Lippincott-Raven Publishers. Volume 21(3), 1 February 1996, pp

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1 Lippincott-Raven Publishers. Volume 21(3), 1 February 1996, pp Impaired Cognitive Functioning After Whiplash Injury of the Cervical Spine [Spine Update] Radanov, Bogdan P. MD * ; Dvorak, Jiri MD From the * Department of Psychiatry, University of Berne, Inselspital, Berne, Switzerland, and Wilhelm Schulthess Hospital, Spine Unit, Zürich, Switzerland. Acknowledgment date: March 8, Supported by the Swiss National Science Foundation, Berne, Switzerland, project number First revision date: October 28, Second revision date: January 20, Acceptance date: July 5, Device status category: 1. Address reprint requests to: Bogdan P. Radanov, MD; Department of Psychiatry; University of Berne; Inselspital, CH Berne; Switzerland Abstract To enhance the awareness of physicians treating whiplash patients, findings from previous research regarding cognitive functioning of these patients are discussed and recommendations for assessment provided. Cognitive disturbances (i.e., deficient attentional functioning

2 and impairment of memory) are frequent complaints in patients after whiplash injury. However, few prospective studies of nonselected patients have been performed. These studies indicate that impaired cognitive functioning relates either to trauma-induced somatic symptoms (i.e., pain) or psychologic symptoms resulting from problems adjusting to trauma-related somatic symptoms. Accordingly, cognitive disturbances after whiplash show a fair rate of recovery, which parallels recovery from trauma-related somatic symptoms. Current research does not indicate disturbances in higher cognitive functions after whiplash. Patients who suffered concussion and victims of so-called whiplash injury of the cervical spine share many common symptoms. This is true particularly for cognitive complaints (i.e., attention or memory). Despite a lack of identifiable organic abnormality, research into concussion has revealed at least transitory impairment of information processing.4 Based on these findings and similar symptoms, several studies have assessed cognitive functioning in whiplash patients.2,11,14,15,23,26 Findings from these studies deserve particular attention because of their possible medical-legal consequences in different insurance schemes. Physicians assessing and treating patients after so-called whiplash injury of the cervical spine (i.e., orthopedic surgeons, rheumatologists, neurologists, and family physicians) face a number of psychologic and cognitive problems in these patients in addition to the otherwise well-known somatic symptoms. An understanding of the former may be crucial in assessing work capacity and estimating the timing of return to work and may play a central role in the settlement of litigation cases. The main focus of this review is to update physicians with empirical data regarding problems in cognitive functioning after whiplash injury. We provide in more detail recommendations about which patients deserve further detailed assessment and who best should investigate such patients by which methods. [black small square] What is Cognitive Functioning? Human behavior is essentially based on three aspects:12 1) intellect or cognition known as the information-handling aspect; 2) emotional, reflecting feelings and motivation; and 3) control, which concerns the

3 expression of behavior. These three aspects are considerably interconnected. The aspect of intellect or cognition consists of the following functions: * receptive functions (for which intact perception is necessary) reflect the ability to acquire, process, classify, and integrate information; * learning and memory, i.e., storage and recall of information; * thinking, i.e., mental organization of information; and * expressive functions, responsible for communication of information, such as speaking. Receptive functions in particular are based on wakefulness, which is necessary for attentiveness. Attention is regarded as a basic cognitive function because it has considerable influence on the ability of a human to perform other (so-called higher) cognitive functions mentioned above. [black small square] What May Cause Impairment in Cognitive Functioning? For many medical professionals cognitive impairment indicates the existence of organic brain damage. This is a major mistake. Although this review is not exhaustive, a few examples may help to clarify some of the causes of impaired cognitive functioning. It may be acquired at birth for different reasons. By taking the patient's history, several aspects of limited intellectual or cognitive ability may be identified in the early childhood. Furthermore, impaired psychologic functioning may compromise cognition.4 The best known examples are depression 4 and schizophrenia. A number of psychoactive substances, in particular those that may reduce the level of wakefulness (alcohol, sedative hypnotics, some analgesics) and compromise attention, may lead to impairment of different aspects of cognition. A traumatic brain injury resulting from a blow to the head is characterized not only by detectable lesions to the brain tissue but essentially by a loss of consciousness, resulting in post-traumatic amnesia. After traumatic brain injury, patients with post-traumatic amnesia frequently have impaired cognitive functioning.5 This is known to occur in the absence of detectable brain lesions. Other factors, such as secondary gain (mainly financial compensation), may lead to reduced motivation to perform a cognitive task and may bias results. Under certain circumstances (particularly where compensation is prominent), a person may simply exaggerate or malinger.3

4 Unfortunately to date, there is no testing procedure that can identify unequivocally patients who exaggerate or fake impairment in cognitive function tests.7 [black small square] Can Whiplash Injury Lead to Lesions of the Brain Tissue? Despite statements to the contrary,8 there is no convincing evidence of morphologic damage to any part of the brain as a result of whiplash injury. Studies with experimental animals 8 supporting such damage are not representative in this regard because acceleration forces used in studies that led to brain damage cannot be translated to the average accidents leading to whiplash injury in humans. Such high acceleration forces in humans can result in brain damage of which the mentioned traumatic loss of consciousness is a sign. Because the latter is indicative of head injury, this should be considered an exclusion criterion for diagnosing whiplash injury.16 Thus, a clear definition of whiplash is needed. In our own research,17,19-21 we adopted a definition of whiplash proposed by Hirsch et al 9 as being medical trauma causing cervical musculoligamental sprain or strain resulting from hyperflexion and hyperextension without fractures or dislocations of the cervical spine. In addition, to avoid overlap with concussion, any head injury or traumatic loss of consciousness (including post-traumatic amnesia) should be an exclusion criterion. Although whiplash may occur caused by impact of the cervical spine from different sides, recent research 24,25 clearly indicated that rotated or inclined head position is a particular risk predisposing to symptoms in the early stage or longterm follow-up period. [black small square] Results From Previous Research With Whiplash Patients There are a number of retrospective studies indicating cognitive impairment in patients after whiplash injury.2,11,14,15,23,26 The impairment found in these studies (Table 1) mainly involved attentional deficits,11,14,15,23 in particular divided attention,15 whereas only one study found deficient memory.26 Although applying an unclear definition of whiplash, none of the studies 2,10,15,23,26 explained the overlap with concussion of eminent importance to derive conclusions regarding cognitive functioning of the patients. This may have led to an overestimation of cognitive problems of whiplash patients in terms of the origin or the degree of impairment.

5 Table 1. Summarized Results From Previous Studies on Cognitive Functioning of Whiplash Patients First Conclusion Because of a lack of clear definition, many previous studies of cognitive functioning confused whiplash with blunt head injury. Other methodologic limitations of previous research include the following: 1. Studies were carried out retrospectively with highly selected patients,2,14,15,23,26 probably including an unknown number of litigation cases. As mentioned previously, this may have influenced patients' illness behavior or motivation for different reasons; 2. Some of the previous studies enrolled small numbers of patients,2,26 which precluded reasonable statistical analysis; 3. Previous research 23,26 included patients with different sociocultural backgrounds, which could influence coping strategies; 4. In previous studies, only some of the enrolled patients underwent testing of cognitive functioning,2,23 which seriously limited the interpretation of results. Follow-up studies of cognitive functioning with recently injured whiplash patients are rare.6,10,17 In one such study,6 only some patients completed testing procedures at all follow-up examinations, which seriously restricted conclusions regarding cognitive functioning in the long term. In addition, comparisons between studies carried out at different sites is difficult for at least two reasons: 1) different methods of assessment, and 2) differences in insurance schemes, some of which may have promoted compensation-seeking behavior. Second Conclusion

6 Because of selection bias, small numbers of observations and societyspecific factors (sociocultural differences, different insurance schemes), analysis of data from retrospective studies failed to provide conclusive results regarding cognitive functioning of whiplash patients. Probably the most serious limitation of previous research was that studies did not consider the interplay between somatic or psychologic consequences of whiplash injury and cognitive performance.6,9 Many somatic symptoms may interfere with cognitive performance, the most prominent of which is pain, which has been shown to influence patients cognitive ability.16,18,23 Recent findings 20 highlight a history of headache as being a considerable risk factor for presentation with protracted symptoms after whiplash, including suffering from headache as a result of injury. This interrelationship is of particular interest because increased frequency and intensity of headache as a result of whiplash may impair attention. Only one other study,18 using a small number of patients, showed a relationship between pain relief and improved cognitive performance in whiplash patients. Moreover, because pain is one of the crucial symptoms in patients after whiplash, analgesics, which may influence cognitive ability, could play an important role in assessment of such patients' cognitive impairment. The relationship between adverse effect of medication and cognitive functioning has been investigated explicitly in only few studies with whiplash patients,6,10,17 one of which highlighted possible correlations with reduced performance levels.17 Third Conclusion Because of a lack of comprehensiveness, i.e., failing to assess in parallel cognitive functioning and psychologic and somatic consequences of trauma or other potentially important factors (i.e., pain or adverse effect of medication), many previous studies probably misinterpreted cognitive deficits in whiplash patients as being primarily trauma-related. In prospective studies with nonselected patients, recruited according to a clear definition of whiplash injury,10,17 the majority of cases showed good recovery of cognitive function to levels comparable with those of normal volunteers. In our own research with 117 nonselected whiplash patients who were followed for 2 years (Radanov BP, Sturzenegger M. Unpublished data), similar improvement in attentional functioning was documented. This was found even in patients remaining symptomatic (n = 21) throughout the 2-year follow-up period (Figure 1). An intriguing finding was that, on average, although there may be an improvement in performance during the

7 first 6 months, thereafter a kind of breakdown in cognitive functioning may be identified (Figure 1). This is true particularly for tests requiring more complex attentional functioning (i.e., Trailmaking test, parts A and B, or Paced Auditory Serial Addition Task) and self-rated cognitive ability.

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10 Figure 1. Course of attentional functioning in a nonselected group of patients symptomatic over a 2-year period after trauma. [white circle]: mean score. -[white circle]- median value. It should be pointed out that recent research does confirm attentional deficit in the early post-traumatic phase after whiplash.6,10,17 As shown in Figure 1, studies with nonselected patients 10,17 suggest that although initially present, such deficit may be reversible. In addition, one of these studies 10 could not confirm disturbance of higher cognitive functions after whiplash (i.e., memory) as previously proposed by other authors.5,26 Finally, the reversibility of impaired cognitive functioning shown in recent studies may be seen as an argument against any relevant brain damage after whiplash. Thus, the assumption of brain-stem or frontal brain damage 6 as a result of this type of injury is not warranted and has yet to be supported by experimental results based on methodologically sound studies. [black small square] Are There Other Possible Explanations for Impaired Cognitive Functioning in Whiplash Patients? From the previous considerations, it can be concluded that impaired cognitive functioning in whiplash patients is rather nonspecific. Similar impairment may be observed in patients suffering from cervical syndromes resulting from rheumatism 16 or headache.22 Apart from previously mentioned adverse effects of medication, at least two other possible explanations for this lack of specificity of cognitive impairment in whiplash patients appear conceivable: 1) a considerable percentage of whiplash patients, like patients with nontraumatic cervical syndrome,16 complain of increased fatigability. Cognitive functioning requires considerable effort 3 that may be seriously impaired in patients complaining of fatigue, thus influencing these patients' performance under real-life circumstances or during testing; 2) in many whiplash patients, different psychologic symptoms can be identified.6,13,15,21 These symptoms are best summarized as adjustment disorder with depressed mood 13 or mixed emotions 15,21 according to the Diagnostic and Statistical Manual of Mental Disorders, third edition, revised. This is important because, as mentioned previously, psychologic problems may impair cognitive functioning.4 Studies of the origin of psychologic complaints in whiplash patients using nonselected samples are rare.19,21 Recent findings,17,21 however, indicated a significant relationship between whiplash injury-induced pain and sleep disturbances. This is an

11 important finding because difficulties adjusting to pain or pain-related sleep disturbance (i.e., a sort of relative sleep deprivation) may initiate severe psychologic problems, such as irritability, and finally contribute to establishing a vicious circle. In addition, one recent study,13 highlighted post-traumatic stress disorder (PTSD) as a consequence of whiplash injury. Post-traumatic stress disorder is a complex psychopathologic syndrome that clearly may lead to diminished cognitive ability of patients. Fourth Conclusion There is increasing evidence from prospective studies with nonselected patients that cognitive complaints of whiplash patients are reversible. An impairment in the long term may result from pain, medication, or psychologic problems resulting from difficulties in adjusting to trauma-related symptoms. [black small square] What Should be Assessed, Who Should Perform the Investigation, and When? Comprehensive Assessment Is Imperative Given the interrelationship between the three aspects of human behavior mentioned previously, it is essential to include all these in the investigation of any person thought to be suffering from cognitive impairment. If not comprehensive, regarding history (including previous performance problems, particularly in school) and clinical assessment, the investigation will offer misleading conclusions. The clinician should be able to establish a positive relationship between cognitive functioning under real-life circumstances, as stated by the patient, and aspects of impaired function observed during the interview or documented by testing procedures. Thus, before testing, the possibility of history of cognitive complaints should be rigorously evaluated. Of particular importance are the type (i.e., detailed description) of cognitive complaints, when these occur (i.e., continuously or under certain circumstances), and the relationship with somatic or psychologic symptoms. Focusing attention on somatic symptoms, such as pain, may lead to so-called mind wandering and reflect an awareness of impaired cognitive functioning. Without clarifying the above-mentioned factors, definitive conclusions concerning the occurrence or origin of cognitive impairment in whiplash patients cannot be drawn. Assessment of Pain Should Be Given Sufficient Attention Because neck pain and headache appear to be important factors in recovery from whiplash 18 and because pain may influence cognitive

12 functioning,23 factors possibly influencing the experience of pain deserve particular attention. Depending on developmental background, patients may report different qualities and intensity of pain. It is necessary to make a judgment regarding which aspects of a patient's history may be relevant to his or her experience of pain, particularly if the symptoms reported differ with what the physician may have expected from the findings. The most prominent of these factors are believed to be frequent or chronic suffering from functional symptoms during childhood or adolescence (e.g., abdominal pain, menstrual pain, nausea, or vomiting), psychologic or behavioral problems (depressed mood, anxiety, suicidal thoughts), or repeated admissions to hospitals, particularly if these were connected with unpleasant experiences. Chronic illness, in particular chronic pain, in close relatives or persons with whom the patient had a relationship frequently correlates with psychogenic pain (so-called modeling ). Individuals who suffered disturbed emotional balance during childhood, puberty, or early adolescence (e.g., nonsupportive relationship with parents or carepersons, and who may have been alcoholics, frequent punishing including battering or sexual abuse) may be prone to report psychogenic pain. A tendency toward psychogenic pain may be found in persons who have high levels of current psychosocial stress (i.e., marital or family problems, financial or job-related problems). In addition, while assessing pain, the clinician should clarify the following points: localization, propagation, aggravation, measures that may diminish pain (including effects of medication), intensity and quality of pain, and the chronology of pain. In persons who show predominantly psychogenic pain, the clinician may face a nonlocalizable pain with the unfamiliar pattern of propagation (e.g., all over the body or one side of the body), lack of effect of therapeutic measures, constant pain of considerably high intensity, and quality in which description of pain is highly emotionally loaded (i.e., destroying, excruciating, deadly). Frequently, such patients, while describing their deadly, everlasting pain that does not respond to any treatment, do not appear unpleasantly affected. It may be assumed that persons who are likely to display psychogenic pain will experience higher levels of subjective cognitive impairment. Somatic, Psychologic, and Cognitive Complaints Should Be Assessed in Parallel Before assessing cognitive functioning of whiplash patient, the investigator must separate head injury from whiplash injury for which purpose to the previously mentioned definition may be helpful. In

13 some patients, e.g., those in whom, according to the history, considerable impairment of cognitive functioning may be suspected, the investigator may prefer to perform some testing (i.e., standardized procedure to assess a function). In contrast to blunt head injuries, for which different recommended testing procedures exist,12 no agreement has been reached regarding assessment of whiplash patients. According to current research data, the emphasis in assessing cognitive functioning after whiplash should be placed on different aspects of attention rather than higher cortical functions (such as memory, control, etc.). Tests may be chosen according to the literature given in the references. It is obvious from the previous that assessment of psychologic and cognitive functioning should be performed in a parallel manner. Such assessment may be performed by a psychiatrist or psychologist skilled in investigating (not only testing!) these functions. Impaired psychologic and cognitive functioning should be given particular attention regarding the length of time before the patient is sent back to work. Resumption of work should be based on consideration of the extent or the origin of impaired psychologic or cognitive functioning. Patients being sent back to work irrespective of their cognitive impairment may show decompensation, which is not necessarily evidence of malingering. It appears reasonable to investigate in detail those patients who, after whiplash, fail to recover within a few weeks of trauma, particularly if increased levels of impaired cognitive or psychologic functions are reported by the patient or relatives. [black small square] Possible Future Perspectives in Whiplash Research A standardized approach in the initial evaluation, with patients chosen according to a strict injury definition and with follow-up evaluation of patients undergoing similar treatment, appears necessary to assess the effect on cognitive functioning in whiplash injury. It will be of great benefit in understanding the outcome to enroll patients from different centers. This will allow a comparison of the possible influence of different sociocultural backgrounds or insurance schemes on illness behavior, of which cognitive ability may be only one facet. In addition, there is strong belief on the part of physicians and attorneys that the influence of compensation in whiplash outcome is most prevalent. Experimental studies to clarify this point are rare and do not support this view.22 Contributions toward understanding the whiplash syndrome and particularly regarding patients' cognitive ability or yet undetected

14 trauma-related brain abnormality (or functional disturbance) may be expected from imaging studies using positron emission tomography (PET) or single photon emission computed tomography (SPECT). The sensitivity of these techniques is high, but norms using drug-free volunteers with negative history of neurologic dysfunctions are yet not established. Bearing this in mind, it will be absolutely imperative to investigate drug-free whiplash patients to avoid misinterpretation resulting from medication artifacts and to avoid further confusion similar to that which emerged from some previous studies of cognitive functioning. In addition, it will be necessary to clarify whether patients with a positive history of headache and those who suffered whiplash injury display similar patterns on PET- or SPECT-scans. Acknowledgment The authors are thank Sidney Show, PhD, Department of Internal Medicine, University of Berne, Switzerland, for editorial assistance. References 1. American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders. 3rd edition, revised. Washington DC: American Psychiatric Association, Berstad JR, Bærum B. Löchen EA, Mogstad TE, Sjaastad O. Whiplash: Chronic organic brain syndrome without hydrocephalus ex vacuo. Acta Neurol Scand 1975;51: Full Text Options Bibliographic Links [Context Link] 3. Binder LM, Villanueva MR, Howieson D, Moore RT. The Rey AVLT recognition memory task measures motivational impairment after mild head trauma. Arch Clin Neuropsychol 1993;8: Full Text Options Bibliographic Links [Context Link] 4. Caine ED. The neuropsychology of depression: The pseudodementia syndrome. In: Grant I, Adams KM, ed. Neuropsychological Assessment of Neuropsychiatric Disorders. New York, Oxford: Oxford University Press, 1986; [Context Link] 5. Gronwall D. Cumulative and persisting effects of concussion on attention and cognition. In: Levin HS, Eisenberg HM, Benton AL, eds. Mild Head Injury. New York: Oxford University Press, 1989; [Context Link] 6. Ettlin TM, Kischka U, Reichmann S, Schmid G. Cerebral symptoms after whiplash injury of the neck: A prospective clinical and neuropsychological study of whiplash injury. J Neurol Neurosurg Psychiatry 1992;55: [Context Link] 7. Faust D. Forensic neuropsychology. The art of practicing a science that does not yet exist. Neuropsychol Rev 1991;2: Full Text Options Bibliographic Links [Context Link]

15 8. Genarelli TA, Adams JH, Graham DI. Acceleration induced head injury in monkey. I. The model, its mechanical and physiological correlates. Acta Neuropathol (Berl) 1981;7(Suppl):23-5. [Context Link] 9. Hirsch SA, Hirsch PJ, Hiramoto H, Weiss A. Whiplash syndrome: Fact or fiction? Orthop Clin North Am 1988;19: Full Text Options Bibliographic Links [Context Link] 10. Keidel M, Yagüez L. Wilhelm H, Diener H-Ch. Prospektiver Verlauf neuropsychologischer Defizite nach zervikozephalem Akzelerationstrauma. Nervenarzt 1992;63: Full Text Options Bibliographic Links [Context Link] 11. Kischka U, Ettlin TM, Heim S, Schmid G. Cerebral symptoms following whiplash injury. Eur Neurol 1991;31: Full Text Options Bibliographic Links [Context Link] 12. Lezak MD. Neuropsychological Assessment. New York, Oxford: Oxford University Press, [Context Link] 13. Mayou R, Bryant B, Duthie R. Psychiatric consequences of road traffic accidents. BMJ 1993;307: Full Text Options Bibliographic Links [Context Link] 14. Olsnes BT. Neurobehavioral findings in whiplash patients with long lasting symptoms. Acta Neurol Scand 1989;80: [Context Link] 15. Radanov BP, Dvorak J, Valach L. Cognitive deficits in patients after soft tissue injury of the cervical spine. Spine 1992;17: Full Text Options Bibliographic Links [Context Link] 16. Radanov BP, Hirlinger I, Di Stefano G, Valach L: Attentional processing in cervical spine syndromes. Acta Neurol Scand 1992;85: Full Text Options Bibliographic Links [Context Link] 17. Radanov BP, Di Stefano G, Schnidrig A, Sturzenegger M. Cognitive functioning after common whiplash: A controlled follow-up study. Arch Neurol 1993;50: Full Text Options Bibliographic Links [Context Link] 18. Radanov BP, Dvorak J, Di Stefano G. Attentional processes in common whiplash before and with immobilisation of the cervical spine. Eur Spine J 1993;2:72-5. [Context Link] 19. Radanov BP, Sturzenegger M, Di Stefano G, Schnidrig A, Mumenthaler M. Ergebnisse der einjährigen Verlaufsstudie nach HWS-Schleudertrauma. Schweiz Med Wochenschr 1993;123: [Context Link] 20. Radanov BP, Sturzenegger M, Schnidrig A, Di Stefano G, Aljinovic M. Factors influencing recovery from headache after common whiplash. BMJ 1993;307: Full Text Options Bibliographic Links [Context Link] 21. Radanov BP, Di Stefano G, Schnidrig A, Sturzenegger M. Common whiplash-psychosomatic or somatopsychic? J Neurol Neurosurg Psychiatry 1994;57: Full Text Options Bibliographic Links [Context Link]

16 22. Schofferman J, Wasserman S. Successful treatment of low back pain and neck pain after a motor vehicle accident despite litigation. Spine 1994;19: Full Text Options Bibliographic Links [Context Link] 23. Schwartz DP, Barth JT, Dane JR, Drenan SE, DeGood DE, Rowlingson JC. Cognitive deficits in chronic pain patients with and without history of head/neck injury: Development of a brief screening battery. Clin J Pain 1987;3: [Context Link] 24. Sturzenegger M, Di Stefano G, Radanov BP, Schnidrig A. Presenting symptoms and signs after whiplash injury: The influence of accident mechanisms. Neurology 1994;44: Ovid Full Text Full Text Options Bibliographic Links [Context Link] 25. Sturzenegger M, Radanov BP, Di Stefano G. The effect of accident mechanisms and initial findings on the long-term course of whiplash injury. J Neurol 1995;242: Full Text Options Bibliographic Links [Context Link] 26. Yarnell PR, Rossie GV. Minor whiplash head injury with major debilitation. Brain Inj 1988;2: Full Text Options Bibliographic Links [Context Link] Key words: assessment; cognitive functioning; whiplash injury Accession Number: Copyright (c) Ovid Technologies, Inc. Version: rel10.4.1, SourceID