INTERNATIONAL JOURNAL OF NEUROSCIENCE

1 https://doi.org/10.1080/00207454.2018.1518905
54
2 55
3 RESEARCH-ARTICLE 56
4 57
5 Hypertensive thalamic hemorrhage: analysis of short-term outcome 58
6 59
7 Jos

e L. Ruiz-Sandovala,b, Erwin Chiquetec, Gustavo Parra-Romeroa, Karina Carrillo-Lozaa, Juan D. Parada- 60
8 Garzaa, H

ector R. Pe
rez-Go

mezd, Miguel R. Ochoa-Plascenciae and Leonardo Aguirre-Portilloe 61
9 a
Department of Neurology, Hospital Civil de Guadalajara ‘Fray Antonio Alcalde’, Guadalajara, Jalisco, M
exico; bTraslational 62
10 Neurociences Institute, Department of Neurosciences, Centro Universitario de Ciencias de la Salud (CUCS), Universidad de 63
11 Guadalajara, Guadalajara, Jalisco, Mexico; cDeparment of Neurology and Psychiatry, Instituto Nacional de Ciencias M
edicas y 64
Nutrici
on ‘Salvador Zubir
an’, Ciudad de M
exico, M
exico; dDeparment of Infectology, Hospital Civil de Guadalajara ‘Fray Antonio
12 Alcalde’, Guadalajara, Jalisco, M
exico; eDepartment of Neurosurgery, Hospital Civil de Guadalajara ‘Fray Antonio Alcalde’, Guadalajara,
65
13 Jalisco, M
exico 66
14 67
15 68
ABSTRACT ARTICLE HISTORY
16 Background: Hypertension is the main cause of intracerebral hemorrhage with a thalamic loca- Received 18 January 2018 69
17 tion frequency that varies from 6% to 26.5%. Revised 30 July 2018 70
Objective: We aimed to identify clinical and radiological features that could impact the short- Accepted 27 August 2018
18 71
term prognosis in patients with hypertensive thalamic hemorrhage (HTH).
19 KEYWORDS 72
Methods: Consecutive patients presenting to a tertiary referral hospital with HTH were analyzed Hypertension; intracerebral
20 from 2010 to 2014. Clinical features at emergency department and a 30-day outcome using the 73
hemorrhage; mortality;
21 modified Rankin Scale (mRS) were obtained. outcome; thalamus 74
22 Results: A total of 104 patients were studied (53 women, mean age 68.2 years, range 27–91 75
years), 91 (87.5%) of them with hypertension history. Mean hemorrhage volume was 12.2 mL
23 (range 2–45 mL), without significant differences according to gender or age group. Irruption into 76
24 the ventricular system occurred in 79 (76%) cases. Thirty-day mortality was 38.5% and occurred 77
25 with a higher frequency in men, in patients with GCS <8, intraventricular irruption, ventriculos- 78
tomy, and intracerebral hemorrhage volumes >15 mL.
26 Conclusions: Although HTH is associated with relatively small hemorrhage volume, it had a 79
27 higher frequency of ventricular irruption and bad prognosis at short-term. 80
28 81
29 82
30 83
31 Introduction Neurosurgery Service of Hospital Civil de Guadalajara 84
32 ‘Fray Antonio Alcalde’ (HCGFAA) with clinical and 85
Intracerebral hemorrhage (ICH) represents 10%–15%
33 tomographic evidence of ICH. In all, 104 patients 86
34 of all acute cerebrovascular events with a higher 87
(26%) corresponded to hypertensive etiology and thal-
35 prevalence observed among Asian and non-white 88
amic location and were selected for the present study
36 American population, which present at younger age 89
purpose. Demographic data, history of main vascular
37 and deeper brain location, with significant mortality 90
risk factors as hypertension, diabetes, dyslipidemia,
38 (30%–35% deaths at 30 days) and morbidity [1,2]. 91
alcohol intake, smoking and clinical features and
39 Thalamic hemorrhage occurrence varies from 6% to 92
Glasgow coma scale (GCS) at hospital presentation
40 26.5% among all ICH locations [3–5]. Thalamic ICH has were registered. Those patients with high alcohol intake 93
41 been poorly reported in spite of this frequency, focusing or with any illicit drug abuse were excluded. Diabetes 94
42 mainly on clinical aspects [3,6–9] and scarcely about and hyperlipidemia were defined by history of diabetes 95
43 prognostic factors [10–15]. The aim of this study is to or hyperlipidemia with or without treatment. 96
44 identify the short-term prognosis determinants of In-hospital complications and a 30-day outcome 97
45 patients with hypertensive thalamic hemorrhage (HTH). were also obtained. All patients of this study had com- 98
46 plete information since hospital arrival, during their hos- 99
47 pital stay and at 30 days post-ICH, and therefore, no 100
48 Patients and methods 101
exclusions applied based on lack of data completeness.
49 During a 4.5-year period a total of 400 patients aged HTH etiology was defined as patient’s history of 102
50 >15 years were admitted to the Neurology and hypertension (with or without antihypertensive 103
51 104
52 CONTACT Jos
e Luis Ruiz Sandoval jorulej-1nj@prodigy.net.mx Servicio de Neurolog
ıa, Hospital Civil de Guadalajara ‘Fray Antonio Alcalde’, 105
53 Hospital 278, Guadalajara, Jalisco C.P. 44280, M
exico. 106
ß 2018 Informa UK Limited, trading as Taylor & Francis Group
 2 J. L. RUIZ-SANDOVAL ET AL.

107 therapy); patients with negative history of hyperten- arrival was not significantly different between genders 160
108 sion, but with or systolic/diastolic blood pressure (SBP/ or age groups. Notably, SBP, DBP, and MAP were sig- 161
109 DBP)
140 or
90 mmHg, respectively, maintained nificantly higher in patients younger than 65 years 162
110 throughout 2 weeks or more after the hospital admis- old. Apart from traditional cardiovascular risk factors, 163
111 sion, and excluding other bleeding etiologies. In some other comorbidities in this cohort were: sleep apnea 164
112 patients, complementary neuroimaging studies were syndrome (n ¼ 3), remote postsurgical brain tumor 165
113 obtained to exclude other causes of ICH, like vascular (n ¼ 2), heart failure (n ¼ 2), lacunar stroke (n ¼ 2), 166
114 malformations or deep cerebral venous thrombosis. large-vessel ischemic stroke (n ¼ 1), pulmonary tuber- 167
115 Patients should also be free of antiplatelet agents or culosis (n ¼ 1), diabetic foot with distal amputation 168
116 anticoagulants at least 1 week before ICH. (n ¼ 1), and cataracts (n ¼ 1). Premorbid mRS was 0 169
117 The first SBP and DBP reading taken on arrival to (asymptomatic) in 97 (93.3%) subjects, of 1 in 4 (3.8%) 170
118 the Emergency Department, before anti-hypertensive and 2 in only 3 (2.9%) patients. 171
119 intervention, was used to calculate two secondary BP Mean hemorrhage volume was 12.2 mL (range 172
120 estimates: pulse pressure (PP) and mean arterial blood 2–45 mL), whereas frequency of ventricular irruption 173
121 pressure (MAP). A head CT scan was obtained in all occurred in 79 patients (76%). Hematoma extension 174
122 patients and it was analyzed to determine ICH volume involving the whole ventricular system occurred in 32 175
123 (according to the ABC/2 method), the presence and cases (30.8%). Surgical EVD was performed in 29 176
124 location of ventricular irruption. Regarding in-hospital patients (37%). The mean hospital stay was 14 days 177
125 evolution, we collected data about conservative or sur- (range 1–82 days). In-hospital systemic complications 178
126 gical management (external ventricular drainage, EVD) occurred in 40 patients (38%), being pneumonia (55%) 179
127 and development of systemic complications in all the most frequent. 180
128 cases. Thirty-day functional status was categorized as Forty patients (38.5%) died within the first 30 days 181
129 a good outcome if the modified Rankin Scale (mRS) of hospitalization. A good outcome (mRS 2) was 182
130 was 2. For purposes of this study we segmented the observed in only 13 cases. A bivariate analysis on 183
131 cohort by age (older or younger than 65 years). potential predictors of 30-day mortality showed an 184
132 Furthermore, for any intervention, futility was not con- association with the male gender, GCS <8, ventricular 185
133 sidered. In-hospital systemic complications were irruption, ventriculostomy or EVD, in-hospital systemic 186
134 defined as the occurrence of medical events, condi- complications and hematoma volume (Table 2). A 187
135 tions or diagnoses during the hospital stay that were Cox-proportional hazards model showed that inde- 188
136 not related to intracranial hypertension or other pendent predictors of 30-day mortality in this data set 189
137 neurological conditions. were hematoma volume >20 mL and irruption into 190
138 Demographic data, risk factors and clinical charac- the ventricular system (Table 3). These two factors 191
139 192
teristics are presented as measures of central tendency. showed internal consistency in bivariate cutoff and
140 193
Analyses of differences between categorical variables actuarial analyses (Figure 1). Q1
141 194
were performed with the chi-square test. Student t test
142 195
was used for the comparison of parametric quantitative
143 Discussion 196
variables while the Mann–Whitney U test was used in
144 197
non-parametric quantitative variables, both for inde- The main risk factor associated with all causes of thal-
145 198
pendent groups. A p < .05 was considered statistically amic hemorrhage in adults is hypertension, ranging
146 199
significant. Al analyses were two-tailed. Local Ethical from 56% to 100% [3,8,11–15], which has been more
147 200
Committee approved the conducting of this study. frequently related to older patients [16]. In our report,
148 201
almost 90% of patients had hypertension history due
149 202
to our study inclusion criteria. Some risk factors like
150 Results 203
tobacco use and alcoholism were more frequent
151 204
A total of 104 patients with HTH, 53 women and 51 among males and in patients <65 years, whereas pre-
152 205
men (mean age 68.2 years, range 27–91 years) were vious ICH occurred more commonly among females.
153 206
studied. Of these patients, 91 patients (87.5%) had a Patients aged <65 years arrived to the emergency
154 207
medical history of hypertension. Smoking and alcohol- room with higher BP values. This age-related differ-
155 208
ism were more frequent among men, while history of ence has been observed in hypertensive ICH in
156 209
previous ICH was predominant amongst females younger patients [3,17]. Various causes for this phe-
157 210
158 (Table 1). Alcoholism was more frequent in patients nomenon have been proposed, including hyperactivity
211
159 younger than 65 years. GCS at emergency department of the autonomic regulatory mechanisms in response to 212
 INTERNATIONAL JOURNAL OF NEUROSCIENCE 3

213 Table 1. Risk factors, clinical and radiological findings of patients with hypertensive thalamic hemorrhage stratified by gender 266
214 and age group. 267
Age 65 Age >65
215 Variable Total (n ¼ 104) Female (n ¼ 53) Male (n ¼ 51) p value years (n ¼ 38) years (n ¼ 66) p value
268
216 Age, median 68.2 (27–91) 69 (30–89) 67 (27–91) .59 52.1 (27–65) 77.5 (66–91) <.001 269
217 (range), years 270
218 Risk factors 271
219 Hypertension his- 91 (87.5) 45 (85) 46 (90) .41 58 (88) .88 272
tory, n (%)
220 Obesity, n (%) 34 (33) 20 (38) 14 (27) .26 12 (32) 22 (33) .85 273
221 Alcoholism, n (%) 11 (11) 0 (0) 11 (22) <.001 7 (18) 4 (6) .04 274
Current smoker, 13 (12.5) 3 (6) 10 (20) .03 6 (16) 7 (11) .44
222 n (%) 275
223 Diabetes mellitus, 21 (20) 11 (21) 10 (20) .88 10 (26) 11 (17) .23 276
n (%)
224 Previous ICH, 16 (15) 12 (23) 4 (8) .04 6 (16) 10 (15) .93
277
225 n (%) 278
226 Blood pressure at hospital arrival 279
227 SBP, mean 171.3 (50) 171.2 (42) 171.3 (57) .99 186.8 (45) 162.2 (40) .001 280
(IR), mmHg
228 DBP, mean 101.7 (20) 103.5 (18) 99.7 (20) .56 110.7 (20) 96.4 (15) .001 281
229 (IR), mmHg 282
MAP, mean 125.5 (27) 126.7 (32) 124.2 (29) .62 136.3 (23) 119.2 (23) .001
230 (IR), mmHg
283
231 GCS at hospital 11.2 (4–15) 11.6 (4–15) 10.9 (4–15) .30 11.7 (6–15) 11.0 (4–15) .23 284
232 arrival, 285
median (range)
233 286
ICH features
234 Volume, mean 12.2 (2–45) 11.4 (2–30) 12.9 (2–45) .86 13.2 (2–45) 11.6 (2–32) .80 287
235 (range), cm3 288
Ventricular irrup- 79 (76) 41 (77) 38 (74) .73 25 (66) 54 (82) .06
236 tion, n (%)
289
237 Ventriculostomy, 29 (28) 13 (24) 16 (31) .43 9 (24) 20 (30) .46 290
238 n (%) 291
Complications, 40 (38) 18 (34) 22 (43) .34 14 (37) 26 (39) .79
239 n (%) 292
240 In-hospital stay, 14 (1–82) 11.7 (1–49) 16.4 (1–82) .21 14.2 (1–82) 13.9 (1–80) .90 293
mean
241 (range), days 294
242 ICH, intracerebral hemorrhage; SBP, systolic blood pressure; DBP, diastolic blood pressure; MAP, mean arterial pressure; GCS, Glasgow Coma Scale; IR, 295
243 interquartile range. 296
244 brain injury with the purpose of maintaining adequate >15 mL, occurrence of systemic complications, and in 297
245 cerebral perfusion [18]. However, we found no associ- those patients who have undergone EVD. When a 298
246 ation among these BP measurements with mortality. multivariate analysis was performed adjusting for 299
247 The mortality frequency associated with all causes potential confounders, only irruption into the ventricu- 300
248 of thalamic hemorrhage is relatively high, either in- lar system and a relatively large hematoma were inde- 301
249 hospital (12%–50%) and at short- and mid-term fol- pendent predictors.Diminished GCS or level of 302
250 low-up (17%–25%) [3,7,11–14]. We observed a high 303
consciousness is an important determinant of in-hos-
251 30-day case fatality rate. This mortality is similar to 304
pital mortality, and this could be explained by the
252 305
that reported by Barraquer-Bordas et al. [8] (39%) and proximity of thalamic hematoma to the reticular acti-
253 306
Tokgoz et al. [19] (33%), also in patients with HTH. vating system [3,13–15]. Recently, it has been proven
254 307
Mortality determinants after thalamic hemorrhage that GCS alone is as effective as other scores in pre-
255 308
have been previously studied, reporting diverse clin- dicting 30-day mortality when comparing various
256 309
ical, neurophysiological, and radiological prognostic grading scores for ICH [21]. This was not the case for
257 310
factors such as consciousness level at admission, HTH in the present study.
258 311
nuchal rigidity, pupillary asymmetry, abnormal motor Studies assessing different ICH location and progno-
259 312
or somatosensory evoked potentials, ICH volume, ICH sis have shown that thalamus involvement has a high
260 313
thalamic topography, ventricular irruption of hemor- mortality; this is partly explained by its anatomical
261 314
rhage, hydrocephalus, systemic complications, and situation surrounding the third ventricle [22,23]. In our
262 315
others [3,10–15,20]. In our bivariate analysis we found analysis, almost 80% of patients had ventricular irrup-
263 316
264 association between mortality and the male gender, tion and it was a predictor of mortality, as reported by
317
265 GCS <8, ventricular irruption, hemorrhage volume other authors [3,13–15,24]. Intraventricular extension 318
 4 J. L. RUIZ-SANDOVAL ET AL.

319 Table 2. In-hospital mortality according to clinical and neuroimaging features in patients 372
320 with hypertensive thalamic hemorrhage. 373
In-hospital mortality
321 374
322 Yes (n ¼ 40) No (n ¼ 64) p value 375
323 Age >65 years, n (%) 28 (70) 38 (59) .27 376
Male gender, n (%) 25 (62) 26 (41) .03
324 Previous ICH, n (%) 7 (17) 9 (14) .64 377
325 Blood pressure at hospital admission 378
SBP, mean (SD), mmHg 168.6 (58) 172.9(31) .66
326 DBP, mean (SD), mmHg 99.8 (20) 102.8 (20) .39 379
327 MAP, mean, (SD), mmHg 123.5 (31) 126.7 (30) .49 380
PP, mean (SD), mmHg 68.8 (40) 70.1 (40) .91
328 GSC at hospital admission <8 points, n (%) 14 (35) 1 (2) <.001 381
329 Ventricular irruption, n (%) 36 (90) 43 (67) .008 382
Ventriculostomy, n (%) 26 (65) 3 (5) <.001
330 Hemorrhage volume
383
331 >5 mL, n (%) 37 (92) 52 (81) .11 384
332 >10 mL, n (%) 22 (55) 24 (37) .08 385
>15 mL, n (%) 15 (37) 11 (17) .02
333 >20 mL, n (%) 11 (27) 5 (8) .007 386
334 Complications, n (%) 26 (65) 14 (22) .001 387
335 ICH, intracerebral hemorrhage; SBP, systolic blood pressure; DBP. diastolic blood pressure; MAP, mean arterial 388
pressure; PP, pulse pressure; GCS, Glasgow Coma Scale; SD, standard deviation.
336 389
337 390
338 Table 3. A Cox proportional-hazards model for prediction of prognosis and to reduce mortality, ICH acute manage- 391
339 30-day mortality in patients with hypertensive thalamic intra- ment continues to be merely supportive. Any compli- 392
340 cerebral hemorrhage. cation, systemic or neurological, overshadows 393
341 Variable Adjusted hazard ratio 95% CI p value prognosis. In our study, 65% of patients who died had 394
342 Intraventricular irruption 2.870 1.470–5.603 .002 395
ICH volume >20 mL 2.161 1.050–4.448 .037
major complications; this percentage is similar to that
343 previous reported by other authors for poor outcome 396
Model adjusted for age, sex, previous intracerebral hemorrhage, previous
344 modified Rankin score, Glasgow coma score, diabetes mellitus, in-hospital patients [15]. Neurological (ventricular irruption, hydro- 397
345 systemic complications, different hemorrhage volume cutoffs, and intra- 398
ventricular hemorrhage locations. Only variables significantly associated
cephalus, hematoma expansion), and systemic compli-
346 in the final model are included in table. cations such as infections (pneumonia and urinary 399
347 CI, confidence interval; ICH, intracerebral hemorrhage. 400
tract infections), venous thrombotic events, hypergly-
348 cemia and increased blood pressure have been the 401
349 most reported complications [25,27,28]. This evidence 402
350 of hematoma is a predictor of mortality due to its 403
potential to cause some complications as hydroceph- emphasizes again the need of treating all HTH
351 patients in an organized Neurocritical Care Unit, where 404
352 alus and damage to periventricular brain structures, 405
especially brainstem [25]. these complications can be prevented or treated.
353 In our hospital, ventriculostomy was associated to a 406
354 Regarding to hematoma volume and outcome, we 407
found an increase in mortality for those patients with bad outcome even when its indication was based on
355 the best neurosurgery staff judgment, presence of 408
356 hematoma size >20 mL. In other studies a hematoma 409
volume >12 mL has been also related to a worse hydrocephalus, GCS, and neurological deterioration.
357 410
prognosis [3,11,15]. This could be easily understood if This paradoxical finding could be assumed as an epi-
358 411
we take into consideration the thalamus dimensions. phenomenon due to the inherent severity of the thal-
359 412
Sen et al. [26], performed measurements of the thal- amic hemorrhage previously detailed.
360 413
amus by MRI, calculating an average volume of Surgical approach as a therapeutic modality in ICH
361 414
13.2 mL. Therefore, the thalamus lacks capacity to con- remains controversial, and this is especially true when
362 415
tain large hematomas, which can also contribute to referring to deep brain territories as thalamus or infra-
363 416
the high ventricular irruption rates. Moreover, ven- tentorial areas. Recent studies agree that the best sur-
364 417
tricular irruption is in function of thalamic hemorrhage gical approach for ventricular irruption after thalamic
365 418
location and volume; if is small and medial it will have hemorrhage might be aspiration with endoscopic
366 419
a ventricular extension, and if it is located more lat- techniques [29–33]. In the present study, no patient
367 420
eral, it will be less likely to communicate in to the was approached by endoscopic surgery in
368 421
369 ventricular system, unless large enough. our hospital. 422
In contrast with ischemic stroke where important One of the weaknesses of our study is the lack of a
370 423
371 advances in acute treatment have shown to improve precise topographic classification of thalamic 424
 INTERNATIONAL JOURNAL OF NEUROSCIENCE 5

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426 479
427 480
428 481
429 482
430 483
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432 485
433 486
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435 488
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437 490
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440 493
441 494
442 495
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446 499
447 Figure 1. Analysis of risk factors independently associated with 30-day mortality in patients with hypertensive thalamic intracere- 500
448 bral hemorrhage. A. Case fatality rate at 30 days with different hemorrhage volume cut-offs (Significantly associated with 30-day 501
mortality in bivariate analysis). B. Kaplan–Meier actuarial analysis on survival rates with hemorrhage volume >20 mL as the risk-
449 502
modifying factor. C. Case fatality rate at 30 days with different intraventricular hemorrhage locations (Significantly associated
450 with 30-day mortality in bivariate analysis). B. Kaplan–Meier actuarial analysis on survival rates with intraventricular irruption as 503
451 the risk-modifying factor. 504
452 505
453 hemorrhage [32,33]. The hematoma must be classified intraventricular irruption and increased mortality. 506
454 into those that involve the internal capsule and those Short-term independent predictors of mortality are 507
455 that respect it, and, importantly, specify its rostral or hematoma volume and irruption into the ventricular 508
456 caudal extension due to its inherent clinical prognostic system. More studies should be performed to deter- 509
457 implications. All these variables must be considered in mine mid- and long-term predictors of outcomes in 510
458 further works together with the use of MRI. this infrequent but devastating form of acute cerebro- 511
459 Also, the sample size may be small for robust prog- vascular disease. 512
460 nostic analyses and therefore, some minor risk factors 513
461 contributions and interactions may be missed, and as 514
462 a consequence, this study should be considered 515
463 hypotheses-generating awaiting for external validation Disclosure statement 516
464 in future research. Our main strength is the analysis 517
No potential conflict of interest was reported by the authors. Q2
465 518
on one of the most lethal and overlooked forms of
466 519
ICH that is commonly assessed with the same prog-
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