DOI: 10.3171/jns.2007.106.6.1051. Sensitivity of patient-specific numerical simulation of cerebal aneurysm hemodynamics to inflow boundary conditions

Sensitivity of patient-specific numerical simulation of cerebal aneurysm hemodynamics to inflow boundary conditions

10.3171/jns.2007.106.6.1051

Crossref journal-article

Journal of Neurosurgery Publishing Group (JNSPG)

Journal of Neurosurgery (1754)

Abstract

Object Due to the difficulty of obtaining patient-specific velocity measurements during imaging, many assumptions have to be made while imposing inflow boundary conditions in numerical simulations conducted using patient-specific, imaging-based cerebral aneurysm models. These assumptions can introduce errors, resulting in lack of agreement between the computed flow fields and the true blood flow in the patient. The purpose of this study is to evaluate the effect of the assumptions made while imposing inflow boundary conditions on aneurysmal hemodynamics. Methods A patient-based anterior communicating artery aneurysm model was selected for this study. The effects of various inflow parameters on numerical simulations conducted using this model were then investigated by varying these parameters over ranges reported in the literature. Specifically, we investigated the effects of heart and blood flow rates as well as the distribution of flow rates in the A1 segments of the anterior cerebral artery. The simulations revealed that the shear stress distributions on the aneurysm surface were largely unaffected by changes in heart rate except at locations where the shear stress magnitudes were small. On the other hand, the shear stress distributions were found to be sensitive to the ratio of the flow rates in the feeding arteries as well as to variations in the blood flow rate. Conclusions Measurement of the blood flow rate as well as the distribution of the flow rates in the patient's feeding arteries may be needed for numerical simulations to accurately reproduce the intraaneurysmal hemodynamics in a specific aneurysm in the clinical setting.

Bibliography

Venugopal, P., Valentino, D., Schmitt, H., Villablanca, J. P., ViÃ±uela, F., & Duckwiler, G. (2007). Sensitivity of patient-specific numerical simulation of cerebal aneurysm hemodynamics to inflow boundary conditions. Journal of Neurosurgery, 106(6), 1051â1060.

Authors 6

Prem Venugopal (first)
Daniel Valentino (additional)
Holger Schmitt (additional)
J. Pablo Villablanca (additional)
Fernando Viñuela (additional)
Gary Duckwiler (additional)

References 26 Referenced 54

10.1115/1.2796081 / J Biomech Eng / Modeling of flow in a stented and nonstented side wall aneurysm model by Aenis (1997)
10.1016/0301-5629(94)90063-9 / Ultrasound Med Biol / A validation study on the intraobserver reproducibility of transcranial color-coded duplex sonography velocity measurements by Baumgartner (1994)
10.1227/00006123-199510000-00023 / Neurosurgery / Computer modeling of intracranial saccular and lateral aneurysms for the study of their hemodynamics by Burleson (1995)
{'key': 'b4-1061051', 'series-title': 'Thromb Haemost', 'first-page': '118', 'article-title': 'Identification of quantifiable hemodynamic factors in the assessment of cerebral aneurysm behavior. On behalf of the Subcommittee on Biorheology of the Scientific and Standardization Committee of the ISTH', 'volume': '79', 'author': 'Burleson', 'year': '1996'} / Thromb Haemost / Identification of quantifiable hemodynamic factors in the assessment of cerebral aneurysm behavior. On behalf of the Subcommittee on Biorheology of the Scientific and Standardization Committee of the ISTH by Burleson (1996)
10.1109/TMI.2005.844159 / IEEE Trans Med Imaging / Efficient pipeline for image-based patient-specific analysis of cerebral aneurysm hemodynamics: technique and sensitivity by Cebral (2005)
10.1117/12.535441 / Proc SPIE / Subject-specific modeling of intracranial aneurysms by Cebral (2004)
10.1023/B:APPL.0000014921.22210.6e / Flow Turbul Combust / Pulastile blood flow in anatomically accurate vessels with mutiple aneurysms: a medical intervention planning application of computational haemodynamics by Chatziprodromou (2003)
10.1016/S0741-5214(03)00944-3 / J Vasc Surg / Use of cine magnetic resonance angiography in quantifying aneurysm pulsatility associated with endoleak by Faries (2003)
10.1016/S0301-5629(00)00226-X / Ultrasound Med Biol / Blood flow velocity using transcranial doppler velocimetry in the middle and anterior cerebral arteries: correlation with sample volume depth by Hart (2000)
{'key': 'b10-1061051', 'series-title': 'AJNR Am J Neuroradiol', 'first-page': '63', 'article-title': 'Computational simulation of therapeutic parent artery occlusion to treat giant vertebrobasilar aneurysm', 'volume': '25', 'author': 'Hassan', 'year': '2004'} / AJNR Am J Neuroradiol / Computational simulation of therapeutic parent artery occlusion to treat giant vertebrobasilar aneurysm by Hassan (2004)
{'key': 'b11-1061051', 'series-title': 'AJNR Am J Neuroradiol', 'first-page': '1075', 'article-title': 'Hemodynamic analysis of an adult vein of galen aneurysm malformation by use of 3d image-based computational fluid dynamics', 'volume': '24', 'author': 'Hassan', 'year': '2003'} / AJNR Am J Neuroradiol / Hemodynamic analysis of an adult vein of galen aneurysm malformation by use of 3d image-based computational fluid dynamics by Hassan (2003)
{'key': 'b12-1061051', 'series-title': 'AJNR Am J Neuroradiol', 'first-page': '1356', 'article-title': 'Computational replicas: anatomic reconstructions of cerebral vessels as volume numerical grids at three-dimensional angiography', 'volume': '25', 'author': 'Hassan', 'year': '2004'} / AJNR Am J Neuroradiol / Computational replicas: anatomic reconstructions of cerebral vessels as volume numerical grids at three-dimensional angiography by Hassan (2004)
{'key': 'b13-1061051', 'series-title': 'AJNR Am J Neuroradiol', 'first-page': '1804', 'article-title': 'Computational approach to quantifying hemodynamic forces in giant cerebral aneurysms', 'volume': '24', 'author': 'Jou', 'year': '2003'} / AJNR Am J Neuroradiol / Computational approach to quantifying hemodynamic forces in giant cerebral aneurysms by Jou (2003)
{'key': 'b14-1061051', 'series-title': 'AJNR Am J Neuroradiol', 'first-page': '2357', 'article-title': 'Correlation between lumenal geometry changes and hemodynamics in fusiform intracranial aneurysms', 'volume': '26', 'author': 'Jou', 'year': '2005'} / AJNR Am J Neuroradiol / Correlation between lumenal geometry changes and hemodynamics in fusiform intracranial aneurysms by Jou (2005)
{'key': 'b15-1061051', 'series-title': 'AJNR Am J Neuroradiol', 'first-page': '2000', 'article-title': 'Flow dynamics in a lethal anterior communicating artery aneurysm', 'volume': '20', 'author': 'Kerber', 'year': '1999'} / AJNR Am J Neuroradiol / Flow dynamics in a lethal anterior communicating artery aneurysm by Kerber (1999)
10.1016/j.ultrasmedbio.2004.08.007 / Ultrasound Med Biol / Compliance of abdominal aortic aneurysms: evaluation of tissue doppler imaging by Long (2004)
10.3233/BIR-1993-303-413 / Biorheology / Hemodynamics in rigid and distensible saccular aneurysms: a numerical study of pulsatile flow characteristics by Low (1993)
10.1114/1.1349703 / Ann Biomed Eng / Factors influencing blood flow patterns in the human right coronary artery by Myers (2001)
10.1063/1.868599 / Phys Fluids / On the determinantion of solenoidal or compressible velocity fields from measurements of passive or reactive scalars by Pearlstein (1995)
10.1016/S0301-5629(00)00293-3 / Ultrasound Med Biol / Flow velocity and flow volume measurements in the extracranial carotid and vertebral arteries in healthy adults: reference data and effects of age by Scheel (2000)
10.1161/01.STR.0000144648.89172.0f / Stroke / Magnitude and role of wall shear stress on cerebral aneurysm: computational fluid dynamic study of 20 middle cerebral artery aneurysms by Shojima (2004)
10.1152/japplphysiol.00171.2001 / J Appl Physiol / Measurement of hemodynamics in human carotid artery using ultrasound and computational fluid dynamics by Starmans-Kool (2002)
10.1002/1098-2353(2000)13:4<231::AID-CA1>3.0.CO;2-T / Clin Anat / Anatomic variations of anterior cerebral artery cortical branches by Stefani (2000)
{'key': 'b24-1061051', 'series-title': 'AJNR Am J Neuroradiol', 'first-page': '559', 'article-title': 'Image-based computational simulation of flow dynamics in a giant intracranial aneurysm', 'volume': '24', 'author': 'Steinman', 'year': '2003'} / AJNR Am J Neuroradiol / Image-based computational simulation of flow dynamics in a giant intracranial aneurysm by Steinman (2003)
10.1161/01.STR.27.11.2086 / Stroke / Hemodynamic study of the anterior communicating artery by Ujiie (1996)
10.1113/jphysiol.1955.sp005276 / J Physiol / Method for the calculation of velocity, rate flow, and viscous drag in arteries when the pressure gradient is known by Womersley (1955)

Dates

Type	When
Created	17 years, 6 months ago (Jan. 24, 2008, 7:48 a.m.)
Deposited	1 year, 5 months ago (March 9, 2024, 5:11 a.m.)
Indexed	1 year ago (July 31, 2024, 12:30 p.m.)
Issued	18 years, 2 months ago (June 1, 2007)
Published	18 years, 2 months ago (June 1, 2007)
Published Print	18 years, 2 months ago (June 1, 2007)

Funders 0

None

BibTeX

@article{Venugopal_2007, title={Sensitivity of patient-specific numerical simulation of cerebal aneurysm hemodynamics to inflow boundary conditions}, volume={106}, ISSN={0022-3085}, url={http://dx.doi.org/10.3171/jns.2007.106.6.1051}, DOI={10.3171/jns.2007.106.6.1051}, number={6}, journal={Journal of Neurosurgery}, publisher={Journal of Neurosurgery Publishing Group (JNSPG)}, author={Venugopal, Prem and Valentino, Daniel and Schmitt, Holger and Villablanca, J. Pablo and Viñuela, Fernando and Duckwiler, Gary}, year={2007}, month=jun, pages={1051–1060} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2024,
        7,
        31
      ]
    ],
    "date-time": "2024-07-31T16:30:45Z",
    "timestamp": 1722443445197
  },
  "reference-count": 26,
  "publisher": "Journal of Neurosurgery Publishing Group (JNSPG)",
  "issue": "6",
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        2007,
        6
      ]
    ]
  },
  "abstract": "<jats:sec>\n<jats:title>Object</jats:title>\n<jats:p>Due to the difficulty of obtaining patient-specific velocity measurements during imaging, many assumptions have to be made while imposing inflow boundary conditions in numerical simulations conducted using patient-specific, imaging-based cerebral aneurysm models. These assumptions can introduce errors, resulting in lack of agreement between the computed flow fields and the true blood flow in the patient. The purpose of this study is to evaluate the effect of the assumptions made while imposing inflow boundary conditions on aneurysmal hemodynamics.</jats:p></jats:sec>\n<jats:sec>\n<jats:title>Methods</jats:title>\n<jats:p>A patient-based anterior communicating artery aneurysm model was selected for this study. The effects of various inflow parameters on numerical simulations conducted using this model were then investigated by varying these parameters over ranges reported in the literature. Specifically, we investigated the effects of heart and blood flow rates as well as the distribution of flow rates in the A<jats:sub>1</jats:sub> segments of the anterior cerebral artery.</jats:p>\n<jats:p>The simulations revealed that the shear stress distributions on the aneurysm surface were largely unaffected by changes in heart rate except at locations where the shear stress magnitudes were small. On the other hand, the shear stress distributions were found to be sensitive to the ratio of the flow rates in the feeding arteries as well as to variations in the blood flow rate.</jats:p></jats:sec>\n<jats:sec>\n<jats:title>Conclusions</jats:title>\n<jats:p>Measurement of the blood flow rate as well as the distribution of the flow rates in the patient's feeding arteries may be needed for numerical simulations to accurately reproduce the intraaneurysmal hemodynamics in a specific aneurysm in the clinical setting.</jats:p></jats:sec>",
  "DOI": "10.3171/jns.2007.106.6.1051",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2008,
        1,
        24
      ]
    ],
    "date-time": "2008-01-24T12:48:31Z",
    "timestamp": 1201178911000
  },
  "page": "1051-1060",
  "source": "Crossref",
  "is-referenced-by-count": 54,
  "title": "Sensitivity of patient-specific numerical simulation of cerebal aneurysm hemodynamics to inflow boundary conditions",
  "prefix": "10.3171",
  "volume": "106",
  "author": [
    {
      "given": "Prem",
      "family": "Venugopal",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Philips Medical Systems North America, Bothell, Washington; and"
        }
      ]
    },
    {
      "given": "Daniel",
      "family": "Valentino",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Radiological Sciences, David Geffen School of Medicine, University of California, Los Angeles, California"
        }
      ]
    },
    {
      "given": "Holger",
      "family": "Schmitt",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Philips Medical Systems North America, Bothell, Washington; and"
        }
      ]
    },
    {
      "given": "J. Pablo",
      "family": "Villablanca",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Radiological Sciences, David Geffen School of Medicine, University of California, Los Angeles, California"
        }
      ]
    },
    {
      "given": "Fernando",
      "family": "Vi\u00f1uela",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Radiological Sciences, David Geffen School of Medicine, University of California, Los Angeles, California"
        }
      ]
    },
    {
      "given": "Gary",
      "family": "Duckwiler",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Radiological Sciences, David Geffen School of Medicine, University of California, Los Angeles, California"
        }
      ]
    }
  ],
  "member": "1754",
  "reference": [
    {
      "key": "b1-1061051",
      "series-title": "J Biomech Eng",
      "doi-asserted-by": "publisher",
      "first-page": "206",
      "DOI": "10.1115/1.2796081",
      "article-title": "Modeling of flow in a stented and nonstented side wall aneurysm model",
      "volume": "119",
      "author": "Aenis",
      "year": "1997"
    },
    {
      "key": "b2-1061051",
      "series-title": "Ultrasound Med Biol",
      "doi-asserted-by": "publisher",
      "first-page": "233",
      "DOI": "10.1016/0301-5629(94)90063-9",
      "article-title": "A validation study on the intraobserver reproducibility of transcranial color-coded duplex sonography velocity measurements",
      "volume": "20",
      "author": "Baumgartner",
      "year": "1994"
    },
    {
      "key": "b3-1061051",
      "series-title": "Neurosurgery",
      "doi-asserted-by": "publisher",
      "first-page": "774",
      "DOI": "10.1227/00006123-199510000-00023",
      "article-title": "Computer modeling of intracranial saccular and lateral aneurysms for the study of their hemodynamics",
      "volume": "37",
      "author": "Burleson",
      "year": "1995"
    },
    {
      "key": "b4-1061051",
      "series-title": "Thromb Haemost",
      "first-page": "118",
      "article-title": "Identification of quantifiable hemodynamic factors in the assessment of cerebral aneurysm behavior. On behalf of the Subcommittee on Biorheology of the Scientific and Standardization Committee of the ISTH",
      "volume": "79",
      "author": "Burleson",
      "year": "1996"
    },
    {
      "key": "b5-1061051",
      "series-title": "IEEE Trans Med Imaging",
      "doi-asserted-by": "publisher",
      "first-page": "457",
      "DOI": "10.1109/TMI.2005.844159",
      "article-title": "Efficient pipeline for image-based patient-specific analysis of cerebral aneurysm hemodynamics: technique and sensitivity",
      "volume": "24",
      "author": "Cebral",
      "year": "2005"
    },
    {
      "key": "b6-1061051",
      "series-title": "Proc SPIE",
      "doi-asserted-by": "publisher",
      "first-page": "319",
      "DOI": "10.1117/12.535441",
      "article-title": "Subject-specific modeling of intracranial aneurysms",
      "volume": "5369",
      "author": "Cebral",
      "year": "2004"
    },
    {
      "key": "b7-1061051",
      "series-title": "Flow Turbul Combust",
      "doi-asserted-by": "publisher",
      "first-page": "333",
      "DOI": "10.1023/B:APPL.0000014921.22210.6e",
      "article-title": "Pulastile blood flow in anatomically accurate vessels with mutiple aneurysms: a medical intervention planning application of computational haemodynamics",
      "volume": "71",
      "author": "Chatziprodromou",
      "year": "2003"
    },
    {
      "key": "b8-1061051",
      "series-title": "J Vasc Surg",
      "doi-asserted-by": "publisher",
      "first-page": "652",
      "DOI": "10.1016/S0741-5214(03)00944-3",
      "article-title": "Use of cine magnetic resonance angiography in quantifying aneurysm pulsatility associated with endoleak",
      "volume": "38",
      "author": "Faries",
      "year": "2003"
    },
    {
      "key": "b9-1061051",
      "series-title": "Ultrasound Med Biol",
      "doi-asserted-by": "publisher",
      "first-page": "1267",
      "DOI": "10.1016/S0301-5629(00)00226-X",
      "article-title": "Blood flow velocity using transcranial doppler velocimetry in the middle and anterior cerebral arteries: correlation with sample volume depth",
      "volume": "26",
      "author": "Hart",
      "year": "2000"
    },
    {
      "key": "b10-1061051",
      "series-title": "AJNR Am J Neuroradiol",
      "first-page": "63",
      "article-title": "Computational simulation of therapeutic parent artery occlusion to treat giant vertebrobasilar aneurysm",
      "volume": "25",
      "author": "Hassan",
      "year": "2004"
    },
    {
      "key": "b11-1061051",
      "series-title": "AJNR Am J Neuroradiol",
      "first-page": "1075",
      "article-title": "Hemodynamic analysis of an adult vein of galen aneurysm malformation by use of 3d image-based computational fluid dynamics",
      "volume": "24",
      "author": "Hassan",
      "year": "2003"
    },
    {
      "key": "b12-1061051",
      "series-title": "AJNR Am J Neuroradiol",
      "first-page": "1356",
      "article-title": "Computational replicas: anatomic reconstructions of cerebral vessels as volume numerical grids at three-dimensional angiography",
      "volume": "25",
      "author": "Hassan",
      "year": "2004"
    },
    {
      "key": "b13-1061051",
      "series-title": "AJNR Am J Neuroradiol",
      "first-page": "1804",
      "article-title": "Computational approach to quantifying hemodynamic forces in giant cerebral aneurysms",
      "volume": "24",
      "author": "Jou",
      "year": "2003"
    },
    {
      "key": "b14-1061051",
      "series-title": "AJNR Am J Neuroradiol",
      "first-page": "2357",
      "article-title": "Correlation between lumenal geometry changes and hemodynamics in fusiform intracranial aneurysms",
      "volume": "26",
      "author": "Jou",
      "year": "2005"
    },
    {
      "key": "b15-1061051",
      "series-title": "AJNR Am J Neuroradiol",
      "first-page": "2000",
      "article-title": "Flow dynamics in a lethal anterior communicating artery aneurysm",
      "volume": "20",
      "author": "Kerber",
      "year": "1999"
    },
    {
      "key": "b16-1061051",
      "series-title": "Ultrasound Med Biol",
      "doi-asserted-by": "publisher",
      "first-page": "1099",
      "DOI": "10.1016/j.ultrasmedbio.2004.08.007",
      "article-title": "Compliance of abdominal aortic aneurysms: evaluation of tissue doppler imaging",
      "volume": "30",
      "author": "Long",
      "year": "2004"
    },
    {
      "key": "b17-1061051",
      "series-title": "Biorheology",
      "doi-asserted-by": "publisher",
      "first-page": "287",
      "DOI": "10.3233/BIR-1993-303-413",
      "article-title": "Hemodynamics in rigid and distensible saccular aneurysms: a numerical study of pulsatile flow characteristics",
      "volume": "30",
      "author": "Low",
      "year": "1993"
    },
    {
      "key": "b18-1061051",
      "series-title": "Ann Biomed Eng",
      "doi-asserted-by": "publisher",
      "first-page": "109",
      "DOI": "10.1114/1.1349703",
      "article-title": "Factors influencing blood flow patterns in the human right coronary artery",
      "volume": "29",
      "author": "Myers",
      "year": "2001"
    },
    {
      "key": "b19-1061051",
      "series-title": "Phys Fluids",
      "doi-asserted-by": "publisher",
      "first-page": "754",
      "DOI": "10.1063/1.868599",
      "article-title": "On the determinantion of solenoidal or compressible velocity fields from measurements of passive or reactive scalars",
      "volume": "7",
      "author": "Pearlstein",
      "year": "1995"
    },
    {
      "key": "b20-1061051",
      "series-title": "Ultrasound Med Biol",
      "doi-asserted-by": "publisher",
      "first-page": "1261",
      "DOI": "10.1016/S0301-5629(00)00293-3",
      "article-title": "Flow velocity and flow volume measurements in the extracranial carotid and vertebral arteries in healthy adults: reference data and effects of age",
      "volume": "26",
      "author": "Scheel",
      "year": "2000"
    },
    {
      "key": "b21-1061051",
      "series-title": "Stroke",
      "doi-asserted-by": "publisher",
      "first-page": "2500",
      "DOI": "10.1161/01.STR.0000144648.89172.0f",
      "article-title": "Magnitude and role of wall shear stress on cerebral aneurysm: computational fluid dynamic study of 20 middle cerebral artery aneurysms",
      "volume": "35",
      "author": "Shojima",
      "year": "2004"
    },
    {
      "key": "b22-1061051",
      "series-title": "J Appl Physiol",
      "doi-asserted-by": "publisher",
      "first-page": "957",
      "DOI": "10.1152/japplphysiol.00171.2001",
      "article-title": "Measurement of hemodynamics in human carotid artery using ultrasound and computational fluid dynamics",
      "volume": "92",
      "author": "Starmans-Kool",
      "year": "2002"
    },
    {
      "key": "b23-1061051",
      "series-title": "Clin Anat",
      "doi-asserted-by": "publisher",
      "first-page": "231",
      "DOI": "10.1002/1098-2353(2000)13:4<231::AID-CA1>3.0.CO;2-T",
      "article-title": "Anatomic variations of anterior cerebral artery cortical branches",
      "volume": "13",
      "author": "Stefani",
      "year": "2000"
    },
    {
      "key": "b24-1061051",
      "series-title": "AJNR Am J Neuroradiol",
      "first-page": "559",
      "article-title": "Image-based computational simulation of flow dynamics in a giant intracranial aneurysm",
      "volume": "24",
      "author": "Steinman",
      "year": "2003"
    },
    {
      "key": "b25-1061051",
      "series-title": "Stroke",
      "doi-asserted-by": "publisher",
      "first-page": "2086",
      "DOI": "10.1161/01.STR.27.11.2086",
      "article-title": "Hemodynamic study of the anterior communicating artery",
      "volume": "27",
      "author": "Ujiie",
      "year": "1996"
    },
    {
      "key": "b26-1061051",
      "series-title": "J Physiol",
      "doi-asserted-by": "publisher",
      "first-page": "553",
      "DOI": "10.1113/jphysiol.1955.sp005276",
      "article-title": "Method for the calculation of velocity, rate flow, and viscous drag in arteries when the pressure gradient is known",
      "volume": "127",
      "author": "Womersley",
      "year": "1955"
    }
  ],
  "container-title": "Journal of Neurosurgery",
  "original-title": [],
  "link": [
    {
      "URL": "https://thejns.org/view/journals/j-neurosurg/106/6/article-p1051.xml",
      "content-type": "text/html",
      "content-version": "vor",
      "intended-application": "text-mining"
    },
    {
      "URL": "https://thejns.org/downloadpdf/journals/j-neurosurg/106/6/article-p1051.xml",
      "content-type": "text/html",
      "content-version": "vor",
      "intended-application": "syndication"
    },
    {
      "URL": "https://thejns.org/downloadpdf/journals/j-neurosurg/106/6/article-p1051.xml",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2024,
        3,
        9
      ]
    ],
    "date-time": "2024-03-09T10:11:08Z",
    "timestamp": 1709979068000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://thejns.org/view/journals/j-neurosurg/106/6/article-p1051.xml"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2007,
        6
      ]
    ]
  },
  "references-count": 26,
  "journal-issue": {
    "issue": "6"
  },
  "URL": "http://dx.doi.org/10.3171/jns.2007.106.6.1051",
  "relation": {},
  "ISSN": [
    "0022-3085"
  ],
  "subject": [],
  "container-title-short": "JNS",
  "published": {
    "date-parts": [
      [
        2007,
        6
      ]
    ]
  }
}