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June 27, 2006; 66 (12) Views & Reviews

Neurosurgery in Parkinson disease

A distressed mind in a repaired body?

M. Schüpbach, M. Gargiulo, M. L. Welter, L. Mallet, C. Béhar, J. L. Houeto, D. Maltête, V. Mesnage, Y. Agid
First published June 26, 2006, DOI: https://doi.org/10.1212/01.wnl.0000234880.51322.16
M. Schüpbach
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M. Gargiulo
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M. L. Welter
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L. Mallet
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C. Béhar
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J. L. Houeto
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D. Maltête
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V. Mesnage
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Y. Agid
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Neurosurgery in Parkinson disease
A distressed mind in a repaired body?
M. Schüpbach, M. Gargiulo, M. L. Welter, L. Mallet, C. Béhar, J. L. Houeto, D. Maltête, V. Mesnage, Y. Agid
Neurology Jun 2006, 66 (12) 1811-1816; DOI: 10.1212/01.wnl.0000234880.51322.16

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Abstract

Objective: To prospectively evaluate the impact of subthalamic nucleus (STN) stimulation on social adjustment in patients with Parkinson disease (PD).

Methods: Before and 18 to 24 months after bilateral STN stimulation, the authors assessed 29 patients with PD for motor disability, cognition (Mattis dementia rating scale, frontal score), psychiatric morbidity (Mini-5.0.0, MADRS, BAS), quality of life (PDQ-39), social adjustment (Social Adjustment Scale), and psychological status using unstructured in-depth interviews.

Results: Despite marked improvement in parkinsonian motor disability, the absence of significant changes in cognitive status, and improvement of activities of daily living and quality of life by the end of the study, social adjustment did not improve. Several kinds of problems with social adjustment were observed, affecting the patients’ perception of themselves and their body, marital situation, and professional life. Marital conflicts occurred in 17/24 couples. Only 9 out of 16 patients who had a professional activity before the operation went back to work after surgery.

Conclusion: After STN stimulation, patients experienced difficulties in their relations with themselves, their spouses, their families, and their socio-professional environment. The authors suggest a multidisciplinary psychosocial preparation and follow-up to help patients and their entourage cope with the sudden changes in their existence following successful neurosurgery.

In advanced stages of severe levodopa-responsive forms of Parkinson disease (PD), bilateral high-frequency stimulation of the subthalamic nucleus (STN) can reduce motor disability and levodopa-related complications.1 Perioperative morbidity is low,2 provided that strict inclusion criteria are used.3 No significant changes in cognitive functions have been observed,4 except in elderly patients with cognitive decline.5 Although some patients may experience psychic disturbances shortly after the operation (confusion, hypomania) or relapse later on into a preexisting disorder (depression, personality disorders),6 STN stimulation improves depression and anxiety.7 Overall, STN stimulation improves the activities of daily living1 of patients with PD and their quality of life.8 Nevertheless, there is often a contrast between the dramatic improvement of parkinsonian disability and an unexpected dissatisfaction on the part of patients who are unable to resume a normal family and social life. To understand and manage the difficulties experienced by patients who undergo neurosurgery and their entourage, we prospectively examined the kinds of social maladjustment experienced by 29 patients with PD before and 18 to 24 months after bilateral STN stimulation.

Methods.

Twenty-nine patients (15 women, mean [± SD] age 52.4 ± 9.0 years) with advanced levodopa-responsive PD (mean disease duration: 10.8 ± 4.8 years) and nothing to contraindicate neurosurgery3 were included in this study between December 2000 and November 2003. Stimulating leads were placed bilaterally in the STN in a single operation9 and were connected to a subcutaneous programmable pulse generator (Kinetra; Medtronic) implanted in the subclavicular area. Electrical parameters (voltage, pulse width, and frequency) were progressively adjusted using an electromagnetic programmer (7532 neurologic programmer, Medtronic). Eighteen to 24 months after surgery, activities of daily living, the severity of parkinsonian motor disability (“on” stimulation “off” drug) and levodopa-related complications, assessed with the Unified PD Rating Scale (UPDRS parts II, III, and IV10), improved by 37%, 67%, and 67% with STN stimulation compared to the preoperative state 1 month before surgery. The daily dose of levodopa equivalent was reduced by 64%. The neuropsychological status (Mattis dementia rating scale11 and frontal scores12) of the patients did not change (table 1).

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Table 1 Preoperative and postoperative clinical characteristics of 29 patients with Parkinson disease

Repeated open, unstructured interviews were conducted by trained psychologists (M.G., C.B.), neurologists (M.S., D.M., V.M., J.L.H.), and a psychiatrist (L.M.) to qualitatively assess the impact of STN stimulation on the patients’ personal, marital, and socio-professional life. Psychopathologic features were evaluated with an in-depth semi-structured psychiatric interview (Mini International Neuropsychiatric Inventory [MINI 5.0.0.]13). Mood and anxiety were assessed with the Montgomery Asberg Depressive Rating Scale (MADRS)14 and the Brief Anxiety Scale (BAS).15 The psychological evaluation consisted of a semi-directive interview exploring work, social life, family life, marital life, relations with children, and an overall score for social adjustment determined with the Social Adjustment Scale (SAS; normal: score 1 and 2; maladjustment: 3 = mild, 4 = moderate, 5 = pronounced, 6 and 7 = severe).16 Disease-specific quality of life was rated with the PDQ-39 auto-questionnaire17 (see table 1).

Case reports.

Patient 1, a 38-year-old female journalist, married with one child, had PD (caused by a mutation in the parkin gene) for 30 years (UPDRS III “off” medication = 32) with motor fluctuations and severe dyskinesias. Before stimulation, in spite of her motor handicap, she was dynamic: “Combating the disease gave meaning to my life. I hope that stimulation will allow me to get on with my life and my projects.” Six months after the operation, the patient was not satisfied in spite of a 75% improvement of her motor handicap and the withdrawal of her antiparkinson medication. She complained that the stimulator was not well programmed and she wanted to be able to adjust it herself at home. After 18 months of stimulation, she was no longer able to work, had a loss of inspiration and a taste for her work and for life in general. “Now I feel like a machine, I’ve lost my passion. I don’t recognize myself anymore.” Her family no longer interested her, she was easily exhausted, and had a loss of vitality (in the absence of a depressive syndrome), which led her to interrupt all professional activity. In short, a loss of vitality and a goal in life occurred despite major improvement of her motor symptoms by STN stimulation.

Patient 2, a 48-year-old male accountant, worked half-time for 7 years because of PD (UPDRS III “off” medication = 57). Before the operation, his wife assisted him in all tasks of daily living, assumed all domestic and financial responsibilities, spent hours with him, and helped him to conceal his disease from his entourage. After 18 months of stimulation, his motor condition was much improved (UPDRS III = 6, levodopa = 550 mg per day). The patient regained confidence in himself and aspired to more autonomy: “I want to recover my social standing and establish new relationships outside my couple. During all these years of illness, I was asleep. Now I am stimulated, stimulated to lead a different life.” Confronted with the radical change in her husband’s behavior, his wife became depressed: “Ever since the operation, I feel lost. Before, when he was sick, we were a perfect couple. Now, he wants to live the life of a young man, go out, meet new people, all of that is intolerable! I would rather he be like he was before, always nice and docile!” The patient persisted in his desire for change: “All these years I allowed myself to be carried like a child, because I didn’t have the means to fight. That period is over, I want to get back the position I left open. I am going to take my life in hand, my life before PD.” In short, a grave marital conflict was caused by the newly regained autonomy of the patient and his wife’s loss of status as caregiver.

Patient 3, a 45-year-old female executive, married with 3 children, had levodopa-responsive PD for 6 years (UPDRS III “off” medication = 19) with severe motor complications. Before the operation, she was ashamed to be sick and concealed her disease from her colleagues and employer. She invested herself in her work, assumed more and more responsibilities, and had great hopes that the operation would help her to progress in her career: “If I’m not operated in the coming months, the beast is going to sleep. As long as I have my work, I still exist; the day I can no longer go to work, it will be as if the curtain came down on my life.” Six months after the operation, she had no trace of a motor handicap (UPDRS III = 1) on only 2.25 mg of pergolide per day. She put off going back to work, however, because she felt anxious, had lumbar pain, dizziness, difficulty walking, but had no neurologic substrate. An episode of severe depression was treated successfully. Eighteen months after the operation, she had tried several times without success to go back to work: “I don’t have the same ability to concentrate as before. I have a lot of work and prefer to spend my time doing other things.” She requested unjustified sick leaves, preferred to go out, buy things on the Internet. She threatened to divorce, although there had been no marital conflict before the operation. She announced her disease to her entourage, was active in associations, and wanted to “be recognized as sick.” In short, a loss of professional status after the operation occurred, in spite of spectacular motor improvement, which was the cause of a marital crisis.

Results.

Behavioral assessments and quality of life.

Although prior to surgery none of the patients had a known active psychiatric disorder severe enough to contraindicate STN stimulation, 14 (48%) had histories of depression and 11 (38%) had previously had generalized anxiety disorder (table 2). After surgery, 7 had depressive episodes (3 for the first time) and 7 generalized anxiety disorder (1 for the first time). In spite of these episodes of major depression and anxiety after surgery, however, the mean ratings for mood (MADRS) and anxiety (BAS) had improved significantly by the end of the study (see table 1). Two patients had histories of hypomania before STN stimulation. During follow-up, hypomania was observed de novo in 6 other patients (see table 2). In contrast, obsessive-compulsive disorders in two patients before neurosurgery disappeared afterwards.18 Panic disorder, agoraphobia, and social phobia, present in the prior medical history of 4, 4, and 5 patients, recurred in 2 patients each after surgery (see table 2).

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Table 2 Psychiatric morbidity in 29 patients with Parkinson disease before neurosurgery and during follow-up

According to the SAS, 6 patients were socially well adjusted before surgery and 12 were mildly, 10 moderately, and 1 markedly maladjusted. The global SAS score was similar 2 years after neurosurgery: 6 patients (21%) were well adjusted, 9, 10, 3, and 1 patients were mildly (31%), moderately (34%), markedly (10%), and severely (3%) maladjusted. Eight patients (28%) improved, 10 (34%) did not change, and 11 (38%) worsened in their overall social adjustment during the study (figure, B). Financial situation, social life, relations with their children, and family life improved more often than they worsened. Marital life and professional activity, however, worsened more often than they improved (see the figure, B). It was impossible to predict the outcome in individual patients, but social adaptation before surgery correlated with social adaptation at follow-up (Spearman’s rank correlation coefficient rho = 0.42, p < 0.05). Although social adjustment did not improve (figure, A), the disease-specific quality of life, as measured with the PDQ-39-summary index, improved significantly by 24% (see table 1).

Figure1
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Figure. Social adjustment before and 18 to 24 months after surgery. (A) The social adjustment ratings for the six subdomains of the SAS and a general rating are given as the means ± SD before (black bars) and after (white bars) neurosurgery. There are no significant differences between the scores before and after surgery. Higher ratings indicate worse social adjustment. The scale ranges from 1 to 7. (B) Changes in the social adjustment of individual patients before and 24 months after surgery. Numbers of patients whose social adjustment evaluated with the SAS did not change (white bars), improved (hatched bars), or worsened (black bars).

Psychological assessments.

Qualitative observations made during repeated in-depth open interviews revealed problems with personal, marital, and socio-professional adjustment after neurosurgery.

The patient’s experience.

Six different types of problems were detected after the operation. 1) Altered body image: Only 6 patients (20%) thought about the implanted material in terms of body image and formed a mental representation of the stimulator and the electrodes. Three of them, all women, had difficulty accepting the presence of an electronic device in their brains (“I feel like a robot”; “I feel like an electronic doll”). After struggling with the idea of being implanted with an electronic device, one patient finally coped well with it and made an artwork of her chest X-ray showing the stimulator. 2) A feeling of strangeness: Nineteen (66%) out of 29 patients expressed a feeling of strangeness and unfamiliarity with themselves after surgery (“I don’t feel like myself any more,” “I haven’t found myself again after the operation”). 3) Loss of vitality: Twelve (41%) of the 29 patients were dissatisfied and had a loss of vitality, and 5 became frankly apathetic. Ten patients (34%) had regained vitality, however, and wanted to make up for lost time. 4) Awakening to the impact of a chronic progressive disease: The sudden improvement after the operation, perceived as a major life event (“like giving birth,” “my second birth”), was in stark contrast with the disability before surgery. Fourteen patients (48%) had feelings of helplessness looking back at the damage PD had done: “Now I can live a normal life, go out, see friends, go to the swimming pool, have a sexual life. But PD has destroyed everything. Today, my life is like a forest without trees: I don’t have any friends or places to see. What’s the use?” 5) Negative anticipation: In spite of successful surgery, 8 patients (28%) felt mentally unable to resume a more normal life style. Although with STN stimulation they could, they did not dare to perform activities that had been impossible with PD before surgery. Past experience led to a negative anticipation that was objectively unjustified after surgery. “My body is cured, but my mind is still sick,” said one patient. 6) Loss of aim in life: Fighting PD was a driving force for many patients that was frustrated in 12 (41%) after surgery (Case 1) causing disorientation. As expressed by another patient: “Before stimulation, I wanted to be like everybody else, I didn’t want to be considered only as sick. I fought for that every day! Now I find myself less impassioned, I regret the period where I did battle. Now it’s the warrior’s repose, I no longer have something to struggle against, my life is empty. I get up every day, but have no goal, no horizon.” None of the patients, however, wanted to stop stimulation and go back on medication only.

The couple.

Twenty-four patients had lived as a couple before surgery. Three divorced during the 2 years of follow-up after surgery, but one patient found a new partner during the study, and another, who was a bachelor, found a spouse. During follow-up, 6 patients rejected their spouse (Case 2), and 11 were rejected by their spouse. Fourteen spouses (58%) were disappointed by the results of surgery and were disconcerted by the patient’s postoperative struggle to adjust. “I gave of myself all these years while he was sick, avoiding saying or doing anything that might be hurtful, but now I can’t stand it any more; he makes no effort, doesn’t budge and waits for me to do everything,” said one spouse. Eight (33%) spouses even became depressed after their partners were successfully operated. Twelve of the 24 couples (50%) were already in a marital crisis before surgery. Three had separated by the end of the study. The remaining 9 were still in crises, which had worsened in 4. Five of the 12 other couples who had no significant marital problems before surgery entered into a crisis after surgery (Case 2).

Professional activity.

Sixteen patients had a professional activity before surgery. Five patients no longer wanted to work after surgery, giving priority to leisure activities: “Before, I thought that work was the most important thing in my life. Now, I want to do other things. I realize that my presence at work is not essential, and that the work gets done even when I’m not there.” Five patients did not feel able to work any more after surgery. Some patients neither could nor wanted to go back to work (Case 3). Seven patients (44%) gave up working after surgery although their motor improvement was often excellent (Case 3).

To summarize, there were reactive psychological difficulties for patients to overcome after surgery. However, operated patients often also had slight and subtle intellectual and psychic symptoms that became apparent only in the course of repeated and thorough unstructured interviews. Patients had more difficulty ordering complex actions and thoughts, anticipating and planning ahead, especially since they had problems with attention and were distractible. Several became more direct in their approach to others, were logorrheic, irritable, and impatient. They expressed their opinions more freely and revealed their formerly concealed PD to outsiders, as if they had become disinhibited. As a result, preexisting tension in a couple or a minor deterioration of professional performance (in terms of reliability, punctuality, correctness, persistence) could degenerate into familial conflicts or maladjustment at work.

Discussion.

There was a contrast between the marked improvement in parkinsonian motor disability, activity of daily living, and quality of life (see table 1) and the fact that social adjustment did not improve (see the figure). This apparent paradox is difficult to explain. However, close individual follow-up and in-depth interviews with patients and their spouses and families revealed three kinds of problems with social adaptation in some but not all patients.

Impact of neurosurgery on the patients’ perception of themselves and their bodies.

This was manifested in several ways. 1) The altered body image may result from difficulty in accepting psychologically the implanted material, as previously described in patients with pacemakers19 and implantable cardioverter defibrillators.20 However, it is surprising that this difficulty was not observed in a greater number of patients. 2, 3) The feeling of strangeness and loss of vitality were associated with a clinically significant apathy in some patients (which was not evaluated quantitatively), but was potentially subclinical in others. Apathy after neurosurgery has been attributed both to stimulation of the STN itself21 and to the reduction of levodopa treatment after surgery.7 The operation is, therefore, likely to contribute to social maladjustment. 4) The marked improvement after STN stimulation also revealed to the patients how seriously PD had affected their lives. This is difficult to cope with, as has previously been seen in patients who underwent surgery for epilepsy.22–24 Furthermore, patients were aware that STN stimulation was not a cure, and that the underlying disease would progress relentlessly. 5) Postoperative adjustment was hampered by negative anticipation since most patients had become used to their parkinsonian handicap and the limitations it imposed on their lives and did not dare to resume normal activities after successful surgery.25 This reaction was transient, however, and could be overcome with psychological support. 6) The loss of an aim in life is easily understandable in patients for whom the struggle against the disease had been a source of strength that helped to keep them going.

Impact of neurosurgery on the couple.

Following neurosurgery, the majority of couples had new or continuing marital conflicts,25 of two types that were not mutually exclusive. In the first case, the patients rejected their spouse, because they had regained autonomy and felt “cured,” but the spouse was disconcerted by the rapidity of the change and could not give up the role of caregiver, overprotecting the patient or trying to maintain his or her dependency (Case 2). In the second case, the patients were rejected by their spouse, who expected that they would resume a normal existence after the operation,25 whereas the patient tried to make it understood that in spite of the operation he or she could not resume his or her life as before. We hypothesize that the improvement of the patient’s condition encouraged dysfunctional couples to separate, because there was less of a moral obligation to remain with a partner who has regained physical independence.

Impact of neurosurgery on professional life.

Work became a secondary issue for many successfully operated patients. Some patients believed that society owed them compensation, and they preferred to engage in leisure activities rather than invest the benefit gained from STN stimulation in work. Others insisted on being recognized as patients with PD, because they felt unable to cope with a professional activity. It is possible that patients in countries in which retirement is financially disadvantageous would have reacted differently than patients in France where this is not the case.

The reasons evoked above for the observed difficulties in social adjustment after STN stimulation are not entirely satisfactory. As previously observed in patients who underwent surgery for intractable epilepsy26 and heart surgery,27 it is likely that operated patients with PD and their entourage needed time to adjust to normal life following relief from the burden of PD and the accompanying social isolation.

Unsuccessful social readjustment cannot be attributed to the failure of neurosurgery, as motor results were excellent, or to cognitive deterioration, as the dementia and frontal scores remained stable (see table 1). Adverse psychic reactions can also be excluded, since mood and anxiety improved substantially (see table 1), although a few patients had positive prior histories of depression and anxiety, which is a known risk factor for adverse events after surgery.3 In contrast, hypomania after neurosurgery was observed in patients who did not have previous histories, and may therefore be a result of the operation. While neuropsychological assessments and psychiatric scales did not show any worsening after surgery, subtle behavioral changes in operated patients were only detectable using open interviews.

The causes of the observed discrete changes in the behavior of the operated patients remain unclear. Social maladjustment in patients with PD may also result from a lack of brain reserve or psychological capacity to adapt at a neurologic level. Whether the patients changed their behavior as a consequence of the operation, or whether STN stimulation did affect the behavior of the patients per se, is a matter of discussion. The human STN is a small structure (0.16 cm3) in which motor, associative, and limbic projections from the pallidum converge.28 The associativo-limbic parts of the STN are close to the optimal surgical target in the sensorimotor part of the structure. STN stimulation might therefore also affect the associativo-limbic territory of the nucleus, resulting in slight frontal (emotional) release. This should be further evaluated.

Conclusion.

The recent history of the treatment of PD by STN stimulation has gone through four phases. In the early 1990s, STN stimulation was shown to have a marked benefit on parkinsonian motor disability.29 In the late 1990s, there was concern that STN stimulation may have deleterious effects on cognition. This was shown not to be the case, however,4 provided that patients were not demented before surgery.3 Although in the 2000s frequent transient psychiatric symptoms were observed postoperatively,6 it was shown that neurosurgery led to an overall improvement in mood,7,30 anxiety,30 and quality of life.31 Now, in spite of the excellent motor outcome, it is clear that the operation can result in poor adjustment of the patient to his or her personal, family, and socio-professional life. Whether this is a purely reactive response to a new situation or whether it is caused by an effect of STN stimulation on behavior, or both, remains to be elucidated. In any case, a multidisciplinary approach should be taken to patient care, including psychosocial preparation in the preoperative phase and postoperative follow-up. This is necessary to help the patients and their entourage better anticipate and cope with unquestionable success of STN stimulation.

Acknowledgment

The authors thank Drs. P. Cornu, D. Dormont, S. Navarro, and B. Pidoux for participation in the neurosurgical procedure; Dr. A.M. Bonnet, Dr. M. Dujardin, and the nurses of the Centre d’Investigation Clinique for providing care to patients; and Dr. M. Ruberg for reviewing the manuscript.

Footnotes

  • Editorial, see page 1799

    See also page 1830

    *These authors contributed equally to the article.

    Supported by grants from the Swiss National Science Foundation and the Swiss PD Association (M.S.).

    Disclosure: The authors report no conflicts of interest.

    Received October 31, 2005. Accepted in final form April 4, 2006.

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Disputes & Debates: Rapid online correspondence

  • Neurosurgery in Parkinson disease. A distressed mind in a repaired body?
    • Mazen G. Jabre, PharmD, Parkinson, Memory & Movement Disorders Center, Notre Dame des Secours Hospital, Byblos/Jbail-Lebanonmazenj@inco.com.lb
    • Boulos-Paul W. Bejjani, MD
    Submitted November 09, 2006
  • Reply from the Authors
    • Yves Agid, Centre d' Investigation Clinique, Inserm U 679, Hopital Pitie-Salpetriere, 47 Bd De L' Hopital, 75013 Paris, Franceagid@ccr.jussieu.fr
    • Michael Schüpbach, Marcela Gargiulo, Marie-Laure Welter, Luc Mallet, Cécile Behar, Jean-Luc Houeto, David Maltête, Valérie Mesnage
    Submitted November 09, 2006
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