Introduction

Approximately 1,200 individuals are diagnosed with primary brain tumour every year in Sweden. In most cases, they have tumours of glial origin. Gliomas are graded according to their aggressiveness. High-grade gliomas (HGG, grades III and IV) are very aggressive with short survival time, while low-grade gliomas (LGG, grades I and II) grow more slowly [1]. Pignatti et al. [2] reported that the median survival time for patients with LGG is 6–7 years but can range up to decades.

Symptoms of LGG depend on the size and the location of the tumour, rate of growth and consequences of increased intracranial pressure [1]. Frequent symptoms are headache, nausea, vomiting, seizures, fatigue and sleepiness [2–4]. Most patients have cognitive dysfunction of various degrees, from mild dysfunction with good information processing and good performance to severe dysfunction with problems in most cognitive domains [5–7]. Neurological deficits also occur; in most cases, motor impairment limited to difficulties with function in the upper limbs [2, 6].

Symptoms of LGG may have implications for the patients’ quality of life. Quality of life in cancer patients may be designated as a multidimensional concept that embodies physical, social and psychological aspects of the patients’ life and the influence of disease-related symptoms [8]. An earlier study showed that patients with LGG had significantly worse quality of life than those with low-grade haematological malignancies [4]. They also had worse quality of life than healthy controls with regard to general health perception, vitality, social functioning and mental health [7].

The consequences of the tumour for everyday life and the uncertainty of the future make great demands on the patients’ ability in coping. Coping may be defined as “cognitive and behavioural efforts to manage specific external and/or internal demands that are appraised as taxing or as exceeding the resources of the person” [9], p 141). Coping has two basic functions, either to manage or alter the problems causing distress or to regulate the emotions caused by these problems. The choice of coping depends on the individuals’ cognitive appraisal of the situation and evaluation of what can be done. In a stressful encounter, people use several different coping strategies [9–11].

Caring for patients with brain tumours is a difficult challenge, as the disease presents not only a threat to life but also specific neurological symptoms which deserve particular attention [12, 13]. During the past decades, many different support and educational groups for cancer patients have been initiated, described and evaluated in the literature [14]. However, no studies about support specifically for patients with LGG are to be found in the literature. One explanation of this is the lack of studies with focus on these patients’ self-reported problems. It was against this background that the present study was undertaken. Its principal aim was to describe function, quality of life and coping with illness-related problems in patients with LGG to evaluate the need of support. A second aim was to investigate how function, quality of life and coping were related.

Materials and methods

Design

The study was cross-sectional and had a descriptive and correlative design. Patients with the diagnosis LGG living in a well-defined geographical area and reported to the Swedish Regional Cancer Register were included. Data was collected by means of questionnaires and an examination by a neurologist.

Sample selection

Patients were selected to the study from the Swedish Regional Cancer Register [15] on 15 November 1999. Patients with a diagnosis of LGG, aged above 18 years and living in the county of Örebro [16] were included. Those who had severe cognitive problems resulting in obvious difficulty in communicating were excluded. Low-grade gliomas (LGG) were defined as tumours of glial origin with malignancy grades I or II according to WHO 2002 or the previously used Kernohan classification [17]. The neurologist responsible for the particular patient made the judgement as to whether they met the inclusion and exclusion criteria for the study.

Forty-seven patients matched the criteria. Two patients with grade III (HGG) were also considered eligible for participation, as they had a clinical pattern of LGG type with exceptionally long periods of stable disease. The patients received written information about the study by post at their home address. A week later, a phone call was made offering further information about the study and enquiring whether they were willing to participate. In the written and the oral information, it was clearly stated that participation was voluntary and that confidentiality was assured. Out of the 49 patients considered eligible for the study, ten declined to participate. Thus, the final study group consisted of 39 patients, corresponding to an 80% participation rate. The research ethics committee of Örebro University Hospital approved the study.

Sample

The study group of 39 patients comprised 27 men (69%) and 12 women (31%). The mean age was 47 years (SD: 14, range: 21–79). Twenty-four patients (62%) were married or cohabiting, while the others were unmarried, separated/divorced or widower. Half the patients had had the diagnosis for more than 10 years and one fourth for more than 26 years (median: 10, quartiles: 4–26, range<1–47). The histological diagnoses were the following: astrocytomas grades I–II (n=16) or grade III (n=1), cerebellar astrocytomas grades I–II (n=5), oligodendrogliomas grades I–II (n=7), mixed oligoastrocytomas grades I–II (n=4) or grade III (n=1), ependymomas grade II (n=4) and other low-grade glioma (n=1). The patients had received different combinations of treatment. Twenty-nine patients (74%) had undergone surgical resection. Of these, 12 had had additional treatment with radiotherapy and six had additional treatment with both radiotherapy and chemotherapy. Another three patients (8%) had been treated with radiotherapy only and two (5%) with radiotherapy and chemotherapy in combination. For five patients (13%) with a long history of disease, complete data about treatment was missing. The ten patients who declined to participate did not differ from the participating patients with regard to age, sex or the duration of the disease (n.s.).

Instruments

A neurologist (AP) assessed the patients’ function in connection with a neurological examination at the neurological outpatient clinic. Questionnaires with instruments for measuring coping and quality of life were administered to the patients in their homes.

Function

The patients’ level of function was assessed by means of observations of motor function and a neurological examination. If needed, the neurologist asked complementary questions about functional ability. Level of function was graded according to the WHO performance status scale [18]. The WHO scale consists of the following categories: “able to carry out all normal activity without restriction” (0), “restricted in all strenuous activity but ambulatory and able to do light work” (1), “ambulatory and capable of all self-care but unable to carry out any work” (2), “capable of only limited self-care, confined to bed or chair more than 50% of waking hours” (3) and “completely disabled, cannot carry on any self-care, totally confined to bed or chair” (4).

Quality of life

The patients’ quality of life was measured with the European Organization for Research and Treatment of Cancer Core Quality of Life Questionnaire (EORTC-QLQ-C30) [19]. It is a 30-item questionnaire containing the following multi-item scales: physical functioning (five items), role functioning (two items), cognitive functioning (two items), emotional functioning (four items), social functioning (two items), fatigue (three items), pain (two items), nausea/vomiting (two items) and global quality of life scale (two items). In addition, single items assess symptoms commonly reported by cancer patients such as dyspnoea, appetite loss, sleep disturbance, constipation and diarrhoea (five items). The questionnaire also includes an item for assessment of the financial impact of the disease (one item). The items concerning physical functioning and role functioning have dichotomous response alternatives. The two items for ratings of global quality of life use 7-point visual analogue scales with “very poor” and “excellent” as endpoints. One of these items assesses overall physical condition, and the other item assesses overall quality of life during the past week. All other items are scored on a 4-point Likert scale from “not at all” to “very much” as response alternatives. As recommended, single items and multi-items in the EORTC-QLQ-C30 were linearly transformed to a 0–100 scale. In the case of the five functioning scales and the scale for global quality of life, higher scores represent better level of functioning/quality of life. In the case of the symptom scales and the scale for financial impact, higher scores indicate higher degree of symptoms and worse financial situation [19, 20].

Reliability of the multi-item scales in the EORTC-QLQ-C30 was evaluated with Cronbach’s alpha. Alpha above 0.7 indicates satisfactory internal consistency [21]. The scales for role functioning and nausea/vomiting had low reliability, with alpha 0.29 and 0.53, respectively. The other multi-item scales had satisfactory internal consistency, with alpha ranging from 0.71 to 0.94.

Coping

Coping was assessed with the Ways of Coping Questionnaire (WCQ) [22]. The scale has previously been translated into Swedish and used for Swedish patient populations [23]. Lundqvist and Ahlström [24] have confirmed that the Swedish version has satisfactory psychometric properties in clinical studies.

The WCQ includes 66 items or statements about ways of coping. The respondents are asked to recall a stressful situation considered as difficult or troubling. In this study, the instructions emphasized that the stressful situation had to be related to the respondent’s disease. Ratings of how often each type of coping is used in the stressful situation are made on a 4-point Likert scale with “does not apply or not used” (0), “used somewhat” (1), “used quite a bit” (2) and “used a great deal” (3) as response alternatives [22].

The WCQ has eight subscales representing different coping strategies. Fifty of the 66 items are included in the subscales as recommended in the manual [22]. The coping strategy “confrontive coping” (six items) is described in the manual as aggressive efforts to alter the situation and suggests some degree of hostility and risk-taking, “planful problem-solving” (six items) is described as deliberate problem-focused efforts to alter the situation coupled with an analytic approach to solving the problem, “distancing” (six items) is described as cognitive efforts to detach oneself and to minimize the significance of the situation, “self-controlling” (seven items) is described as efforts to regulate one’s feelings and actions, “seeking social support” (six items) is described as efforts to seek emotional, informational and tangible support, “accepting responsibility” (four items) acknowledges one’s own role in the problem and attempts to put things right, “escape-avoidance” (eight items) is described as wishful thinking and behavioural efforts to escape or avoid the problem, and “positive reappraisal” (seven items) is described as efforts to create positive meaning by focusing on personal growth [22].

Reliability tests showed that five of the eight subscales had satisfactory internal consistency, with Cronbach’s alpha ranging from 0.72 to 0.82. Somewhat lower alpha was found in the case of the subscales for self-controlling (0.68), escape-avoidance (0.62) and confrontive coping (0.69).

Statistics

There are two methods for scoring the WCQ subscales. Raw scores give an idea of the extent to which items from a particular subscale are used. Relative scores describe the overall contribution of items from a subscale to the coping process relative to the other subscales [22]. Both raw scores and relative scores were calculated for the subscales in the WCQ.

Besides descriptive statistics, Spearman’s rank correlation coefficient was used for investigating relationships between function, quality of life and coping strategies. Spearman’s rank correlation is the appropriate choice for analyses of ordinal scales [25]. Only results of the correlation analyses with p < 0.01 were considered statistically significant. The statistical computer program, SPSS 14.0, used for statistical analyses, gives the exact p-value except when the p-value is less than 0.001.

Results

Function

The neurologist’s ratings of the patients’ level of function showed that 15 patients (39%, n=39) were able to carry out all normal activity without restriction, while eight (21%) were unable to carry out strenuous activity but able to do light work. Another 12 patients (31%) were ambulatory and capable of all self-care but unable to carry out any work. One patient (2%) was capable of only limited self-care and in bed or chair half the waking hours. Two patients (5%) were completely disabled and totally confined to the bed or chair. Data on one patient (2%) was missing. There was no significant correlation between the neurologist’s rating of the patients’ level of function and the patients’ age or the duration of the disease (n.s.).

Quality of life

Descriptive statistics for scores of the EORTC-QLQ-C30 (Table 1) showed that the median values were lower for self-reported role, cognitive and emotional functioning than for the other functioning scales. Thus, the patients reported more difficulties in these domains than in physical and social functioning. The median values were higher for symptoms of fatigue, sleep disturbance and pain, which means that the patients reported more problems with these symptoms than with other symptoms (Table 1). One of the items in the subscale for fatigue concerned tiredness. The patients’ ratings revealed that 30 patients (77%) had felt tired during the last week, from “a little” to “very much”. The rest of the patients had “no problems at all” with tiredness. Twenty-one patients (54%) reported sleep disturbances and 21 patients reported pain (54%), varying from “a little” to “very much”. Few patients had economic problems related to the disease.

Table 1 Self-reported functioning, global quality of life and symptoms in patients with low-grade gliomas (n=38)
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Concerning the ratings of global quality of life, one fourth of the patients had scores of 50 or less (Table 1). One of the two items in the global quality of life scale runs as follows: “How would you rate your overall quality of life during the past week?” Seventeen patients (45%) scored 4 or less on the 7-point visual analogue scale for this item, indicating low overall quality of life. No one reported the overall quality of life to be “very poor”, which was the endpoint of the scale. Analyses of relationships between the item evaluating overall quality of life, the other multi-item scales and single items in the EORTC-QLQ-C30, revealed that there was a significant relationship between overall quality of life and fatigue (rho: −0.70, p< 0.001), emotional functioning (rho: 0.59, p< 0.001), cognitive functioning (rho: 0.57, p< 0.001), pain (rho: −0.51, p=0.001), physical functioning (rho: 0.50, p=0.002), social functioning (rho: 0.48, p=0.002) and role functioning (rho: 0.46, p=0.004). Neither age, sex, marital status nor disease duration was related to overall quality of life (n.s.).

Coping

Five of the 66 items in the WCQ were rated higher than the others (Table 2). They were used by a majority of the patients (79–82%) and had the median value, 2, corresponding to “quite a bit”. The relative scores for the subscales (Table 3) showed that positive reappraisal dominated as coping strategy, followed by seeking social support, distancing, self-controlling and escape-avoidance. Planful problem-solving and confrontive coping, which are problem-focused coping strategies, were less used. Accepting responsibility was used least of all. There was no significant relationship between coping strategies and age, sex, marital status or disease duration (n.s.).

Table 2 The most frequent statements about coping in patients with low-grade gliomas (n=38)
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Table 3 Strategies for coping with stressful illness-related situations reported by the patients with low-grade gliomas (n=38)
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Relationships between function, quality of life and coping strategies

Correlation analyses showed that there was a significant relationship between the neurologist’s ratings of the patients’ level of function and the patients’ ratings of their social functioning (rho: −0.61, p<0.001), role functioning (rho: −0.57, p<0.001), physical functioning (rho: −0.55, p<0.001) and symptoms of appetite loss (rho: 0.47, p=0.003) in the EORTC-QLQ-C30-scale. Thus, ratings of low level of function made by the neurologist were associated with low levels of self-reported functioning in these domains and with increased symptoms of appetite loss. The neurologist’s ratings of the patients’ level of function had no relationship with any other of the scales or items in the EORTC-QLQ-C30 (n.s.) or with choice of coping strategy (n.s.).

Correlation analyses of relationships between the patients’ ratings of coping in the WCQ and their ratings of the multi-item scales and single items in the EORTC-QLQ-C30, showed that coping by escape-avoidance was significantly related to emotional functioning (rho: −0.58, p<0.001). Confrontive coping was significantly related to financial impact of the disease (rho: 0.59, p<0.001) and role functioning (rho: −0.53, p=0.001). There was no relationship between coping and the other scales or items in the EORTC-QLQ-C30 (n.s).

Discussion

The neurologist’s ratings of the patients’ level of function showed that nearly all of the patients with LGG were capable of self-care, but less than half were able to carry out normal activities without restriction. With regard to self-reported problems, the majority of them reported tiredness and about half of them had sleep disturbances. It confirmed results of an earlier interview study, which showed that fatigue and sleepiness were the most prominent problems experienced by patients with low-grade glioma [3]. According to a review study, fatigue is a devastating symptom in brain tumour, which requires specific information and education for the patients and their families. Light daily exercise to preserve physical fitness, a healthy diet and regular sleeping should be encouraged [13]. Half the patients in this study had felt pain during the last week. The aforementioned review study also showed that pain occurs in half of brain tumour patients [13].

One fourth of the patients in this study had scores less than 50 on the cognitive functioning scale, indicating low level of cognitive functioning with difficulties in concentration and memory. Cognitive impairment may be a result of the tumour itself but also of the treatments [13]. An earlier study found that antiepileptic drugs may cause cognitive impairment in patients with LGG [26]. A disadvantage of the present study was that symptoms of epilepsy were not included in the questions. About 80% of low-grade gliomas have been found to involve epilepsy. It could be an important risk factor for difficulties in everyday life [13].

Compared with patients with HGG, who answered the EORTC-QLQ-C30 about 2 months after diagnosis [20], the patients in the present study reported better physical, role and social functioning. They reported difficulties with cognitive and emotional functioning to the same extent as the patients with a more aggressive tumour. Ratings of global quality of life were similar in both patient groups. With regard to symptoms, the patients in this study reported less fatigue and nausea but had more pain. Ratings of the other symptoms were similar in both patient groups.

The version of EORTC-QLQ-C30 used in this study asks patients to make overall assessments of “physical condition” and “quality of life”, which are then combined into a global quality of life scale. For the purpose of making correlation analyses of significant relationships with quality of life experienced without influence of the physical condition, the two items were separated. Nearly half the patients (45%) had scores indicating low overall quality of life. The results of the correlation analyses, investigating relationships between overall assessment of quality of life and the other scales in EORTC-QLQ-C30 showed that fatigue had the strongest relationship with overall assessment of quality of life. A negative relationship between fatigue and quality of life has also been observed in patients with HGG [27]. Overall assessment of quality of life also had a moderate relationship with emotional and cognitive functioning and a somewhat weaker relationship with physical, social and role functioning and pain. This result suggests that mental problems have a stronger impact on experience of quality of life than physical ones. The assessment of level of function by the neurologist had no relationship with the patients’ self-assessment of overall quality of life.

The relationships found between the neurologist’s ratings of the patients’ level of function and self-reported role, social and physical functioning in this study confirm the results of an earlier study showing that the patients with lower levels of observed function usually had considerable handicap, more cognitive problems and more psychological symptoms [28]. In the present study, social functioning concerned relationship with family and ability to carry out social activities, and role functioning concerned the ability to carry out activities at home. The results suggest that observations of the patients’ function could indicate the need of social support and family support. There was also a significant relationship between impaired observed function and loss of appetite. Change in appetite/weight is common in patients with brain tumour. Appetite loss can stem from altered taste, nausea, dysphagia, depression, fear of eating or effects of treatment [13]. Health care staff needs to find the reason for appetite loss to prevent malnutrition.

Out of the five most used ways of coping, four were aimed at regulating emotions by means of escaping, changing the significance of the situation or creating positive meaning. Only one of them had a more problem-focused character involving aggressive efforts to alter the situation. The analyses of the subscales confirmed the dominance of emotion-focused coping. Emotion-focused coping strategies are usually dominant in stressful situations where nothing can be done [9, 10, 29]. Comparisons with coping in patients with other chronic neurological diseases revealed that coping by positive reappraisal and escape-avoidance were more frequent among the patients with LGG in this study than among patients with muscular dystrophy (MD) and post-polio syndrome (PPS) [23]. Thus, the patients with LGG more often tried to change the significance of the situation or tried to escape mentally. A possible explanation is that the patients with MD and PPS experience loss of function as the major threat, while patients with LGG have to manage not only loss of function but also the always imminent threat of death. It was also observed in this study that use of coping by escape-avoidance was associated with lower level of emotional functioning—that is, greater degree of tension, irritation, depression and worry. This corresponds to the results of a review study indicating that patients with cancer who use coping by escape-avoidance usually experience a high level of emotional distress [30]. There has been an immense amount of research about coping during the last 20 years, mainly based on questionnaires. The most widely used instrument to assess coping is the WCQ [31]. However, this study was the first research about coping with LGG by means of questionnaire. Further research is needed to verify our results.

Increasing attention has been paid in the literature to intervention for the purpose of improving the patient’s ability to cope to the extent that there can be “successful problem-solving” or acceptance of the situation. The first step for designing an intervention consisting of psychological care or coping support is to consider the nature and controllability of the stressors faced by the patient and to identify whether the coping used is related to high or low quality of life [32]. Coping support means the development of coping skills based on the specific problems the patient experiences in everyday life. Thoits [33] has developed a model for support related to coping [9]: 1) Instrumental support denotes what is done to enhance the person’s capacity for problem-focused coping; 2) Informative support denotes advice, guidance and other such means of backing up both problem-focused and emotion-focused coping; 3) Emotional support denotes what is done to facilitate the person’s capacity for emotion-focused coping [33, 34].

One threat to the internal validity of this study was false responses because of the patients’ cognitive dysfunction. For that reason, patients with severe cognitive problems and obvious difficulty in communicating were not included. This was dictated by the desire to obtain results as true as possible, without influence of cognitive impairment. Also, the answers in the questionnaires were scrutinized before analysis regarding accuracy and logical pattern. One patient was then excluded from statistical analysis because of several missing items in the EORTC-QLQ-C30 and the WCQ. Still, it could be asked whether cognitive problems have influenced the results of the study. Low reliability of the scales in the instruments used could be explained by cognitive difficulties concerning understanding. In a study of patients with HGG, it was questioned whether cognitive problems explained that the scale for cognitive functioning had very low reliability (α=0.34) [20]. In our study, one-fourth reported somewhat low levels of cognitive functioning, but the reliability of the cognitive functioning scale was good (α=0.71). Instead, it was low reliability of the role functioning scale in the EORTC-QLQ-C30 (0.29). It was also observed in studies of patients with HGG [20] and patients with lung cancer [19]. In a later, revised version of the EORTC-QLQ-C30, the two items dealing with role functioning have been reworded. The revised version was not available in Swedish translation when this study started. Some of the scales in the WCQ had questionable reliability, but taken together, the reliability of the scales was better in this study than in studies of patients with MD and PPS [23].

The WCQ consists of 66 items, 16 of which are not assigned to any scale [22]. From a research-ethical point of view, expecting disabled people to complete an instrument in which a fourth of the items are not to be used is highly objectionable. First, patients with poor resources will have to make an unnecessarily large effort. Second, the patients may have difficulty in concentrating throughout the questionnaire, which will increase the error variances and lead to ambiguous results. Therefore, it is recommended that these 16 items be deleted from WCQ in future research [24].

Correlation analyses are an exploratory method for investigating relationships among many variables. A problem is that even with a modest number of variables, the number of significant correlation coefficients is large [25]. So that correlation coefficients should not be significant purely by chance, p<0.01 was chosen as the significance level. However, a lower significance level increases the risk of missing genuine associations. Further research with larger samples is needed to verify our results.

Implications

The results of a previous qualitative study within the same study group showed that persons with low-grade glioma experienced a wide range of problems influencing almost every area of life [35]. Previous studies have revealed that long-term survivorship is associated with more problems than generally expected and that manifold interventions in the psychosocial area during long-term cancer survival are required [36]. The most prominent consequences of the LGG in this study were in the domains Role, Cognitive and Emotional functioning. Problems with pain, fatigue and sleep disturbance were most frequent. These results indicate that a multidisciplinary team is needed for assessment and treatment of the different problems in patients with low-grade gliomas. Furthermore, the results of this study suggest that special attention should be paid to patients who use escape-avoidance as a means of coping. This coping strategy was associated with emotional distress and such patients may be in need of special support. These results indicate the need of developing a support programme tailored to the different medical, physical and psychosocial needs of persons with LGG. Further research about these patients and their family situation and about encounters with health-care staff, is urgently required to ensure quality of care.