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Quantitative and qualitative aspects of learning and memory in common whiplash patients: A 6-month follow-up study
Pergamon
Archivesof ClinicalNeuropsychology,Vol.I I, No. 8, pp. 661-676, 1996 Copyright9 1996NationalAcademyof Neuropsychology Printedin the USA.All rightsreserved 0887-6177/96$15.00+ .00
SSDI 0887-6177(95)00058-5
Quantitative and Qualitative Aspects of Learning and Memory in Common Whiplash Patients: A 6-Month Follow-Up Study Giuseppe Di Stefano Klinik Bethesda, Clinic for Epilepsy and Neurorehabilitation, CH-3233 Tschugg, Switzerland
Bogdan P. Radanov Department o f Psychiatry, University o f Berne, A4urtenstrasse 21, CH-3010 Berne, Switzerland
Quantitative and qualitative aspects of learning and memory were assessed in a series o f 86 unselected common whiplash patients in a follow-up setting. Factors possibly interfering with learning and memory (e.g., age, educational attainment, attentional functioning, headache, and utilized medication) were evaluated in conjunction. Cognitive functions were assessed soon after trauma (M = 7.3 days) and again 6 months later. According to self-reported health status at 6 months, patients were divided into asymptomatic (n = 58, i.e., fully recovered) and symptomatic groups (n = 28). Both groups were then compared with respect to their test scores from baseline and follow-up examinations. No systematic differences in quantitative or qualitative aspects of learning and memory between the symptomatic and asymptomatic patient groups or between patients and normal controls were found. In contrast, symptomatic patients were found to perform worse in attentional tests than asymptomatic patients at baseline examination. This might indicate that subjective complaints of memory impairment or forgetfulness after common whiplash may not really reflect problems in learning and memory but rather some degree of attentional deficit. Copyright
9 1996National Academyof Neuropsychology
In recent years, an increasing number of studies examining the sequelae of whiplash injuries were performed. Patients who suffered whiplash injury have been found to complain of a variety of symptoms such as neck pain, headache, dizziness, and blurred vision (BaUa, 1982; Maimaris, Barnes, & Allen, 1988; Radanov, Di Stefano, Schnidrig, et al., 1991; Radanov, Sturzenegger, & Di Stefano, 1995). Many whiplash patients also report injury-related cognitive Address correspondence to: Giuseppe Di Stefano, Clinical Neuropsychologist, Klinik Bethesda, Clinic for Epilepsy and Neurorehabilitation, CH-3233 Tschugg, Switzerland. This study was supported by the Swiss National Science Foundation (Project Number 3.883-0.88) and the Swiss Accident Insurance Company (Schweizerische Unfallversicherungsanstalt), General Agency, Berne. We acknowledge the editorial assistance of Dorothee Ward. 661
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G. Di Stefano and B. P. Radanov
problems (Balla, 1982; Radanov et al., 1991; Radanov, Hirlinger, Di Stefano et al., 1992). Among these, forgetfulness appears to be quite prominent (Radanov et al., 1991, 1992, 1995). Studies on cognitive performance of whiplash patients carried out to date primarily focused on attention (Berstad, Baemm, L6chen et al., 1975; Kischka, Ettlin, Heim et al., 1991; Olsnes, 1989; Radanov et al., 1992; Schwartz, Barth, Dane et al., 1987; Yarnell & Rossie, 1988) and mainly demonstrated a certain degree of attentional impairment. While assessing memory of whiplash patients, previous studies exclusively considered global aspects of performance, whereas qualitative aspects (e.g., error type, evaluation of learning strategies) were neglected. For example, Yarnell and Rossie (1988) found 70% of their sample impaired on Rey's-Ten-Word Memory Test and Berstad et al. (1975) found an impaired memory function in 7 out of 9 whiplash patients. In contrast to these two studies, Kischka et al. (1991) and Olsnes (1989) failed to find systematically impaired memory in whiplash patients. The only comprehensive and prospective study failed to find any learning and memory deficits in common whiplash patients (Di Stefano & Radanov, 1995). The present study attempts to provide a comprehensive evaluation of learning and memory in an unselected sample of recently injured common whiplash patients. To specify quantitative and qualitative aspects of learning and memory, a major focus was set on factors possibly interfering with leaming and memory (i.e., age, educational attainment, attentional functioning, headache, and utilized medication) were assessed in conjunction. Memory problems after common whiplash could account for disability and are therefore relevant from a socioeconomic and medico-legal point of view. Common whiplash is considered a soft-tissue injury of the cervical spine due to sudden acceleration/deceleration of the head (Macnab, 1971). The diagnosis in this study excludes fractures or dislocations of the cervical spine (Hirsch, Hirsch, Hiramoto, & Weiss, 1988). In addition, any head contact trauma or altered consciousness (including posttraumatic amnesia) in the present study are considered as exclusion criteria. According to the aforementioned definition, common whiplash is not expected to result in lesions of any area of the brain. For this reason, impairment of learning and memory due to organic brain damage cannot be expected. However, inasmuch as attentional impairment was documented in whiplash patients (Berstad et al., 1975; Kischka et al., 1991; Schwartz et al., 1987; Radanov et al., 1992; Yamell & Rossie, 1988), and impaired attention is thought to influence learning processes (Fisk & Schneider, 1984; Hasher & Zacks, 1979), memory problems in whiplash patients may be due to deficient attentional functioning. This is the hypothesis to be tested. Patients and Methods
To obtain an unselected sample, we repeatedly announced this study in Swiss Medical Journal and circulated letters to primary care physicians. Physicians were asked to refer patients who had recently suffered common whiplash within the shortest possible time after trauma. At referral, a baseline examination was performed. Follow-up examination was carried out at a 6-month intervals. During follow-up, the referring physician remained responsible for patients' treatment. According to the Swiss accident insurance system, the treating physician is responsible for certification of injury-related disability. If temporarily unable to work because of the injury, the patient receives a proportional amount of salary. If permanent disability is expected (i.e., no therapeutic measure is likely to improve the patient's health status), a permanent disability assessment is initiated. This usually happens many months after the accident. Screening criteria included: 1. Injury according to the aforementioned definition.
Learning and Memory in Whiplash Patients
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2. Negative history of head trauma or persistent neurological disfunctions. 3. German as the patient's native language (because all tests were administered in German language). 4. Age less than 55 years (patients' age was limited to exclude possible age-related cognitive impairment). From 131 consecutively referred patients, 31 failed to meet the criteria, while 14 additional patients dropped out at the follow-up examination. Patients in the present study [n = 86; mean age = 31.1 (SD = 9.5); mean educational attainment = 12.7 (SD = 2.6); female: n = 51, male: n = 35; patients at fault: n = 20 (24%); rear-end accidents (i.e., struck from behind): n = 50 (58%); mean interval between accident and baseline examination = 7.3 days (SD = 4.0)] were injured exclusively in automobile accidents and were fully covered by accident insurance. The results of these 86 patients were compared with 11 normal volunteers [mean age = 31.6 (SD = 5.0); mean educational attainment = 13.5 (SD -- 2.5); female: n = 9, male: n = 2]. There were no significant differences (p > 0.05) in age, educational attainment, or gender between normal volunteers and whiplash patients. According to self-reported health status at the 6-month examination, the patient group (n = 86) was divided into asymptomatic (patients who fully recovered) and symptomatic groups (still-symptomatic patients). The groups' results from both baseline and 6-month examinations were compared. Basic data of these groups are presented in Table 1. Examinations of whiplash patients included a complete physical and neurological examination, cervical spine X-rays (only at baseline), a semistructured interview, and a set of forreal tests. Interviews focused on subjective complaints and screening for utilized medication. Medication used within 48 hours before the actual examination was coded according to its possible influence on cognitive abilities (i.e., psychotropic substances such as benzodiazepines or analgesics containing muscle relaxants were considered to possibly influence cognitive abilities). Formal testing included the following.
Learning and memory. According to the employed definition of whiplash there is no rationale for brain damage, and insofar a material specific memory impairment should not be expected. For this reason we decided to employ a test which is most reliable in assessing quantitative and qualitative aspects of learning and memory. The California Verbal Learning Test (CVLT) by Delis, Kramer, Kaplan, Ober, & Fridlund (1987) has been considered a test assessing both levels and underlying strategies of performance (Crosson, Novack, Trenerry, & Craig, 1988). As the CVLT is widely used in clinical routine, it is be described in detail. A German version of the CVLT prepared by Dr. J. Ilmberger was used. In analyzing performance on CVLT, we followed mainly the suggestions of Crosson et al. (1988): As there can be wide variations in the number of List A items recalled in the learning trials, it is not useful to take the absolute number of perseverations and intrusions for statistical analyses (e.g., the presence of one intrusion for a patient who recalled two List A items has a different significance as the presence of one intrusion for a patient who recalled 15 List A items). For this reason, the number of intrusions and perseverations was set in relation to the total response output (i.e., correct answers + intrusions + perseverations) in each trial. Thus, intrusions and perseverations were calculated as a percentage of the total response output. Production of clusters depends directly on the number of correctly recalled items. Thus, if a patient would recall more List A items, he/she would have a greater opportunity to make cluster responses. To equate the patients for the number of possible cluster responses, the number of actual cluster responses was expressed as a percentage of the total possible cluster responses.
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To test the present study's hypothesis the assessment of the performance on CVLT was analyzed in relation to attentional functioning which included the following: Attention span was assessed for the auditory modality by the Digit Span, a subtest from Wechsler memory scale (Wechsler, 1945) and for the visuospatial modality using the Corsi Block Tapping Test (Milner, 1971). Scoring for both was total items recall, in forward and reverse order. Focussed attention was tested by the Number Connection Test (Oswald & Roth, 1987), which requires connecting numbered circles from 1-90 in order as quickly as possible. The final score is the average time in seconds of the four performed trials. Speed of information processing was assessed using the Trail Making Test, Parts A and B (Reitan, 1958). Trail Making Test Part A requires connecting consecutively numbered circles whereas Part B involves alternating letters and numbers. Scoring was time in seconds to finish each of the parts. Divided attention was measured using the Paced Auditory Serial Addition Task (PASAT) by Gronwall (1977). While listening to a recorded series of single digits, patients have to continuously add up digits, always two at a time: the second to the first, the third to the second and so on, verbally reporting each sum to the clinician. In the applied version this test consists of five trials containing 60 digits each. The intervals between consecutive digits for the five trials were 2.4, 2.0, 1.6, 1.2, and 0.8 seconds. Performance was recorded by the average error score of the completed trials. At baseline and the follow-up examinations, parallel versions of CVLT and Trail Making Test were used alternating. Statistical analyses were performed using the Statistical Package for Social Sciences (SPSS-X, 1988). RESULTS
Prerequisite Results At the follow-up examination, 28 patients subjectively reported persisting injury-related complaints (above all headache and neck pain), and are referred to as the symptomatic group. The reported subjective complaints of this group are shown in Table 2. The remaining 58 patients reported complete remission during follow-up (asymptomatic group). At baseline, symptomatic patients indicated significantly more forgetfulness, whereas there were no differences between the groups regarding concentration problems (Table 3). At baseline, medication possibly influencing cognitive performance (from the following main pharmacological groups: benzodiazepines, hydroxyzine, barbiturates, chloroxazone) was utilized by 54% of patients who at 6 months comprized the symptomatic group and 24% of patients who were asymptomatic at 6 months (Z2 = 5.6, p < 0.01). At the follow-up examination, 29% of symptomatic group patients still utilized medication possibly compromizing cognitive abilities. Furthermore, asymptomatic and symptomatic groups differed with regard to the average length of educational attainment (Table 1). To clarify possible influence on test performance due to group differences in educational attainment and utilized medication, the following analyses were performed: the influence of educational attainment on the variables from CVLT was tested using Person's correlation coefficient (r). The influence of utilized medication (possibly influencing cognitive ability vs. no medication or medication without influence on cognitive ability) on test performance was tested using Mann-Whitney test. Correlations between educational attainment and the 39 variables from CVLT at baseline and follow-up examination varied between r = -0.25 and r = 0.20, one of which proved significant (p < 0.05). At baseline and 6-month examinations, there was no significant influence
666
G. Di Stefano and B. P. Radanov
TABLE 2 Subjective Complaints of Symptomatic Patients at
Follow-Up Examination Follow-Up Examination Symptomatic Group (n = 28) Symptomsa
%
Neck pain Headache Shoulder pain Back pain Blurred vision Dizziness Finger paresthesia Difficulty swallowing Fatigueb Anxietyc Sleep disturbancesd Sensitivity to noise Irritability
86 82 46 32 46 25 25 4 57 43 39 39 50
aA combination of symptoms should be considered. bSubjects stated increasing levels of fatigue during the day due to involvement in different activities (no chronic fatigue was assessed). Cphobic reaction as a consequence of being a driver (most subjects avoided driving after the accident) or passenger in congested traffic. Post-traumatic stress disorder according to DSM-IU-R (30) could not be diagnosed. In particular, it was considered that the accident did not fulfill the criteria of being outside the usual human experience as required by the DSM-HI~-R. dDifficulties in falling asleep or sleep interruption, due to pain exclusively.
o f the u t i l i z e d m e d i c a t i o n o n test p e r f o r m a n c e as assessed b y M a n n - W h i t n e y test with Bonferroni correction. To further clarify the possible side effects o f the drugs o n cognitive skills, a subgroup analysis was performed. S y m p t o m a t i c patients at follow-up e x a m i n a t i o n were divided into a group u s i n g n o m e d i c a t i o n (71% o f s y m p t o m a t i c patients) a n d a group u s i n g medication with possible influence o n cognitive performance (29% o f s y m p t o m a t i c patients). It seems n o t e w o r t h y that all patients from the latter group c o m p l a i n e d about headache. Cognitive test p e r f o r m a n c e o f both groups was compared b y M a n n - W h i t n e y U Test with Bonferroni correction. N o n e o f the learning and m e m o r y variables as assessed b y CVLT showed signifi-
TABLE 3
Subjective Cognitive Complaints Follow-Up Examination
Baseline Asymptomatic Group (n = 58) n (% of Group) Forgetfulness Concentration problems
4 (7) 10 (17)
Symptomatic Group (n = 28) n (% of Group)
Chi-Square Test
Symptomatic Group (n = 28) n (% of Group)
10 (36) 10 (36)
p < 0.01 p > 0.05
9 (32) 14 (50)
Learning and Memory in Whiplash Patients
667
cant group differences. Regarding attention, both tests assessing divided attention proved significant (Trail Making Test Part 2: p = 0.006; PASAT: p = 0.002). Regarding learning and memory and attention, symptomatic patients complaining about headache at follow-up examination (82%) were compared with those symptomatic patients without headache (18%). The Mann-Whitney U Test analyses with Bonferroni correction showed no significant influence of headache on the mentioned cognitive variables. Symptomatic patients with headache or with medication at follow-up examination did not report more subjective concentration problems or forgetfulness than those symptomatic patients without headache or medication, as chi-square tests showed. Results on Learning and Memory Testing Learning trials at baseline examination. Correct answers, perseverations, intrusions, and clusters were analyzed by performing one multivariate analysis of variance (MANOVA) for each. Each analysis was a 2 groups (asymptomatic vs. symptomatic) • 5 learning trials analysis of variance (ANOVA) with repeated measures on trials. For correct answers (Table 4) there was no significant difference between the groups (p > 0.05). For both, the asymptomatic and symptomatic groups there was a significant improvement (i.e., increase in output) in correct answers during five learning trials, F(4, 336) = 296.43, p < 0.001. There was a significant decrease in the proportion of intrusions (Table 5) as related to the total response output during five trials, F(4, 336) = 76.43, p < 0.01, for which, however, no significant difference between the asymptomatic and symptomatic groups was found (p > 0.05). There was a significant increase of the proportion of perseverations (Table 6) during the five learning trials, F(4, 336) = 10.43, p < 0.001, however, lacking significant differences between the groups (p > 0.05). There was a significant increase in cluster production during learning trials, F(4, 332) = 21.15, p < 0.001, in both the asymptomatic and symptomatic group (Table 7). There was no significant difference between the groups in this regard (p > 0.05). Learning trials at 6-month examination. All four MANOVAs as performed at baseline were repeated at the 6-month examination. However, neither for the sum of correct answers (Table 4), nor for the proportion of perseverations (Table 6), or intrusions (Table 5) nor for the sum of produced clusters (Table 7), there were differences between the asymptomatic and the symptomatic groups (p > 0.05). The results show a significant increase of the sum of correct answers, F(4, 336) = 210.35, p < 0.001, and of the proportion of clusters, F(4, 336) = 27.07, p < 0.001, a significant decrease of the proportion of intrusions, F(4, 336) = 3.96, p < 0.01, and a significant variation in the proportion of perseverations, F(4, 336) = 3.03, p < 0.05, during the five learning trials in both groups. List B at baseline and 6-month examination. At both baseline and 6-month examination, ANOVAs with group (asymtomatic and symptomatic) as factor variable revealed no significant differences (p > 0.05) in respect to the sum of correct answers in List B (Table 4), proportion of intrusions (Table 5) and perseverations (Table 6) or sum of clusters (Table 7). Delayed recall trials at baseline examination. Regarding correct responses, MANOVA (Groups • Delays • Trial types) (2 • 2 • 2) revealed no significant difference (p > 0.05) between the asymptomatic and symptomatic groups (Table 4). Moreover, there was no significant influence of two delays or two trial types (p > 0.05). Analyses of intrusions (Table 5) and perseverations (Table 6) (both as a percentage of total response output) were calculated by MANOVA, whereby no differences were found between the groups (p > 0.05).
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There was no influence on percentage of intrusions and perseverations due to delay type. However, significant influence was calculated for the trial type (regarding intrusions: F(1, 84) = 7.40, p < 0.01; regarding perseverations: F(1, 84) = 14.39, p < 0.001. The proportion of produced clusters was caluculated as described for learning trials in a 2 groups x 2 trial types ANOVA with repeated measures on trial. In regard to cluster production (Table 7) a significant group difference was found, F(1, 84) = 4.25, p < 0.05. There was a significant improvement in the two trials, F(1, 84) = 13.34, p < 0.001. To test our hypothesis whether group differences in memory performance as found in delayed recall cluster production may be due to different levels of attentional functioning, we performed six ANCOVAs (2 groups x 2 trial types with repeated measures with alternatively one of six scores of the attentional testing as covariable). By these analyses, the group difference in cluster production did not reveal a significant level (p > 0.05), when the effect of Digit Span, Corsi Block Tapping, Trail Making Test-Part A, Trail Making Test-Part B, Number Connenction Test, or PASAT was parcelled out. Delayed recall trials at 6-month examination. With regard to correct answers (Table 4) there were no differences between the asymptomatic and symptomatic groups as calculated by MANOVA (p > 0.05). However, the influence of the trial type, F(1, 84) = 4.97, p < 0.05, and of the delay type, F(1, 84) = 4.01, p < 0.05, on the proportion of correct answers was significant. The groups did not significantly differ in regard to the proportion of intrusions (Table 5) or perseverations (Table 6). A significant influence of trial type on perseverations, F(1, 84) = 14.89, p < 0.001, and intrusions, F(1, 84) = 5.80, p < 0.05, was found. The MANOVA for clusters (Table 7) was performed as described for the baseline examination and did not reveal significant group differences nor differences due to the delay type (p > 0.05). Recognition trial at baseline and 6-month examination. As computed by one-way ANOVA, at baseline and 6-month examination (Table 4) the groups did not significantly differ in recognition performance (p > 0.05). Learning and memory results of the control group. To test the level of performance and changes in performance due to retesting in both patient groups, a group of normal volunteers underwent the same testing procedure as the patients group during a 3-month interval. The performance in CVLT (correct answers, intrusions, perseveration, and clusters) was analyzed using one-way ANOVA (three groups, i.e., asymptomatic, symptomatic, and normal volunteers as factor variable) and employing Tukey test. At the initial investigation (corresponding to baseline examination in the patients group) normal volunteers differed significantly only in 1 of 39 tested variables from asymptomatic and symptomatic groups. On retesting (corresponding to the 6-month examination in the patients group) 2 out of 39 variables showed significant differences. Relationship between objective test results and subjective cognitive complaints. To clarify the relationship between subjective complaints of forgetfulness and concentration problems on one part and the objective test results on CVLT on the other, the learning and memory performance of those patients complaining of these symptoms was compared with the learning and memory performance of the asymptomatic patients and those symptomatic patients not complaining of these symptoms. At follow-up examination, patients complaining about forgetfulness did not perform worse in any variable of the CVLT, as compared by MannWhitney test. Patients complaining about concentration problems performed worse in 3 out of 39 CVLT variables.
Learning and Memory in WhiplashPatients
673
Results on Attentional Processing Results of asymptomatic and symptomatic groups and the group of normal volunteers are presented in Table 8. One-way ANOVA with Tukey test was employed to compare the results on attentional tests. At baseline, symptomatic group scored significantly worse (p < 0.05) than normal volunteers in Digit Span, Number Connection Test, and PASAT. At follow-up examination, no significant differences were found between the three groups.
Relationship between objective and subjective attentional results. To clarify the relationship between subjective complaints of forgetfulness and concentration problems on one part and the objective test results on attentional processing on the other, the attentional performance of those patients complaining of these symptoms was compared with the attentional performance of the asymptomatic patients and those symptomatic patients not complaining of these symptoms. Patients complaining about forgetfulness at 6-month examination did not perform worse in either of the attentional tests as compared by Mann-Whitney test. In contrast, those 14 patients, who complained about concentration problems at follow-up examination, performed significantly worse in Corsi Block Tapping Test (U = 230.5, p < 0.01), Number Connection Test (U = 323.0, p < 0.05), Trail Making Test, Part A (U = 283.5, p < 0.05), and PASAT (U = 267.5, p < 0.05), as compared with those 72 patients who did not complain of concentration problems. Relationship between subjective cognitive complaints and possibly interfering factors. In the subgroup of symptomatic patients, the possible effect of interfering factors (i.e., headache, medication, and fatigue) on subjective forgetfulness and concentration problems was tested by chi-square test with continuity correction. None of the tests proved significant. This result shows that subjective forgetfulness and concentration problems in the symptomatic group were not secondary to headache, medication, or fatigue. DISCUSSION The principal aim of the present study was to assess quantitative and qualitative aspects of learning and memory in an unselected sample of recently injured common whiplash patients. Clearly defined injury criteria were employed and an unselected group of patients was examined. According to the definition of the injury, patients with head trauma and thus also patients with possible brain lesions were excluded. Subjective complaints indicative for impaired memory have been documented in previous studies (Radanov et al., 1991, 1992, 1995). To date, only one study on learning and memory in whiplash patients assessing both qualitative aspects of performance (e.g., error type, evaluation of learning strategies) was performed (Di Stefano & Radanov, 1995). Many studies suggested attentional deficits in whiplash patients (Berstad et al., 1975; Kischka et al., 1991; Olsnes, 1989; Radanov et al., 1992; Schwartz et al., 1987; Yarnell & Rossie, 1988). Although there is some disagreement on the relationship between attention and memory (Fisk & Schneider, 1984), some authors assume that deficient attentional functioning leads to some impairment of encoding operations (Hasher & Zacks, 1979). Thus, the question arised as to whether whiplash patients' complaints of leaky memory may reflect a memory impairment that is secondary to attentional deficits. For this reason, in the present study, learning and memory was evaluated in conjunction with attentional functioning. Although the applied memory test assesses exclusively the verbal modality of learning and memory, this fact does not appear relevant in discussing the present study's results. As brain lesions were excluded, there is no rationale to assume material-specific memory impairment. To
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account for this this fact, we applied the CVLT (Delis et al., 1987), a test being considered comprehensive regarding the assessment of quantitative and qualitative aspects of learning and memory (Crosson et al., 1988). Present results do not show a major impairment of learning and memory following common whiplash. In respect to both quantitative and qualitative aspects of learning and memory, statistical analyses did not reveal systematic differences between those patients who remained symptomatic and those who fully recovered. This is true for the baseline and the follow-up examinations. We found only one significant difference between the groups regarding the proportion of produced clusters in the delayed recall trials at baseline examination. In view of the many applied statistical analyses, this significant difference should be interpreted as an occasional finding (i.e., type I error). Moreover, the patient groups did not differ in any aspect of learning and memory from normal controls 6 months after injury. Results of attentional functioning tests indicated that some of the investigated patients may suffer from attentional impairment early after injury. However, an improvement of attentional functioning during follow-up was documented in both groups. Nevertheless, patients from the symptomatic group complaining of concentration problems performed worse in 4 out of 7 tests assessing attentional functioning, when compared with patients from the asymptomatic group who did not complain of concentration problems. This result appears of particular importance, probably indicating that there may be a subgroup of symptomatic patients suffering from objective and subjective cognitive problems related to deficient attentional functioning. This, in turn, may indicate that whiplash patients label impaired attentional functioning as forgetfulness, which is not to be confused with objective memory problems. Additionally, the possibility that factors other than attention might be responsible for the reports of forgetfulnes should be considered. Indeed, in this sample, symptomatic patients had a lower education than asymptomatic patients. However, the subjective attentional complaints could not be explained by the adverse effects of medication or headache. In our opinion, other factors, such as pretraumatic emotional or psychosocial problems, cannot explain the existence of cognitive complaints. This is clearly shown by recent prospective research in common whiplash patients (Radanov et al., 1991). The explanation that we, in contrast to some previous studies (Berstad et al., 1975; Yarnell & Rossie, 1988), could not confirm significant impairment of learning and memory in whiplash patients, may be as follows: 1. Previous research (Berstad et al., 1975; Yarnell & Rossie, 1988) may have included a number of patients who, additionally to whiplash injury, had suffered a mild head injury. Such an injury, even without detectable brain lesion as demonstrated by CT or MR-Scan (Eisenberg & Levin, 1989), may lead to significant impairment of cognitive abilities (Gronwall, 1989). 2. Poor levels of cognitive functioning in whiplash injury may be due to analgesic medication which may influence cognitive abilities, as discussed elsewehere (Radanov, Di Stefano, Schnidrig, Sturzenegger, & Augustiny, 1993). Thus, previous studies may have neglected this fact in interpreting results. 3. Reactive psychopathological changes, such as anxiety and depression, which may result from frustration due to inability in regaining pretraumatic levels of physical, social, and professional functioning, may also lead to problems in cognitive functioning (Van Zomeren & Van den Burg, 1985). In conclusion, the present study's results show that complaints of memory impairment of whiplash patients, which are usually referred to as forgetfulness, indeed may reflect some degree of attentional deficit instead of problems in learning and memory.
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REFERENCES Balla, J. I. (1982). The late whiplash syndrome: A study of an illness in Australia and Singapore. Culture, Medicine and Psychiatry, 6, 191-210. Berstad, J. R., B~erum, B., L~k:hen, E. A., Mogstad, T. E., & Sjaastad, O. (1975). Whiplash: Chronic organic brain syndrome whithout hydrocephalus ex vacuo. Acta Neurologica Scandinavica, 51, 268-284. Crosson, B., Novack, T. A., Trenerry, M. R., & Craig, P. L. (1988). California Verbal Learning Test (CVLT) performance in severely head-injured and neurologically normal adult males. Journal of Clinical and Experimental Neuropsychology, 10, 754-768. Delis, D. C., Kramer, J., Kaplan, E., Ober, B. A., & Fridlund, A. (1987). The California Verbal Learning Test. New York: Psychological Corporation. Di Stephano, G., and Radanov, B. P. (1995). Course of attention and memory after common whiplash: A two-year prospective study with age, education, and gender pair-matched patients. Acta Neurologica Scandinavica, 91, 346-352. Eisenberg, H. M., & Levin, H. S. (1989). Computed tomography and magnetic resonance imagin in mild to moderate head injury. In H. S. Levin, H. M. Eisenberg, & A. L. Benton (eds), Mild head injury (pp. 133-141). New York: Oxford University Press. Fisk, A. D., & Schneider, W. (1984). Memory as a function of attention, level of processing, and automatization. Journal of Experimental Psychology [Learning, Memory and Cognition], 10, 181-197. Gronwall, D. M. A. (1977). Paced auditory serial addition task: A measure of recovery from concussion. Perceptual and Motor Skills, 44, 367-373. Gronwall, D. M. A. (1989). Cumulative and persisting effects of concussion on attention and cognition. In H. S. Levin, H. M. Eisenberg, & A. L. Benton (Eds.), Mild head injury (pp. 153-162). New York: Oxford University Press. Hasher, L., & Zacks, R. T. (1979). Automatic and effortful processes in memory. Journal of Experimental Psychology [General], 108, 356-388. Hirsch, S. A., Hirsch, P. J., Hiramoto, H., & Weiss, A. (1988). Whiplash syndrome-fact or fiction? Orthopedic Clinics of North America, 19, 791-795. Kischka, U., Ettlin, T., Helm, S., & Schmid, G. (1991). Cerebral symptoms following whiplash injury. European Neurology, 31, 136-140. Macnab, I. (1971). The "Whiplash Syndrome." Orthopedic Clinics of North America, 2, 389-403. Maimaris, C., Barnes, M. R., & Allen, M. J. (1988). "Whiplash injuries" of the neck: A retrospective study. Injury, 19, 393-396. Milner, B. (1971). Interhemispheric differences in the localization of psychological processes in man. British Medical Bulletin, 27, 272-277. Olsnes, B. T. (1989). Neurobehavioral findings in whiplash patients with long-lasting symptoms. Acta Neurologica Scandinavica, 80, 584-588. Oswald, W. D., & Roth, E. (1987). Der Zahlen-Verbindungs-Test. Grttingen: Verlag ftir Psychologie Dr. C. J. Hogrefe. Radanov, B. P., Di Stefano, G., Schnidrig, A., & Ballinari, P. (1991). Role of psychosocial stress in recovery from common whiplash. Lancet, 338, 712-715. Radanov, B. P., Di Stefano, G., Schnidrig, A., Sturzenegger, M., & Augustiny, K. E (1993). Cognitive functioning after common whiplash: A controlled follow-up study. Archives of Neurology, 50, 87-91. Radanov, B. P., Hirlinger, I., Di Stefano, G., & Valach, L. (1992). Attentional processing in cervical spine syndromes. Acta Neurologica Scandinavica, 85, 358-362. Radanov, B. P., Sturzenegger, M., & Di Stefano, G. (1995). Long-term outcome after whiplash injury. A 2-year follow-up considering features of injury mechanism and somatic, radiologic and psychosocial findings. Medicine, 74, 281-297. Reitan, R. M. (1958). Validity of the Trail Making Test as an indication of organic brain damage. Perceptual and Motor Skills, 8, 251-256. Schwartz, D. P., Barth, J. T., Dane, J. R., Drenan, S. E., DeGood, D. E., & Rowlingson, J. C. (1987). Cognitive deficits in chronic pain patients with and without history of head/neck injury: Development of a brief screening battery. Clinical Journal of Pain, 3, 94-I01. SPSS-X User's Guide (3rd ed.). (1988). Chicago: McGraw-Hill. Van Zomeren, A. H., & Van Den Burg, W. (1985). Residual complaints of patients two years after severe head injury. Journal of Neurology, Neurosurgery and Psychiatry, 48, 21-28. Wechsler, D. A. (1945). A standardized memory scale for clinical use. Journal of Psychology, 19, 87-95. Yarnell, P. R., & Rossie, G. V. (1988). Minor whiplash head injury with major debilitation. Brain Injury, 2, 255-258.
Archivesof ClinicalNeuropsychology,Vol.I I, No. 8, pp. 661-676, 1996 Copyright9 1996NationalAcademyof Neuropsychology Printedin the USA.All rightsreserved 0887-6177/96$15.00+ .00
SSDI 0887-6177(95)00058-5
Quantitative and Qualitative Aspects of Learning and Memory in Common Whiplash Patients: A 6-Month Follow-Up Study Giuseppe Di Stefano Klinik Bethesda, Clinic for Epilepsy and Neurorehabilitation, CH-3233 Tschugg, Switzerland
Bogdan P. Radanov Department o f Psychiatry, University o f Berne, A4urtenstrasse 21, CH-3010 Berne, Switzerland
Quantitative and qualitative aspects of learning and memory were assessed in a series o f 86 unselected common whiplash patients in a follow-up setting. Factors possibly interfering with learning and memory (e.g., age, educational attainment, attentional functioning, headache, and utilized medication) were evaluated in conjunction. Cognitive functions were assessed soon after trauma (M = 7.3 days) and again 6 months later. According to self-reported health status at 6 months, patients were divided into asymptomatic (n = 58, i.e., fully recovered) and symptomatic groups (n = 28). Both groups were then compared with respect to their test scores from baseline and follow-up examinations. No systematic differences in quantitative or qualitative aspects of learning and memory between the symptomatic and asymptomatic patient groups or between patients and normal controls were found. In contrast, symptomatic patients were found to perform worse in attentional tests than asymptomatic patients at baseline examination. This might indicate that subjective complaints of memory impairment or forgetfulness after common whiplash may not really reflect problems in learning and memory but rather some degree of attentional deficit. Copyright
9 1996National Academyof Neuropsychology
In recent years, an increasing number of studies examining the sequelae of whiplash injuries were performed. Patients who suffered whiplash injury have been found to complain of a variety of symptoms such as neck pain, headache, dizziness, and blurred vision (BaUa, 1982; Maimaris, Barnes, & Allen, 1988; Radanov, Di Stefano, Schnidrig, et al., 1991; Radanov, Sturzenegger, & Di Stefano, 1995). Many whiplash patients also report injury-related cognitive Address correspondence to: Giuseppe Di Stefano, Clinical Neuropsychologist, Klinik Bethesda, Clinic for Epilepsy and Neurorehabilitation, CH-3233 Tschugg, Switzerland. This study was supported by the Swiss National Science Foundation (Project Number 3.883-0.88) and the Swiss Accident Insurance Company (Schweizerische Unfallversicherungsanstalt), General Agency, Berne. We acknowledge the editorial assistance of Dorothee Ward. 661
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G. Di Stefano and B. P. Radanov
problems (Balla, 1982; Radanov et al., 1991; Radanov, Hirlinger, Di Stefano et al., 1992). Among these, forgetfulness appears to be quite prominent (Radanov et al., 1991, 1992, 1995). Studies on cognitive performance of whiplash patients carried out to date primarily focused on attention (Berstad, Baemm, L6chen et al., 1975; Kischka, Ettlin, Heim et al., 1991; Olsnes, 1989; Radanov et al., 1992; Schwartz, Barth, Dane et al., 1987; Yarnell & Rossie, 1988) and mainly demonstrated a certain degree of attentional impairment. While assessing memory of whiplash patients, previous studies exclusively considered global aspects of performance, whereas qualitative aspects (e.g., error type, evaluation of learning strategies) were neglected. For example, Yarnell and Rossie (1988) found 70% of their sample impaired on Rey's-Ten-Word Memory Test and Berstad et al. (1975) found an impaired memory function in 7 out of 9 whiplash patients. In contrast to these two studies, Kischka et al. (1991) and Olsnes (1989) failed to find systematically impaired memory in whiplash patients. The only comprehensive and prospective study failed to find any learning and memory deficits in common whiplash patients (Di Stefano & Radanov, 1995). The present study attempts to provide a comprehensive evaluation of learning and memory in an unselected sample of recently injured common whiplash patients. To specify quantitative and qualitative aspects of learning and memory, a major focus was set on factors possibly interfering with leaming and memory (i.e., age, educational attainment, attentional functioning, headache, and utilized medication) were assessed in conjunction. Memory problems after common whiplash could account for disability and are therefore relevant from a socioeconomic and medico-legal point of view. Common whiplash is considered a soft-tissue injury of the cervical spine due to sudden acceleration/deceleration of the head (Macnab, 1971). The diagnosis in this study excludes fractures or dislocations of the cervical spine (Hirsch, Hirsch, Hiramoto, & Weiss, 1988). In addition, any head contact trauma or altered consciousness (including posttraumatic amnesia) in the present study are considered as exclusion criteria. According to the aforementioned definition, common whiplash is not expected to result in lesions of any area of the brain. For this reason, impairment of learning and memory due to organic brain damage cannot be expected. However, inasmuch as attentional impairment was documented in whiplash patients (Berstad et al., 1975; Kischka et al., 1991; Schwartz et al., 1987; Radanov et al., 1992; Yamell & Rossie, 1988), and impaired attention is thought to influence learning processes (Fisk & Schneider, 1984; Hasher & Zacks, 1979), memory problems in whiplash patients may be due to deficient attentional functioning. This is the hypothesis to be tested. Patients and Methods
To obtain an unselected sample, we repeatedly announced this study in Swiss Medical Journal and circulated letters to primary care physicians. Physicians were asked to refer patients who had recently suffered common whiplash within the shortest possible time after trauma. At referral, a baseline examination was performed. Follow-up examination was carried out at a 6-month intervals. During follow-up, the referring physician remained responsible for patients' treatment. According to the Swiss accident insurance system, the treating physician is responsible for certification of injury-related disability. If temporarily unable to work because of the injury, the patient receives a proportional amount of salary. If permanent disability is expected (i.e., no therapeutic measure is likely to improve the patient's health status), a permanent disability assessment is initiated. This usually happens many months after the accident. Screening criteria included: 1. Injury according to the aforementioned definition.
Learning and Memory in Whiplash Patients
663
2. Negative history of head trauma or persistent neurological disfunctions. 3. German as the patient's native language (because all tests were administered in German language). 4. Age less than 55 years (patients' age was limited to exclude possible age-related cognitive impairment). From 131 consecutively referred patients, 31 failed to meet the criteria, while 14 additional patients dropped out at the follow-up examination. Patients in the present study [n = 86; mean age = 31.1 (SD = 9.5); mean educational attainment = 12.7 (SD = 2.6); female: n = 51, male: n = 35; patients at fault: n = 20 (24%); rear-end accidents (i.e., struck from behind): n = 50 (58%); mean interval between accident and baseline examination = 7.3 days (SD = 4.0)] were injured exclusively in automobile accidents and were fully covered by accident insurance. The results of these 86 patients were compared with 11 normal volunteers [mean age = 31.6 (SD = 5.0); mean educational attainment = 13.5 (SD -- 2.5); female: n = 9, male: n = 2]. There were no significant differences (p > 0.05) in age, educational attainment, or gender between normal volunteers and whiplash patients. According to self-reported health status at the 6-month examination, the patient group (n = 86) was divided into asymptomatic (patients who fully recovered) and symptomatic groups (still-symptomatic patients). The groups' results from both baseline and 6-month examinations were compared. Basic data of these groups are presented in Table 1. Examinations of whiplash patients included a complete physical and neurological examination, cervical spine X-rays (only at baseline), a semistructured interview, and a set of forreal tests. Interviews focused on subjective complaints and screening for utilized medication. Medication used within 48 hours before the actual examination was coded according to its possible influence on cognitive abilities (i.e., psychotropic substances such as benzodiazepines or analgesics containing muscle relaxants were considered to possibly influence cognitive abilities). Formal testing included the following.
Learning and memory. According to the employed definition of whiplash there is no rationale for brain damage, and insofar a material specific memory impairment should not be expected. For this reason we decided to employ a test which is most reliable in assessing quantitative and qualitative aspects of learning and memory. The California Verbal Learning Test (CVLT) by Delis, Kramer, Kaplan, Ober, & Fridlund (1987) has been considered a test assessing both levels and underlying strategies of performance (Crosson, Novack, Trenerry, & Craig, 1988). As the CVLT is widely used in clinical routine, it is be described in detail. A German version of the CVLT prepared by Dr. J. Ilmberger was used. In analyzing performance on CVLT, we followed mainly the suggestions of Crosson et al. (1988): As there can be wide variations in the number of List A items recalled in the learning trials, it is not useful to take the absolute number of perseverations and intrusions for statistical analyses (e.g., the presence of one intrusion for a patient who recalled two List A items has a different significance as the presence of one intrusion for a patient who recalled 15 List A items). For this reason, the number of intrusions and perseverations was set in relation to the total response output (i.e., correct answers + intrusions + perseverations) in each trial. Thus, intrusions and perseverations were calculated as a percentage of the total response output. Production of clusters depends directly on the number of correctly recalled items. Thus, if a patient would recall more List A items, he/she would have a greater opportunity to make cluster responses. To equate the patients for the number of possible cluster responses, the number of actual cluster responses was expressed as a percentage of the total possible cluster responses.
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To test the present study's hypothesis the assessment of the performance on CVLT was analyzed in relation to attentional functioning which included the following: Attention span was assessed for the auditory modality by the Digit Span, a subtest from Wechsler memory scale (Wechsler, 1945) and for the visuospatial modality using the Corsi Block Tapping Test (Milner, 1971). Scoring for both was total items recall, in forward and reverse order. Focussed attention was tested by the Number Connection Test (Oswald & Roth, 1987), which requires connecting numbered circles from 1-90 in order as quickly as possible. The final score is the average time in seconds of the four performed trials. Speed of information processing was assessed using the Trail Making Test, Parts A and B (Reitan, 1958). Trail Making Test Part A requires connecting consecutively numbered circles whereas Part B involves alternating letters and numbers. Scoring was time in seconds to finish each of the parts. Divided attention was measured using the Paced Auditory Serial Addition Task (PASAT) by Gronwall (1977). While listening to a recorded series of single digits, patients have to continuously add up digits, always two at a time: the second to the first, the third to the second and so on, verbally reporting each sum to the clinician. In the applied version this test consists of five trials containing 60 digits each. The intervals between consecutive digits for the five trials were 2.4, 2.0, 1.6, 1.2, and 0.8 seconds. Performance was recorded by the average error score of the completed trials. At baseline and the follow-up examinations, parallel versions of CVLT and Trail Making Test were used alternating. Statistical analyses were performed using the Statistical Package for Social Sciences (SPSS-X, 1988). RESULTS
Prerequisite Results At the follow-up examination, 28 patients subjectively reported persisting injury-related complaints (above all headache and neck pain), and are referred to as the symptomatic group. The reported subjective complaints of this group are shown in Table 2. The remaining 58 patients reported complete remission during follow-up (asymptomatic group). At baseline, symptomatic patients indicated significantly more forgetfulness, whereas there were no differences between the groups regarding concentration problems (Table 3). At baseline, medication possibly influencing cognitive performance (from the following main pharmacological groups: benzodiazepines, hydroxyzine, barbiturates, chloroxazone) was utilized by 54% of patients who at 6 months comprized the symptomatic group and 24% of patients who were asymptomatic at 6 months (Z2 = 5.6, p < 0.01). At the follow-up examination, 29% of symptomatic group patients still utilized medication possibly compromizing cognitive abilities. Furthermore, asymptomatic and symptomatic groups differed with regard to the average length of educational attainment (Table 1). To clarify possible influence on test performance due to group differences in educational attainment and utilized medication, the following analyses were performed: the influence of educational attainment on the variables from CVLT was tested using Person's correlation coefficient (r). The influence of utilized medication (possibly influencing cognitive ability vs. no medication or medication without influence on cognitive ability) on test performance was tested using Mann-Whitney test. Correlations between educational attainment and the 39 variables from CVLT at baseline and follow-up examination varied between r = -0.25 and r = 0.20, one of which proved significant (p < 0.05). At baseline and 6-month examinations, there was no significant influence
666
G. Di Stefano and B. P. Radanov
TABLE 2 Subjective Complaints of Symptomatic Patients at
Follow-Up Examination Follow-Up Examination Symptomatic Group (n = 28) Symptomsa
%
Neck pain Headache Shoulder pain Back pain Blurred vision Dizziness Finger paresthesia Difficulty swallowing Fatigueb Anxietyc Sleep disturbancesd Sensitivity to noise Irritability
86 82 46 32 46 25 25 4 57 43 39 39 50
aA combination of symptoms should be considered. bSubjects stated increasing levels of fatigue during the day due to involvement in different activities (no chronic fatigue was assessed). Cphobic reaction as a consequence of being a driver (most subjects avoided driving after the accident) or passenger in congested traffic. Post-traumatic stress disorder according to DSM-IU-R (30) could not be diagnosed. In particular, it was considered that the accident did not fulfill the criteria of being outside the usual human experience as required by the DSM-HI~-R. dDifficulties in falling asleep or sleep interruption, due to pain exclusively.
o f the u t i l i z e d m e d i c a t i o n o n test p e r f o r m a n c e as assessed b y M a n n - W h i t n e y test with Bonferroni correction. To further clarify the possible side effects o f the drugs o n cognitive skills, a subgroup analysis was performed. S y m p t o m a t i c patients at follow-up e x a m i n a t i o n were divided into a group u s i n g n o m e d i c a t i o n (71% o f s y m p t o m a t i c patients) a n d a group u s i n g medication with possible influence o n cognitive performance (29% o f s y m p t o m a t i c patients). It seems n o t e w o r t h y that all patients from the latter group c o m p l a i n e d about headache. Cognitive test p e r f o r m a n c e o f both groups was compared b y M a n n - W h i t n e y U Test with Bonferroni correction. N o n e o f the learning and m e m o r y variables as assessed b y CVLT showed signifi-
TABLE 3
Subjective Cognitive Complaints Follow-Up Examination
Baseline Asymptomatic Group (n = 58) n (% of Group) Forgetfulness Concentration problems
4 (7) 10 (17)
Symptomatic Group (n = 28) n (% of Group)
Chi-Square Test
Symptomatic Group (n = 28) n (% of Group)
10 (36) 10 (36)
p < 0.01 p > 0.05
9 (32) 14 (50)
Learning and Memory in Whiplash Patients
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cant group differences. Regarding attention, both tests assessing divided attention proved significant (Trail Making Test Part 2: p = 0.006; PASAT: p = 0.002). Regarding learning and memory and attention, symptomatic patients complaining about headache at follow-up examination (82%) were compared with those symptomatic patients without headache (18%). The Mann-Whitney U Test analyses with Bonferroni correction showed no significant influence of headache on the mentioned cognitive variables. Symptomatic patients with headache or with medication at follow-up examination did not report more subjective concentration problems or forgetfulness than those symptomatic patients without headache or medication, as chi-square tests showed. Results on Learning and Memory Testing Learning trials at baseline examination. Correct answers, perseverations, intrusions, and clusters were analyzed by performing one multivariate analysis of variance (MANOVA) for each. Each analysis was a 2 groups (asymptomatic vs. symptomatic) • 5 learning trials analysis of variance (ANOVA) with repeated measures on trials. For correct answers (Table 4) there was no significant difference between the groups (p > 0.05). For both, the asymptomatic and symptomatic groups there was a significant improvement (i.e., increase in output) in correct answers during five learning trials, F(4, 336) = 296.43, p < 0.001. There was a significant decrease in the proportion of intrusions (Table 5) as related to the total response output during five trials, F(4, 336) = 76.43, p < 0.01, for which, however, no significant difference between the asymptomatic and symptomatic groups was found (p > 0.05). There was a significant increase of the proportion of perseverations (Table 6) during the five learning trials, F(4, 336) = 10.43, p < 0.001, however, lacking significant differences between the groups (p > 0.05). There was a significant increase in cluster production during learning trials, F(4, 332) = 21.15, p < 0.001, in both the asymptomatic and symptomatic group (Table 7). There was no significant difference between the groups in this regard (p > 0.05). Learning trials at 6-month examination. All four MANOVAs as performed at baseline were repeated at the 6-month examination. However, neither for the sum of correct answers (Table 4), nor for the proportion of perseverations (Table 6), or intrusions (Table 5) nor for the sum of produced clusters (Table 7), there were differences between the asymptomatic and the symptomatic groups (p > 0.05). The results show a significant increase of the sum of correct answers, F(4, 336) = 210.35, p < 0.001, and of the proportion of clusters, F(4, 336) = 27.07, p < 0.001, a significant decrease of the proportion of intrusions, F(4, 336) = 3.96, p < 0.01, and a significant variation in the proportion of perseverations, F(4, 336) = 3.03, p < 0.05, during the five learning trials in both groups. List B at baseline and 6-month examination. At both baseline and 6-month examination, ANOVAs with group (asymtomatic and symptomatic) as factor variable revealed no significant differences (p > 0.05) in respect to the sum of correct answers in List B (Table 4), proportion of intrusions (Table 5) and perseverations (Table 6) or sum of clusters (Table 7). Delayed recall trials at baseline examination. Regarding correct responses, MANOVA (Groups • Delays • Trial types) (2 • 2 • 2) revealed no significant difference (p > 0.05) between the asymptomatic and symptomatic groups (Table 4). Moreover, there was no significant influence of two delays or two trial types (p > 0.05). Analyses of intrusions (Table 5) and perseverations (Table 6) (both as a percentage of total response output) were calculated by MANOVA, whereby no differences were found between the groups (p > 0.05).
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There was no influence on percentage of intrusions and perseverations due to delay type. However, significant influence was calculated for the trial type (regarding intrusions: F(1, 84) = 7.40, p < 0.01; regarding perseverations: F(1, 84) = 14.39, p < 0.001. The proportion of produced clusters was caluculated as described for learning trials in a 2 groups x 2 trial types ANOVA with repeated measures on trial. In regard to cluster production (Table 7) a significant group difference was found, F(1, 84) = 4.25, p < 0.05. There was a significant improvement in the two trials, F(1, 84) = 13.34, p < 0.001. To test our hypothesis whether group differences in memory performance as found in delayed recall cluster production may be due to different levels of attentional functioning, we performed six ANCOVAs (2 groups x 2 trial types with repeated measures with alternatively one of six scores of the attentional testing as covariable). By these analyses, the group difference in cluster production did not reveal a significant level (p > 0.05), when the effect of Digit Span, Corsi Block Tapping, Trail Making Test-Part A, Trail Making Test-Part B, Number Connenction Test, or PASAT was parcelled out. Delayed recall trials at 6-month examination. With regard to correct answers (Table 4) there were no differences between the asymptomatic and symptomatic groups as calculated by MANOVA (p > 0.05). However, the influence of the trial type, F(1, 84) = 4.97, p < 0.05, and of the delay type, F(1, 84) = 4.01, p < 0.05, on the proportion of correct answers was significant. The groups did not significantly differ in regard to the proportion of intrusions (Table 5) or perseverations (Table 6). A significant influence of trial type on perseverations, F(1, 84) = 14.89, p < 0.001, and intrusions, F(1, 84) = 5.80, p < 0.05, was found. The MANOVA for clusters (Table 7) was performed as described for the baseline examination and did not reveal significant group differences nor differences due to the delay type (p > 0.05). Recognition trial at baseline and 6-month examination. As computed by one-way ANOVA, at baseline and 6-month examination (Table 4) the groups did not significantly differ in recognition performance (p > 0.05). Learning and memory results of the control group. To test the level of performance and changes in performance due to retesting in both patient groups, a group of normal volunteers underwent the same testing procedure as the patients group during a 3-month interval. The performance in CVLT (correct answers, intrusions, perseveration, and clusters) was analyzed using one-way ANOVA (three groups, i.e., asymptomatic, symptomatic, and normal volunteers as factor variable) and employing Tukey test. At the initial investigation (corresponding to baseline examination in the patients group) normal volunteers differed significantly only in 1 of 39 tested variables from asymptomatic and symptomatic groups. On retesting (corresponding to the 6-month examination in the patients group) 2 out of 39 variables showed significant differences. Relationship between objective test results and subjective cognitive complaints. To clarify the relationship between subjective complaints of forgetfulness and concentration problems on one part and the objective test results on CVLT on the other, the learning and memory performance of those patients complaining of these symptoms was compared with the learning and memory performance of the asymptomatic patients and those symptomatic patients not complaining of these symptoms. At follow-up examination, patients complaining about forgetfulness did not perform worse in any variable of the CVLT, as compared by MannWhitney test. Patients complaining about concentration problems performed worse in 3 out of 39 CVLT variables.
Learning and Memory in WhiplashPatients
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Results on Attentional Processing Results of asymptomatic and symptomatic groups and the group of normal volunteers are presented in Table 8. One-way ANOVA with Tukey test was employed to compare the results on attentional tests. At baseline, symptomatic group scored significantly worse (p < 0.05) than normal volunteers in Digit Span, Number Connection Test, and PASAT. At follow-up examination, no significant differences were found between the three groups.
Relationship between objective and subjective attentional results. To clarify the relationship between subjective complaints of forgetfulness and concentration problems on one part and the objective test results on attentional processing on the other, the attentional performance of those patients complaining of these symptoms was compared with the attentional performance of the asymptomatic patients and those symptomatic patients not complaining of these symptoms. Patients complaining about forgetfulness at 6-month examination did not perform worse in either of the attentional tests as compared by Mann-Whitney test. In contrast, those 14 patients, who complained about concentration problems at follow-up examination, performed significantly worse in Corsi Block Tapping Test (U = 230.5, p < 0.01), Number Connection Test (U = 323.0, p < 0.05), Trail Making Test, Part A (U = 283.5, p < 0.05), and PASAT (U = 267.5, p < 0.05), as compared with those 72 patients who did not complain of concentration problems. Relationship between subjective cognitive complaints and possibly interfering factors. In the subgroup of symptomatic patients, the possible effect of interfering factors (i.e., headache, medication, and fatigue) on subjective forgetfulness and concentration problems was tested by chi-square test with continuity correction. None of the tests proved significant. This result shows that subjective forgetfulness and concentration problems in the symptomatic group were not secondary to headache, medication, or fatigue. DISCUSSION The principal aim of the present study was to assess quantitative and qualitative aspects of learning and memory in an unselected sample of recently injured common whiplash patients. Clearly defined injury criteria were employed and an unselected group of patients was examined. According to the definition of the injury, patients with head trauma and thus also patients with possible brain lesions were excluded. Subjective complaints indicative for impaired memory have been documented in previous studies (Radanov et al., 1991, 1992, 1995). To date, only one study on learning and memory in whiplash patients assessing both qualitative aspects of performance (e.g., error type, evaluation of learning strategies) was performed (Di Stefano & Radanov, 1995). Many studies suggested attentional deficits in whiplash patients (Berstad et al., 1975; Kischka et al., 1991; Olsnes, 1989; Radanov et al., 1992; Schwartz et al., 1987; Yarnell & Rossie, 1988). Although there is some disagreement on the relationship between attention and memory (Fisk & Schneider, 1984), some authors assume that deficient attentional functioning leads to some impairment of encoding operations (Hasher & Zacks, 1979). Thus, the question arised as to whether whiplash patients' complaints of leaky memory may reflect a memory impairment that is secondary to attentional deficits. For this reason, in the present study, learning and memory was evaluated in conjunction with attentional functioning. Although the applied memory test assesses exclusively the verbal modality of learning and memory, this fact does not appear relevant in discussing the present study's results. As brain lesions were excluded, there is no rationale to assume material-specific memory impairment. To
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Learning and Memory in Whiplash Patients
675
account for this this fact, we applied the CVLT (Delis et al., 1987), a test being considered comprehensive regarding the assessment of quantitative and qualitative aspects of learning and memory (Crosson et al., 1988). Present results do not show a major impairment of learning and memory following common whiplash. In respect to both quantitative and qualitative aspects of learning and memory, statistical analyses did not reveal systematic differences between those patients who remained symptomatic and those who fully recovered. This is true for the baseline and the follow-up examinations. We found only one significant difference between the groups regarding the proportion of produced clusters in the delayed recall trials at baseline examination. In view of the many applied statistical analyses, this significant difference should be interpreted as an occasional finding (i.e., type I error). Moreover, the patient groups did not differ in any aspect of learning and memory from normal controls 6 months after injury. Results of attentional functioning tests indicated that some of the investigated patients may suffer from attentional impairment early after injury. However, an improvement of attentional functioning during follow-up was documented in both groups. Nevertheless, patients from the symptomatic group complaining of concentration problems performed worse in 4 out of 7 tests assessing attentional functioning, when compared with patients from the asymptomatic group who did not complain of concentration problems. This result appears of particular importance, probably indicating that there may be a subgroup of symptomatic patients suffering from objective and subjective cognitive problems related to deficient attentional functioning. This, in turn, may indicate that whiplash patients label impaired attentional functioning as forgetfulness, which is not to be confused with objective memory problems. Additionally, the possibility that factors other than attention might be responsible for the reports of forgetfulnes should be considered. Indeed, in this sample, symptomatic patients had a lower education than asymptomatic patients. However, the subjective attentional complaints could not be explained by the adverse effects of medication or headache. In our opinion, other factors, such as pretraumatic emotional or psychosocial problems, cannot explain the existence of cognitive complaints. This is clearly shown by recent prospective research in common whiplash patients (Radanov et al., 1991). The explanation that we, in contrast to some previous studies (Berstad et al., 1975; Yarnell & Rossie, 1988), could not confirm significant impairment of learning and memory in whiplash patients, may be as follows: 1. Previous research (Berstad et al., 1975; Yarnell & Rossie, 1988) may have included a number of patients who, additionally to whiplash injury, had suffered a mild head injury. Such an injury, even without detectable brain lesion as demonstrated by CT or MR-Scan (Eisenberg & Levin, 1989), may lead to significant impairment of cognitive abilities (Gronwall, 1989). 2. Poor levels of cognitive functioning in whiplash injury may be due to analgesic medication which may influence cognitive abilities, as discussed elsewehere (Radanov, Di Stefano, Schnidrig, Sturzenegger, & Augustiny, 1993). Thus, previous studies may have neglected this fact in interpreting results. 3. Reactive psychopathological changes, such as anxiety and depression, which may result from frustration due to inability in regaining pretraumatic levels of physical, social, and professional functioning, may also lead to problems in cognitive functioning (Van Zomeren & Van den Burg, 1985). In conclusion, the present study's results show that complaints of memory impairment of whiplash patients, which are usually referred to as forgetfulness, indeed may reflect some degree of attentional deficit instead of problems in learning and memory.
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