Decompressive craniectomy in malignant middle cerebral artery infarction: family perception, outcome and prognostic factors

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NEUROCIRUGÍA www.elsevier.es/neurocirugia

Clinical Research

Decompressive craniectomy in malignant middle cerebral artery infarction: family perception, outcome and prognostic factors夽 Pablo García-Feijoo a,∗ , Alberto Isla a , Exuperio Díez-Tejedor b , Beatriz Mansilla a , Alexis Palpan Flores a , Miguel Sáez-Alegre a , Catalina Vivancos a a b

Servicio de Neurocirugía, Hospital Universitario La Paz, Madrid, Spain Servicio de Neurología, Hospital Universitario La Paz, Madrid, Spain

a r t i c l e

i n f o

a b s t r a c t

Article history:

Background: The prognosis of one hemisphere malignant infarction creates doubt among

Received 22 November 2018

neurosurgeons about decompressive hemicraniectomy indication. What results are

Accepted 7 July 2019

achieved in the short to medium term? Are families satisfied with the surgery once the

Available online xxx

patient is at home? In the present study, we analyze our experience in this matter during the last thirteen years.

Keywords:

Methods: In our review, twenty-one patients were included from 2004 to 2017, according to

Malignant middle cerebral artery

the protocol for the management of ischaemic stroke that is implemented in our institu-

infarction

tion. The relatives were interviewed by telephone. The functional outcome at discharge, 3

Decompressive craniectomy

months, 1 year, and at present was measured using the modified Rankin scale (mRS).

Outcome

Results: Patient age was shown to be directly related to the mRS (r = 0.56; p = 0.035) and 37.5%

mRS

achieved a good outcome (mRS≤3). 78.9% of the interviewed relatives would repeat the

Family

surgical decision. Conclusion: We present a 21 patients group where the best outcome was achieved in patients ≤60 years old. The severe neurological sequelae in patients with malignant infarction subjected to decompressive hemicraniectomy are tolerated and accepted by most families to the benefit of survival. We must not let this family satisfaction hide the prognosis, having to contextualize it within the real ambulatory situation of the patients. ˜ ˜ S.L.U. All rights © 2019 Sociedad Espanola de Neurocirug´ıa. Published by Elsevier Espana, reserved.

夽 Please cite this article as: García-Feijoo P, Isla A, Díez-Tejedor E, Mansilla B, Palpan Flores A, Sáez-Alegre M, et al. Craniectomía descompresiva en el infarto malignode arteria cerebral media: percepción familiar, resultados y factores pronósticos. Neurocirugía. 2019. https://doi.org/10.1016/j.neucie.2019.07.002 ∗ Corresponding author. E-mail address: [email protected] (P. García-Feijoo). ˜ ˜ S.L.U. All rights reserved. 2529-8496/© 2019 Sociedad Espanola de Neurocirug´ıa. Published by Elsevier Espana,

NEUCIE-391; No. of Pages 7

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Craniectomía descompresiva en el infarto malignode arteria cerebral media: percepción familiar, resultados y factores pronósticos r e s u m e n Palabras clave:

Objetivo: El pronóstico en los infartos malignos de un hemisferio siembra dudas entre los

Infarto maligno de arteria

neurocirujanos a la hora de indicar una hemicraniectomía descompresiva. ¿Qué resultados

cerebral media

a corto y medio plazo se obtienen? ¿están las familias satisfechas con la cirugía una vez con

Craniectomía descompresiva

el enfermo en su domicilio?. En el presente trabajo analizamos nuestra experiencia en esta

Resultados

˜ materia en los últimos 13 anos.

mRS

Material y métodos: Incluimos en nuestra revisión a 21 pacientes intervenidos entre 2004 y

Familia

2017 siguiendo la vía clínica de nuestro centro para el ictus. Se entrevistó a los familiares ˜ y actual con la escala vía telefónica. Se midió el resultado funcional al alta, 3 meses, 1 ano modificada de Rankin (mRS). Resultados: La edad demostró estar directamente relacionada con la mRS (r = 0.56; p = 0.035) y en el 37.5% se obtuvo un buen resultado (mRS≤3). El 78.9% de los familiares entrevistados repetiría la decisión quirúrgica tomada. Conclusiones: Aportamos un grupo de 21 pacientes sometidos a craniectomía descompresiva por infarto maligno donde los mejores resultados funcionales se han dado entre los <60 ˜ anos. Las graves secuelas neurológicas en pacientes con infarto maligno sometidos a hemicraniectomía descompresiva fueron toleradas y aceptadas por la mayoría de familias a favor de su supervivencia. No debemos dejar que esta satisfacción familiar camufle el pronóstico, teniendo que contextualizarla dentro de la situación real ambulatoria de los pacientes. ˜ ˜ S.L.U. Todos de Neurocirug´ıa. Publicado por Elsevier Espana, © 2019 Sociedad Espanola los derechos reservados.

Introduction In our area, cerebrovascular diseases have an incidence of more than 55,000 cases per year and are a major cause of years of life lost (YLL) and years lived with disability (YLD),1,2 not to mention the high healthcare costs.3 In 10–15%4,5 of middle cerebral artery infarctions a phenomenon known as malignant infarction occurs. Damaged brain tissue generates oedema. As the oedema spreads, it compromises regional blood flow, culminating in a large infarction, which exerts a mass effect. This leads to an uncontrolled increase in intracranial pressure, which affects the rest of the parenchyma and brainstem, leading to severe neurological deterioration, followed by cerebral herniation and death.6 Once this process has begun, we know that even with the best intensive medical management, the mortality rate is close to 80%.4–6 Consequently, at this point one last surgical treatment step is considered as the only chance of saving life. The procedure is decompressive craniectomy,6–8 where part of the skull is removed to allow a swelling brain the room to expand. Performing this procedure on patients with already established severe neurological damage, with high chances of severe sequelae and the lack of precise clinical pathways to follow, can be extremely disconcerting for healthcare professionals having to make multidisciplinary decisions about how to approach malignant infarction. We present here a retrospective review of decompressive craniectomies performed to treat malignant infarction in our centre. We assessed the functional prognosis, the impact and

the utility of the surgery. Our aim was to obtain an overall view of the process, to be able to use the data in future cases when considering this procedure, and so offer more objective information to the families and healthcare professionals involved in making such an important decision.

Material and methods Inclusion criteria Our review includes 21 patients treated in our centre by decompressive hemicraniectomy for a malignant infarction over the last 13 years (2004–2017). The clinical pathway of our stroke centre was followed. Participants’ age was restricted to those over 18, with a diagnosis of malignant infarction originating in the middle cerebral artery and valid medical history and available imaging tests.

Questionnaires Specific questionnaires were addressed to family members of the patients and interviews were carried out by telephone, using the DESTINY-S5 and other study surveys as a model.9 Information was collected on the current situation, home autonomy and opinion of family members. We interviewed family members of survivors and of the deceased. The modified Rankin scale (mRS) was chosen as it is a validated and specific scale within the scope of stroke, in addition to being the most used by other working groups.4,5

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Table 1 – Patient characteristics.

Table 2 – Main complications recorded after decompressive hemicraniectomy.

Gender Male Female Location Left MCA Right MCA Dominance Right-handed Left-handed Age ≤60 years >60 years Previous functional status mRS ≤1 mRS >1

11 (52.38%) 10 (47.62%) 10 (47.62%) 11 (52.38%) 21 (100%) 0 (0%)

Complication

Frequency

Pneumonia Urinary tract infections Pressure sores Shunt-dependent hydrocephalus Surgical revision post-cranioplasty Tracheobronchitis External ventricular drain

42.85% 42.85% 21.42% 16.66% 15.38% 14.28% 7.14%

14 (66.66%) 7 (33.33%) 21 (100%) 0 (0%)

MCA: middle cerebral artery; mRS: modified Rankin Scale. An even number of male and female patients were included and all were right-handed, assuming left brain dominance. Two thirds of those operated on were aged 60 or younger.

The mRS score was calculated at different points after surgery: discharge, 3 months, 12 months and current (at the time of the survey). In the vast majority of cases it was possible to obtain the discharge and 3-month mRS scores using those reported in the discharge reports and at outpatient check-ups.

Results Epidemiological data and surgical technique The mean age at the time of the intervention was 54.76 ± 8.67 years, with the range being 35–69 (Table 1). The majority were active workers outside the home (68.4%) whose contributions accounted for 100% (26.3%) or a portion (52.6%) of household income. This was a homogeneous population with all those operated on having good family support. Broad frontotemporoparietal hemicraniectomy was performed in all cases (>12 cm in length anterior-posterior), with the technical aspects at the discretion of the surgeon. We are aware of how important it is to achieve good decompression in this type of surgery,10–16 so in all cases the bone flap was taken as far as the middle cranial fossa floor. Our clinical pathway considers 48 h as ideal indication for decompression, and over 80% had been operated on within the first 72 h of the onset of stroke. Mean NIHSS on admission was 17.87 (±4.27). Glasgow Coma Scale (GCS) score prior to surgery was 7.81 ± 2.23 and there was a mid-line shift on the CT of 8.975 ± 3.06 mm.

Complications The main complications are shown in Table 2. Mechanical ventilation was required in 100% of cases and 42.85% required tracheostomy. Hydrocephalus, which is relatively common after decompressive craniectomy (30–48.7%17,18 ), occurred in 16.66% of cases in our series and was treated by ventriculoperitoneal

shunt; one patient also required a temporary external ventricular drain. Among the survivors at 12 months post-intervention (n = 16) the bone flap was replaced in 81.25% (n = 13). The bone flap was not replaced in two patients in a minimally conscious state and waking coma, or in a third who refused the surgery. There was one case of aesthetic defect of the autologous cranioplasty which meant it had to be replaced by a synthetic one, and one case of infection of the flap by Pseudomonas aeruginosa, for which it had to be removed. In 28.57% of our patients, there was haemorrhagic transformation of the infarction, in all cases occurring before surgery, with 75% being intraparenchymal (PH) and 25% petechial (IH). The functional outcomes in this group were no worse than in those who did not suffer bleeding events, and their mRS was 3 at 12 months; in the group without transformation, mRS was 3.5. It has been suggested that type II (PH-2) may lead to worse outcomes in functional terms.19 Al-Jehani et al. showed that the presence of different forms of haemorrhagic transformation did not affect the functional prognosis if they survived the hemicraniectomy.19 In these patients there were more thrombectomies and thrombectomies combined with fibrinolysis.

Functional outcomes In the analysis of the functional outcomes we excluded the deceased patients (mRS 6) as their functional recovery could not be assessed. At discharge, the mean mRS was 4.53 ± 0.51; at three months post-intervention, 4.12 ± 1.02; and at 12 months, 3.57 ± 1.01. The “current” moment means the mRS on the date of the telephone interview (2017) and includes patients with very different recovery times since surgery (from a few months to 13 years), in addition to different ages at presentation. Here we measured a mean mRS of 3.46 ± 1.06. There is a clear tendency (Fig. 1) towards a worse functional prognosis (higher mRS) in older patients (r = 0.56; p = 0.035). To classify the functional outcomes as good or poor, there are a number of ethical, individual and socio-cultural considerations which do not represent the reason for this study. In DESTINY-S5 this was considered as one of the main objectives of the study and the international consensus states that a result can be classified as acceptable when the mRS is less than or equal to 3 (Moderate disability: requiring some help but able to walk without assistance, with the aid of a walking stick).

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Good outcome (mRS 0-3)

5

Poor outcome (mRS 4-5) Death

3

<50 years (n=5)

2

Progress

Current mRS

4

1 40

50 Male

60 Current age Female

70

80

Current

75%

25%

0%

1 year

75%

25%

0%

3 months

75%

25%

Discharge 0% 0%

Fitted values

0% 0%

100% 20%

40%

60%

80%

100%

Coefficient of correlation = 0.56

50-60 years (n=9)

Progress

Fig. 1 – Relationship between current age and current mRS. The mRS at 12 months after surgery in relation to age was also shown to be related, and despite the small sample size, it was almost statistically significant. mRS: modified Rankin Scale.

Current

37.50%

1 year

37.50%

37.50%

75%

12.50%

20%

11.11% 60%

40%

100%

80%

60 years (n=7)

Progress

Current 0%

20%

60%

14.28%

85.71%

3 months 0%

0%

33.33%

66.66% 20%

1 year

85.71%

Discharge0% 20%

40%

14.28% 60%

80%

100%

Fig. 2 – Analysis of functional prognosis by age subgroups. mRS: modified Rankin Scale.

Survival function 1.00

0.75

0.50

0.25

0.00 0

Mobility is fundamental in the assessment of functional outcomes and carries a great weight in the mRS. Among those who survive more than 12 months, 55% are able to walk, 30.76% usually use a wheelchair; either alone or assisted; almost 40% use an orthotic device, the most com-

12.50%

88.88%

0%

Autonomy and language

50%

3 months 12.50% Discharge 0%

At 12 months, half of our patients had poor outcomes (mRS 4 or 5), 12.5% had died and 37.5% had good outcomes. Virtually none of the patients recovered the same functional autonomy as prior to the stroke, and only one case had an mRS of 1. In the age analysis we obtained differences which, due to the sample size, did not reach statistically significant levels, but which are consistent with the literature in this regard.20,21 We divided our patients into three groups: aged <50, aged 50–60 and aged >60 (Fig. 2). The best outcomes were among the youngest patients, where three out of four evolved favourably, and we found no cases of death in the postoperative period or during follow-up. Most of the cases were in the 50–60-year-old age range (n = 9). In this subgroup, one in three had good outcomes and the mortality rate was 12.5% at 12 months. The worst outcomes were among the over-60 s; only 20% had an mRS ≤3 at one year and the mortality rate was double that of the 50–60-year-olds. One year after surgery, the young patients (<50) had improved 1.85 points on average in the mRS compared to discharge, while amongst the over-60 s any improvement was much less noticeable, with only 0.75 points of recovery on average. There is an instantaneous decrease (Fig. 3 in the first section of the survival function, corresponding to postoperative deaths among our patients (9.53%, n = 2), which is sustained for the first 12 months. Over 75% of our patients lived beyond eight years.

25%

365

730 1095 1460 1825 2190 2555 2920 3285 3650 4015 4380

Days since surgery

Fig. 3 – Survival function after decompressive craniectomy.

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Outpatient situation 80% 70% 60% 50% 40% 30% 20% 10% 0% Hired home carer

At home alone

Answers the telephone

Manages Depression medication

Vegetative Dominant Goes out state hemisphere every day global aphasia

Driving again

Fig. 4 – Outpatient situation: includes patients who survived the stroke and have at least one year of follow-up since surgery; 35.7% managed to return home to the extent that they could be alone at home for long periods of time; 22.22% of the families needed to hire a home care assistant, although in the surveys carried out up to 85.71% of the patients need help for activities of daily living, and in most cases this is provided by the relatives themselves;42.85% are able to manage their own medication.

mon being a walking stick and an anti-equine splint. Only 15% mobilise unaided (Fig. 4). Another 15% of our series (n = 2) remain permanently bedridden due to their severe neurological sequelae; 50% of the patients were discharged from a rehabilitation centre and 36% were referred to other hospitals or other medical departments for rehabilitation purposes; and 14% returned to their homes with an outpatient rehabilitation programme. In left middle cerebral artery infarctions mixed aphasia was the most common type (80%). At the “current” point, 28.6% of global aphasia was reported, with 57.1% incomplete motor aphasia in varying degrees and 14.3% pure complete motor. Almost a quarter of our patients failed to achieve adequate communication skills: vegetative state (n = 1); minimally conscious state (n = 1); global aphasia (n = 2). A total of 55.5% of patients with their language abilities affected (n = 9) achieved at least partial recovery of their ability to communicate (n = 5). We have included in this group the cases of pure complete (n = 1) and incomplete (n = 4) motor aphasia. Of the respondents, 42.85% have been diagnosed at some point with depression which required treatment, two thirds being females, while in the first degree relatives, there was an incidence of 27.2%.

Discussion The results of our review can help neurosurgeons in deciding when to indicate hemicraniectomy, and provide family members and other medical staff with a realistic idea of the prognosis. The novelty of this study is the use of the family as the connecting thread. The ideal age established by the international community in which hemicraniectomy is indicated is 60 or under1,5,14,20,22,23 (level of evidence Ia, grade of recommendation A). For patients over the age of 60, the established evidence for good outcomes is Ib, with grade of recommendation A.

5

The current mRS in relation to the current age (2017) maintained a statistically significant relationship (p = 0.035) which reflects the importance of age in the recovery prognosis. It was the only prognostic factor found in this review directly related to the functional outcomes (r = 0.56). Some 75% of young patients (<50 years) were able to achieve good outcomes, while only 20% of those over 60 did so. The post-intervention mortality rate among the older patients was double that of the younger patients. In DESTINY II24 and others25 hemicraniectomy was assessed in people over 60, and although it can improve survival, it did not produce the same good functional outcomes as seen in young patients. In our series, a good correlation was found between the functional outcomes at 12 months and the current situation, so we recommend an Outpatient assessment at this point of the recovery process as a prognostic marker of the functional benefit provided. Neither being male, nor the midline shift, GCS score or the affected side were related to the functional outcomes in our patients. A patient’s ability to communicate, which will usually be more damaged when the dominant hemisphere is affected, can influence the neurosurgeon’s decision in terms of the indication for surgery.5,20 Authors such as, Benejam et al reviewed the outpatient situation using Sickness Impact Profile scores, they found no relationship between the affected hemisphere, different clinical parameters, except in the communication section (p = 0.003).26 We also found the infarcted hemisphere not todecisive in our group of patients, as the measuring instrument used (mRS) does not cover the aspect of language in particular. As our review showed, studies conducted on this subject claim that aphasia is not necessarily permanent in the dominant hemisphere. Moreover, if the surgery is early and the patient is young, they will have a better chance of recovering language, although probably not in full. Therefore, hemicraniectomy should not be rejected in patients with infarctions of the dominant hemisphere for that reason alone. Other studies in this area27 sustain that two out of three patients will have aphasia 12 months after decompressive craniectomy in the dominant hemisphere, and up to 62% of aphasic patients will meet DSM criteria for depression (11–33% for non-aphasics). Among those who survive longer than 12 months, 64.28% return to their homes, while 28.57% are permanently institutionalised in some type of centre. This point is of great importance as, with our indication for decompression craniectomy, potentially almost a third of patients will not be able to return to their homes and, despite having good initial family support, their families will not be able to cope with the burden. In our series, 35.7% of survivors at one year said they could remain alone at home without assistance for a variable period of time. One of our main objectives was to find out whether or not patients and family members were satisfied with the surgery. This issue can be difficult to measure, as there is a significant bias due to the ethical and socioeconomic individualities of each family.

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They were asked the question, “Would you make the same decision (decompressive hemicraniectomy) again with your family member?”; 78.94% answered that they would, which correlates quite well with the data obtained by previous studies in this area2,9,15,28 ; 15.7% said they would not and 5.2% did not answer. Among those not satisfied, we found the presence of very severe sequelae, such as waking coma, blindness and complete aphasia, and the fact that this group of patients was older than the satisfied group (age 61 vs 52.7). The resignation in terms of the sequelae of a malignant infarction which was noted during the telephone conversations does not prevent family members from singing the praises of the life-saving nature of the hemicraniectomy, and the role of the neurosurgeon, previously non-existent, is seen to be greatly reinforced and supported, including at the family level. In light of the data, the families express complete approval of hemicraniectomy, showing us how important it is that we mediate more when it comes to making decisions for others. We must not fall into the so-called disability paradox, which tends to underestimate a person’s ability to adapt to a new disability situation. Many interviewees seemed hesitant before answering the question, while others were even offended to be asked whether performing life-saving surgery on their family member had been the right thing to do. The moral aspect that constantly permeates our work can cause our interviewees not to answer freely or not to be as honest as we might hope, camouflaging what they are really thinking. These rates of acceptance must therefore be contextualised to give us a holistic view of what the prognosis of decompressed malignant infarction really involves through more objective data, as we provide in this review. In the indication for decompression surgery, the decision about which ultimately falls to the neurosurgeon, the family must take an active part, and we must not ignore the patient’s own wishes in life. It is the duty of the neurosurgeon to concisely inform about the prognosis of a malignant infarction before performing decompression surgery on a patient, and in this study we have added further data on a standard Spanish population.

Conclusions Among the parameters analysed to assess our outcomes, it seems to be only age that worsens the prognosis. The midline shift, the level of consciousness measured by the Glasgow Coma Scale and the infarction in the left (dominant) hemisphere had no negative prognostic significance with our measurement tools. The functional status at discharge of older patients (aged >60) will be more similar to their final outcome after 12 months, while in younger patients (especially aged <50) in our series the margin of improvement is far superior. We consider one year post-intervention as a good time to assess the functional outcome after decompressive craniectomy at the Neurosurgery Outpatient Clinic. In our study we used the family as a connecting thread, and we want to highlight their role as active participants in deci-

sion making, since they will be the cornerstone of the future of these patients. The high satisfaction rate with surgery is a faithful reflection that despite the severe neurological damage suffered, this is a disability that families are willing to tolerate. This family satisfaction should not camouflage the prognosis, so we must contextualise the results with the real outpatient situation of the patients.

Conflicts of interest The authors declare that they have no conflicts of interest.

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