Join the 200th Anniversary Celebration

Original Article

The Risk of Subarachnoid and Intracerebral Hemorrhages in Blacks as Compared with Whites

Joseph P. Broderick, M.D., Thomas Brott, M.D., Thomas Tomsick, M.D., Gertrude Huster, M.H.S., and Rosemary Miller, R.N.

N Engl J Med 1992; 326:733-736March 12, 1992

Abstract
Abstract

Background

Stroke is an important cause of death among blacks, and intracerebral and subarachnoid hemorrhages account for nearly half of all early deaths from stroke. The present study investigates whether blacks and whites differ in their risk of having either intracerebral or subarachnoid hemorrhage.

Methods

We reviewed the medical records, autopsy reports, and CT scans of all patients suspected of having had an intracerebral or subarachnoid hemorrhage during 1988 among the nearly 1.3 million people in the Greater Cincinnati metropolitan area. There were 221 cases of first spontaneous intracranial hemorrhage among 1,086,462 whites (159 intracerebral and 62 subarachnoid hemorrhages), and 45 cases among 171,718 blacks (27 intracerebral and 18 subarachnoid hemorrhages). Blacks had 2.1 times the risk of subarachnoid hemorrhage of whites (95 percent confidence interval, 1.3 to 3.6) and 1.4 times the risk of intracerebral hemorrhage (95 percent confidence interval, 0.9 to 2.1). In those under the age of 75, the risk of intracerebral hemorrhage among blacks was 2.3 times that of whites (95 percent confidence interval, 1.5 to 3.6), whereas the risk among blacks 75 or older was one fourth that of whites (95 percent confidence interval, 0.1 to 0.8). Deaths within 30 days of intracerebral or subarachnoid hemorrhage accounted for 1.9 years of life lost per 1000 blacks under 65 years of age, as compared with 0.5 year per 1000 whites. Young and middle-aged blacks have a substantially higher risk of subarachnoid or intracerebral hemorrhage than whites of similar age. These types of stroke are important causes of excess mortality among young and middle-aged blacks. (N Engl J Med 1992;326: 733–6.)

Media in This Article

Table 1Incidence of Subarachnoid and Intracerebral Hemorrhage among Blacks and Whites during 1988.*
Table 2Risk of Subarachnoid or Intracerebral Hemorrhage among Blacks as Compared with Whites.
Article

INTRACEREBRAL and subarachnoid hemorrhages account for nearly half of all early deaths from stroke in population-based studies.1 2 3 Several community studies have included data on intracerebral and subarachnoid hemorrhages,2 3 4 5 6 7 8 9 but information from black or biracial communities is minimal.4 , 9

We undertook a study of spontaneous intracranial hemorrhage in Greater Cincinnati to determine whether blacks and whites differ significantly in their risk of intracerebral or subarachnoid hemorrhage. The proportion of blacks (14 percent) among the 1,267,924 people in the five-county Greater Cincinnati metropolitan area during 1980 was similar to that in the U.S. population (12 percent), as was the median age (29 vs. 30 years). CT scanning, available at all hospitals in the region as well as at outpatient facilities, is part of the standard evaluation of stroke in the community.

Methods

The medical records of all patients who had a possible intracerebral or subarachnoid hemorrhage in the Greater Cincinnati metropolitan area during 1988 were reviewed, including those in the record systems of all the acute care hospitals and coroners' offices in the five-county region, which includes two counties in Ohio and three counties in Kentucky. The catchment area for the 20 hospitals exceeds the geographic area of the five counties, ensuring that all cases of stroke that involved hospitalization were identified. Some cases of intracerebral or subarachnoid hemorrhage may have eluded identification, such as any that occurred in a nursing home or at home without hospitalization and without autopsy. The International Classification of Disease, 9th Revision, Clinical.Modification (ICD-9-CM) codes used for retrieving medical records included those for intracerebral hemorrhage (431 and 432.9), subarachnoid hemorrhage (430), cerebral aneurysm (437.3), arteriovenous malformation (747.81), and cerebrovascular accident (436). The primary and all secondary discharge diagnoses were included as part of the screening process. Since cases were often coded according to discharge date, we screened the records of potential case patients between January 1, 1988, and March 1, 1989, but we included only those with onset of hemorrhage from January 1 through December 31, 1988. All medical records were reviewed by a trained nurseabstractor under the close supervision of a neurologist. The abstracted clinical data and all available CT and magnetic resonance imaging films were evaluated by a neurologist. Films were unavailable for 25 of the 253 hospitalized patients; in these cases the CT report in the medical record was used. Except for those identified by autopsy records alone, all the patients had at least one CT scan performed. A neuroradiologist reviewed the CT films when both intracerebral and subarachnoid hemorrhages were present.

Intracerebral hemorrhage was defined as a clinical history and examination consistent with an intracerebral hemorrhage (sudden onset of headache, change in level of consciousness, or focal neurologic deficit), accompanied by a focal collection of blood within the brain parenchyma that was detected by CT scanning or at autopsy. Traumatic intracerebral hemorrhage and hemorrhagic cerebral infarction were excluded. Subarachnoid hemorrhage was defined as blood in the subarachnoid spaces, not caused by trauma, detected by CT scanning or at autopsy, or a clinical history and examination consistent with subarachnoid hemorrhage (sudden onset of severe headache or change in level of consciousness), with xanthochromia and many red cells in the cerebrospinal fluid. Cases of both intracerebral and subarachnoid hemorrhage were categorized as subarachnoid if the source of bleeding was an aneurysm or if the neuroradiologist's review indicated a subarachnoid origin of bleeding, and as intracerebral if a parenchymal source of bleeding was more likely. Cases of brain hemorrhage limited to the ventricles were classified as intracerebral (five cases). Inclusion in the study required that the patient's residence at the onset of hemorrhage have a ZIP Code in the five-county region. The numbers of blacks (171,718) and whites (1,086,462) in the five counties, according to the 1980 U.S. census, served as the denominators for calculating age- and sex-adjusted incidence rates. Although breakdowns according to age were not yet available from the 1990 census, the population of the five-county region increased by only 2.5 percent between 1980 and 1990, and the black proportion rose from 13.5 percent to 14.4 percent. Confidence intervals for the incidence rates, as adjusted for age and sex to the 1980 U.S. population, were calculated with a Poisson distribution.10

The overall risks of subarachnoid hemorrhage and intracerebral hemorrhage for blacks and whites were determined with MantelHaenszel tests.11 , 12 The overall risks for blacks and whites, as adjusted for age and sex to the 1980 U.S. population, were calculated and compared.11 The rates of survival for 30 days after intracerebral or subarachnoid hemorrhage were calculated for blacks and whites by Kaplan–Meier life-table analysis13 and compared by a log-rank test. The number of years of potential life lost before the age of 65,14 a measure of premature mortality, was calculated for intracerebral and subarachnoid hemorrhage for blacks and whites. All P values were two-tailed.

Results

Examination of 3233 medical records detected 266 cases of first spontaneous intracranial hemorrhage (186 intracerebral and 80 subarachnoid hemorrhages) among whites and blacks during 1988. Two intracerebral hemorrhages and 11 subarachnoid hemorrhages were identified by autopsy reports alone, and 2 subarachnoid hemorrhages were identified through clinical evaluation and lumbar puncture. All the other hemorrhages were documented by CT scanning.

The 266 patients consisted of 221 whites (159 with intracerebral and 62 with subarachnoid hemorrhages) and 45 blacks (27 with intracerebral and 18 with subarachnoid hemorrhages). The age- and sex-adjusted incidence of subarachnoid hemorrhage per 100,000 population was 12 for blacks (95 percent confidence interval, 6 to 17) and 6 for whites (95 percent confidence interval, 4 to 7). Blacks had a higher incidence of subarachnoid hemorrhage than whites in every adult age group (Table 1Table 1Incidence of Subarachnoid and Intracerebral Hemorrhage among Blacks and Whites during 1988.*). The age- and sex-adjusted incidence of intracerebral hemorrhage per 100,000 population was 19 for blacks (95 percent confidence interval, 12 to 26) and 15 for whites (95 percent confidence interval, 12 to 17). The age-specific incidence rates for intracerebral hemorrhage were higher among adult blacks than adult whites up to the age of 75, after which the rates in whites were substantially higher (Table 1). Overall, the incidence rates for intracerebral hemorrhage increased markedly with age, whereas the rates for subarachnoid hemorrhage increased slightly after the age of 35 (Table 1). The 95 percent confidence intervals for the difference in incidence rates between blacks and whites were 0.3 to 11.5 for subarachnoid hemorrhage, -3.3 to 11.6 for intracerebral hemorrhage, and 0.8 to 19.4 for all hemorrhages combined.

Considering all age groups together, blacks had twice the risk of subarachnoid hemorrhage of whites (Table 2Table 2Risk of Subarachnoid or Intracerebral Hemorrhage among Blacks as Compared with Whites.). Although the risk of intracerebral hemorrhage for all age groups together was not significantly different among blacks and whites, the risk of intracerebral hemorrhage among blacks under the age of 75 was 2.3 times that for whites (95 percent confidence interval, 1.5 to 3.6). By contrast, for those 75 or older, blacks had approximately one fourth the risk of intracerebral hemorrhage of whites (95 percent confidence interval, 0.1 to 0.8).

Since 95 percent of the black population in the five-county study area lives in Hamilton County, we checked whether white patients with stroke from the area's perimeters could have been treated outside the study region. The nearest hospitals outside the region had no admissions for intracerebral or subarachnoid hemorrhage from our five-county area. Of the 74 blacks who died of cerebrovascular disease in Hamilton County during 1988, 8 (11 percent) had an autopsy, as compared with 7 of 221 whites (3 percent). To determine whether the use of CT scanning and therefore the rate of identification of intracranial hemorrhage differed between blacks and whites, we reviewed the records of all the patients admitted to one of the largest urban study hospitals during 1988 with a diagnosis of "unspecified cerebrovascular disease or cerebrovascular accident" (ICD-9-CM code 436). Of 79 blacks, 67 (85 percent) underwent CT scanning or magnetic resonance imaging, as compared with 52 of 62 whites (84 percent).

The 30-day mortality from subarachnoid hemorrhage was not significantly different among blacks (50 percent) and whites (44 percent), and for intracerebral hemorrhage it was identical (44 percent). The amount of potential life lost because of subarachnoid or intracerebral hemorrhage was 1.9 years per 1000 blacks under 65 years of age, as compared with 0.5 year per 1000 whites.

Two causes of the 80 cases of subarachnoid hemorrhage were verifiable: ruptured aneurysm, as documented by angiography (31 cases), at autopsy (9), or during the operative removal of an associated parenchymal hemorrhage (3); and arteriovenous malformation (2 cases, both documented at autopsy). Of the remaining 35 hospitalized patients with subarachnoid hemorrhage, 11 had normal angiograms. The poor clinical condition of the rest precluded cerebral angiography. No aneurysm was seen in 11 of the 42 patients who underwent angiography. Of the 80 patients with subarachnoid hemorrhage, 41 (51 percent) had a history of hypertension (10 of 18 blacks [56 percent] and 31 of 62 whites [50 percent]).

Causes of the 186 cases of intracerebral hemorrhage included a ruptured arteriovenous malformation (10) and hemorrhage into a tumor (3). Other associated factors included the use of anticoagulant agents (nine), thrombolytic therapy for a pulmonary embolism (one) or myocardial infarction (one), and acute cocaine ingestion (one). Of the 186 patients, 128 (69 percent) had a history of hypertension (110 of 159 whites [69 percent] and 18 of 27 blacks [67 percent]).

Discussion

This population-based study demonstrates that blacks have a greater risk of subarachnoid hemorrhage than whites. This observation may reflect different distributions of risk factors for subarachnoid hemorrhage,15 , 16 such as the increased prevalence of hypertension among blacks17 and of cigarette smoking among black men.18 To investigate whether black race is an independent risk factor for subarachnoid hemorrhage19 would require a large case–control or cohort study.

We expected to find a significantly increased risk of intracerebral hemorrhage among blacks because of their higher prevalence of hypertension,18 a condition closely associated with hemorrhage.4 , 19 20 21 22 Although the overall risk was not significantly different, blacks under the age of 75 proved to have a 2.3 times greater risk of intracerebral hemorrhage than whites. Among blacks 75 or older, the risk of intracerebral hemorrhage fell to only one fourth that for whites. Elderly black patients with intracerebral hemorrhage may be less likely than whites to be evaluated at an acute care hospital and to have the diagnosis corroborated by CT scanning. Alternatively, most blacks at risk for intracerebral hemorrhage may have hemorrhages at earlier ages, leaving those who survive into their 70s and 80s at lower risk. The importance of hypertension, or other risk factors, in the pathogenesis of intracerebral hemorrhage may also vary with age and race.4

The increased risk of brain hemorrhage among young and middle-aged blacks mirrors the excess mortality from stroke among blacks in the United States during 1985.23 In the National Health and Nutrition Examination Survey I Epidemiologic Follow-up Study, cerebrovascular disease accounted for 28 percent of the excess mortality among blacks as compared with whites 35 to 77 years old.1 In the present study, deaths within 30 days of intracerebral or subarachnoid hemorrhage accounted for 1.9 years of potential life lost per 1000 blacks under the age of 65, as compared with 0.5 year per 1000 whites. Subarachnoid and intracerebral hemorrhages are thus a major cause of excess mortality among young and middle-aged blacks.

Our study suggests that advancing age is more important as a risk factor for intracerebral hemorrhage than for subarachnoid hemorrhage. The incidence of intracerebral hemorrhage increased markedly with advancing age, as reported in previous incidence studies,2 3 4 , 8 whereas the rate of subarachnoid hemorrhage increased only slightly after the age of 35. The incidence of both subarachnoid and intracerebral hemorrhage may have been underestimated in the older groups, since the autopsy rate during 1988 for those under 65 years of age (30 percent) was much higher than the rate for those 65 and older (7 percent). However, even with undercounting of subarachnoid and intracerebral hemorrhages in the elderly, the marked age differential between intracerebral and subarachnoid hemorrhages would not have been altered.

Potential biases are unlikely to have confounded our findings. Blacks are reported to be less likely to seek medical attention for chest pain than whites.24 If this behavior also applies to stroke symptoms, the difference we report between blacks and whites in the risk of subarachnoid and intracerebral hemorrhage would be an underestimate of the actual difference. The use of CT imaging among black and white patients hospitalized for stroke was similar in the present study and an earlier three-community study25 and is unlikely to account for the differences between blacks and whites. The lower autopsy rates among whites in the present study may have resulted in a slight underestimate of the actual number of cases among whites. The coding of discharge diagnoses of stroke is performed by medical-record personnel without attention to race and does not explain the observed racial differences. Although unlikely, undercounting of blacks in the census could have led to a slight overestimation of the risk of brain hemorrhage among blacks.

Supported by a grant (A3295–01) from the American Heart Association.

We are indebted to the departments of medical records and radiology at the following Greater Cincinnati hospitals: the Bethesda Hospitals, Children's Hospital Medical Center, Christ Hospital, Deaconess Hospital, Good Samaritan Hospital, Jewish Hospital, the Mercy Hospitals, Providence Hospital, St. Elizabeth Medical Center Hospitals, St. Francis—St. George Hospital, St. Luke's Hospitals, University Hospital Medical Center, and the Veterans Affairs Medical Center; we are also indebted to the coroners' offices of Hamilton, Clermont, Kenton, Boone, and Campbell counties; Jane Arnold, Cincinnati Department of Statistics; Dr. Stephen R. Howe; Dr. Vicki Wells, Cincinnati Department of Health; Dr. Vicki Hertzberg, Department of Environmental Health, University of Cincinnati; and Patti Jahn.

Source Information

From the Departments of Neurology (J.P.B., T.B., R.M.), Radiology (T.T.), and Internal Medicine (G.H.), University of Cincinnati Medical Center, Cincinnati. Address reprint requests to Dr. Broderick, at the Department of Neurology, University of Cincinnati Medical Center, 231 Bethesda Ave., Cincinnati, OH 45267–0525.

References

References

  1. 1

    Otten MW, Teutsch SM, Williamson DF, Marks JS. The effect of known risk factors on the excess mortality of black adults in the United States . JAMA 1990;263:845–50.
    CrossRef | Web of Science | Medline

  2. 2

    Broderick JP, Phillips SJ, Whisnant JP, O'Fallon WM, Bergstralh EJ. Incidence rates of stroke in the eighties: the end of the decline in stroke? Stroke 1989;20:577–82.
    CrossRef | Web of Science | Medline

  3. 3

    Bamford J, Sandercock P, Dennis M. Burn J. Warlow C. A prospective study of acute cerebrovascular disease in the community: the Oxfordshire Community Stroke Project — 1982–86. 2. Incidence, case fatality rates and overall outcome at one year of cerebral infarction, primary intracerebral and subarachnoid haemorrhage . J Neurol Neurosurg Psychiatry 1990;53:16–22.
    CrossRef | Web of Science | Medline

  4. 4

    Brott T. Thalinger K, Hertzberg V. Hypertension as a risk factor for spontaneous intracerebral hemorrhage . Stroke 1986;17:1078–83.
    CrossRef | Web of Science | Medline

  5. 5

    Drury I, Whisnant JP, Garraway WM. Primary intracerebral hemorrhage: impact of CT on incidence . Neurology 1984;34:653–7.
    Web of Science | Medline

  6. 6

    Ingall TJ. Whisnant JP, Wiebers DO, O'Fallon WM. Has there been a decline in subarachnoid hemorrhage mortality? Stroke1989;718–24.
    CrossRef | Web of Science | Medline

  7. 7

    Bonita R, Beaglehole R, North JDK. Subarachnoid hemorrhage in New Zealand: an epidemiological study . Stroke 1983;14:342–7.
    CrossRef | Web of Science | Medline

  8. 8

    Friday G, Lai SM, Alter M, et al. Stroke in the Lehigh Valley: racial/ethnic differences . Neurology 1989;39:1165–8.
    Web of Science | Medline

  9. 9

    Gross CR, Kase CS, Mohr JP, Cunningham SC, Baker WE. Stroke in South Alabama: incidence and diagnostic features — a population based study . Stroke 1984;15:249–55.
    CrossRef | Web of Science | Medline

  10. 10

    Keyfitz N. Sampling variance of standardized mortality rates . Hum Biol 1966;38:309–17.
    Web of Science | Medline

  11. 11

    Kleinbaum DG, Kupper LL, Morgenstern H. Epidemiologic research: principles and quantitative methods. Belmont, Calif.: Lifetime Learning Publications, 1982.

  12. 12

    Breslow NE, Day NE. Statistical methods in cancer research. Vol. 1. The analysis of case–control studies. Lyon, France: International Agency for Research on Cancer, 1980. (IARC scientific publications no. 32.)

  13. 13

    Kaplan EL, Meier P. Nonparametric estimation from incomplete observations . J Am Stat Assoc 1958;53:457–81.
    CrossRef | Web of Science

  14. 14

    Premature mortality in the United States: public health issues in the use of years of potential life lost . MMWR 1986;35:Suppl 2S:1S–11S.
    Medline

  15. 15

    Bonita R. Cigarette smoking, hypertension and risk of subarachnoid hemorrhage: a population-based case–control study . Stroke 1986;17:831–5.
    CrossRef | Web of Science | Medline

  16. 16

    Shinton R, Beevers G. Meta-analysis of relation between cigarette smoking and stroke . BMJ 1989;298:789–94.
    CrossRef | Web of Science | Medline

  17. 17

    Subcommittee on Definition and Prevalence of the 1984 Joint National Committee. Hypertension prevalence and the status of awareness, treatment, and control in the United States . Hypertension 1985;7:457–68.
    Web of Science | Medline

  18. 18

    National Center for Health Statistics. Health, United States, 1989. Hyattsville, Md.: Public Health Service, 1990. (DHHS publication no. (PHS) 90–1232.)

  19. 19

    Klatsky AL, Armstrong MA, Friedman GD. Racial differences in cerebrovascular disease hospitalizations . Stroke 1991;22:299–304.
    CrossRef | Web of Science | Medline

  20. 20

    Tanaka H, Ueda Y, Hayashi M, et al. Risk factors for cerebral hemorrhage and cerebral infarction in a Japanese rural community . Stroke 1982;13:62–73.
    CrossRef | Web of Science | Medline

  21. 21

    Okada H, Horibe H, Yoshiyuki O, Hayakawa N, Aoki N. A prospective study of cerebrovascular disease in Japanese rural communities, Akabane and Asahi. Part 1: evaluation of risk factors in the occurrence of cerebral hemorrhage and thrombosis . Stroke 1976;7:599–607.
    CrossRef | Web of Science | Medline

  22. 22

    Abu-Zeid HA, Choi NW, Maini KK, Hsu PH, Nelson NA. Relative role of factors associated with cerebral infarction and cerebral hemorrhage: a matched pair case–control study . Stroke 1977;8:106–12.
    CrossRef | Web of Science | Medline

  23. 23

    Polednak AP. Racial and ethnic differences in disease. New York: Oxford University Press, 1989.

  24. 24

    Strogatz DS. Use of medical care for chest pain: differences between blacks and whites . Am J Public Health 1990;80:290–4.
    CrossRef | Web of Science | Medline

  25. 25

    Howard G, Brockschmidt JK, Coull BM, et al. The community hospital-based stroke programs in North Carolina, Oregon and New York. V. Stroke diagnosis: factors influencing the diagnostic evaluation of patients following acute stroke . J Clin Epidemiol 1991;44:293–301.
    CrossRef | Web of Science | Medline

Citing Articles (88)

Citing Articles

  1. 1

    Xian Fu, Ka Sing Wong, Jade W. Wei, Xiangyan Chen, Yueqing Lin, JinSheng Zeng, Ruxun Huang, Qingchun Gao. (2012) Factors associated with severity on admission and in-hospital mortality after primary intracerebral hemorrhage in China. International Journal of Stroken/a-n/a
    CrossRef

  2. 2

    H. Bart Brouwers, Joshua N. Goldstein. (2011) Therapeutic Strategies in Acute Intracerebral Hemorrhage. Neurotherapeutics
    CrossRef

  3. 3

    Pamela Flood, Guohua Li. (2011) A Terrible Headache in Obstetric Anesthesia. Anesthesiology1
    CrossRef

  4. 4

    Brian T. Bateman, Vanessa A. Olbrecht, Mitchell F. Berman, Rebecca D. Minehart, Lee H. Schwamm, Lisa R. Leffert. (2011) Peripartum Subarachnoid Hemorrhage. Anesthesiology1
    CrossRef

  5. 5

    Navdeep Sangha, Nicole R. Gonzales. (2011) Treatment Targets in Intracerebral Hemorrhage. Neurotherapeutics 8:3, 374-387
    CrossRef

  6. 6

    Hua Zhu, Qin Li, Ming Feng, Yun-Xin Chen, Hao Li, Jin-Jiang Sun, Chun-Hua Zhao, Ren-Zhi Wang, Erwan Bezard, Chuan Qin. (2011) A new cerebral hemorrhage model in cynomolgus macaques created by injection of autologous anticoagulated blood into the brain. Journal of Clinical Neuroscience
    CrossRef

  7. 7

    Eric M. Bershad, José I. Suarez. 2011. Aneurysmal Subarachnoid Hemorrhage. , 589-615.
    CrossRef

  8. 8

    Carlos S. Kase, Steven M. Greenberg, J.P. Mohr, Louis R. Caplan. 2011. Intracerebral Hemorrhage. , 531-588.
    CrossRef

  9. 9

    André A. le Roux, M. Christopher Wallace. (2010) Outcome and Cost of Aneurysmal Subarachnoid Hemorrhage. Neurosurgery Clinics of North America 21:2, 235-246
    CrossRef

  10. 10

    Geoffrey P. Colby, Alexander L. Coon, Rafael J. Tamargo. (2010) Surgical Management of Aneurysmal Subarachnoid Hemorrhage. Neurosurgery Clinics of North America 21:2, 247-261
    CrossRef

  11. 11

    Jeremy L Rempel, Richard I Aviv. (2010) Current advances in CT imaging of stroke. Imaging in Medicine 2:2, 165-179
    CrossRef

  12. 12

    Peter McColgan, Kyaw Zayar Thant, Pankaj Sharma. (2010) The genetics of sporadic ruptured and unruptured intracranial aneurysms: a genetic meta-analysis of 8 genes and 13 polymorphisms in approximately 20,000 individuals. Journal of Neurosurgery 112:4, 714-721
    CrossRef

  13. 13

    Robert Ayer, Wanqiu Chen, Takashi Sugawara, Hidenori Suzuki, John H. Zhang. (2010) Role of gap junctions in early brain injury following subarachnoid hemorrhage. Brain Research 1315, 150-158
    CrossRef

  14. 14

    Theresa N. Dang, Glenda M. Bishop, Ralf Dringen, Stephen R. Robinson. (2010) The putative heme transporter HCP1 is expressed in cultured astrocytes and contributes to the uptake of hemin. Glia 58:1, 55-65
    CrossRef

  15. 15

    Khalid A. Hanafy, R. Morgan Stuart, Luis Fernandez, J. Michael Schmidt, Jan Claassen, Kiwon Lee, E. Sander Connolly, Stephan A. Mayer, Neeraj Badjatia. (2010) Cerebral inflammatory response and predictors of admission clinical grade after aneurysmal subarachnoid hemorrhage. Journal of Clinical Neuroscience 17:1, 22-25
    CrossRef

  16. 16

    Brad E. Zacharia, Bartosz T. Grobelny, Ricardo J. Komotar, E. Sander Connolly, J. Mocco. (2010) The influence of race on outcome following subarachnoid hemorrhage. Journal of Clinical Neuroscience 17:1, 34-37
    CrossRef

  17. 17

    Masatoshi Koga, Kazunori Toyoda, Masaki Naganuma, Kazuomi Kario, Jyoji Nakagawara, Eisuke Furui, Yoshiaki Shiokawa, Yasuhiro Hasegawa, Satoshi Okuda, Hiroshi Yamagami, Kazumi Kimura, Yasushi Okada, Kazuo Minematsu. (2009) Nationwide survey of antihypertensive treatment for acute intracerebral hemorrhage in Japan. Hypertension Research 32:9, 759-764
    CrossRef

  18. 18

    Irene Nikaina, Konstantinos N. Paterakis, Georgios M. Hadjigeorgiou, Vissarion Christodoulou, Apostolos Karantanas, Antonios Karavelis, Apostolos Komnos. (2009) Brain Tissue Oxygen Pressure and Prognosis in Spontaneous Intracerebral Hematomas. Neurosurgery Quarterly 19:3, 174-177
    CrossRef

  19. 19

    Sung-Pil Joo, Tae-Sun Kim, Il-Kwon Lee, Jung-Kil Lee, Bo-Ra Seo, Jae-Hyoo Kim, Soo-Han Kim. (2009) The role of collagen type I α2 polymorphisms: intracranial aneurysms in Koreans. Surgical Neurology 72:1, 48-53
    CrossRef

  20. 20

    Hua Lu, Ji-Xin Shi, Hui-Lin Chen, Chun-Hua Hang, Han-Dong Wang, Hong-Xia Yin. (2009) Expression of monocyte chemoattractant protein-1 in the cerebral artery after experimental subarachnoid hemorrhage. Brain Research 1262, 73-80
    CrossRef

  21. 21

    Louis R. Caplan, D. Eric Searls, Fong Kwong Sonny Hon. (2009) Cerebrovascular Disease. Medical Clinics of North America 93:2, 353-369
    CrossRef

  22. 22

    Pawan D. Patel, Jose L. Velazquez, Rohit R. Arora. (2009) Endothelial dysfunction in African-Americans. International Journal of Cardiology 132:2, 157-172
    CrossRef

  23. 23

    Tuan V. Nguyen, Kiran Chandrashekar, Zhen Qin, Andrew D. Parent, Jun Zhang. (2009) Epidemiology of Intracranial Aneurysms of Mississippi: a 10-year (1997-2007) Retrospective Study. Journal of Stroke and Cerebrovascular Diseases 18:5, 374
    CrossRef

  24. 24

    Hasan Kocaeli, Mario Zuccarello. (2008) Management of Spontaneous Intracerebral Hematomas. Neurosurgery Quarterly 18:3, 207-215
    CrossRef

  25. 25

    Jerzy P. Szaflarski, Angela Y. Rackley, Dawn O. Kleindorfer, Jane Khoury, Daniel Woo, Rosemary Miller, Kathleen Alwell, Joseph P. Broderick, Brett M. Kissela. (2008) Incidence of seizures in the acute phase of stroke: A population-based study. Epilepsia 49:6, 974-981
    CrossRef

  26. 26

    D. Hänggi, H.-J. Steiger. (2008) Spontaneous intracerebral haemorrhage in adults: a literature overview. Acta Neurochirurgica 150:4, 371-379
    CrossRef

  27. 27

    Robert H. Andres, Raphael Guzman, Angélique D. Ducray, Pasquale Mordasini, Atul Gera, Alain Barth, Hans R. Widmer, Gary K. Steinberg. (2008) Cell replacement therapy for intracerebral hemorrhage. Neurosurgical FOCUS 24:3-4, E16
    CrossRef

  28. 28

    Valery L. Feigin, Suzanne Barker-Collo, Harry McNaughton, Paul Brown, Ngaire Kerse. (2008) Long-term neuropsychological and functional outcomes in stroke survivors: current evidence and perspectives for new research. International Journal of Stroke 3:1, 33-40
    CrossRef

  29. 29

    Ricardo J. Komotar, Brad E. Zacharia, Ricky Valhora, J. Mocco, E. Sander Connolly. (2007) Advances in vasospasm treatment and prevention. Journal of the Neurological Sciences 261:1-2, 134-142
    CrossRef

  30. 30

    Katja E. Wartenberg, Stephan A. Mayer. (2007) Reducing the risk of ICH enlargement. Journal of the Neurological Sciences 261:1-2, 99-107
    CrossRef

  31. 31

    Vibhor Krishna, Dong H. Kim. (2007) Ethnic differences in risk factors for subarachnoid hemorrhage. Journal of Neurosurgery 107:3, 522-529
    CrossRef

  32. 32

    Gene R. Pesola. (2007) Continuous Mean Arterial Pressure Estimation in the Setting of Intracerebral Hemorrhage. Academic Emergency Medicine 14:8, 740-742
    CrossRef

  33. 33

    Albert Yuh-Jer Shen, Janis F. Yao, Somjot S. Brar, Michael B. Jorgensen, Wansu Chen. (2007) Racial/Ethnic Differences in the Risk of Intracranial Hemorrhage Among Patients With Atrial Fibrillation. Journal of the American College of Cardiology 50:4, 309-315
    CrossRef

  34. 34

    Timothy H. Rainer, Ka Sing Wong, Wynnie Lam, Nicole Y.L. Lam, Colin A. Graham, Y.M. Dennis Lo. (2007) Comparison of plasma β-globin DNA and S-100 protein concentrations in acute stroke. Clinica Chimica Acta 376:1-2, 190-196
    CrossRef

  35. 35

    Ana M. Pascual, Jose V. López-Mut, Vicente Benlloch, Raquel Chamarro, Jose Soler, Miguel J.A. Láinez. (2007) Perfusion-Weighted Magnetic Resonance Imaging in Acute Intracerebral Hemorrhage at Baseline and during the 1st and 2nd Week: A Longitudinal Study. Cerebrovascular Diseases 23:1, 6-13
    CrossRef

  36. 36

    J Mocco, Brad E. Zacharia, Ricardo J. Komotar, E. Sander Connolly. (2006) A review of current and future medical therapies for cerebral vasospasm following aneurysmal subarachnoid hemorrhage. Neurosurgical FOCUS 21:3, 1-7
    CrossRef

  37. 37

    Boris Krischek, Ituro Inoue. (2006) The genetics of intracranial aneurysms. Journal of Human Genetics 51:7, 587-594
    CrossRef

  38. 38

    H. B. Huttner, E. Jüttler, A. Hug, M. Köhrmann, P. D. Schellinger, T. Steiner. (2006) Antikoagulanzienassoziierte Hirnblutungen. Der Nervenarzt 77:6, 671-681
    CrossRef

  39. 39

    Robert P. Ostrowski, Austin R. Colohan, John H. Zhang. (2006) Molecular mechanisms of early brain injury after subarachnoid hemorrhage. Neurological Research 28:4, 399-414
    CrossRef

  40. 40

    Valery Feigin, Kristie Carter, Maree Hackett, P Alan Barber, Harry McNaughton, Lorna Dyall, Mei-hua Chen, Craig Anderson. (2006) Ethnic disparities in incidence of stroke subtypes: Auckland Regional Community Stroke Study, 2002–2003. The Lancet Neurology 5:2, 130-139
    CrossRef

  41. 41

    Suarez, Jose I., Tarr, Robert W., Selman, Warren R., . (2006) Aneurysmal Subarachnoid Hemorrhage. New England Journal of Medicine 354:4, 387-396
    Full Text

  42. 42

    Neeraj Badjatia, Jonathan Rosand. (2005) Intracerebral Hemorrhage. The Neurologist 11:6, 311-324
    CrossRef

  43. 43

    David Rosen, Roberta Novakovic, Fernando D. Goldenberg, Dezheng Huo, Maria E. Baldwin, Jeffrey I. Frank, Axel J. Rosengart, R. Loch Macdonald. (2005) Racial differences in demographics, acute complications, and outcomes in patients with subarachnoid hemorrhage: a large patient series. Journal of Neurosurgery 103:1, 18-24
    CrossRef

  44. 44

    Franklin A. Marden, Soma Sinha Roy. (2005) Endovascular management of intracerebral and subarachnoid hemorrhage. Current Treatment Options in Cardiovascular Medicine 7:3, 197-209
    CrossRef

  45. 45

    Akio Morita, Satoru Fujiwara, Kazuo Hashi, Hiroshi Ohtsu, Takaaki Kirino. (2005) Risk of rupture associated with intact cerebral aneurysms in the Japanese population: a systematic review of the literature from Japan. Journal of Neurosurgery 102:4, 601-606
    CrossRef

  46. 46

    Peng Roc Chen, Kai Frerichs, Robert Spetzler. (2004) Natural history and general management of unruptured intracranial aneurysms. Neurosurgical FOCUS 17:5, 1-6
    CrossRef

  47. 47

    Philip B. Gorelick. (2004) Epidemiology of transient ischemic attack and ischemic stroke in patients with underlying cardiovascular disease. Clinical Cardiology 27:S2, 4-11
    CrossRef

  48. 48

    Edward M. Manno. (2004) Subarachnoid hemorrhage. Neurologic Clinics 22:2, 347-366
    CrossRef

  49. 49

    Giovanni Grasso. (2004) An overview of new pharmacological treatments for cerebrovascular dysfunction after experimental subarachnoid hemorrhage. Brain Research Reviews 44:1, 49-63
    CrossRef

  50. 50

    Tanja Rundek, Ralph L. Sacco. 2004. Outcome following Stroke. , 35-57.
    CrossRef

  51. 51

    Wouter I. Schievink, Mary Riedinger, Tajinder K. Jhutty, Paul Simon. (2004) Racial Disparities in Subarachnoid Hemorrhage Mortality: Los Angeles County, California, 1985–1998. Neuroepidemiology 23:6, 299-305
    CrossRef

  52. 52

    Carlos S. Kase, J.P. Mohr, Louis R. Caplan. 2004. Intracerebral Hemorrhage. , 327-376.
    CrossRef

  53. 53

    Steven M. Greenberg. 2004. Cerebral Amyloid Angiopathy. , 693-705.
    CrossRef

  54. 54

    G. Edward Vates, Joseph M. Zabramski, Robert F. Spetzler, Michael T. Lawton. 2004. Intracranial Aneurysms. , 1279-1335.
    CrossRef

  55. 55

    Matthew E. Fewel, B. Gregory Thompson, Julian T. Hoff. (2003) Spontaneous intracerebral hemorrhage: a review. Neurosurgical FOCUS 15:4, 1-16
    CrossRef

  56. 56

    Nader Pouratian, Neal F. Kassell, Aaron S. Dumont. (2003) Update on management of intracerebral hemorrhage. Neurosurgical FOCUS 15:4, 1-6
    CrossRef

  57. 57

    Alfredo Quinones-Hinojosa, Mittul Gulati, Vineeta Singh, Michael T. Lawton. (2003) Spontaneous intracerebral hemorrhage due to coagulation disorders. Neurosurgical FOCUS 15:4, 1-17
    CrossRef

  58. 58

    Lars Lindgaard, Vagn Eskesen, Flemming Gjerris, Niels Vidiendal Olsen. (2003) Familial Aggregation of Intracranial Aneurysms in an Inuit Patient Population in Kalaallit Nunaat (Greenland). Neurosurgery 52:2, 357-363
    CrossRef

  59. 59

    Jeanette Mitchell. (2002) Vertebral artery atherosclerosis: a risk factor in the use of manipulative therapy?. Physiotherapy Research International 7:3, 122-135
    CrossRef

  60. 60

    M ZUCCARELLO, N ANDALUZ, K WAGNER. (2002) Minimally invasive therapy for intracerebral hematomas. Neurosurgery Clinics of North America 13:3, 349-354
    CrossRef

  61. 61

    D WOO, J BRODERICK. (2002) Spontaneous intracerebral hemorrhage: epidemiology and clinical presentation. Neurosurgery Clinics of North America 13:3, 265-279
    CrossRef

  62. 62

    C SKIDMORE, J ANDREFSKY. (2002) Spontaneous intracerebral hemorrhage: epidemiology, pathophysiology, and medical management. Neurosurgery Clinics of North America 13:3, 281-288
    CrossRef

  63. 63

    Bryce Weir. (2002) Unruptured intracranial aneurysms: a review. Journal of Neurosurgery 96:1, 3-42
    CrossRef

  64. 64

    Adnan I. Qureshi, M. Fareed K. Suri, Abutaher M. Yahia, Jose I. Suarez, Lee R. Guterman, L. Nelson Hopkins, Rafael J. Tamargo. (2001) Risk Factors for Subarachnoid Hemorrhage. Neurosurgery 49:3, 607-613
    CrossRef

  65. 65

    R. Loch Macdonald, Marcus Stoodley, Bryce Weir. (2001) Intracranial Aneurysms. Neurosurgery Quarterly 11:3, 181-198
    CrossRef

  66. 66

    P. K. Sarkar, C. D'Souza, S. Ballantyne. (2001) Treatment of aneurysmal subarachnoid haemorrhage in elderly patients. Journal of Clinical Pharmacy and Therapeutics 26:4, 247-256
    CrossRef

  67. 67

    Qureshi, Adnan I., Tuhrim, Stanley, Broderick, Joseph P., Batjer, H. Hunt, Hondo, Hideki, Hanley, Daniel F., . (2001) Spontaneous Intracerebral Hemorrhage. New England Journal of Medicine 344:19, 1450-1460
    Full Text

  68. 68

    Daniel L. Labovitz, Ralph L. Sacco. (2001) Intracerebral hemorrhage: update. Current Opinion in Neurology 14:1, 103-108
    CrossRef

  69. 69

    Kernan, Walter N., Viscoli, Catherine M., Brass, Lawrence M., Broderick, Joseph P., Brott, Thomas, Feldmann, Edward, Morgenstern, Lewis B., Wilterdink, Janet Lee, Horwitz, Ralph I., . (2000) Phenylpropanolamine and the Risk of Hemorrhagic Stroke. New England Journal of Medicine 343:25, 1826-1832
    Full Text

  70. 70

    (2000) Part 3: Adult Basic Life Support. Resuscitation 46:1-3, 29-71
    CrossRef

  71. 71

    (2000) Part 7: The Era of Reperfusion. Resuscitation 46:1-3, 239-252
    CrossRef

  72. 72

    James M. Gebel, Joseph P. Broderick. (2000) INTRACEREBRAL HEMORRHAGE. Neurologic Clinics 18:2, 419-438
    CrossRef

  73. 73

    Gwendolyn Ford Lynch, Philip B. Gorelick. (2000) STROKE IN AFRICAN AMERICANS. Neurologic Clinics 18:2, 273-290
    CrossRef

  74. 74

    Richard C. Seestedt, Michael R. Frankel. (1999) Intracerebral hemorrhage. Current Treatment Options in Neurology 1:2, 127-137
    CrossRef

  75. 75

    Masataka Nishimura, Takashi Uzu, Takashi Fujii, Setsuko Kuroda, Satoko Nakamura, Takashi Inenaga, Genjiro Kimura. (1999) Cardiovascular complications in patients with primary aldosteronism. American Journal of Kidney Diseases 33:2, 261-266
    CrossRef

  76. 76

    Adnan I. Qureshi, Jose I. Suarez, Parag D. Parekh, Gene Sung, Romergryko Geocadin, Anish Bhardwaj, Rafael J. Tamargo, John A. Ulatowski. (1998) Risk Factors for Multiple Intracranial Aneurysms. Neurosurgery 43:1, 22-26
    CrossRef

  77. 77

    J. Monstrey. (1998) Epidemiology of subarachnoid haemorrhage. European Journal of Anaesthesiology 15:Supplement 17, 70-71
    CrossRef

  78. 78

    Franz H. Messerli. (1997) HYPERTENSION IN SPECIAL POPULATIONS. Medical Clinics of North America 81:6, 1335-1345
    CrossRef

  79. 79

    WAYNE W. LAMORTE, THAYER E. SCOTT, JAMES O. MENZOIAN. (1996) Relationship of Cardiovascular Risk Factors to Racial Differences in Femoral Bypass Surgery and Abdominal Aortic Aneurysmectomy in Massachusetts. Annals of the New York Academy of Sciences 800:1 The Abdominal, 25-35
    CrossRef

  80. 80

    Daryl W. Thompson, Anthony J. Furlan. (1996) CLINICAL EPIDEMIOLOGY OF STROKE. Neurologic Clinics 14:2, 309-315
    CrossRef

  81. 81

    Wouter I. Schievink, Daniel J. Schaid, Virginia V. Michels, David G. Piepgras. (1995) Familial aneurysmal subarachnoid hemorrhage: a community-based study. Journal of Neurosurgery 83:3, 426-429
    CrossRef

  82. 82

    Han Soo Chang, Takaaki Kirino. (1995) Quantification of operative benefit for unruptured cerebral aneurysms: a theoretical approach. Journal of Neurosurgery 83:3, 413-420
    CrossRef

  83. 83

    Wouter I. Schievink, Eelco F. M. Wijdicks, David G. Piepgras, Chu-Pin Chu, W. Michael O'Fallon, Jack P. Whisnant. (1995) The poor prognosis of ruptured intracranial aneurysms of the posterior circulation. Journal of Neurosurgery 82:5, 791-795
    CrossRef

  84. 84

    S Loncaric. (1995) 3-D image analysis of intra-cerebral brain hemorrhage from digitized CT films. Computer Methods and Programs in Biomedicine 46:3, 207-216
    CrossRef

  85. 85

    Wayne W. LaMorte, Thayer E. Scott, James O. Menzoian. (1995) Racial differences in the incidence of femoral bypass and abdominal aortic aneurysmectomy in Massachusetts: Relationship to cardiovascular risk factors. Journal of Vascular Surgery 21:3, 422-431
    CrossRef

  86. 86

    John P. Weaver, Marc Fisher. (1994) Subarachnoid hemorrhage: An update of pathogenesis, diagnosis and management. Journal of the Neurological Sciences 125:2, 119-131
    CrossRef

  87. 87

    Joseph P. Broderick, Thomas Brott, Thomas Tomsick, Rosemary Miller, Gertrude Huster. (1993) Intracerebral hemorrhage more than twice as common as subarachnoid hemorrhage. Journal of Neurosurgery 78:2, 188-191
    CrossRef

  88. 88

    (1992) Intracranial Hemorrhage in Blacks as Compared with Whites. New England Journal of Medicine 327:8, 568-568
    Full Text

Letters