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Francisco, M.D.Clinical Associate Professor of Physical Medicine and Rehabilitation, University of Texas Health Sciences Center; Adjunct Assistant Professor of Physical Medicine and Reha

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Textbook of Traumatic Brain Injury

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Gerard E Francisco, M.D.

Clinical Associate Professor of Physical Medicine and Rehabilitation, University

of Texas Health Sciences Center; Adjunct Assistant Professor of Physical Medicine and Rehabilitation, Baylor College of Medicine; Associate Director, Brain Injury and Stroke Program, The Institute for Rehabilitation and Research, Houston, Texas

Douglas I Katz, M.D.

Associate Professor of Neurology, Boston University School of Medicine, Boston, Massachusetts; Medical Director, Brain Injury Programs, Healthsouth Braintree Rehabilitation Hospital, Braintree, Massachusetts

Jeffrey S Kreutzer, Ph.D.

Professor of Physical Medicine and Rehabilitation, Neurosurgery, and Psychiatry, Virginia Commonwealth University, Medical College of Virginia Campus, Richmond, Virginia

Professor, Department of Rehabilitation Medicine, Thomas Jefferson

University; Director, Moss Rehabilitation Research Institute, Albert Einstein Healthcare Network, Philadelphia, Pennsylvania

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Washington, DCLondon, England

Textbook of Traumatic Brain Injury

Edited by

Jonathan M Silver, M.D.

Thomas W McAllister, M.D.

Stuart C Yudofsky, M.D.

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Note: The authors have worked to ensure that all information in this book is accurate at the time of publication and

consistent with general psychiatric and medical standards, and that information concerning drug dosages, schedules, and routes of administration is accurate at the time of publication and consistent with standards set by the U.S Food and Drug Administration and the general medical community As medical research and practice continue to advance, however, therapeutic standards may change Moreover, specific situations may require a specific therapeutic response not included in this book For these reasons and because human and mechanical errors sometimes occur, we recommend that readers follow the advice of physicians directly involved in their care or the care of a member of their family.Books published by American Psychiatric Publishing, Inc., represent the views and opinions of the individual authors and do not necessarily represent the policies and opinions of APPI or the American Psychiatric Association

Copyright © 2005 American Psychiatric Publishing, Inc

ALL RIGHTS RESERVED

Manufactured in the United States of America on acid-free paper

First Edition

Typeset in Adobe’s Janson and Frutiger

American Psychiatric Publishing, Inc

1000 Wilson Boulevard

Arlington, VA 22209-3901

www.appi.org

Library of Congress Cataloging-in-Publication Data

Textbook of traumatic brain injury / edited by Jonathan M Silver, Thomas W McAllister,

Stuart C Yudofsky. 1st ed

p ; cm

Includes bibliographical references and index

ISBN 1-58562-105-6 (hardcover : alk paper)

1 Brain damage I Silver, Jonathan M., 1953- II McAllister, Thomas W

III Yudofsky, Stuart C

[DNLM: 1 Brain Injuries complications 2 Mental Disorders etiology 3 Brain

Injuries rehabilitation 4 Mental Disorders diagnosis 5 Mental Disorders therapy

WL 354 T355 2005]

RC387.5.T46 2005

617.4'81044 dc22

2004050262

British Library Cataloguing in Publication Data

A CIP record is available from the British Library

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To the courage of our patients:

"Who can foresee what will come?

Do with all your might whatever you are able to do."

—Ecclesiastes

To the devotion of our families:

Orli, Elliot, Benjamin, and Leah

Jeanne, Ryan, Lindsay, and Craig

Beth, Elissa, Lynn, and Emily

"A fruitful bough by a well;

Whose branches run over the wall."

—Genesis 49:22

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Contributors xiii Foreword xviiSarah and James Brady

Lawrence D Chu, M.S., M.P.H., Ph.D

2 Neuropathology 27Thomas A Gennarelli, M.D

David I Graham, M.B.B.Ch., Ph.D

3 Neurosurgical Interventions 51Roger Hartl, M.D

Jamshid Ghajar, M.D., Ph.D

4 Neuropsychiatric Assessment 59Kimberly A Arlinghaus, M.D

Arif M Shoaib, M.D

Trevor R P Price, M.D

5 Structural Imaging 79Erin D Bigler, Ph.D

6 Functional Imaging 107Karen E Anderson, M.D

Katherine H Taber, Ph.D

Robin A Hurley, M.D

7 Electrophysiological Techniques 135David B Arciniegas, M.D

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22 Balance Problems and Dizziness 393

Edwin F Richter III, M.D

23 Vision Problems 405

Neera Kapoor, O.D., M.S

Kenneth J Ciuffreda, O.D., Ph.D

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x i v Contributors

Laura A Flashman, Ph.D.

Associate Professor of Psychiatry, Department of

Psychi-atry, Division of NeuropsychiPsychi-atry, Dartmouth Medical

School, Lebanon, New Hampshire; New Hampshire

Hospital, Concord, New Hampshire

Jason R Freeman, Ph.D.

Associate Director, Brain Injury and Sports Concussion

Institute, University of Virginia School of Medicine,

Charlottesville, Virginia

Carl T Fulp, M.S.

Predoctoral Fellow, Traumatic Brain Injury Laboratory,

Department of Neurosurgery, University of Pennsylvania

School of Medicine, Philadelphia, Pennsylvania

Thomas A Gennarelli, M.D.

Professor and Chair, Department of Neurosurgery,

Med-ical College of Wisconsin, Milwaukee, Wisconsin

Patricia L Gerbarg, M.D.

Assistant Professor of Clinical Psychiatry, New York

Medical College, Valhalla, New York

Jamshid Ghajar, M.D., Ph.D.

President, Brain Trauma Foundation, New York, New York

Wayne A Gordon, Ph.D.

Jack Nash Professor, Department of Rehabilitation

Medi-cine, Mount Sinai School of MediMedi-cine, New York, New York

David I Graham, M.B.B.Ch., Ph.D.

Professor and Head of Neuropathology, Institute of

Neu-rological Sciences, Southern General Hospital, Glasgow,

Scotland

Roger Hartl, M.D.

Assistant Professor of Neurosurgery, Department of

Neurological Surgery, Joan and Sanford I Weill Cornell

Medical College, Cornell University, New York, New

York

Mary R Hibbard, Ph.D.

Professor, Department of Rehabilitation Medicine,

Mount Sinai School of Medicine, New York, New York

Andrew Hornstein, M.D.

Assistant Clinical Professor of Psychiatry, Columbia

University College of Physicians and Surgeons, New

York, New York; Attending Psychiatrist, Head Injury

Services, Helen Hayes Hospital, West Haverstraw, New

York

Robin A Hurley, M.D.

Associate Professor, Departments of Psychiatry and

Radiology, Wake Forest University School of

Medi-cine, Winston-Salem, North Carolina; Clinical

Associ-ate Professor, Department of Psychiatry, Baylor

College of Medicine, Houston, Texas; Associate Chief

of Staff/Mental Health, Hefner VAMC, Salisbury,

North Carolina

Ricardo E Jorge, M.D.

Assistant Professor of Psychiatry, Roy J and Lucille A

Carv-er College of Medicine, UnivCarv-ersity of Iowa, Iowa City, Iowa

Neera Kapoor, O.D., M.S.

Associate Clinical Professor, Department of Clinical ences and Director, Raymond J Greenwald RehabilitationCenter, SUNY State College of Optometry, New York,New York

Sci-Thomas Kay, Ph.D.

Assistant Clinical Professor, Department of RehabilitationMedicine, New York University School of Medicine; RuskInstitute of Rehabilitation Medicine, New York, New York

Richard E Kennedy, M.D.

Assistant Professor, Departments of Psychiatry and ical Medicine & Rehabilitation, Virginia CommonwealthUniversity School of Medicine, Richmond, Virginia

Phys-Edward Kim, M.D.

Associate Professor of Psychiatry, University of Medicineand Dentistry of New Jersey–Robert Wood JohnsonMedical School, Piscataway, New Jersey

Jess F Kraus, M.P.H., Ph.D.

Professor of Epidemiology, University of California, LosAngeles, School of Public Health; Director, Southern Cal-ifornia Injury Prevention Research Center, Los Angeles,California

Associ-Mark R Lovell, Ph.D.

Director, Sports Medicine Concussion Program,

Universi-ty of Pittsburgh Medical Center, Pittsburgh, Pennsylvania

Pitts-Michael F Martelli, Ph.D.

Clinical Associate Professor, Department of Physical cine and Rehabilitation, University of Virginia, Charlottes-ville, Virginia; Clinical Assistant Professor, Departments ofPsychology and Psychiatry, Virginia Commonwealth Uni-versity Health System, Richmond, Virginia; ConcussionCare Centre of Virginia, Ltd., Tree of Life, L.L.C., GlenAllen, Virginia

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Medi-Contributors x v

Jeffrey E Max, M.B.B.Ch.

Professor, In-Residence, Department of Psychiatry,

Uni-versity of California, San Diego, School of Medicine;

Di-rector of Neuropsychiatric Research, Children's Hospital

and Health Center, San Diego, California

Thomas W McAllister, M.D.

Professor of Psychiatry, Department of Psychiatry,

Sec-tion of Neuropsychiatry, Dartmouth Medical School,

Lebanon, New Hampshire

Scott McCullagh, M.D.

Assistant Professor, Neuropsychiatry Program,

Universi-ty of Toronto, Sunnybrook and Women’s College

Hospi-tal, Toronto, Ontario, Canada

Tracy K McIntosh, Ph.D.

Professor of Neurosurgery and Director, Traumatic

Brain Injury Laboratory, Department of Neurosurgery,

University of Pennsylvania School of Medicine,

Philadel-phia, Pennsylvania

Norman S Miller, M.D.

Professor of Psychiatry and Medicine, Department of

Psychiatry, Michigan State University College of Human

Medicine, East Lansing, Michigan

Keith Nicholson, Ph.D.

Comprehensive Pain Program, Toronto Western

Hospi-tal, Toronto, Ontario, Canada

Alison Moon O'Shanick, M.S., C.C.C.-S.L.P.

Center for Neurorehabilitation Services, Midlothian,

Virginia

Gregory J O’Shanick, M.D.

Medical Director, Center for Neurorehabilitation

Servic-es, Midlothian, Virginia; National Medical Director, Brain

Injury Association of America, McLean, Virginia

Mary F Pelham, Psy.D.

Neuropsychologist, Moss Rehab, Elkins Park Hospital,

Elkins Park, Pennsylvania

Kirsten Plehn, Ph.D.

Fellow in Clinical Neuropsychology, Department of

Psy-chiatric Medicine, University of Virginia School of

Med-icine, Charlottesville, Virginia

Irwin W Pollack, M.D., M.A.

Emeritus Professor of Psychiatry, University of Medicine

and Dentistry of New Jersey–Robert Wood Johnson

Medical School, Piscataway, New Jersey

Trevor R P Price, M.D.

Private Practice of General Adult Psychiatry, Geriatric

Psy-chiatry, and NeuropsyPsy-chiatry, Bryn Mawr, Pennsylvania

Vani Rao, M.D.

Assistant Professor, Division of Geriatric Psychiatry andNeuropsychiatry, Department of Psychiatry and Behav-ioral Sciences, Johns Hopkins University School of Med-icine, Baltimore, Maryland

William E Reynolds, D.D.S., M.P.H.

Public Service Professor, School of Social Welfare, andClinical Associate Professor, School of Public Health,State University at Albany, Albany, New York

Edwin F Richter III, M.D.

Associate Clinical Director, Rusk Institute of tion Medicine, New York, New York

Rehabilita-Robert G Robinson, M.D.

Paul W Penningroth Professor and Head of Psychiatry,Roy J and Lucille A Carver College of Medicine, Uni-versity of Iowa, Iowa City, Iowa

Donald C Rojas, Ph.D.

Associate Professor of Psychiatry, University of ColoradoHealth Sciences Center, Denver, Colorado

Pamela Rollings, M.D.

Adult Psychiatry, Wellspan Behavioral Health, Division

of Neurosciences, Behavioral Health Services, WellspanHealth–Delphic Office, York, Pennsylvania

Nicolas C Royo, Ph.D.

Postdoctoral Fellow, Traumatic Brain Injury Laboratory,Department of Neurosurgery, University of PennsylvaniaSchool of Medicine, Philadelphia, Pennsylvania

Saori Shimizu, M.D., Ph.D.

Postdoctoral Fellow, Traumatic Brain Injury Laboratory,Department of Neurosurgery, University of PennsylvaniaSchool of Medicine, Philadelphia, Pennsylvania

Arif M Shoaib, M.D.

Clinical Assistant Professor, Department of Psychiatry,University of Texas Health Science Center at Houston,Houston, Texas

Jennifer Spiro, M.S.

Research Coordinator, Division of Geriatric Psychiatryand Neuropsychiatry, Department of Psychiatry and Be-havioral Sciences, Johns Hopkins University School ofMedicine, Baltimore, Maryland

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x v i Contributors

Katherine H Taber, Ph.D.

Research Health Scientist, Research and Education

Ser-vice Line, Hefner VAMC, Salisbury, North Carolina;

Re-search Fellow, School of Health Information Sciences,

University of Texas Health Science Center at Houston,

Houston, Texas

Paula T Trzepacz, M.D.

Clinical Professor of Psychiatry, University of

Missis-sippi School of Medicine, Jackson, MissisMissis-sippi; Adjunct

Professor of Psychiatry, Tufts University School of

Medicine, Boston, Massachusetts; Medical Director,

U.S Neurosciences, Lilly Research Laboratories,

Indi-anapolis, Indiana

Gary J Tucker, M.D.

Emeritus Professor, Department of Psychiatry,

Uni-versity of Washington School of Medicine, Seattle,

Washington

Thomas N Ward, M.D.

Associate Professor of Medicine, Section of Neurology,

Dartmouth-Hitchcock Medical Center, Lebanon, New

Hampshire

Deborah L Warden, M.D.

Associate Professor of Neurology and Psychiatry, formed Services University of the Health Sciences, Be-thesda, Maryland; National Director, Defense andVeterans Brain Injury Center, Walter Reed Army MedicalCenter, Washington, D.C

Ross Zafonte, D.O.

Professor and Chair, Department of Physical Medicineand Rehabilitation, University of Pittsburgh School ofMedicine, Pittsburgh, Pennsylvania

Nathan D Zasler, M.D.

Clinical Associate Professor, Department of PhysicalMedicine and Rehabilitation, University of Virginia,Charlottesville, Virginia; Concussion Care Centre of Vir-ginia, Ltd., Pinnacle Rehabilitation, Inc., Tree of Life,L.L.C., Glen Allen, Virginia

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4 TEXTBOOK OF TRAUMATIC BRAIN INJURY

T A B L E 1 – 1 Case identification, source, and brain injury severity criteria and scoring: selected United States incidence studies

1974

Head injury with evidence of presumed brain involvement (i.e., concussion with LOC, PTA, or neurological signs of brain injury or skull fracture.

1) Fatal (<28 days) 2) Severe: intracranial hematoma, contusion, or LOC >24 hours, or PTA >24 hours

3) Moderate: LOC or PTA 30 minutes to 24 hours, skull fracture or both

4) LOC or PTA <30 minutes without skull fracture Klauber et al

California, 1981

Physician-diagnosed physical damage from acute mechanical energy exchange resulting in concussion, hemorrhage, contusion, or laceration

of brain.

Modified GCS Severe= ≤8; moderate=9–15 plus hospital stay

of 4–8 hours and brain surgery, or abnormal CT,

or GCS 9–12; mild=all others, GCS 13–15 Whitman et al

1) Fatal 2) Severe=intracranial hematoma, LOC/PTA >24 hours contusion

3) Moderate=LOC or PTA 30 minutes to <24 hours 4) Mild=LOC to PTA <30 minutes

5) Trivial=remainder MacKenzie et al

Thurman et al

1996

Utah 1990–1992 Discharge data from all 40 acute care

hospitals using ICD-9-CM codes 800.0–801.9, 803.0–804.9, and 850.0–854.1 in any primary or secondary data fields.

1) Initial GCS: severe= ≤8; moderate=9–12; mild=13–15

2) Demonstrated intracranial traumatic lesions 3) Focal abnormalities on neurologic examination Centers for

Discharge data from all state hospitals

or health care providers.

No severity data reported.

ICDMAP using as many as five ICD discharge diagnoses

Severe TBI=fatal or ISS ≥9

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Epidemiology 5

computed tomography (CT) (Marshall et al 1991) The

Glasgow Coma Scale (GCS; Jennett and Teasdale 1981)

is commonly used for the initial assessment of severity

The GCS, a clinical prognostic indicator, is an important

contribution to standardizing early assessment of the

se-verity of brain injury (Table 1–2) Although its application

was intended to be repeated, typical current practice

gen-erally consists of a single observation Herein lies one of

the major difficulties in the application of the GCS: not

knowing in various studies when the GCS was

adminis-tered during the early stages of treatment In some

stud-ies, the GCS was administered at the scene of the injury

or during emergency transport, whereas in others it was

done on arrival at the emergency department or just

be-fore hospital admission; in still others, the time of

assess-ment was not reported

Obviously, GCS results during the hospital course

change according to patient improvement or

deteriora-tion For proper comparison of research findings, the

GCS should be administered at approximately the same

time postinjury Assessment on arrival at the emergency

department is recommended

An inherent weakness of the GCS is its limited

rele-vance to some patients with brain injuries The GCS is

Sosin et al 1996 United States 1991 Self-reported data from U.S National

Health Interview Survey Injury Supplement for mild and moderate brain injury defined as loss of consciousness in previous 12 months.

Severity not evaluated

Thurman and

Guerrero 1999

United States 1980–

1995

All hospital discharge records with one

or more ICD codes of 800.0–801.9, 803.0–804.9, or 850.0–854.1 from the National Hospital Discharge Survey.

ICDMAP used to convert ICD codes to approximate AIS scores: 1–2=mild; 3=moderate; 4–6=severe

Jager et al 2000 United States 1992–

1994

Same ICD codes as Thurman et al

1996; identified from U.S National Hospital Ambulatory Medical Care Survey.

Severity not evaluated

al 1996; identified from U.S

National Hospital Ambulatory Medical Care Survey.

Severity not evaluated

Note. LOC=loss of consciousness; PTA=posttraumatic amnesia; GCS=Glasgow Coma Scale (Jennett and Teasdale 1981); ICD=International sification of Diseases; ICD-9-CM=International Classification of Diseases, 9th Revision, Clinical Modification (World Health Organization 1986); CNS=central nervous system; CT=computed tomography; TBI=traumatic brain injury; AIS=Abbreviated Injury Scale; ISS=Injury Severity Score.

Clas-T A B L E 1 – 1 Case identification, source, and brain injury severity criteria and scoring: selected United

States incidence studies (continued)

Study

Location

T A B L E 1 – 2 Glasgow Coma Scale

Eye opening (E) Spontaneous 4

Verbal response (V) Oriented 5

Confused conversation 4 Inappropriate words 3 Incomprehensible sounds 2

Coma score (E + M + V)=3–15

Source Adapted from Jennett B, Teasdale G: Management of Head

In-juries Philadelphia, PA, FA Davis, 1981.

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6 TEXTBOOK OF TRAUMATIC BRAIN INJURY

difficult or impossible to apply to young children, patients

with significant facial swelling from blunt trauma,

pa-tients under the influence of alcohol or other substances,

and patients who are not able to respond to the verbal

component because of language differences or an inability

to comprehend The current emergency department

practice of immediate intubation or sedation may further

invalidate (or restrict) GCS measurements Regardless of

these restrictions, the GCS remains one of the most

con-sistently used measures of brain injury severity

Epidemiological studies of patients with brain injuries

are infrequently undertaken, and in the past 10 years, more

reliance has been placed on administrative data sets to

esti-mate the incidence and features of persons with TBI Such

data sources include the U.S National Health Interview

Survey (NHIS), U.S National Hospital Ambulatory

Med-ical Care Survey (NHAMCS), U.S National Hospital

Dis-charge Survey (NHDS), and equivalent data sets from

in-dividual states and groups of states (see Table 1–1)

In discussing the nature and severity of injury, we have

drawn some information from a large brain injury cohort

study conducted in San Diego County, California, during

the early 1980s (Kraus et al 1984) For the purposes of

this chapter, we focus on the specifics of diagnosis,

con-sidering skull fracture status as an important confounding

factor In addition, we provide basic information on the

relationship between demographic characteristics such as

age, sex, and socioeconomic status (SES) and the severity

and type of brain injury Finally, we develop a predictive

model for outcome at hospital discharge

All epidemiological studies involving people

hospital-ized with brain injury indicate that a large majority of

pa-tients treated in emergency departments and admitted to

hospitals (for observation or treatment) have sustained

what has been termed mild traumatic brain injury

(MTBI)—that is, one with a GCS score of 13–15 Because

this injury occurs so often and the information on the

in-juries and outcomes is so incomplete, a Consequences of

Mild TBI section addressing the nature of the available

data and selected aggregate findings on outcome

parame-ters has been included toward the end of this chapter

Estimates of Occurrence of Brain Injury

Incidence

Data summarized in Figure 1–1 show that brain injury

occurrence rates range from a low of 92 per 100,000

pop-ulation in seven states (Thurman and Guerrero 1999) to

a high of 618 per 100,000 population in a United States

national survey (Sosin et al 1996) Caution must be taken

in interpreting these findings because brain injury tions, criteria for diagnoses, and sources were not thesame in all studies (see Table 1–1) In addition, the preci-sion of population-at-risk estimates varied considerably(i.e., some rates were based on catchment area populationestimates in noncensus years)

defini-Nevertheless, a current average rate of fatal plus tal hospitalized brain injuries reported in all United Statesstudies is approximately 150 per 100,000 population peryear If the highest and lowest estimates are excluded fromconsideration, the estimated rate is approximately 120 per100,000 per year, which is the estimate used in this chapterfor purposes of disability estimation

nonfa-Brain Injury Death and Death Rates

In 2001, 157,078 people died from acute traumaticinjury—approximately 6.5% of all deaths in the UnitedStates (Centers for Disease Control and Prevention2002) The exact percentage of deaths involving signifi-cant brain injury is not precisely known, but data fromOlmsted County, Minnesota (Annegers et al 1980), andSan Diego County, California (Kraus et al 1984), suggestthat approximately 50% are caused by trauma to thebrain National Center for Health Statistics multiple-cause-of-death data indicate that an average of approxi-mately 28% of all injury deaths involve significant braintrauma (Sosin et al 1995) This percentage is probablyincorrect because, as the investigators pointed out, thecase-finding process relied on a limited set of specificinjury diagnoses Furthermore, the actual death certifi-cates were not examined—a crucial problem when “mas-sive multiple trauma” is recorded on the death certificatebut specific body locations and types of trauma are notrecorded Sosin et al (1989) reported a possible underes-timate in the actual proportion of fatal brain injury of23%–44%

The reported brain injury fatality rate varies from 14

to 30 per 100,000 population per year (Figure 1–2) Therange in rates probably reflects a lack of specificity of di-agnosis on some death certificates

Nonfatal Brain Injury

National estimates of nonfatal brain injury for the UnitedStates have been derived from the National Health Inter-view Survey (NHIS; Sosin et al 1996), the National Hos-pital Ambulatory Medical Care Survey (NHAMCS; Jager

et al 2000), the National Hospital Discharge Survey(NHDS; Thurman and Guerrero 1999), and the NationalCenter for Injury Prevention and Control (NCIPC;Thurman et al 1999) The NHIS reported that approxi-

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Epidemiology 7

mately 1.5 million head injuries occur per year (Sosin et

al 1996) However, this estimate includes self-reported

concussions and skull fractures, as well as a mixture of

dif-ferent types of intracranial injuries requiring professional

medical care, some with and some without neurological

trauma The extent of emergency department and non–

emergency department diagnosis and treatment of brain

injury is unknown The Centers for Disease Control and

Prevention (CDC) reported to Congress in 1999 that

more than 5 million Americans, or 2% of the nation’s

population, were living with TBI-related disabilities

(Thurman et al 1999)

A large number of TBI cases are caused by sports and

physical activity From July 2000 to June 2001, an

esti-mated 350,000 persons were treated in emergency

de-partments for sports- and recreation-related head

inju-ries; of these persons, 200,000 were diagnosed with abrain injury (Gotsch et al 2002) Countless sports-relatedTBIs go unreported because the majority are MTBIcases—for example, concussions without loss of con-sciousness (Collins et al 1999) Identification of thesecases is vital for proper treatment and prevention of long-term deleterious effects

On a reexamination of the NHIS database for 1985–

1986, Fife (1987) concluded that only 16% of all head juries resulted in an admission to a hospital Hence, onlyone of six people with head (not necessarily brain) injuryrequire hospitalization As expected, findings from NHIS,NHAMCS, and NHDS vary widely (see Figure 1–1) be-cause the data sources are so different from one another

in-An estimate derived from published sources rized in Figure 1–3 and Table 1–3) suggests that approxi-

(summa-F I G U R E 1 – 1 Brain injury rates: selected United States studies.

A=United States estimate 1980–1995 (Thurman and Guerrero 1999); B=Colorado 1991–1992 (Gabella et al 1997); C=Colorado,

Missouri, Oklahoma, Utah 1990–1992 (Centers for Disease Control and Prevention 1997); D=Utah 1990–1992 (Thurman et al 1996); E=Maryland 1986 (MacKenzie et al 1989); F=United States estimate 1981 (Fife 1987); G=Rhode Island 1979–1980 (Fife et

al 1986); H=San Diego County, CA, 1981 (Kraus et al 1986); I=Olmsted County, MN, 1965–1974 (Annegers et al 1980); J=United States estimate 1974 (Kalsbeek et al 1980); K=Virginia 1978 (Jagger et al 1984); L=Bronx, NY, 1980–1981 (Cooper et al 1983);

M=San Diego County, CA, 1978 (Klauber et al 1981); N=Chicago area 1979–1980 (Whitman et al 1984); O=United States estimate

1992–1994 (Jager et al 2000); P=United States estimate 1991 (Sosin et al 1996).

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8 TEXTBOOK OF TRAUMATIC BRAIN INJURY

mately 234,000 people were discharged from hospitals in

the United States in 1998 with a brain injury diagnosis;

based on 1998 census estimates of 270 million persons, a

hospital admission rate of approximately 87 per 100,000

population per year is deduced The hospital discharge

rate is useful for estimating the annual disability rate from

injury (discussed later in Estimation of Number of New

Disabilities) The difference in estimates obtained using

average incidence values in aggregate United States

stud-ies versus data from hospital discharges or visits is because

of definitional variation The actual United States

inci-dence rate is presumed, therefore, to range from 100 to

150 per 100,000 population per year

The relative importance of brain injury discharge

fre-quencies is illustrated in Table 1–3 As seen, the brain

in-jury discharge rate is the third highest compared with

other major central nervous system (CNS) diagnoses

The hospital discharge count (or rate) shown in Figure 1–3

and Table 1–3 is not the true figure, because not all cases

are found within the International Classification of eases discharge diagnoses used to identify brain injurycases (see Table 1–1) The purpose of gathering informa-tion on brain injury occurrence rates is threefold: to mon-itor changes in incidence in the population, to evaluatethe effects of specific countermeasures, and to identifyhigh- (or low-) risk groups and exposure circumstances

Dis-Characteristics of High-Risk Groups

Age

All studies of brain injury occurrence in the United Statesshow that people ages 15–24 years are at the highest risk.Patterns in age-specific rates (Figure 1–4) illustrate atleast two high-risk age groups: those ages 15–24 years andthose older than age 64 years It is noteworthy that ratesfor people younger than age 10 years (and particularly

F I G U R E 1 – 2 Brain injury fatality rates: selected United States studies.

A=Virginia 1978 (Jagger et al 1984); B=United States estimate 1981 (Fife 1987); C=United States estimate 1992 (Sosin et al 1995); D=Olmsted County, MN, 1965–1974 (Annegers et al 1980); E=San Diego County, CA, 1978 (Klauber et al 1981); F=Chicago area

1979–1980 (Whitman et al 1984); G=Bronx, NY, 1980–1981 (Cooper et al 1983); H=San Diego County, CA, 1981 (Kraus et al.

1984).

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Epidemiology 9

those younger than age 5 years) are high in some studies

reporting age-specific data The age-related risk

distribu-tion reflects differences in exposure, particularly to motor

vehicle crashes

Gender

All incidence reports published worldwide indicate that

brain injuries are far more frequent among men than

women, and United States studies have found a rate ratio

of approximately 1.6–2.8 (Figure 1–5) Variation in rate

ratios cannot be attributed solely to reporting differences

The differences in rate ratios may reflect different exposure

levels For example, there may be a higher proportion of

injuries connected with motor vehicle crashes (which

involve more males) as compared with injuries connected

with falls in the home (which involve more females)

Race or Ethnicity

Some studies show higher brain injury incidence in

non-whites compared with non-whites, but there is justifiable concern

over the quality of the data used to derive the rates Because

hospital reporting practices vary widely in recording

ethni-city or race in medical records, racial or ethnic differences inbrain injury rates have yet to be determined accurately

Alcohol

The positive association between blood alcohol tration (BAC) and risk of injury is well established for allexternal causes of injuries, including motor vehiclecrashes, general aviation crashes, drownings, and violence(Smith and Kraus 1988) Less studied is the role of alco-hol and the outcome of specific kinds and anatomicallocations of injuries such as CNS trauma and burns.Although animal studies demonstrate a variety of physio-logical effects of alcohol on CNS injuries, human data areunequivocal In one study (Kraus et al 1989), 56% ofadults with a brain injury diagnosis had a positive BACtest result It is noteworthy that 49% of those adultstested had a BAC that was at or above the legal level(0.10%) The prevalence of a positive BAC varied byseverity of brain injury; the highest prevalence was amongthose with MTBI compared with those with moderate orsevere brain injury (71% vs 49%, respectively) However,selection bias may occur in emergency department BACtesting of injured people with different severities or types

concen-T A B L E 1 – 3 Frequency of selected first-listed diagnoses for inpatients discharged from short-stay, nonfederal hospitals, 1998

Number of discharges ( × 1000)

Discharge rate (per 100,000 population)

191 Malignant neoplasm of brain 32 11.8

431, 432 Intracerebral and intracranial hemorrhage 87 32.2

434 Occlusion of cerebral arteries 309 114.3

436, 437 Other cerebrovascular disease 195 72.2

Note Brain injuries include any listed diagnoses.

a International Classification of Diseases, 9th Revision, Clinical Modification (ICD-9-CM; World Health Organization 1986).

b Includes ICD-9-CM codes 800, 801, 803, 804, 850, 851, 852, 853, 854, 905, 907 These codes may not include all admissions with brain injuries but include diagnoses such as skull fracture with and without concussion, contusion, or hemorrhage and late effects of skull fracture or intracranial injury.

Source Reprinted from Popovic JR, Kozak LJ: “National Hospital Discharge Survey: Annual Summary, 1998.” Vital and Health Statistics 13:1–194,

2000 Used with permission.

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1 0 TEXTBOOK OF TRAUMATIC BRAIN INJURY

of injuries or different inherent sociodemographic orexternal-cause features For example, blood testing wasless frequent for males, young adults, people with mildbrain injuries, and those injured from falls Despite thispotential bias, Kraus et al (1989) found that the BAClevel was positively associated with physician-diagnosedneurological impairment and length of hospitalization

Recurrent TBI

Annegers and associates (1980) were the first to measurethe relative risk (RR) of recurrent TBI in their epidemio-logical study of head injuries in Olmsted County, Minne-sota They estimated the RR of a second TBI among thosewith an earlier TBI at approximately 2.8–3.0 times that ofthe general noninjured population The RR of recurrentTBI given an initial head injury increased with age, and the

RR of a third TBI given a second head injury was between7.8 and 9.3 times that of an initial head injury in the popu-lation Salcido and Costich (1992) reviewed the published

F I G U R E 1 – 3 Estimated annual brain injury

frequency.

aSource. Sosin et al (1995) and Kraus et al (1994).

bSource. National Hospital Discharge Survey, 1995–1996

(Thurman and Guerrero 1999).

cSource. National Health Interview Survey, 1991 (Sosin et al.

1996).

F I G U R E 1 – 4 Peak age groups at risk for brain injury: selected United States studies.

A=United States estimate 1992–1994 (Jager et al 2000); B=United States estimate 1991 (Sosin et al 1996); C=San Diego County, CA, 1981

(Kraus et al 1986); D=Virginia 1977–1979 (Rimel 1981); E=Colorado 1991–1992 (Gabella et al 1997); F=Colorado, Missouri, Oklahoma, Utah 1990–1992 (Centers for Disease Control and Prevention 1997); G=Utah 1990–1992 (Thurman et al 1996).

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Epidemiology 1 1

literature on recurrent TBI in 1992 and concluded that

repetitive injury may be due to three possible causes:

repeated exposure to an external or environmental factor

(e.g., alcohol abuse), some internal factor that gives rise to

increased vulnerability, or a combination of external or

environmental factors and internal vulnerability The

liter-ature has established a strong association between

recur-rent TBI and alcohol abuse (Kreutzer et al 1990; Ruff et al

1990) Effective interventions after TBI must incorporate

alcohol cessation even for those with the less serious forms

of injury

Recurrent TBI has been the subject of many reports

in the area of head injury in sports Case reports (Cantu

and Voy 1995; Kelly et al 1991; Saunders and Harbaugh

1984) and case series studies (Jordan and Zimmerman

1990) have highlighted the need to carefully mentor the

concussed player before permitting his or her return to

sporting exposures There is no evidence that repeatedbrain injuries in sports lead to unusual risk of TBI in non-sports–associated exposures

Socioeconomic Status

The NHIS for 1985–1987 (Collins 1990) showed that theestimated average annual number of injuries and the ratesper 100 people per year are highest in families at the lowestincome levels This finding was also observed by Kraus et

al (1986) in San Diego County, California; by Whitman et

al (1984) in two socioeconomically different communities

in Chicago; and by Sosin et al (1996) in the United States

In the Kraus et al (1986) study, the surrogate for individualSES was median family income per census tract, and, in thereport by Sosin et al (1996), family income was the variableused for SES Multivariate analysis by Kraus et al (1986)

F I G U R E 1 – 5 Male/female brain injury rate ratios: selected United States studies.

A=Virginia 1978 (Jagger et al 1984); B=Rhode Island 1979–1980 (Fife et al 1986); C=San Diego County, CA, 1981 (Kraus et al.

1986); D=Maryland 1986 (MacKenzie et al 1989); E=United States estimate 1974 (Kalsbeek et al 1980); F=Bronx, NY, 1980–1981 (Cooper et al 1983); G=Chicago area 1979–1980 (Whitman et al 1984); H=Colorado 1991–1992 (Gabella et al 1997); I=Colorado, Missouri, Oklahoma, Utah 1990–1992 (Centers for Disease Control and Prevention 1997); J=Utah 1990–1992 (Thurman et al 1996); K=Olmsted County, MN, 1965–1974 (Annegers et al 1980); L=United States estimate 1992–1994 (Jager et al 2000);

M=United States estimate 1991 (Sosin et al 1996).

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1 2 TEXTBOOK OF TRAUMATIC BRAIN INJURY

and Sosin et al (1996) suggested that using race and/or

ethnicity as a proxy for SES may be inappropriate Other

aspects of exposure nested within the socioeconomic

envi-ronment should be explored, such as low income and living

alone (Sosin et al 1996)

Characteristics of High-Risk Exposures

Published studies use inconsistent classifications of

exter-nal cause of injury, which restricts any meta-aexter-nalysis of

cause of brain injury Broad groupings of external causes

(Figure 1–6) can be used to make general statements about

the nature of the exposures associated with brain injury

Despite the limitations of the categorization of

exter-nal cause, available data suggest that the most frequent

type of exposure associated with fatal and nonfatal brain

injury is transport Transport includes automobiles, cles, motorcycles, aircraft, watercraft, and others (e.g.,farm equipment) The most common transport-relatedexternal cause is motor vehicle crashes (Figure 1–7).Falls are the second leading cause of brain injury andare associated most frequently with older age (see Figure1–6) Assault-related brain injury, most frequently in-volving the use of firearms, is an important factor inpenetrating brain injuries (Centers for Disease Controland Prevention 1997; Cooper et al 1983; Kraus et al.1984; Sosin et al 1995; Thurman et al 1996; Whitman

bicy-et al 1984) It is not possible to identify brain injuries lated to sports or recreation in some studies because theyhave been grouped into an “other” category In at leastfour studies (Annegers et al 1980; Kraus et al 1984;Sosin et al 1996; Whitman et al 1984), sports wereidentified as a significant exposure for brain injury A

re-F I G U R E 1 – 6 Percentage distribution of brain injuries by external cause: selected United States studies.

A=United States estimate 1974 (Kalsbeek et al 1980); B=Virginia 1978 (Jagger et al 1984); C=San Diego County, CA, 1978 (Klauber

et al 1981); D=San Diego County, CA, 1981 (Kraus et al 1984); E=Olmsted County, MN, 1965–1974 (Annegers et al 1980);

F=Chicago area 1979–1980 (Whitman et al 1984); G=Bronx, NY, 1980–1981 (Cooper et al 1983); H=Maryland 1986 (MacKenzie

et al 1989); I=Rhode Island 1979–1980 (Fife et al 1986); J=Colorado, Missouri, Oklahoma, Utah 1990–1992 (Centers for Disease Control and Prevention 1997); K=United States estimate 1992–1994 (Jager et al 2000); L=United States estimate 1991 (Sosin et al 1996); M=Utah 1990–1992 (Thurman et al 1996).

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Epidemiology 1 3

major caveat in this discussion is that in some studies all

bicycle-related exposures have been classified as

trans-portation related Kraus et al (1987) found that

approx-imately two-thirds of the brain injuries related to

bicy-cles are not because of collisions with motor vehibicy-cles

The dominant form of exposure in motor vehicle

crashes is as an occupant of a road vehicle Classification

difficulties across studies do not allow for

characteriza-tion of occupant locacharacteriza-tion (i.e., driver vs passenger), but

it is possible to categorize motor vehicle–related

expo-sures into three general groups: vehicle occupants,

rid-ers on motorcycles, and pedestrians or bicyclists Brain

injuries are most frequent in the vehicle occupants

group Motorcyclists also frequently sustain brain

inju-ries There are no data on the actual number of people

who are occupants or riders on motorcycles; hence, data

on specific rates of occurrence cannot be derived

Spe-cial note should be made of the report from Taiwan (Lee

et al 1990), where motorcyclists, including scooter

riders, form the largest portion of the motor vehicle–related brain injury problem in the population

Severity and the Types of Brain Injury

All studies published before 1996 showed that the est proportion of brain injuries were “mild” (i.e., gener-ally, a GCS score of 13–15) The distribution of the sever-ity of brain injury, as assessed by the GCS, is shown inFigure 1–8 In terms of emergency department visits andhospital admissions, the majority of brain injuries in peo-ple who were hospitalized over the past 25 years were ofmild severity Among those people admitted to a hospitalalive, the severity distribution is approximately 80% mild(GCS score of 13–15), 10% moderate (GCS score of 9–12), and 10% severe (GCS score of 8 or less) The lowerproportion of mild brain injuries (and higher proportion

great-of moderate and severe injuries) found in the Virginia

F I G U R E 1 – 7 Percentage distribution of brain injuries for subcauses of motor vehicle–related exposures: selected studies.

A=San Diego County, CA, 1981 (Kraus et al 1986); B=San Diego County, CA, 1978 (Klauber et al 1981); C=Olmsted County, MN,

1965–1974 (Annegers et al 1980); D=Virginia 1978 (Jagger et al 1984); E=Seattle 1981 (Gale et al 1983); F=Taiwan 1977–1987

(Lee et al 1990).

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1 4 TEXTBOOK OF TRAUMATIC BRAIN INJURY

study (Jagger et al 1984) reflects the nature of the referral

institution (i.e., serious injuries were more likely to be

referred to the University of Virginia Hospital from the

surrounding catchment area)

Reports published over the past 5–7 years show that

the severity of TBI in hospitalized patients is more

equally divided among mild, moderate, and severe

cat-egories of injury (Thurman and Guerrero 1999;

Thur-man et al 1996) Changes in hospital admission

prac-tices may be the reason underlying the dramatic

decline in proportions of patients admitted with

MTBI The effect of these practices in short- or

long-term outcomes is unknown and should be the focus of

current research

Hospital Discharges and Diagnoses

Information on people discharged from short-stay

non-federal hospitals in the United States in 1998 is available

through the NHDS (Popovic and Kozak 2000) Thisdata source provides information on any listed diagnosis

of brain injury coded according to the InternationalClassification of Diseases, 9th Revision, Clinical Modi-fication (ICD-9-CM; World Health Organization1986) Data on discharge rates with any listed braininjury diagnosis are summarized in Figures 1–9 and 1–10.The rate for those discharged with a brain injury fromshort-stay hospitals during 1998 was approximately 87per 100,000 population The rate for males was twice ashigh as that for females Figure 1–10 shows that mostpeople discharged from a hospital with a brain injurywere diagnosed as having a hemorrhage, contusion, orlaceration without fracture of the skull Approximately18% of the discharges involved “other intracranialinjury” without skull fracture, and intracranial injurywith fracture represented approximately 22% of all hos-pital discharges

The only age-specific national data on hospital charges are grouped into four generally heterogeneous age

dis-F I G U R E 1 – 8 Percentage severity distribution of brain injuries: selected United States studies.

A=Olmsted County, MN, 1965–1974 (Annegers et al 1980); B=Virginia 1978 (Jagger et al 1984); C=San Diego County, CA, 1981

(Kraus et al 1986); D=Chicago area 1979–1980 (Whitman et al 1984); E=Maryland 1986 (MacKenzie et al 1989); F=San Diego County, CA, 1978 (Klauber et al 1981); G=United States estimate 1980–1995 (Thurman and Guerrero 1999).

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Epidemiology 1 5

groups (see Figure 1–9) Those younger than age 15 years

(showing the lowest discharge rates in Figure 1–9) include

infants, toddlers, young children, and adolescents; each

group has various types of exposures The 15- to

44-year-old group combines people in their late 20s, 30s, and early

40s with those who are generally at highest risk of brain

in-jury (i.e., those ages 15–24 years), thus dramatically

reduc-ing the incidence shown in Figure 1–9 for this larger age

range It should be noted that the aggregate age-specific

in-jury incidence rates (reported in Figure 1–4) are

consider-ably higher than the age-specific discharge rates from the

NHDS (see Figure 1–9) One possible explanation for the

high brain injury rate among hospital discharges for infants

is “birth trauma,” a diagnosis that is excluded from most

brain injury databases Patients who died at the scene of

in-jury, during emergency transport, or in the emergency

fa-cility are not included in the estimates

In evaluating these data, it should be noted that NHDS

data are based on discharges from short-stay hospitals, but

some injured people may have been admitted to multiple

hospitals or to the same hospital on multiple occasions for

the same injury Hence, the discharge does not represent amutually exclusive occurrence, and a patient who had one

or more admissions to one or more hospitals during theobservation period is counted multiple times Independentinformation from our experience suggests that multiplehospital admissions are relatively common, particularly intoday’s climate of different payment requirements for pub-lic versus private institutions

Types of Brain Lesions

Although the literature is replete with reports describingbrain trauma, each report typically is based on a clinicalseries from a single institution Few epidemiological stud-ies have addressed the question of the nature and severity

of brain lesions, and for this purpose, specific data wereretrieved from the 1981 San Diego County cohort study(Kraus et al 1984) In this study, clinical information wasuniformly recorded from the physician’s notes in themedical record The reader should be aware that these

F I G U R E 1 – 9 Sex- and age-specific (in years) brain injury hospital discharges per 100,000 population: United States 1998 All listed diagnoses.

Source Reprinted from Popovic JR, Kozak LJ: “National Hospital Discharge Survey: Annual Summary, 1998.” Vital and Health

Statistics 13:1–194, 2000 Used with permission.

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