accurately determined and these mood disturbances could reflect early occult malignant processes [3]. The association between depressive illness and cancer has been explored by comparing the incidence of cancer deaths in the general population with that among patients previously treated for depression. Two studies report an increase in cancer mortality in male patients [4, 51, two found no such increase [6, 71. Prospective studies * To whom correspondence and reprint requests should be addressed: Imperial Medical Oncology Unit, Western General Hospital, Edinburgh EH4 ZXU. 129

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of male psychiatric patients [8] and medical patients of both sexes [9] failed to show any correlation between measures of depressed mood and subsequent cancer deaths. It is of interest then that an association has been demonstrated between major depressive disorders and changes in immune function which could facilitate carcinogenesis [lo] but whether depressive illness has a role as an antecedent of cancer remains uncertain. Stressful life ellents

Clinical observations have repeatedly associated cancer proneness with the loss of significant relationships [ Ill. Epidemiological studies, however, have shown no excess risk of breast cancer in bereaved women [ 121 and no increase in cancer mortality rates following loss of a spouse [13]. These studies offer no information about such potentially crucial intervening variables as individual coping style or social support. Some support for clinical observations is emerging from biological research where immuno-suppression has been demonstrated following bereavement [14]. Several studies have considered a wider range of stressful life events most usually comparing women with benign and malignant breast disease [IS, 161 and failing to demonstrate a significant increase in the number or intensity of stressful life events in cancer patients. There remains a problem of placing events in time and these studies have been criticized for the lack of ‘normal’ controls as well as for the assessment methods used. Burgess [17] points out the pitfalls of generalizing from one disease group to another since some malignancies may be more influenced by the immune or hormonal system than others. Although Horne and Picard [18] found loss of a significant relationship associated with lung cancer and Lehrer [19] concluded life events were a contributory factor in the onset of gastric cancer, causation cannot be attributed on the basis of these correlational data. Ramirez [20] attempted to overcome the methodological problems of previous studies by using a more reliable measure of life events [21] and considering the time to recurrence of women whose breast cancer had remitted. This small case control study suggested a significant association between life stress and recurrence of disease. A larger prospective study is now needed. PrrsonalitJ- jhctors

It has been argued increasingly in life events research that the degree of stress experienced is mediated by the personal meaning of the event and by personality factors which determine coping strategies. Cooper et cd. [22] in a prospective study of women undergoing breast examination found fewer stressful life events in the group who were found subsequently to have cancer. However, this group experienced more severely stressful events and these wotnen were more likely to report suppressing their feelings and having fewer coping skills. A similar pattern has been described at the onset of cervical cancer [23] and malignant melanoma, particularly in younger patients [24]. Controversy surrounding the role of personality factors in the development of cancer is usefully reviewed by Temoshok [25]. A degree of concordance is emerging in the characteristics attibuted to the cancer prone, or Type C, personality [26, 271. These included conformity/compliance. stoicism and unassertiveness but the cardinal

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feature is emotional control, more specifically the suppression of behavioural reactions to negative emotions such as anger [28]. Suppression of emotion has long been thought a key factor in the development of psychosomatic disorders [29] where stress is dealt with at the expense of increased physiological activation. What remains unproven is whether the biological changes associated with this behaviour have significance in promoting carcinogenesis [3]. A recent study identified similar personality factors discriminating between susceptibility and resilience to cervical cell change. The authors [30] suggest chronic psychological distress with associated immunosuppression can potentiate the development of virally induced neoplasia and propose neuroendocrine changes as a mediating process. Their model is highly speculative but it does suggest specific avenues for future research. The current view is that it is not stress itself but the individual’s specific behavioural and biological responses to that stress which are relevant to carcinogenesis. Neuroendocrine, immunological and psychosocial factors needed to be investigated together in prospective longitudinal studies. Implications

for outcome

Four categories of psychological factors have been implicated in the survival of cancer patients: adjustment to illness, emotional expression, will to live and emotional stress, several studies report finding no such association [3 1, 321. Methodological problems make it particularly difficult to evaluate conflicting results. More good prospective studies of adequate size are required to provide for multivariate analysis which should include known biological prognostic indicators as well as the proposed psychological variables. Adequate studies need to take account of the type and severity of the disease and its treatment when comparing short and long-term survivors. The psychological measures used need to be of proven reliability and validity and comparability of results would be improved by standardization of outcome measures. Few studies meet these criteria but the literature has been recently reviewed elsewhere [17,25, 331 and Temoshok has developed an interesting, if highly speculative, model of a process of adaptation to reconcile apparently discrepant findings [25]. The prognostic relevance of psychological adjustment to cancer has been most consistently studied by Greer et al. Their well known early work identifying four categories of response to cancer (fighting spirit, denial, stoic acceptance, hopeless/ helpless) with prognostic significance in early breast cancer [34, 351 has led to the development of a questionnaire method of assessing ‘mental adjustment to cancer’ [36,37] and a cognitive/behavioural intervention which aims to induce the attitudes believed to be associated with the most favourable prognosis. A randomized controlled study to evaluate this approach is currently underway [38].

PSYCHOLOGICAL

CONSEQUENCES

OF CANCER

AND

CHEMOTHERAPY

The side-effects of cancer chemotherapy affect the cognitive, emotional and behavioural functioning of the patient. The degree of toxicity which is acceptable may vary depending on whether the treatment intent is curative or palliative

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but accurate information about morbidity is required to inform decision making for individual patients and in policy making. The most common side-effects of chemotherapy are nausea and vomiting, hair loss, immunosuppression and tiredness. Patients may also experience psychological side-effects as a result of conditioning, of the direct action of drugs on the brain or as a consequence of the emotional demands of the experience. From the psychological perspective on occasion it can be difficult to discriminate between symptoms of the disease and side-effects of treatment. Cognitille impairment The impact on cognitive function is sometimes overlooked. Significant impairment of higher mental functions is expected in primary and secondary brain tumours but may also result from other physiological processes or from treatment (e.g. non-metastatic encephalopathy, metabolic disturbances, drug toxicity and crania1 irradiation). Cerebral toxicity is not always well recognized or systematically documented. There have been sporadic reports of gross cognitive impairment, usually confusional states, occurring in response to many of the commonly used chemotherapeutic agents and more chronic processes of intellectual deterioration have been reported in children treated for leukaemia [39]. Without formal testing more subtle impairment (e.g. concentration or memory) is likely to go undetected among adult patients. Depressed mood and raised anxiety can interfere with cognitive function and should be assessed concurrently. A review of the literature reveals scant data. In a series of 50 oncology admissions Silberfarb et al. [40] found nine patients cognitively impaired. The deficits were not attributable to depression or anxiety but were significantly associated with the use of chemotherapy. The sample size was too small to consider the effect of specific cytotoxic agents which are in any case often used in combination. Interferon is being used increasingly to augment the action of cytotoxic drugs. There have been encouraging results in terms of anti-tumour activity but neurotoxicity has been reported [41]. CNS side-effects appear dose-related and reversible on stopping treatment. Impaired concentration and slowness of cerebration have been observed but not systematically measured [42]. Full evaluation of the morbidity associated with interferon should include psychometric assessment. Impairment of cognitive function is not always reversible. Nineteen per cent of a sample of lymphoma patients continued to complain of memory impairment a year after diagnosis, although in remission and off treatment [43]. Deficits ranging from mild intellectual impairment to gross dementia have been reported in retrospective studies of long-term survivors of small cell lung cancer [44, 451. Typically these patients had multimodal therapy and the choice of cytotoxic agents and their scheduling relative to prophylactic cranial irradiation are thought to be important determinants of morbidity. A prospective multicentre study is now underway in Britain to clarify this point. Impaired information processing capacity may require special consideration in doctor-patient communication and can cause significant distress and difficulty to patients in daily living. The importance of assessing cognitive function should not be overlooked.

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Nausea and vomiting

Pharmacological side-effects result from the damage chemotherapy does to non-cancerous tissue. Gastrointestinal problems are among the most common and most distressing, triggered by the local and central action of cytotoxic drugs. The emetic potential of different cytotoxic agents can be specified and there has been considerable research in the development of anti-emetic drugs to combat the problem. Jacobsen et al. [46] found that when pharmacological variables were held constant, individual differences in gastrointestinal distress could be predicted by patients’ past history of nausea, expectations of chemotherapy and level of anxiety, but the study used only subjective reports of gastrointestinal symptoms. If the results are borne out using more objective measures (e.g. observed episodes of emesis), these findings will be important for clinical practice since initial prescription of anti-emetics tends to reflect the properties of the drug therapy rather than individual susceptibility. It has become clear that these same factors contribute to the development of conditioned responses which further add to patients’ distress. Conditioned

responses

The extensive literature on conditioned aversive responses to chemotherapy has already been well reviewed [4749]. A review of prospective longitudinal studies [49] suggested approximately 45% of adult cancer patients experience nausea, vomiting and related symptoms such as taste aversions due to associative learning. Estimates of prevalence vary with the definition of the syndrome, with sample and treatment characteristics and with assessment methods used [50, 511. Conditioned responses can occur before, during or after treatment triggered by cues in any sensory modality associated with the administration of chemotherapy. Anticipatory nausea and/or vomiting, which is easiest to distinguish from drug induced effects, has received most research attention. In clinical practice anticipatory nausea is often unreported and undetected though it can be severe enough to threaten compliance in 10% of cases [48]. Burish and Carey [52] categorize variables associated with anticipatory symptoms into those facilitating the conditioned aversive response (e.g. severe post-treatment nausea/vomiting; long infusions; more emetogenic drugs such as cisplatin) and individual difference variables (e.g. high anxiety and previous motion sickness). Considerable research effort has been expended in evaluating psychological interventions for reducing conditioned responses to chemotherapy. Hypnosis [53], progressive muscle relaxation with guided imagery [54] and systematic desensitization [55] have all proved efficacious in controlled studies. The management of postchemotherapy nausea and vomiting is the critical variable, and as anti-emetic control has improved, a reduction in the severity, if not the prevalence, of conditioned responses has been observed [56]. The hitherto separate pharmacological and psychological research efforts now need to be integrated into developing optimal anti-emetic treatment strategies [52]. Current psychological interventions are too costly in terms of staff time to be as widely applicable as anti-emetic medication and there is a need to consider more cost effective delivery if treatment is to be made available to all who could benefit from it.

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There is also a need now to give more attention which cancer patients experience as distressing.

to other symptoms

and side-effects

P&n Pain management is a major topic in oncology and there are important psychological considerations. A recent study [57] confirms that chronic pain results in increased levels of anxiety and depression in cancer patients and that these disturbances can reduce pain thresholds and complicate the development of appropriate pain management strategies. These issues are not peculiar to patients treated with chemotherapy and will not therefore be reviewed here.

Data about the impact of cancer and its treatment on body image are scarce and largely concerned with the outcome of mutilating surgery [58, 591. Many cytotoxic drugs (e.g. doxorubicin, cyclophosphamide and vinblastine) cause alopecia. Hair regrows when treatment stops and wigs are supplied on request. There is little empirical evidence about the psychological impact of hair loss [60] though the prospect can result in treatment refusal [61]. Disturbances of body image are found clinically to lower self confidence, mood and sexual function and to impair personal relationships and social activity. Phobic avoidance of social situations is not uncommon. These remediable problems, which can be triggered by other features such as weight loss, are often not detected until they have become disabling. Further studies are needed to encourage earlier identification of problems and optimal intervention strategies. Sexual jiitzction The impact of cytotoxic therapy on reproductive function and thus on sexuality is sometimes underestimated. By disrupting the normal production of hormones and interfering with gametogenesis. chemotherapy can induce amenorrhoea and premature menopause in women, infertility in men. Following treatment for cancer up to 50% of previously sexually active patients report some diminution of sexual interest, frequency or performance. Problems were judged severe in IO-20% of cases [62]. Physical debility may compound hormonal problems but some of the difficulties are psychological in origin and the possibility of concomitant affective disorder should be considered. Many patients feel cancer has made them physically unattractive [63]. Clearly the partner’s attitude is also crucial. Improved communication in this sensitive area, both between couples and between doctors and their patients, could relieve many common difficulties [64] though some patients with more severe problems could benefit from specialist counselling.

A summary of recent studies suggest that one-quarter to one-half of cancer patients are likely to be suffering from depression and/or anxiety at any given time [62]. The causes may be biological or psychological, related to the illness and its treatment or coincidental. The risk of psychiatric morbidity is particularly high with adjuvant chemotherapy [65]. Chemotherapy as the first line of treatment may be better tolerated

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although a significant correlation has been reported between the number and severity of side-effects and the development of an affective disorder [43]. The development of conditioned responses has also been linked to mood disturbance [49]. The specific drugs used are relevant. Silberfarb et al. [66] found patients randomized to a regime including vincristine were more depressed than comparable patients randomized to a similar regime without vincristine. There was no significant difference between the groups in tumour response and the mood difference was attributed to action of vincristine on biogenic amines. Interferon induces a constellation of ‘flu-like symptoms. In the context of viral infection these symptoms are commonly associated with depression [67] and a significant increase in anxiety and depression has been reported in patients receiving interferon for chronic hepatitis B infection, relative to untreated matched controls [42]. Assessment of psychological morbidity has not routinely been undertaken among patients treated with interferon and studies are under way in the ICRF Medical Oncology Unit in Edinburgh to monitor this. The value of early detection of psychological morbidity is widely accepted but questions remain about the assessment and treatment of these disturbances. The attribution of symptoms in physically ill patients to somatic and psychiatric causes can be difficult to determine and transient reactions need to be discriminated from clinically significant disorders requiring treatment. The diagnostic validity of three screening measures for this purpose is currently being tested [68-711 but more work is needed to clarify the clinical significance of scores obtained from different populations of cancer patients (e.g. early vs advanced disease). There has been a lamentable dearth of treatment outcome studies. Some evaluation of drug treatment has been documented [72, 731 but given that depressive illness is rarely severe in this group and generally characterized by negative thinking, it is disappointing that Tarrier and Maguire’s work has not been more extensively followed up [74,75]. They found cognitive therapy in conjuction with anti-depressant medication superior to anti-depressants alone with the advantage that cognitive therapy relieved anxiety about recurrence and facilitated longer term adaptation. Future work should, however, control for placebo effects and clarify whether cognitive therapy has a real advantage over less formal supportive therapy in this population. The use of anxiolytic drugs to treat anxiety states is common practice but not well documented [76]. Behavioural techniques are increasingly used. There have been a few well controlled studies but Bridge er al. reported an advantage to relaxation plus imagery over relaxation alone in reducing tension and depression in breast cancer. Both interventions were superior to supportive therapy alone [77]. Elements of cognitive therapy appear in the adjuvant psychological therapy being developed by Greer et al. [38]. Although progammes of psychological support are increasingly being advocated, Feinstein [78] warns against the possibility of doing harm by introducing approaches that upset the defence system the patient habitually uses and the conclusion of Watson’s review of the case for psychosocial intervention would seem still to be valid. She indicates that a selective service is needed and should be targetted at patients at high risk for psychological morbidity. The advantages of one type of support over another remain unproven [79].

136

ANNCULL INFORMATION

NEEDS

AND

COMMUNICATION

Impact of diagnosis and treatment

There is an extensive literature on doctor-patient communication [80] and the particular needs of cancer patients have been well documented [81]. Initially concern focused on the emotional impact of telling the patient the diagnosis [82] but it is increasingly recognized that communication needs to be an ongoing process which will involve the patient’s relationship with a multidisciplinary team [83]. Current literature emphasizes the need to improve the communication skills of doctors and nurses to allow earlier identification of psychological distress and to improve the quality of supportive care offered to all patients [84-871. It is important not to blur the boundaries between the information and advice giving which is an integral part of the role of health care staff and the current burgeoning of interest in counselling. Problems in the development of oncology counselling have been very well summarized by Fallowfield [88] who emphasizes the need for specialist training and support for counsellors whose optimal use as a resource requires better evaluation. Informed

consent

There is a world wide trend towards increasingly stringent informed consent regulations particularly for randomized clinical trials. Recent reports [89,90] highlight medical ambivalence about information requirements which seem to conflict with doctors’ traditional responsibility to the individual patient. An interesting body of work emerging from Canada highlights doctors’ failures to recognize patients’ misconceptions about their treatment [91] and is attempting to define more precisely the information patients need to give their informal consent to any treatment 2921. In Britain attention has recently turned to the implications of offering patients a choice of treatment when there is no concensus about which is more effective (e.g. recent studies reported patients’ ability to play a part in selecting their own primary treatment for operable breast cancer without inducing added distress [93.94]). Other cancer patient groups need to be considered and there is a continuing need for empirical study of the information process involved in decision making by both doctors and patients about cancer treatment and clinical trials.

QUALITY

OF LIFE STUDIES

Traditionally the effectiveness of any cancer treatment is assessed in terms of tumour response and patients’ survival time. As the morbidity associated with treatment was increasingly recognized. the importance of evaluating the quality as well as the duration of that time has been recognized. No review of the psychological aspects of cancer and chemotherapy would be complete without reference to the vast body of work which has grown around efforts to define and measure the ‘quality of life’ of cancer patients. It is beyond the scope of this article to undertake a comprehensive review of this literature. Some excellent summaries have already been published [95-981. This field encapsulates all the problems of psychosocial oncology already mentioned. There has been a lack of theory or even definition to guide research.

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The consensus now tends to view quality of life (QL) as a multidimensional dynamic concept requiring subjective assessment, repeated at intervals over time. Minimally it includes some assessment of the physical experience of illness and treatment, and the impact on personal and social functioning. There have been immense methodological and practical problems in developing adequate measures of QL. Some authors have sought a global index while others have used different combinations of domains with problems then of how to weight subscale contributions to some aggregate score. There are conflicting demands for measures to be brief enough for ease of administration as an endpoint in clinical trials and yet comprehensive enough to summarize meaningfully the patients’ experience. There is no single QL measure for cancer patients which can be universally recommended. The state of the art, as for all good research, depends on having a specific question to ask and selecting the best of the available techniques to address it. SUMMARY

Research in the psychological aspects of cancer and chemotherapy has reached an exciting stage of development. More acceptable standards of scientific rigour are being applied to thinking and research, spanning a wide range of important issues from prognostic indicators to the evaluation of treatment trials. It is important to remember that patients do not exist in isolation and that the impact of disease and treatment is also felt by their care givers. The burden which falls on spouses and other primary carers and the importance of their contribution to patients’ adaptation to illness should not be underestimated [99]. By the same token the emotional demands particularly on nursing and junior medical staff are increasingly recognized with developing interest in optimal means of providing staff support [loo]. Thus the field is still expanding. It requires the continuing collaborative effort of a wide range of professional disciplines to improve our understanding of the psychological aspect of oncology for all cancer patients and those who care for them. REFERENCES I. 2. 3. 4. 5. 6. 7. 8. 9.

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