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Neurology: Clinical Practice logoLink to Neurology: Clinical Practice
. 2021 Apr;11(2):158–166. doi: 10.1212/CPJ.0000000000000852

Predicting Language Outcome After Left Hemispherotomy

A Systematic Literature Review

Karen Lidzba 1,✉, Sarah E Bürki 1, Martin Staudt 1
PMCID: PMC8032409  PMID: 33842069

Abstract

Objective

Hemidecortication is a therapeutic option in patients with drug-resistant structural epilepsy. If surgery is performed early enough in left-hemispheric pathology, the plasticity of the developing brain may enable the right hemisphere to take over language—if this has not occurred before surgery. A systematic overview of potential predictors of language outcome after left hemidecortication in children is warranted.

Methods

In a systematic literature review, we analyzed 58 studies on language lateralization after congenital or postneonatally acquired left-hemispheric pathology, and on language outcome after left-sided hemidisconnection, such as hemispherotomy. Single-subject data were pooled to determine the distribution of lateralization across etiologies in congenital lesions and across age groups in acute postneonatal lesions. A hierarchical linear regression assessed the influence of age at surgery, lesion type, age at seizure onset, and presurgery language function on language outcome after left hemidecortication.

Results

In acute postneonatal lesions, younger age at injury was significantly associated with right-sided language lateralization (Cramér V = 0.458; p = 0.039). In patients with hemidecortication, age at surgery was not significantly associated with language outcome (Cramér V = −0.056; p = 0.584). Presurgical language function was the most powerful predictor for postsurgical language outcome (F4,47 = 7.35, p < 0.0001), with good presurgical language bearing the risk of postsurgical deterioration. In congenital pathology, right-sided language lateralization was most frequent in pre-/perinatal stroke (Cramér V = 0.357; p < 0.0001).

Conclusions

We propose a presurgical decision algorithm with age, presurgical language function, language lateralization, and left-hemispheric structural pathology as decision points regarding surgery.

Right-hemispheric reorganization is common after left-sided pre-/perinatal brain lesions.1–6 But how long will the plastic window be open, preventing a child from retaining aphasia after left-sided hemispherotomy?

We insufficiently understand the factors predicting language outcome after hemidecortication. Rasmussen's and Milner's series of Wada tests in epileptic patients demonstrated that the developing brain can represent language in the right hemisphere after a left-hemispheric lesion.7 The neurosurgical literature often assumes as common knowledge that recovery from extensive damage to left-hemispheric language areas is possible until school age.7,8 However, studies trying to identify a timeframe conclude that regarding hemidecortication, age seems to be less important than etiology.9 In their “Review of cognitive outcome after hemidecortication in humans,” Vargha-Khadem and Polkey10 demonstrated that even after late left hemispherectomies, language outcome could be surprisingly good. The interactions between age at insult, lesion type, epilepsy onset/severity, and postsurgical seizure freedom may determine whether language can be retained or recovered after left hemidecortication.

We analyzed publications addressing language in patients with pre-/peri- and postnatal left-hemispheric brain pathology (acute and progressive), with and without hemispherotomy. To inform a clinical decision algorithm regarding possibility for surgical treatment, we asked the following questions:

  1. (a) What are the age limits for successful right-hemispheric language reorganization and (b) which factors can modify these limits? Literature suggests 3 modifying factors: epilepsy, language delay, and progressive pathology.9,11,12

  2. How does, in congenital pathology, the type of brain lesion influence language reorganization?

Methods

For this review, we followed the PRISMA guidelines as completely as possible within our research question. Although the review was not registered, we make all data used available in the supplementary tables.

Literature Search and Article Selection

We conducted a systematic hierarchical search of PubMed (pubmed.org) and PsycINFO (via ebscohost.com) for studies published after the review of Vargha-Khadem and Polkey.10 Inclusion criteria were left-hemispheric pathology, age at injury <18 years, information on language lateralization (language fMRI/MEG/PET and hemidecortication), and publication date (January 1992–June 2018). We included studies with mixed adult/pediatric samples when they presented individual pediatric data. For language lateralization, we accepted fMRI, MEG, and PET. Wada tests were not accepted because in many recent publications, they were conducted unilaterally (or not further specified), leaving bilateral language lateralization possible. The exclusion criterion was potentially bilateral brain damage (e.g., traumatic brain injury or tuberous sclerosis complex).

Search terms were (“stroke” OR “brain infarction” OR “lesion” OR “malformation” OR “hemiparesis” OR “hemiplegia” OR “cerebral palsy”) AND (“prenatal” OR “perinatal” OR “congenital” OR “neonatal” OR “infant” OR “child” OR “adolescent”) AND (“language” AND (“lateralization” OR “lateralisation” OR “representation” OR “organization” OR “organisation” OR “reorganization” OR “reorganisation” OR “hemispherectomy” OR “hemispherotomy” OR “hemidecortication” OR “epilepsy surgery”)) AND (“1992/01/01”[MDAT]: “2018/06/30”[MDAT]).

Using self-developed electronic data extraction forms, we screened titles and abstracts for inclusion criteria, assessed all resulting full texts for eligibility, and categorized them according to one of the research questions (done by Karen Lidzba, Martin Staudt, Sarah Bürki, and Eva Franz): (1a) Age limits: Acute, non-progressive left-hemispheric lesions acquired postneonatally; (1b) Age limits: Hemi-decortication; (2) Underlying brain lesion: congenital pathology.

After the automatic search, we searched resulting articles for additional references and processed them in the same way. In cases of missing data in the publications, we contacted the authors.

Quality Assessment and Assessment of Bias

The Newcastle-Ottawa Scale13 provides quality assessment of case-control and cohort studies for systematic reviews. Although 5 of the 9 points are designed for the use in treatment studies, 4 of the items score population selection. For the sake of uniformity throughout our review, we used these 4 items to assess the quality of all studies included in this review, being comparative or not. In noncomparative studies, we assessed case definition and representativeness; in studies with control group, we also scored selection and definition of controls. We excluded studies if case definition was unsatisfactory. As yet, no validation has been published for the Newcastle-Ottawa Scale,13 and there is 1 critical evaluation pointing out some caveats regarding the rating of, e.g., outcome measures.14 However, because of the lack of better instruments, we opted for the truncated version that has been used before.15

Regarding assessment of bias, we adopted 5 categories of the reporting bias as assessed in Cochrane reviews,16 although we could not review intervention studies for which these categories were originally created. Table e-1 (links.lww.com/CPJ/A175) lists our (in part arbitrary) definitions for risk levels in the bias types.16 We approached the duplicate publication bias by including only the last of several studies from the same group with potentially the same patients.

Data Analyses

Age Limits for Successful Right-hemispheric Language Reorganization

We categorized language function as normal, mildly impaired, and severely impaired, based on the information given in the articles. If standardized language measures were reported, we used SDs as thresholds: less than 1 SD below mean (normal); 1 to 1.5 SD below mean (mildly impaired); and more than 1.5 SD below mean (severely impaired). If the authors did not conduct standardized tests (due to inclusion of very young or cognitively very impaired patients), we adopted their clinical impression as reported in the article. For all analyses, we set p < 0.05 as threshold of significance.

Acute Postneonatal Lesions

We included all patients with acute, postneonatally acquired focal brain lesions with documented aphasia (as defined in the original article) and language lateralization at follow-up (principal outcome measures). We included patients who fell ill before age 3 years if the lesion affected left-sided language areas on neuroimaging.

We categorized language lateralization, either adopting the authors' categorization or based on laterality indices (LIs) provided in the publication. If the authors provided both regional and hemispheric LI, we used the more specific regional LI. We categorized values between −0.2 and +0.2 as bilateral and values ≥0.2 or ≤−0.2 as right or left lateralized (direction varies between groups). We assumed successful right-hemispheric language reorganization if normal/mildly impaired language was associated with right-hemispheric language lateralization. We categorized age at injury as infancy (≤2 years) and childhood/adolescence (≥3 years).

Modifiers of Age Limits: Epilepsy, Language Function, and Progressive Pathology

We included patients with left hemidecortication, when the publication included data on pre- and post-surgery language performance. The principal summary measure was the difference between post- and presurgical language function. We categorized pre-/post-surgery difference in language function as follows: improvement/deterioration for gain/loss ≥1 SD in standardized language assessment (or verbal IQ) or shift to better/lower category and no change for the remainder. We assumed successful right-hemispheric language reorganization if language did not deteriorate after surgery.

To further characterize the potential modifiers of age limits for successful right-hemispheric language reorganization, we performed a hierarchical linear regression on the variable pre-/post-surgery language change (deterioration and no deterioration), with the following predictors entered stepwise: (1) age at hemidecortication (months), (2) lesion type (malformation; pre-/perinatal stroke; Rasmussen encephalitis; Sturge-Weber syndrome), (3) age at seizure onset (months), and 4) presurgery language function (severely impaired, mildly impaired, and normal). We excluded postneonatal stroke due to the negligible sample size (n = 3).

Influence of the Underlying Brain Lesion

To answer the second research question, we analyzed the single-subject language lateralization data available of all patients with congenital pathology, i.e., brain malformations, developmental tumors, and pre-/perinatally acquired focal lesions. These analyses were independent of language performance data.

Results

Search Output

Figure 1 illustrates the search output, and table e-2 (links.lww.com/CPJ/A175) lists all 58 resulting articles grouped by category. We found mostly single-case studies and case series (postneonatal lesions: 7/12; hemidecortication: 20/25; congenital lesions: 8/26). Five studies on postneonatal lesions, 10 on hemidecortication, and 7 on congenital lesions included a control group. For case definition (according to the Newcastle-Ottawa Scale), most studies relied on MRI plus other clinical data. Around half of the studies had adequate case representativeness (postneonatal lesions: 6/12; hemidecortication: 15/25; congenital lesions: 10/26).

Figure 1. Search Output and PRISMA Steps.

Figure 1

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aExclusion criteria: no or wrong pathology/surgery (n = 36); no data on language/language representation (n = 22); no (individual) child data (n = 3); pure methods article (n = 10); no study (n = 12); and article not in English (n = 6). bAdditional references from articles and reviews in search output. cExclusion criteria: no relation made between side/age at injury and language outcome (n = 18); insufficient or missing lesion characterization (n = 8); same patients reported in more than 1 article (n = 5); no language outcome or (fMRI or PET) lateralization reported (n = 13); and pure methods article (n = 5).

Risk of reporting bias was low to medium for data on congenital and postneonatal lesions and medium to high for data on hemidecortication (figure e-1, links.lww.com/CPJ/A174).

Age Limits for Successful Right-hemispheric Language Reorganization

Acute Postneonatal Lesions

Statistical Analysis

Individual data on language lateralization were available in 31 patients fulfilling all inclusion criteria (tables e-2 and e-3, links.lww.com/CPJ/A175). Lesions acquired until age 2 years showed a higher proportion of subsequent right-hemispheric language representation than those acquired after age 2 years (Cramér V = 0.458; p = 0.039; figure 2).

Figure 2. Successful Right-hemispheric Language Lateralization After Acute Postneonatally Acquired Left-hemispheric Lesions to a Previously Healthy Brain.

Figure 2

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Figures in chart are absolute numbers.

Narrative Literature Review

Right-hemispheric language lateralization is rare following postneonatally acquired left-hemispheric stroke.17–22 Most patients with successful right-hemispheric language reorganization were younger than 3 years.22,23 In patients with lesions acquired between 3 and 5 years of age, fMRI lateralization was bilateral or left.17,18,21 In children aged 5 years and older at the time of injury, language recovery has been associated with left-lateralized language on the short term,17 but with right lateralization on the long term.19

Patient groups who had recovered from aphasia after postneonatally acquired left-hemispheric cerebral vascular insult demonstrated right-lateralized, bilateral, or left-lateralized language in fMRI, whereas the language of healthy controls and that of recovered patients with adult aphasia were left lateralized.4,17,18 Lesion characteristics did not seem to be related to language lateralization.4,18

Modifiers of Age Limits: Epilepsy, Language Function, and Progressive Pathology

Statistical Analyses

We identified 59 patients with sufficient language data before and after left-sided hemidecortication (tables e-2 and e-4, links.lww.com/CPJ/A175). Younger age at surgery correlated at trend level with positive postsurgical language outcome (Spearman ρ = −0.248, p = 0.058, 2 tailed).

In the hierarchical linear regression analysis (table 1), age at surgery did not predict postsurgical language outcome. Lesion type added 9% to the variance explained by the first model, age at seizure onset added 17% to the second model, and presurgical language function added 21% to the third model. The final model with all 4 predictors was most meaningful (F4,47 = 7.35, p < 0.0001). Presurgical language function was the only relevant coefficient in this model. Patients with initially impaired language function had a good chance to remain stable or improve postsurgically, whereas patients with initially good language function had a risk of deterioration (figure 3).

Table 1.

Hierarchical Stepwise Regression Analysis on the Predictors of Postsurgical Language Outcome Compared With Presurgical Language Function (Deterioration vs No Deterioration)

graphic file with name NEURCLINPRACT2019044370TT1.jpg

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Figure 3. Change in Language Function After Left-sided Hemidecortication.

Figure 3

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Presurgical language function, etiology, and age at surgery. (A) Patients with impaired presurgical language. (B) Patients with normal presurgical language.

Narrative Literature Review

Across patients with drug-resistant epilepsy, etiology predicts postsurgical language outcome9,24–28 much better than age at surgery.9,25,29 Patients with large malformations of cortical development demonstrate the least linguistic progress after surgery, whereas patients with Rasmussen encephalitis or infarctions fare better. Etiology determines age at seizure onset and age at surgery.26 Irrespective of etiology or hemisphere, patients improved in language function for at least 12 months postsurgery,25 especially those with better presurgical cognitive development.28 Shorter epilepsy duration and successful withdrawal of antiepileptic medication correlated with better postsurgery language function.25

Patients with brain malformations are young at seizure onset and surgery is often performed at an early age. Compared with other groups, their intelligence and language performance is lowest before and after surgery.26,30–32 Children with malformations often continue to have seizures postoperatively,8,28 and seizure control predicts postoperative language development.9

Patients with Rasmussen encephalitis often have a better preoperative cognitive and linguistic level than patients with other etiologies.26 Left-hemispheric perinatal infarctions leading to drug-resistant epilepsy in infancy often entail severe mental retardation presurgically, but accelerated development postsurgically.33 In contrast to malformations, acquired and progressive pathology is associated with laterality effects in language function, both pre- and postsurgically.9,26,29,34 Left-sided surgery may lead to postsurgical aphasia (as defined by the authors of the original articles) or severe language deficits in patients between 6 and 17 years initially35–38 and to subnormal language function at longer follow-up.27,37,38 In Rasmussen encephalitis, language often deteriorates presurgically and may shift to the right hemisphere.38–40 Published data on postsurgical language recovery are largely based on case reports and draw a heterogeneous picture (table e-2, links.lww.com/CPJ/A175).

Influence of An Underlying Congenital Brain Lesion

Statistical Analyses

We included 134 patients with congenital left-hemispheric lesions and language lateralization data (tables e-2 and e-5, links.lww.com/CPJ/A175). Patients had left-hemispheric malformations of cortical development (n = 41; focal cortical dysplasia, heterotopia, and polymicrogyria), developmental tumors (n = 25; dysembryoplastic neuroepithelial tumor and ganglioglioma), and pre- or perinatal stroke (n = 68; venous infarctions and arterial ischemic stroke). Most studies determined language lateralization by fMRI word generation tasks (N = 19). One study each reported MEG and PET data.

Lateralization differed between lesion types (Cramér V = 0.357; p < 0.0001; figure 4). Right-lateralized language was frequent in pre-/perinatal stroke (60% right/25% bilateral/15% left), whereas it was rare in brain malformations (18% right/15% bilateral/68% left). The group of developmental tumors showed an intermediate pattern (35% right/12% bilateral/54% left).

Figure 4. Language Lateralization After Congenital Left-sided Brain Pathology.

Figure 4

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Absolute patient numbers in the graph.

Narrative Literature Review

Age should be a first switch in our algorithm: any brain younger than 3 years seems to be able to represent language in the right hemisphere without obvious deficits.

Pre- or perinatally acquired left-hemispheric stroke was often associated with right-lateralized or bilateral activation for a range of language tasks, especially concerning expressive language.1–5,41 Right-hemispheric regions involved in language processing typically mirrored the left-hemispheric ones in healthy controls.1–3,41 Compared with normal controls regarding variability of brain activation, patients involved additional supramodal brain regions in language tasks, leading the authors to infer the usage of alternative strategies.2,42 Lesion size did not correlate with language lateralization.2,5,41 In patients with pre-/perinatal infarctions, damage to the Broca area,3 the facial motor tract,1 or the insular cortex and the supramarginal gyrus6 might be predictors for right-hemispheric language representation.

Brain malformations and developmental tumors rarely induced right-hemispheric language representation,43–45 unless the lesion involved the left inferior or middle frontal gyri.24,46 Malformed brain regions usually did not harbor language; however, it tended to be localized in close vicinity.47 Age at epilepsy onset inconsistently correlated with language lateralization.12,43,44 Only few studies assessed language performance in detail, and the results are inconsistent, with better verbal functions being correlated both with typical37 and with atypical language lateralization.48

Discussion

Based on this literature review, we developed an algorithm aiding the decision-making process before left-sided surgery, with respect to the preservation of language (figure 5).

Figure 5. Flowchart of the Proposed Decision Algorithm Based on the Results of the Literature Review.

Figure 5

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Admittedly, we have inferred this algorithm from a low-level evidence base. Because of ethical reasons, randomized controlled trials do not—and probably will not ever—exist on left-sided hemispherotomy in children with language as primary outcome. Thus, our suggestions must stay tentative, and decisions must always be based on the individual case.

Age should be a first switch in our algorithm: any brain younger than 3 years seems to be able to represent language in the right hemisphere without obvious deficits. During the first 3 years of life, surgery can therefore be assumed low risk regarding language outcome. This is in line with recent data suggesting that, during the first 3 years of life, surgery outcome on general cognitive development is favorable.49,50 Obviously, the third birthday is an arbitrary cutoff derived from the little data available in the literature—a broad landmark rather than a definite milestone.

In children older than 3 years, the presence or absence of language function is the next checkpoint. In a preverbal child, there are 2 options: either the child remains nonspeaking or it develops language after surgery—maybe facilitated by the cessation of seizures. This assumption is based on the hierarchical regression results, where presurgical language function dominated all other predictors (age at surgery, age at seizure onset, and pathology) with respect to postsurgical language outcome. Children with impaired presurgical language function had a good chance to improve or remain stable, whereas children with good language function had a risk of deterioration.

The role of the underlying brain lesion becomes relevant when language mapping is not possible or inconclusive.

The role of the underlying brain lesion becomes relevant when language mapping is not possible or inconclusive. In brain malformations and developmental tumors, language is usually represented in the left hemisphere.24,47 Pre- or perinatally acquired infarctions have a high probability of right-hemispheric language representation; however, 40% of these patients still have left-hemispheric contribution. Thus, in speaking patients older than 3 years, without language lateralization data, left-sided surgery can always produce a language loss.

For these individual considerations, literature on patients who underwent left-sided hemidecortication is informative. It illustrates that language outcome depends on a complex interplay of type and location of underlying pathology, presurgical language function, age at seizure onset, and age at surgery. If a brain is to be protected from destruction by a progressive disease such as Rasmussen encephalitis, the risk of aphasia is often accepted. The published cases demonstrate that even adolescents can recover considerably from postsurgical aphasia. Importantly, postsurgery seizure control determined, in part, linguistic development.27

Our study has several limitations. We used databases to retrieve the studies analyzed. The fact that we excluded most studies identified and that we retrieved a large part from other sources illustrates the lack of consent on definitions and diagnoses in the field of language representation, language reorganization, and early brain lesions or childhood epilepsy. Compared with the randomized controlled trials in common diseases, study quality is relatively low with respect to case representativeness or—if included at all—the selection of controls, but all studies reliably characterized the underlying disease. With respect to outcome variables, we had to work with broad categorization, based on standardized testing in some cases, but relying on clinical impression in others. By including case reports, we must acknowledge publication bias as a relevant danger: unexpected individual courses of disease are published more often than cases with a less spectacular outcome. However, the large proportion of case studies reflects the low prevalence of hemidecortication, and thus, a case report on this condition in a child is still worthwhile whatever the outcome. In addition, in all 3 analyses, we also included data from larger studies, and these data do match the case report data.

Acknowledgment

The authors thank Eva Franz for her help with article screen and quality check and Prof. Ilves and Dr. Elkana for their willingness to provide additional data.

Appendix. Authors

Appendix.

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Study Funding

No targeted funding reported.

Disclosure

The authors report no disclosures relevant to the manuscript. Full disclosure form information provided by the authors is available with the full text of this article at Neurology.org/cp.

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