Psychosomatics 46:233-243, June 2005
© 2005 The Academy of Psychosomatic Medicine
Relationship of Tumor Burden and Patients’ Minimization of Distress in Facing Surgery for Gastric Cancer
Jan Svedlund, M.D., Ph.D.,
Marianne Sullivan, Ph.D.,
Bengt Liedman, M.D., Ph.D., and
Lars Lundell, M.D., Ph.D.
Received Feb. 2, 2004; revision received July 22, 2004; accepted Aug. 12, 2004. From the Psychiatry Section, Institute of Clinical Neuroscience; the Health Care Research Unit, Institute of Internal Medicine; and the Department of Surgery, Sahlgrenska University Hospital, Göteborg University, Göteborg, Sweden. Address correspondence and reprint requests to Dr. Svedlund, Department of Psychiatry, Sahlgrenska University Hospital, SE-413 45 Gothenburg, Sweden; jan.svedlund{at}neuro.gu.se (e-mail).
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ABSTRACT
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Patients with gastric cancer considered amenable to a curative surgical procedure on the basis of a conventional preoperative workup (N=98) answered health-related quality-of-life questionnaires and completed a psychiatrist’s interview before the intervention. All patients were blinded to the type of surgical procedure that would ultimately be performed; 64 patients eventually received a potentially curative resection, and 34 had palliative surgery. The curative resection group reported significantly more hopelessness before the operation than the palliative surgery group. The latter group had more eating dysfunction but minimized their distress to a greater degree than those with a more limited tumor burden. Eating dysfunction, hopelessness, and the tendency to minimize distress were independent predictors of prognosis. The findings highlight the need for careful medical interviewing to enhance patient-physician communication about symptoms and signs of malignant diseases.
Key Words: Gastric cancer • stress • coping • depression • quality of life
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INTRODUCTION
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Gastric carcinoma is one of the main causes of mortality by cancer.1 Although the incidence is decreasing in the Western world, gastric cancer still remains the second most common cancer worldwide and therefore poses a significant health problem.2 Preventive measures are as yet largely nonexistent, and beneficial effects of different adjuvant radio- or chemotherapy regimens remain to be proven.3 Only radical surgery offers these patients a chance of cure, but the prognosis depends fundamentally on the extent of transmural tumor invasion and local spread at the moment of treatment.4
Much effort has been made to increase the detection of early lesions of gastric cancer. In low incidence areas, such as the Western world, screening programs are not cost-effective. Instead, detection depends on whether people seek medical attention at an early stage and on whether physicians notice the symptoms and signs and are ready to embark on a diagnostic workup program.5 The increased improvement and availability of endoscopic and other diagnostic measures are of course essential in shortening doctors’ delay in initiating workups; but another dimension that must be incorporated in the diagnostic approach is physicians’ sensitivity to patients’ beliefs about the significance of physical symptoms.
One characteristic of gastric cancer patients is the unspecific nature of the symptoms. The insidious onset of often vague gastric cancer symptoms may give the patient the opportunity and time to mobilize psychological defense mechanisms such as denial and rationalization. If such mechanisms are involved when the patient seeks medical attention, it is important for the physician to be aware of them in order to better interpret the information given by the patient.
The aim of the present study was to elucidate and describe psychological mechanisms and reactions that are operational in gastric cancer patients who are referred for surgical treatment and to clarify the relationships between health perception (reflected in measures of health-related quality of life), psychopathology, social maladjustment, and tumor status in patients with carcinoma of the stomach that is considered amenable to a curative surgical procedure.
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METHOD
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Study Design and Treatments
Consecutive patients with carcinoma of the stomach (antrum, corpus, and fundus) were preoperatively screened for tumor status and general physical fitness and to evaluate their suitability for a major surgical procedure such as total or subtotal gastrectomy. All patients (N=98) considered amenable to a curative surgical procedure after the preoperative workup were subsequently asked to participate in a controlled long-term outcome study of reconstructive procedures with the aim of determining consequences of gastrectomy for patients’ quality of life.6 They all agreed to participate.
All operations were performed by surgeons specialized in upper gastrointestinal surgery. The final decision regarding treatments was made at the time of the surgery. In 64 patients the surgeon considered a curative resection to be feasible, and for these patients a potentially curative operation was performed. Use of curative resection meant that all visible tumor could be resected (TNM stage T3, NX, M0). Two patients with T4 tumors with extension to the colonic mesentery and the left liver lobe were also considered for a curative operation. At the time of surgery, frozen section methods were used to assure tumor-free margins to the esophagus. There was a complete accordance between the frozen section findings and the final histopathology reports. Thirty-four patients were, at the time of exploration, found to have a tumor burden that was not amenable to curative resection, and 20 of these patients had in fact an exploratory laparatomy only. Data on patients’ sociodemographic and clinical characteristics, current medications, and smoking and drinking habits are presented in Table 1 and Table 2. The surgical and patient selection procedures were described in detail elsewhere.6,7
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TABLE 1. Sociodemographic Characteristics at Study Admission of Gastric Cancer Patients Who Later Underwent Potentially Curative Versus Palliative Proceduresa
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TABLE 2. Clinical Characteristics at Study Admission of Gastric Cancer Patients Who Later Underwent Potentially Curative Versus Palliative Proceduresa
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All patients were interviewed before surgery and rated by one of two psychiatrists. Both the raters and the patients were blinded to the type of surgical procedure to be performed, as the final decision regarding treatment (curative versus palliative) was made at the time of surgery. The interview included self-report measures and was conducted within 1 week before surgery after the diagnosis had been established and disclosed to the patient. One patient refused to answer questions about mental symptoms, and two patients were not able to complete the interview because of fatigue. The ratings were based on the patient’s reports covering the week before the assessment. The duration of the interview varied, but usually less than 90 minutes were needed.
The study protocol was approved by the local ethics committee, and informed consent was obtained from each patient at entrance to the study.
Evaluation of Quality of Life
At present no single definition of quality of life has been universally adopted. On the other hand, there is general agreement on a set of dimensions of health-related quality of life, and a few standardized instruments have received considerable recognition. On the basis of clinical experience, it is considered vitally important to include patients’ own assessment of symptoms, physical functioning, role performance, and well-being, as well as their general health perceptions, in an operational definition of quality of life.8–12 This approach to evaluating quality of life was adopted in the present study.
Interviewer Rating Scales
Gastrointestinal Symptom Rating Scale
The Gastrointestinal Symptom Rating Scale13 is an interview-based rating scale designed to evaluate a wide range of gastrointestinal symptoms. It is a widely used measure with proven psychometric features and clinical relevance.13,14 The Gastrointestinal Symptom Rating Scale includes 15 items rated on a 7-step scale on which steps 0, 1, 2, and 3 are defined by descriptive anchors specified for each item, with 0 indicating absence and 3 an extreme degree of the symptom. Half-step ratings are used when not all of the criteria for step 0, 1, 2, or 3 are met. The following five dimensions were identified on the basis of a factor analysis14 and were used in this study: Abdominal pain syndrome (abdominal pain, sucking sensations, nausea), reflux syndrome (heartburn, acid regurgitation), indigestion syndrome (borborygmus, abdominal distention, eructation, increased flatus), diarrhea syndrome (increased passage of stools, loose stools, urgent need for defecation), and constipation syndrome (decreased passage of stools, hard stools, feeling of incomplete evacuation). The Gastrointestinal Symptom Rating Scale data are presented as syndrome scores and a total score.
Eating Dysfunction Scale
A scale consisting of one disease-specific item that measured eating dysfunction was developed for this study. The Eating Dysfunction Scale had a structure similar to that of the Gastrointestinal Symptom Rating Scale and was expected to share the same psychometric properties. The item was constructed on the basis of clinical experience and reports in the literature on symptoms associated with eating in patients who had undergone gastrectomy. The item was rated on a 7-step scale on which steps 0, 1, 2, and 3 were defined by descriptive anchors; half-step ratings were used when not all of the criteria for step 0, 1, 2, or 3 were met. The rating was based on an open-ended clinical interview in which the patient was encouraged to describe in his or her own words any symptoms associated with eating. The interviewer then decided which steps in the scale had not been fully covered and asked the patient to elaborate on these areas. If the information provided was not sufficient for the rating, more specific questions were asked. The instructions to raters were as follows: "Rate according to symptom intensity, frequency, and impact on daily living, as well as the size of the meal. Distinguish from reduced appetite and specific food intolerance." The following descriptive anchors were included in the scale: 0, no eating dysfunction; 1, early postprandial feeling of satiety but the patient is able to eat a normal sized meal, although with some discomfort and with a need for extra meals; 2, need for meals of smaller than normal size, and eating is associated with frequent episodes of prolonged discomfort, that is, pain or fatigue interfering with many social activities; and 3, inability to eat and need for parenteral nutrition.
Karnofsky Performance Status Scale
The Karnofsky Performance Status Scale15 emphasizes physical performance and dependence. The patients were rated by the psychiatrist after the interview was completed. The scale is a single-item measure describing the physical dimension of quality of life, rather than social and psychological aspects. It is thus limited as an indicator of quality of life, but it does provide information that is complementary to patients’ subjective assessment of somatic symptoms. The scale score ranges from 0 (dead) to 100 (normal status), with descriptive anchors for every tenth step of the scale.
Self-Report Measures
Body Symptom Scale
The original Body Symptom Scale16 consists of 36 short descriptions of various common somatic complaints aggregated into five dimensions of subjective bodily discomforts. Scores range from 1 to 4 for each item, with a high score implying more discomfort. In this study, the three most relevant dimensions were used; they were neurasthenic symptoms (nine items), vegetative symptoms (seven items), and digestive symptoms (six items). Scores were calculated for each dimension, and an overall Body Symptom Scale score was calculated. In this study, the scale was usually self-administered, after being introduced by the psychiatrist. However, if the patient preferred, the scale was administered by the interviewer.
Mood Adjective Check List
The Mood Adjective Check List16 was used for self-assessment of emotional state and mental well-being. It consists of 71 adjectives measuring six bipolar dimensions and constitutes a comprehensive evaluation of several aspects of mood. For our study, the three main dimensions, with a total of 38 items—pleasantness/unpleasantness, activation/deactivation, and calmness/tension—were used, as in the study by Lundqvist et al.17 The items were presented in random order to the patient, who rated them in relation to his or her current mood on a scale from 1 to 4, on which high scores indicate emotional well-being. Scores were calculated for each dimension, and an overall Mood Adjective Check List score was calculated. Similar to the Body Symptom Scale, the Mood Adjective Check List was as a rule self-administered.
Sickness Impact Profile
The Sickness Impact Profile18,19 contains 136 items that describe functional limitations across 12 well-defined areas of everyday living: ambulation, body care and movement, mobility, social interaction, emotional behavior, communication, alertness behavior, sleep and rest, home management, work, recreation and pastimes, and eating. Each item describes a sickness-related dysfunction. A scale score is calculated for each of the 12 areas from weighted item scores reflecting the severity of dysfunction. The scale scores are expressed as a percentage of maximum dysfunction. A physical index is calculated from scores on three scales (ambulation, body care and movement, mobility), a psychosocial index from scores on four scales (emotional behavior, social interaction, alertness behavior, communication), and a total index from scores on all 12 scales. Higher scores imply more dysfunction. In this study, the Sickness Impact Profile was interviewer-administered.
Evaluation of Psychopathology and Maladjustment
Comprehensive Psychopathological Rating Scale
The original Comprehensive Psychopathological Rating Scale20 is composed of 65 interview-based scaled items covering a wide range of psychiatric signs and symptoms and has been used extensively. It was designed either to be applied in full or to be used as a pool of items from which subscales can be drawn depending on the project for which the rating is used. For this study, 22 items appropriate for patients with gastric cancer were extracted. All items are rated on a 7-step scale, on which 0, 1, 2, and 3 have been operationally defined. Half-step ratings are used to increase the sensitivity. The higher the score, the more pronounced is the sign or symptom. On the basis of clinical experience, the items were grouped into three dimensions: neurasthenic syndrome (seven items), anxiety syndrome (seven items), and depressive syndrome (nine items). The Comprehensive Psychopathological Rating Scale data are presented as syndrome scores and a total score.
Hopelessness
The Comprehensive Psychopathological Rating Scale does not cover affects of helplessness and hopelessness that reflect insufficient coping while facing surgery shortly after having received information about the diagnosis. The ability to tolerate feelings of hopelessness may be aided by the psychic defense of repression or denial. Measurement of how the patient masters feelings of hopelessness had a direct bearing on the aim of our study. Therefore, we constructed a measure of hopelessness consisting of one item. The item was analogous to the Comprehensive Psychopathological Rating Scale items and could be expected to share the same psychometric properties. The instructions to raters were as follows: "Rate according to intensity, frequency, and duration of feelings of hopelessness reflecting insufficient capacity required to cope with the situation." The possible scores were 0, believes in a change for the better and has faith in available resources, even though the situation may be troublesome; 1, despairs and doubts at times whether there will be opportunities to straighten things up; 2, frequently experiences that he or she lacks the capacity required to cope with the situation; 3, constant feelings of helplessness and hopelessness, he or she has given up, sees no way to master the situation.
Patient’s Distress and Minimizing
Two items were extracted from the Structured and Scaled Interview to Assess Maladjustment21 in accordance with the rules of the instrument and were used for between-group comparisons of prognostic variables. One item, "patient’s distress," was included as a supplement to the Karnofsky Performance Status Scale to cover the extent of patients’ overall distress. This item reflected the intensity of distress related to the illness and the extent to which it displaces pleasure and affects the patient’s enjoyment of life. The second item, "minimizing," was included to cover the rater’s opinion about the degree of denial or verbal minimizing of the patient’s distress. The Structured and Scaled Interview to Assess Maladjustment is an interview-based instrument for measuring social maladjustment. The original scale contains 60 items. Each item is rated on an 11-step scale with five anchoring definitions phrased in terms unique to each item. A high score implies more maladjustment.
Social adjustment
Another six items were extracted from the Structured and Scaled Interview to Assess Maladjustment to give clinically relevant background data. An attempt was made to cover aspects of social adjustment that reflect the degree of social support and the extent of opportunities in the current environment for patients to communicate their feelings and thereby obtain help in coping with the illness. One item, "isolated," measures social isolation and deals with the number, type, and closeness of social contacts. If the response to this item is "no," the patient is assumed to have a fairly wide and diverse circle of friends and acquaintances. For the second item, "reticent," the scope is the frequency and extent of actively avoiding personal disclosures of health status to family of origin. If the response to this item is "no," the patient does not avoid confiding freely in parents, brothers, or sisters. The third item, "constrained," assesses the extent to which the patient tries to explain his or her feelings to immediate family members. If the response is "no," the patient is considered to be frank and open with immediate family members. The fourth item, "feeling emotionally deprived," deals with the need for warmth and attention from the spouse or children. A "no" response indicates that the patient does not feel the need to search for more warmth or attention from the spouse or children. The fifth item, "sexually inactive," refers to any activity between consenting persons that is frankly directed at obtaining orgasm by a mutually acceptable technique of bodily contact. If the response is "no," the patient has not attempted to have sex in last year. Finally, the sixth item, "feeling sexually deprived," includes a sense of deprivation, whether through lack of opportunity, poor performance, or weak appetite. A "no" response indicates that the patient feels no sense of being deprived of sex.
Statistical Analysis
The dependent variable was the outcome of the surgeon’s decision to perform a potentially curative or palliative resection. We expected no difference in patients’ attitudes facing surgery, and thus the null hypothesis of no difference between the two groups was applied. Between-group comparisons were performed with Fisher’s nonparametric permutation test22 in two steps. First, patient characteristics (Table 1 and Table 2) were compared to detect confounding factors. Second, between-group comparisons of the quality-of-life indices and measures of psychopathology and maladjustment were made, and variables with a p value less than 0.01 were entered into a forward stepwise logistic regression analysis. To restrict the number of variables examined, only the total scores for composed measures were analyzed. All significance tests were two-tailed and conducted at the 1% significance level to allow for type I errors incurred in the analysis. In all, 10 variables (Table 3, Table 4, Figure 1)) were formally tested, and, of those variables, three were included as possible regressors in the stepwise logistic regression. To describe possible type I errors, the upper limit of the expected number of false significances was calculated according to the following standard formula:  [N – n()]/(1 – ), where N is the number of tests, n() is the number of significances at the level, and alpha is the significance level. In our study, the upper level of false significances was thus estimated to be 0.071. The descriptive between-group comparisons, including comparisons of syndromes, dimensions, and scores on subscales of the composed measures (Table 3 and Table 4), used common effect size calculations (mean difference between groups divided by the pooled standard deviation) to acknowledge the large (>0.80), moderate (0.50 to<0.80), and small (0.20 to<0.50) effect sizes.23
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TABLE 3. Psychiatrists’ Pretreatment Ratings on Measures of Quality of Life, Psychopathology, and Maladjustment for Gastric Cancer Patients Who Later Underwent Potentially Curative Versus Palliative Procedures
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TABLE 4. Pretreatment Scores on Self-Rated Quality-of-Life Measures of Gastric Cancer Patients Who Later Underwent Potentially Curative Versus Palliative Procedures
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FIGURE 1. Mean Pretreatment Ratings by Psychiatrists of Minimization of Distress by Patients Who Later Underwent Potentially Curative (N=64) Versus Palliative (N=34) Procedures for Gastric Cancer
aSignificantly greater minimization (p<0.01, Fisher’s nonparametric permutation test [adjusted for age and sex], two-tailed). The upper level of false significances is estimated to be 0.071.
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RESULTS
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The difference between the groups in mortality rates was highly significant, as expected. Patients who underwent the potentially curative procedure had a first-year mortality rate of 20%, and another 14% died during the second postoperative year. The corresponding figures for the patients who underwent palliative procedures were 82% and 15%, respectively.
No significant differences between the groups were found in analyses of patients’ characteristics and background data. The two groups had similar sociodemographic characteristics (Table 1). Clinical characteristics, use of psychotropic medications, and smoking and drinking habits were also similar in the two groups (Table 2).
The primary between-group comparisons of the quality-of-life indices and measures of psychopathology and maladjustment showed significantly more eating dysfunction but less hopelessness and feelings of giving up in patients with a more advanced tumor burden (Table 3 and Table 4). This response pattern was further supported by the psychiatrists’ ratings of the degree of denial or verbal minimizing of the patient’s distress. According to the psychiatrists, who were blinded to patients’ group affiliation, the patients with a more advanced tumor burden (who received palliative surgery) minimized their distress significantly more than the patients with a more limited tumor burden (who received curative surgery) (Figure 1).
The descriptive between-group comparisons, including comparisons of syndromes, dimensions, and scores on subscales of the composed measures (Tables 3 and 4), revealed an expected difference in eating dysfunction detected by the Sickness Impact Profile. Patients who underwent palliative procedures had more eating problems compared with the curatively treated patients (effect size=0.90 [large]). However, the patients with a more advanced tumor burden reported less tension, according to their scores on the Mood Adjective Check List (effect size=0.50 [moderate]).
The logistic regression analysis showed that two variables—eating dysfunction and hopelessness—were independently predictive of prognosis (Table 5). With only psychological variables entered in the model, the tendency to minimize distress, as measured by the Structured and Scaled Interview to Assess Maladjustment, was the best predictor of a more advanced tumor burden (Table 6).
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TABLE 5. Logistic Regression Analysis of Clinical, Psychopathology, and Maladjustment Variables Predicting Prognosis in Gastric Cancer Patients Who Later Underwent Potentially Curative (N=64) Versus Palliative (N=34) Proceduresa
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TABLE 6. Logistic Regression Analysis of Psychological Variables Predicting Prognosis in Gastric Cancer Patients Who Later Underwent Potentially Curative (N=64) Versus Palliative (N=34) Proceduresa
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DISCUSSION
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Physicians often fail to address or even recognize the coping mechanisms patients use to deal with life-threatening events such as stomach cancer. In this study, patients with unresectable gastric cancer minimized self-evident distress more than patients who had a curative procedure. Patients with unresectable gastric cancer also reported less hopelessness than did patients with resectable gastric cancer, which supports the role of self-denied distress in patients with unresectable gastric cancer. Consistent with these findings, patients who underwent palliative surgery also tended to feel less tension, as measured by the Mood Adjective Check List. To our knowledge, this dichotomy between level of tumor burden and denial versus feeling hopeless has not been reported previously.
The fact that both the raters and the patients were blinded to the type of surgery supports the validity of the results. The relatively small number of patients makes it likely that the magnitude of the true difference between the groups represents a clinically worthwhile effect. The interrater reliability of the observer-rater measures of psychopathology and social maladjustment was previously established by the same psychiatrists who rated the patients in this study.24 There is thus reason to believe that sufficient interrater reliability strengthened the results.
Quality of life is now considered an important patient-reported outcome of therapeutic endeavors in cancer care.25 Although not designed to have quality of life as the primary outcome measure, many studies have compared different therapies in terms of quality of life (by means of randomized controlled trials with between-group analyses) or examined change of quality of life after specific therapies (by means of clinical studies with within-group analyses).26,27 We, and others, have reported impairments in disease-specific quality of life with an increased gastrointestinal symptom burden, whereas the generic aspects of quality of life improved after curative surgery, until relapse occurred.6,28 Patients’ expectations for survival seemed to be of utmost importance.
What makes the present study of particular interest is the double-blind procedure, that is, all patients were scheduled for a "curative resection" after a conventional preoperative workup. They were all examined by abdominal ultrasound, chest X-ray, and gastroscopy with no evidence of incurable disease. The one-third of the patients who at the time of the operation were found to have an unresectable tumor scored better in the generic aspects of quality of life. What is the explanation for this counterintuitive finding? One possible explanation concerns patients’ delay in seeking medical attention. Psychological distress may mobilize individuals to seek medical attention at an early stage, but those with a premorbid tendency to minimize symptoms may seek medical attention at a later stage of their disease. This possibility is unlikely, because we found no difference between the groups in time from onset of symptoms to the first visit to a doctor. Furthermore, we found no differences between groups in the closeness of social contacts and extent of actively avoiding personal disclosures of health status to family members. It is interesting to note that there were no differences between the groups on the components of the Gastrointestinal Symptom Rating Scale. Hence, differences in psychological distress could not be attributed to differences in general gastrointestinal symptoms experienced as a result of having gastric cancer. Presumably patients with unresectable gastric cancer intuitively sensed their ultimate fate, owing at least in part to their more severe eating dysfunction. A true difference between groups in eating dysfunction was supported by highly significant differences in their scores on two assessment instruments, the Eating Dysfunction Scale and the Sickness Impact Profile. Therefore, one could speculate that a diffuse awareness of the seriousness of their disease made the patients suppress worries to comfort themselves and remain in psychic balance. It would have been preferable to analyze possible group differences regarding the specific type of gastric carcinoma to uncover any inconsistent patterns, because some types may be associated with greater discomfort yet better prognosis, and others might produce less discomfort but be associated with poorer outcomes. However, compared with the effect of tumor stage on prognosis, the type of tumor is of marginal importance. The surgeon’s decision to perform a potentially curative resection was accordingly based on the tumor stage rather than the type of tumor. Furthermore, in the early stages of gastric carcinoma, the symptom profile is diffuse and no specific association can be detected between any symptom and either the location of the tumor or the histomorphological type. The presence of hitherto unknown tumor-specific factors influencing both the patients’ mood and the aggressiveness of the tumor can of course not be excluded.
What are the clinical implications of the present results? The message to clinicians concerns the importance of the skills needed in patient-physician communication about symptoms and signs of malignant diseases. For instance, patients’ denial is a common phenomenon in the early phase of facing the bad news of a cancer diagnosis. It is important for the physician to be aware of the tendency of some patients to minimize their distress to deal with a major life event. We have, as stated above, no reason to believe that this reaction is related to premorbid personality traits. Instead, studies of cancer and other serious diseases have shown that the effect of the diagnosis is often followed by denial in the early phase.29 Awareness of this phenomenon is useful in interviewing patients. It is important for the physician to pay attention to the way patients present their problems and needs and to debrief patients by using probe questions in cases of uncertainty. A key implication of our findings is that it is useful for physicians to understand the cognitive processes employed by respondents in comprehending and interpreting questions in stressful situations and in formulating and providing answers to those questions.
Regardless of the tentative psychological explanations of the observed differences between the palliative and curative groups, the study emphasizes the importance of assessing eating dysfunction with simple measures, such as the Eating Dysfunction Scale, to identify patients with a particular risk for cancer among the many patients seeking medical attention for vague dyspeptic complaints. It is unlikely that the increased symptom burden perceived by the palliative group would have been noticed with a more general approach.30
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ACKNOWLEDGMENTS
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This study was supported by grants from the Swedish Medical Research Council and the Assar Gabrielsson Research Foundation.
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REFERENCES
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ABSTRACT
INTRODUCTION
