J Neurol Surg A Cent Eur Neurosurg 2015; 76(01): 46-55
DOI: 10.1055/s-0034-1372438
Original Article
Georg Thieme Verlag KG Stuttgart · New York

Predictors of Treatment Delay in Aneurysmal Subarachnoid Hemorrhage Patients

J. Manuel Sarmiento
1   Department of Neurosurgery, Cedars-Sinai Medical Center, Los Angeles, California, United States
Debraj Mukherjee
1   Department of Neurosurgery, Cedars-Sinai Medical Center, Los Angeles, California, United States
Kristin Nosova
1   Department of Neurosurgery, Cedars-Sinai Medical Center, Los Angeles, California, United States
Wouter I. Schievink
1   Department of Neurosurgery, Cedars-Sinai Medical Center, Los Angeles, California, United States
Michael J. Alexander
1   Department of Neurosurgery, Cedars-Sinai Medical Center, Los Angeles, California, United States
Chirag G. Patil
1   Department of Neurosurgery, Cedars-Sinai Medical Center, Los Angeles, California, United States
Miriam Aracely Nuno
1   Department of Neurosurgery, Cedars-Sinai Medical Center, Los Angeles, California, United States
› Author Affiliations
Further Information

Publication History

21 November 2013

03 January 2014

Publication Date:
12 May 2014 (online)


Background and Purpose Expeditious treatment is critical in patients with aneurysmal subarachnoid hemorrhage (aSAH) due to the risk of rebleeding. This study aimed to define predictors of treatment delay among aSAH patients.

Methods A retrospective study of the Nationwide Inpatient Sample database identified patients diagnosed with SAH between 2002 and 2007. Patient's characteristics such as age, gender, race, insurance, SAH severity, treatment (coil versus clip), and other factors were studied. The Cochrane-Armitage test was used to assess delayed care trends by procedure, time of treatment, and hospital volume. Multivariate logistic regression evaluated factors associated with treatment delays.

Results A total of 38,827 patients were admitted between 2002 and 2007; 69.0% were women and 61% were white. The overall median age was 52 years. More patients underwent treatment with surgical clipping than with endovascular coiling (60.4% versus 39.6%, respectively). Overall, 74% of hospital admissions occurred on weekdays; the remaining 26% occurred on weekends. Multivariate analysis revealed that older age (odds ratio [OR]: 1.1; p = 0.0004) and surgical clipping versus endovascular coiling (OR: 1.3; p = 0.02) were independent predictors of delayed treatment (i.e., >2 days from admission). Nonwhite patients experienced greater treatment delays on weekdays compared with white patients (OR: 1.4; p = 0.01). Furthermore, patients treated in low-volume hospitals were significantly more likely to experience delays than those treated in higher volume hospitals (OR: 2.0; p = 0.007).

Conclusions Risk factors associated with treatment delay in aSAH patients include older age, nonwhite race, surgical clipping, and admission to low surgical volume hospitals.

  • References

  • 1 National Research Council. Executive summary. Crossing the Quality Chasm: A New Health System for the 21st Century. Washington, DC: The National Academies Press; 2001
  • 2 Connolly Jr ES, Rabinstein AA, Carhuapoma JR , et al; American Heart Association Stroke Council; Council on Cardiovascular Radiology and Intervention; Council on Cardiovascular Nursing; Council on Cardiovascular Surgery and Anesthesia; Council on Clinical Cardiology. Guidelines for the management of aneurysmal subarachnoid hemorrhage: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 2012; 43 (6) 1711-1737
  • 3 Kassell NF, Torner JC, Jane JA, Haley Jr EC, Adams HP. The International Cooperative Study on the Timing of Aneurysm Surgery. Part 2: Surgical results. J Neurosurg 1990; 73 (1) 37-47
  • 4 Ohman J, Heiskanen O. Timing of operation for ruptured supratentorial aneurysms: a prospective randomized study. J Neurosurg 1989; 70 (1) 55-60
  • 5 de Gans K, Nieuwkamp DJ, Rinkel GJ, Algra A. Timing of aneurysm surgery in subarachnoid hemorrhage: a systematic review of the literature. Neurosurgery 2002; 50 (2) 336-340; discussion 340–342
  • 6 Hillman J, Fridriksson S, Nilsson O, Yu Z, Saveland H, Jakobsson KE. Immediate administration of tranexamic acid and reduced incidence of early rebleeding after aneurysmal subarachnoid hemorrhage: a prospective randomized study. J Neurosurg 2002; 97 (4) 771-778
  • 7 Kassell NF, Torner JC. Aneurysmal rebleeding: a preliminary report from the Cooperative Aneurysm Study. Neurosurgery 1983; 13 (5) 479-481
  • 8 Naidech AM, Janjua N, Kreiter KT , et al. Predictors and impact of aneurysm rebleeding after subarachnoid hemorrhage. Arch Neurol 2005; 62 (3) 410-416
  • 9 Ohkuma H, Tsurutani H, Suzuki S. Incidence and significance of early aneurysmal rebleeding before neurosurgical or neurological management. Stroke 2001; 32 (5) 1176-1180
  • 10 World Health Organization. International Classification of Diseases and Related Health Problems. Geneva, Switzerland: WHO; 1993
  • 11 Hoh BL, Rabinov JD, Pryor JC, Carter BS, Barker II FG. In-hospital morbidity and mortality after endovascular treatment of unruptured intracranial aneurysms in the United States, 1996–2000: effect of hospital and physician volume. AJNR Am J Neuroradiol 2003; 24 (7) 1409-1420
  • 12 Barker II FG, Amin-Hanjani S, Butler WE , et al. Age-dependent differences in short-term outcome after surgical or endovascular treatment of unruptured intracranial aneurysms in the United States, 1996–2000. Neurosurgery 2004; 54 (1) 18-28; discussion 28–30
  • 13 Cowan Jr JA, Ziewacz J, Dimick JB, Upchurch Jr GR, Thompson BG. Use of endovascular coil embolization and surgical clip occlusion for cerebral artery aneurysms. J Neurosurg 2007; 107 (3) 530-535
  • 14 Shea AM, Reed SD, Curtis LH, Alexander MJ, Villani JJ, Schulman KA. Characteristics of nontraumatic subarachnoid hemorrhage in the United States in 2003. Neurosurgery 2007; 61 (6) 1131-1137; discussion 1137–1138
  • 15 Andaluz N, Zuccarello M. Recent trends in the treatment of cerebral aneurysms: analysis of a nationwide inpatient database. J Neurosurg 2008; 108 (6) 1163-1169
  • 16 Crowley RW, Yeoh HK, Stukenborg GJ, Medel R, Kassell NF, Dumont AS. Influence of weekend hospital admission on short-term mortality after intracerebral hemorrhage. Stroke 2009; 40 (7) 2387-2392
  • 17 Elixhauser A, Steiner C, Harris DR, Coffey RM. Comorbidity measures for use with administrative data. Med Care 1998; 36 (1) 8-27
  • 18 Shukla R, Fisher R, Fisher R. Testing of 3M's APR-DRG risk adjustment for hospital mortality outcomes. Abstr Academy Health Services Res Health Policy Meeting 2002; 19: 11
  • 19 Gonnella JS, Louis DZ, Gozum MVE , et al. Disease Staging: Clinical and Coded Criteria. Version 5.27 ed. Ann Arbor, MI: Thomson Reuters; 2010. . Available at: http://www.hcup-us.ahrq.gov/db/nation/nis/DiseaseStagingV5_27ClinicalandCodedCriteria.pdf
  • 20 Khatri R, Tariq N, Vazquez G, Suri MF, Ezzeddine MA, Qureshi AI. Outcomes after nontraumatic subarachnoid hemorrhage at hospitals offering angioplasty for cerebral vasospasm: a national level analysis in the United States. Neurocrit Care 2011; 15 (1) 34-41
  • 21 Nuño M, Patil CG, Lyden P, Drazin D. The effect of transfer and hospital volume in subarachnoid hemorrhage patients. Neurocrit Care 2012; 17 (3) 312-323
  • 22 Hop JW, Rinkel GJ, Algra A, van Gijn J. Case-fatality rates and functional outcome after subarachnoid hemorrhage: a systematic review. Stroke 1997; 28 (3) 660-664
  • 23 Starke RM, Connolly Jr ES ; Participants in the International Multi-Disciplinary Consensus Conference on the Critical Care Management of Subarachnoid Hemorrhage. Rebleeding after aneurysmal subarachnoid hemorrhage. Neurocrit Care 2011; 15 (2) 241-246
  • 24 Locksley HB. Natural history of subarachnoid hemorrhage, intracranial aneurysms and arteriovenous malformations. J Neurosurg 1966; 25 (3) 321-368
  • 25 Hijdra A, Vermeulen M, van Gijn J, van Crevel H. Rerupture of intracranial aneurysms: a clinicoanatomic study. J Neurosurg 1987; 67 (1) 29-33
  • 26 Broderick JP, Brott TG, Duldner JE, Tomsick T, Leach A. Initial and recurrent bleeding are the major causes of death following subarachnoid hemorrhage. Stroke 1994; 25 (7) 1342-1347
  • 27 Baltsavias GS, Byrne JV, Halsey J, Coley SC, Sohn MJ, Molyneux AJ. Effects of timing of coil embolization after aneurysmal subarachnoid hemorrhage on procedural morbidity and outcomes. Neurosurgery 2000; 47 (6) 1320-1329; discussion 1329–1331
  • 28 Dalbayrak S, Altas M, Arslan R. The effects of timing of aneurysm surgery on vasospasm and mortality in patients with subarachnoid hemorrhage. Acta Neurol Belg 2011; 111 (4) 317-320
  • 29 Lawson MF, Chi YY, Velat GJ, Mocco JD, Hoh BL. Timing of aneurysm surgery: the International Cooperative Study revisited in the era of endovascular coiling. J Neurointerv Surg 2010; 2 (2) 131-134
  • 30 Ross N, Hutchinson PJ, Seeley H, Kirkpatrick PJ. Timing of surgery for supratentorial aneurysmal subarachnoid haemorrhage: report of a prospective study. J Neurol Neurosurg Psychiatry 2002; 72 (4) 480-484
  • 31 Whitfield PC, Kirkpatrick PJ. Timing of surgery for aneurysmal subarachnoid haemorrhage. Cochrane Database Syst Rev 2001; (2) CD001697
  • 32 Wong GK, Boet R, Ng SC , et al. Ultra-early (within 24 hours) aneurysm treatment after subarachnoid hemorrhage. World Neurosurg 2012; 77 (2) 311-315
  • 33 Dorhout Mees SM, Molyneux AJ, Kerr RS, Algra A, Rinkel GJ. Timing of aneurysm treatment after subarachnoid hemorrhage: relationship with delayed cerebral ischemia and poor outcome. Stroke 2012; 43 (8) 2126-2129
  • 34 Schievink WI, van der Werf DJ, Hageman LM, Dreissen JJ. Referral pattern of patients with aneurysmal subarachnoid hemorrhage. Surg Neurol 1988; 29 (5) 367-371
  • 35 Bell CM, Redelmeier DA. Mortality among patients admitted to hospitals on weekends as compared with weekdays. N Engl J Med 2001; 345 (9) 663-668
  • 36 Kostis WJ, Demissie K, Marcella SW, Shao YH, Wilson AC, Moreyra AE ; Myocardial Infarction Data Acquisition System (MIDAS 10) Study Group. Weekend versus weekday admission and mortality from myocardial infarction. N Engl J Med 2007; 356 (11) 1099-1109
  • 37 Hasegawa Y, Yoneda Y, Okuda S , et al; Acute Stroke Rehabilitation Study Group. The effect of weekends and holidays on stroke outcome in acute stroke units. Cerebrovasc Dis 2005; 20 (5) 325-331
  • 38 Crowley RW, Yeoh HK, Stukenborg GJ, Ionescu AA, Kassell NF, Dumont AS. Influence of weekend versus weekday hospital admission on mortality following subarachnoid hemorrhage. Clinical article. J Neurosurg 2009; 111 (1) 60-66
  • 39 Bell CM, Redelmeier DA. Waiting for urgent procedures on the weekend among emergently hospitalized patients. Am J Med 2004; 117 (3) 175-181
  • 40 Saposnik G, Baibergenova A, Bayer N, Hachinski V. Weekends: a dangerous time for having a stroke?. Stroke 2007; 38 (4) 1211-1215
  • 41 Becker DJ. Do hospitals provide lower quality care on weekends?. Health Serv Res 2007; 42 (4) 1589-1612
  • 42 Siddiq F, Chaudhry SA, Tummala RP, Suri MF, Qureshi AI. Factors and outcomes associated with early and delayed aneurysm treatment in subarachnoid hemorrhage patients in the United States. Neurosurgery 2012; 71 (3) 670-677; discussion 677–678
  • 43 Schievink WI, Riedinger M, Jhutty TK, Simon P. Racial disparities in subarachnoid hemorrhage mortality: Los Angeles County, California, 1985–1998. Neuroepidemiology 2004; 23 (6) 299-305
  • 44 Cross III DT, Tirschwell DL, Clark MA , et al. Mortality rates after subarachnoid hemorrhage: variations according to hospital case volume in 18 states. J Neurosurg 2003; 99 (5) 810-817
  • 45 Krumholz HM, Herrin J, Miller LE , et al. Improvements in door-to-balloon time in the United States, 2005 to 2010. Circulation 2011; 124 (9) 1038-1045
  • 46 Broderick JP, Brott T, Tomsick T, Huster G, Miller R. The risk of subarachnoid and intracerebral hemorrhages in blacks as compared with whites. N Engl J Med 1992; 326 (11) 733-736
  • 47 Sacco RL, Boden-Albala B, Gan R , et al. Stroke incidence among white, black, and Hispanic residents of an urban community: the Northern Manhattan Stroke Study. Am J Epidemiol 1998; 147 (3) 259-268
  • 48 Johnston SC, Selvin S, Gress DR. The burden, trends, and demographics of mortality from subarachnoid hemorrhage. Neurology 1998; 50 (5) 1413-1418
  • 49 Bruno A, Carter S, Qualls C, Nolte KB. Incidence of spontaneous subarachnoid hemorrhage among Hispanics and non-Hispanic whites in New Mexico. Ethn Dis 1997; 7 (1) 27-33
  • 50 Ayala C, Greenlund KJ, Croft JB , et al. Racial/ethnic disparities in mortality by stroke subtype in the United States, 1995–1998. Am J Epidemiol 2001; 154 (11) 1057-1063
  • 51 Ayala C, Croft JB, Greenlund KJ , et al. Sex differences in US mortality rates for stroke and stroke subtypes by race/ethnicity and age, 1995–1998. Stroke 2002; 33 (5) 1197-1201
  • 52 McIver JI, Friedman JA, Wijdicks EF , et al. Preoperative ventriculostomy and rebleeding after aneurysmal subarachnoid hemorrhage. J Neurosurg 2002; 97 (5) 1042-1044
  • 53 Leake CB, Brinjikji W, Kallmes DF, Cloft HJ. Increasing treatment of ruptured cerebral aneurysms at high-volume centers in the United States. J Neurosurg 2011; 115 (6) 1179-1183
  • 54 Schiff RL, Ansell DA, Schlosser JE, Idris AH, Morrison A, Whitman S. Transfers to a public hospital. A prospective study of 467 patients. N Engl J Med 1986; 314 (9) 552-557
  • 55 Gordon HS, Rosenthal GE. Impact of interhospital transfers on outcomes in an academic medical center. Implications for profiling hospital quality. Med Care 1996; 34 (4) 295-309
  • 56 Obremskey W, Henley MB. A comparison of transferred versus direct admission orthopedic trauma patients. J Trauma 1994; 36 (3) 373-376