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10.1245/ASO.2006.05.023
Annals of Surgical Oncology 13:864-871 (2006)
© 2006 Society of Surgical Oncology
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Original Article

Quality of Life After Hyperthermic Isolated Limb Perfusion for Locally Advanced Extremity Soft Tissue Sarcoma

Katja M. J. Thijssens, MD1, Josette E. H. M. Hoekstra-Weebers, MSc, PhD2, Robert J. van Ginkel, MD, PhD1 and Harald J. Hoekstra, MD, PhD1

1 Department of Surgical Oncology, University Medical Center Groningen, University of Groningen, P.O. Box 30.001, 9700, RB Groningen, The Netherlands
2 Department of Psychosocial Services, University Medical Center Groningen, University of Groningen, Groningen, The Netherlands

Correspondence: Address correspondence and reprint requests to: Harald J. Hoekstra, MD, PhD; E-mail: h.j.hoekstra{at}chir.umcg.nl.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Quality of life (QoL) and posttraumatic stress symptoms (PTSS) were studied in patients with soft tissue sarcoma (STS) of the extremities treated with isolated limb perfusion and delayed resection, with or without adjuvant irradiation.

Methods: Forty-one patients received a questionnaire that included the RAND-36 and Impact of Event Scale.

Results: Thirty-nine STS survivors (16 [41%] male and 23 [59%] female; median age, 59 years; range, 15–78 years) participated in the questionnaire survey (response rate, 95%). The median age at perfusion was 49 years (range, 14–72 years). No significant differences were found in mean scores between STS survivors and the reference group with the exception of a worse physical functioning. Patients with amputations showed significantly worse physical and social functioning and more role limitations than patients whose limbs were saved. Eleven patients (28%) had a PTSS score of 0, and eight patients (20.5%) had a score ≥ 26, which suggested the need for psychological counseling. None of these eight patients had lost a limb. Patients who indicated that the choice of treatment was made by the surgeon rather than collaboratively showed significantly decreased social functioning, more role limitations, and intrusion. Greater treatment satisfaction was significantly related to better social functioning, more vitality, better general health perception, less intrusion, avoidance, and total Impact of Event Scale scores.

Conclusions: Even though STS survivors’ QoL was different from that of a reference group only in physical functioning, one fifth of the patients had PTSS. An amputation, the physician’s decision rather than the patient’s decision for the perfusion treatment and a low satisfaction with the performed treatment negatively influenced QoL.

Key Words: Sarcoma • Isolated limb perfusion • Quality of life • Stress response symptoms


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
For decades, soft tissue sarcomas (STS) were known for their poor long-term outcome with respect to local tumor control and survival, as well as functional outcome. Developments in diagnostic imaging and surgical treatment with adjuvant radiotherapy were the cornerstones of the evolution over the past 30 years. Nowadays, STS patients have 5-year survival rates of 60% to 70%.1,2 For patients with primarily irresectable locally advanced STS, the so-called hyperthermic isolated limb perfusion (ILP) with tumor necrosis factor (TNF)-{alpha} and melphalan became available in the early 1990s, with a limb salvage rate of 82%.3 The survival of patients with extremity STS is not influenced by limb salvage procedures.4

The limb salvage treatment of STS with ILP is a combined-modality treatment of regional chemotherapy followed by delayed extensive surgical resections with or without surgical reconstructions and/or adjuvant high dose radiotherapy, sometimes followed by systemic chemotherapy with curative or palliative intent. ILP treatment is time consuming and has an uncertain outcome. The risk of losing a limb after a limb salvage procedure is determined by the risk of perioperative complications, local recurrences, and short- and long-term treatment-induced morbidity.

Patients who are alive after treatment for a potentially fatal disease are often analyzed in terms of overall and disease-free survival. However, less attention is paid to their quality of life (QoL) in these years gained. Health is defined by the World Health Organization as a state of complete physical, mental and social well-being and not merely the absence of disease or infirmity. Medical oncologists were one of the first groups of physicians to implement QoL measurements into practice as the question was raised to what extent quantity of life was gained at the expense of QoL.5 The need to investigate the QoL and the psychological consequences of this combined treatment became increasingly clear as more patients with extremity STS became long-term survivors. It is often hypothesized that for many people with cancer, the survivor advantages of the intensive treatment far outweigh the potential long-term side effects.6 Findings in the literature are inconsistent concerning that matter: worse, equal or even better QoL in cancer survivors than in a healthy comparison group have been reported.7,8 However, specific subgroups at risk for a worse QoL have been identified, such as survivors who are single, less educated, less involved in decision making, or less satisfied with the received medical treatment.9,10 Little is known about the QoL of patients with locally advanced, primary irresectable STS of a limb who undergo TNF-based ILP as an intentional limb-saving treatment.

This study was conducted to gain insight into the QoL in this intensively treated group of patients and into aspects possibly affecting these patients’ QoL. The study investigated whether STS survivors differ in QoL from a reference group and evaluated whether QoL and stress response symptoms in STS survivors are related to (1) sociodemographic aspects (sex, age, education level, employment, and marital status) and to (2) disease-related (time period since perfusion, limb survival, local recurrence, presence of metastases, and comorbidity) and treatment-related (i.e., involvement in the choice of treatment and satisfaction with treatment) aspects.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Procedure and Patients
All patients with locally advanced STS who underwent ILP with TNF-{alpha} and melphalan and an intentional limb salvage treatment during the time period 1991 to 2003 were eligible for the study. None of the patients had metastases at the time of the ILP treatment. Patients who were alive received a letter explaining the aim of the study, an invitation to participate in the questionnaire survey, and a prepaid return envelope.

All patients underwent a complex diagnostic and therapeutic pathway. Before treatment started, the option of amputation or an intentional limb-saving treatment with ILP was discussed. This study focuses on the STS patients who received the intentional limb-saving tumor treatment. The affected limb received an ILP with TNF-{alpha} and melphalan followed by delayed resection This technique was described previously.11 Most patients received adjuvant radiotherapy (60–70 Gy).11 During the entire range of the intentional limb-saving procedure, it was possible that patients would still lose a limb as a result of irresectability, vascular complications, wound-healing disturbances, or radiation-induced complications.3 The TNF-{alpha}–based ILP-containing treatment and the series of patients were recently extensively described.3,11 All patients were treated by following institutional guidelines.

Measurements
Sociodemographic (sex, age, education level, and employment and marital status) and disease-related (time period since perfusion, limb survival, local recurrence, presence of metastases at the time of questionnaire completion, and comorbidity) data were assessed from all patients. On a five-options scale, patients could fill in their perception of actual involvement in the decision for treatment. Answers ranged from ‘‘the doctor only’’ (1) to ‘‘the doctor and myself in equal extent’’ (3) to ‘‘me only’’ (5).12 In addition, patients were asked to score their satisfaction with treatment received on a five-point scale from ‘‘very good’’ to ‘‘very bad.’’ Patients were invited to indicate reasons for satisfaction and dissatisfaction.

Health-related QoL was investigated with a Dutch-language version of the RAND-36,13 a multidimensional self-report questionnaire that is identical to the Short Form 3614 but uses a different scoring method. The RAND-36 consists of the following domains: physical functioning (10 items), social functioning (2 items), role impairment due to physical problems (4 items), role impairment due to emotional problems (3 items), mental health (5 items), vitality (4 items), pain (2 items), general health perception (5 items), and health change (1 item). After recoding and transformation, scores on the subscales could range from 0 to 100. Higher scores indicate a better QoL. The internal consistency of the subscales for the respondents in this study was good ({alpha} ranged from .70 to .92). Normative data are available for the healthy Dutch population. The normative data compromise the mean scores of a group of 1063 men (35%) and women (65%) from a random sample of the population register of a municipality in the Netherlands (108,000 inhabitants). The mean age of the persons in the total random sample was 44 years (range, 18–89 years).13

Posttraumatic stress symptoms (PTSS) were measured with the Dutch version of the Impact of Event Scale (IES).15,16 This scale is often used in studies on cancer patients.17 In this study, information was obtained about the degree to which treatment for a sarcoma was influencing the current daily life of the respondent. Fifteen items measured intrusion (intrusively experiencing ideas, images, feelings, or bad dreams about the event; seven items) and avoidance of unpleasant feelings or memories of the event (eight items) by using the answer categories not at all (0), rarely (1), sometimes (3), and often (5) (intrusion: range, 0–35; avoidance: range, 0–40). Items of the two subscales are summed to compute a total score (range, 0–75). A total score of > 26 is a strong indication of clinically significant PTSS for which psychological help is recommended. The internal consistency of this questionnaire was good ({alpha} was .84 for intrusion, .76 for avoidance, and .85 for the total IES score).

Statistics
Statistical analyses were performed by using SPSS for Windows (version 12.0; SPSS Inc., Chicago, IL). Unpaired t-tests were computed to compare STS survivors with the reference group in the domains of QoL. Pearson correlations, unpaired t -tests, and nonpara-metric Mann-Whitney and Kruskal-Wallis tests were conducted to examine the effects of sociodemographics and treatment- and disease-related variables on the outcome measures. Correlation coefficients <.30 indicate a weak association, those between .30 and .50 indicate a moderately strong association, and those >.50 indicate a strong association.18


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Forty-one (57%) of the 73 patients who had been treated with an intentional limb salvage procedure for locally advanced, irresectable STS at the Department of Surgical Oncology at the University Medical Center Groningen since 1991 were still alive. Thirty-nine patients (16 [41%] male and 23 [59%] female; median age, 59 years; range, 15–78 years) participated in the questionnaire survey (response rate, 95%). The median age at perfusion was 49 years (range, 14–72 years). The median time since perfusion was 7 years (range, 1–13 years). A fifth of the patients had completed primary school only, and only one patient had a university degree. The median education level was lower secondary school. A little more than one third of the patients had a job, and one third was retired. More than two thirds (69%) of the STS survivors was married or cohabiting (Table 1Go).


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  		TABLE 1. Sociodemographic and disease-related characteristicsa
 
Successful limb salvage was achieved in 30 patients, and 9 patients underwent an amputation of the affected limb. Amputation of the affected limb was due to massive necrosis after ILP, local recurrence, or critical leg ischemia.3 The decision to amputate was not influenced by the presence of metastases. At the time of this study, four (44%) of the nine patients whose limbs were amputated had metastases. Of the 30 patients whose limbs were saved, 6 patients (20%) had metastases at the time of questionnaire completion. Thirty-three patients had a sarcoma in the lower limb (31% thigh, 21% knee, and 33% lower leg), and six (15%) had metastases in the upper limb. Three patients had local recurrence, and 10 patients had distant metastases at the time of filling in the questionnaire (Table 1Go). The vast majority did not experience comorbidity.

Nine patients responded that the choice was made by the physician alone, and two patients indicated that the choice was made by themselves. Almost half of the patients judged that the physician mainly made the choice of treatment, with their participation. Thirty patients were very or rather satisfied with the treatment, three patients were not, and six scored the answer as neutral. Involvement in treatment choice and satisfaction with treatment were not significantly related (Table 2Go).


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  		TABLE 2. Treatment choice and satisfaction and relationship between the two variablesa
 
Independent t-tests showed no significant differences in mean scores between the STS survivors and the reference group in most aspects of QoL, except in physical functioning (P < .001) and role limitations due to physical problems (P = .01). A tendency for a worse social functioning was found (P = .09; Table 3Go). Eleven patients (28%) had a total stress response symptom score of 0. Eight patients (20.5%) had a score ≥ 26, which suggested that psychological counseling was needed.


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  		TABLE 3. Quality of life of STS survivors who underwent ILP and a reference group and comparison between the two groups
 
No significant differences were found between male and female patients in QoL and PTSS. Younger STS survivors scored better on physical functioning than older ones (r = –.34; P = .035). Educational level was not significantly related to QoL or PTSS in STS patients. There was a significant difference in only one domain of QoL when patients employed for wages were compared with the rest: they experienced significantly less pain (Mann-Whitney U-test, –2.47; P = .014). Having or not having a partner did not affect functioning in STS survivors. A Mann-Whitney test showed that those whose limb was amputated reported significantly worse physical (U = –2.41; P = .016) and social (U = –2.27; P = .023) functioning, and they reported more role limitations due to physical (U = –2.39; P = .017) and emotional (U = –2.45; P = .014) problems than those whose limbs could be saved. No significant differences were found in mental health, vitality, pain, general health perception, avoidance, intrusion, and total IES between the two groups. No significant relationships were found between time since initial treatment and the various QoL domains and PTSS.

If patients had metastases at the time of the survey, they reported significantly worse physical functioning (U = –2.13; P = .034) and more role limitations due to physical (U = –2.14; P = .032) and emotional (U = –2.92; P = .004) problems. There were no differences in the other areas of QoL or in intrusion, avoidance, and total stress response symptoms. None of the nine patients with amputations had a score ≥ 26 on the total IES. Of the 10 patients with metastases, 2 had a score ≥ 26. The effects of the incidence of local recurrence and chronic diseases on QoL and STS could not be examined because only a few patients had experienced local recurrence (n = 3) or experienced comorbidity (n = 4).

Kruskal-Wallis tests showed that those who were less involved in the decision for treatment had significantly higher scores on intrusion ({chi}2 = 11.37; P = .023). Also, they tended to report more total IES ({chi}2 = 9.12; P = .058) and a worse social functioning ({chi}2 = 9.17; P = .057). Greater treatment satisfaction was related to a better social functioning (r = –.36; P = .024), more vitality (r = –.32; P = .046), and a better general health perception (r = –.36; P = .028). Higher treatment satisfaction was significantly associated with less intrusion (r = .57; P < .0001), avoidance (r = .35; P = .27), and total IES (r = .58; P < .0001). These correlation coefficients ranged from moderately strong to strong.

Fourteen patients (36%) indicated additionally why they were satisfied with the treatment, 18 (46%) indicated why treatment had discouraged them, and 7 (18%) mentioned both positive and negative aspects of treatment. Positive experiences mentioned by 16 of 21 of the patients were that they were satisfied with the final result and the fact that the course of treatment was as explained and therefore expected. The remaining five mentioned that they experienced the treatment positively because they had expected worse and because they had experienced little pain. Discouraging arguments mentioned were the intensity of treatment (20 of 25), a long recovery period (9 of 25), or the fact that they had been seriously ill as a consequence of the treatment (6 of 25).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The aim of this study was to gain insight into the QoL and PTSS of patients with locally advanced, primary irresectable STS of a limb who underwent an intensive and extensive sarcoma treatment that consisted of a TNF-{alpha}–based ILP followed by delayed surgical resection with or without adjuvant high-dose external beam radiotherapy as an intentional limb-saving treatment.

Physical functioning and role limitations due to physical problems were the only domains in which our group of patients scored significantly lower than the reference group. The problems perceived in the physical domains could be explained by the resection of a large muscular compartment and often adherent structures in the affected part of the limb that the sarcoma patients had undergone. Obviously, such invasive surgery affects the physical functioning of these sarcoma patients. However, functioning in the remaining QoL domains in these patients was the same as in the reference group. It has been suggested that patients with cancer seem to change their internal standards and their expectations about life during treatment. Other studies also postulate that cancer patients evaluate QoL according to their new expectations and different standards.5,19 The limitations patients experience in physical functioning do not seem to affect functioning in the other QoL domains.

The finding of a surprisingly high percentage (20.5%) of patients having clinically increased PTSS is in contrast to literature showing a prevalence of clinically high PTSS among people with cancer, varying from 3% to 12%, depending on the cancer treatment.20–23 The 20.5% PTSS rate found is this study is comparable to rates with more traditional traumatic events in general samples, such as rape, war, disaster, and accidents.21 To distinguish those in our group of patients who had more problems concerning QoL and PTSS, we investigated the effects of sociodemographic and disease- and treatment-related variables.

Sociodemographics
Younger STS survivors scored better on physical functioning than older STS survivors. Some other QoL studies also showed that the physical autonomy score was affected by age.24,25 In the other QoL domains and PTSS, we found no associations with age. This is in contrast with the literature reporting that younger age is a risk factor for psychosocial distress, anxiety, and depressive symptoms among cancer survivors.19,26

Other sociodemographic variables, such as sex, education level, and marital status, were not related to QoL and PTSS in our studies. This is different from findings in literature that show that women tend to develop somatic complaints more quickly after negative life events,24,27 that a higher educational level is associated with a higher QoL in the general population,19,24 and that having a partner is a predictor of better well-being in the general population, particularly in men.19,26 There was a significant difference in one domain of QoL when patients employed for wages were compared with the rest: they experienced significantly less pain. This could be a chance finding. Another suggestion is that work provides a distraction and reduces pain sensations. More research is needed to evaluate this finding.

Illness-Related Variables
Patients with an amputated limb had a worse QoL score in physical and social functioning and in role limitations due to physical and emotional problems. This is in contrast with the literature, which showed no differences in QoL between patients whose limb was amputated and patients who were treated with conservative surgery and adjuvant radiation treatment.28–30 These studies, however, describe patients who were randomized between amputation and limb-saving treatment. In our group, all treatments started intentionally with a limb-saving purpose. Our results suggest that once the patients are on the pathway where limb-saving treatment seems possible, an eventual amputation actually may make a difference that results in a decreased perception of QoL in some domains.

Even though more QoL problems were found in patients whose limb was amputated, it seemed that none of these patients had a posttraumatic response symptom score that was indicative of need for professional psychosocial care. A hypothesis for this phenomenon is that the loss of a limb releases patients from the insecurity of a possible loss in the future. The threat of local recurrence and further damage to the limb due to long-term effects of radiation or vascular incompetence may be like a sword above the head that may fall at any moment. An equal percentage (20%) of patients with metastasized disease and in the complete study group had a clinically increased PTSS score. Patients with metastasis did have problems in physical functioning and role limitations due to physical and emotional problems.

We found no effect of time in relation to QoL; this suggests that physical functioning problems are more permanent. In Lampert and associates’ study,31 patients with lower extremity STS were more at risk to become disabled than patients with STS in other areas of the body. In our own data, the number of upper extremity STS patients (n = 3) was too small to detect significant differences in QoL and PTSS compared with patients whose affected limb was a lower extremity.

Choice of Treatment
This study shows that patients who indicated that the surgeon made the treatment choice rather than they themselves showed decreased social functioning, more role limitations due to physical problems, and higher levels of intrusion. This is in agreement with other studies reporting that patients benefit from participating in medical decision making.10 Despite all the reasonable doubts patients may have, it seems important that the patient at least be involved in the final decision for his or her treatment. Other studies also mention that patients who perceive that they have decisional control in their treatment may regain perception of control over the disease as well. This may ultimately lead to a higher QoL.32–36 It may be that greater attention should be paid to the communication of treatment options and their consequences to the patient so that the patient is better able to make an informed decision.

Our results also showed that patients who were more satisfied with treatment reported less PTSS and a better QoL—a finding in line with earlier research.10,37–40 In contrast to other studies, no significant relationship was found in this study between decision involvement and treatment satisfaction.10,39

In the light of data indicating that 20.5% of the STS survivors experience PTSS symptoms even years after treatment and that patients, in particular those whose limb was amputated, have problems in the physical QoL domains, identifying ways to prevent or relieve these symptoms should be considered. A suggestion would be a multimodal rehabilitation program including a physical and a psychosocial program that might help reduce the problems in the physical domains and the psychosocial distress in these patients. An intensive multifocus rehabilitation program for cancer patients after completion of their cancer treatment seemed to have immediate and longer-term beneficial effects on physiological functioning and QoL.41 Furthermore, attention should be paid to the issue of collaborative decision making, which may be better achieved with informing the patient more comprehensively about treatment options and possible consequences. Attention to communication issues may also increase patient satisfaction.

The inclusion of a validated generic QoL questionnaire and the high response rate (95%) are the strengths of this study. However, only 41 patients (57%) of the original study population of 73 patients were eligible because the remaining 32 patients were dead at the time of the survey. In addition, this study was a retrospective cross-sectional study. The measurement of QoL in STS patients is a dynamic rather than a static process that requires reassessment. Consecutive QoL measurements may give insight into change over time and causal relationships between variables.

Received for publication May 24, 2005. Accepted for publication December 1, 2005.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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M. L. Hoven-Gondrie, K. M. J. Thijssens, J. H. B. Geertzen, E. Pras, R. J. van Ginkel, and H. J. Hoekstra
Isolated Limb Perfusion and External Beam Radiotherapy for Soft Tissue Sarcomas of the Extremity: Long-Term Effects on Normal Tissue According to the LENT-SOMA Scoring System
Ann. Surg. Oncol., May 1, 2008; 15(5): 1502 - 1510.
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