Cognitive Deficits

A Controlled Study of Cognitive Deficits in Children With Chronic Lyme Disease

Felice A. Tager, Ph.D.

Brian A. Fallon, M.D.

John Keilp, Ph.D.

Marian Rissenberg, Ph.D.

Charles Ray Jones, M.D.

Michael R. Liebowitz, M.D.

Although neurologic Lyme disease is known to cause cognitive dysfunction in adults, little is

known about its long-term sequelae in children. Twenty children with a history of new-onset

cognitive complaints after Lyme disease were compared with 20 matched healthy control sub-

jects. Each child was assessed with measures of cognition and psychopathology. Children with

Lyme disease had significantly more cognitive and psychiatric disturbances. Cognitive deficits were

still found after controlling for anxiety, depression, and fatigue. Lyme disease in children may be

accompanied by long-term neuropsychiatric disturbances, resulting in psychosocial and academic

impairments. Areas for further study are discussed. (The Journal of Neuropsychiatry and Clinical

Neurosciences 2001; 13:500–507)

Lyme disease (LYD) is a multisystemic illness caused by the tick-borne spirochete Borrelia burgdorferi (Bb).

LYD, the most common tick-borne illness in the United States,1 may manifest in a variety of ways: dermatologic,

arthritic, ophthalmologic, cardiac, and neuropsychiatric.2 The incidence and spread of the disease increased

during the 1980s,3 stabilizing somewhat in the late 1990s. Children below the age of 9 are at a high risk for

Bb infection,4 with many new cases of Lyme occurring among persons younger than 14 years.5

The neuropsychiatric symptoms of LYD in adults have been described,6,7 but little has been published

about the neuropsychiatric effect of the disease in children and adolescents. In adults, deficits in attention and

memory have been reported.8,9 In children, a controlled study of cognitive symptoms investigated a sample of

all children and adolescents who presented to a LYD clinic, most of whom presented with rheumatological

symptoms, had been diagnosed early, and had been treated appropriately for LD.10 These children were

found to have an excellent prognosis for unimpaired functioning. However, this sample may not be represen-

tative of all children diagnosed with LYD, especially those who present initially with neurocognitive prob-

lems and /or those who were not treated until many months after the initial infection. Our preliminary data

using symptom-driven reports suggest that children who develop chronic LYD have psychiatric and cogni-

tive difficulties in the area of attention and memory.11

However, subjective reports of cognitive dysfunction are not often correlated with objective findings. In a case

series,12 12 of 86 children (14%) developed neurocognitive symptoms associated with chronic LYD. If a sub-

group of children develop cognitive problems associated with LYD, then teachers, parents, and physicians

should be aware of this possibility.

In addition, if our preliminary findings are replicated in a controlled study, then in Lyme-endemic areas it

may be reasonable for LYD to be considered in the differential diagnosis of new-onset neurocognitive

disorders in children and adolescents.

This study examined the question of whether a subgroup of children with a history of LYD and persistent

cognitive complaints have objective cognitive deficits, independent of psychiatric comorbidity.

friends, and relatives. In addition, control subjects were recruited from flyers posted at Columbia Presbyterian

Medical Center, although many of these self-referred children were not eligible because they were not fluent

in English. Negative enzyme-linked immunosorbent assay and Western blot tests were required for control sub-

jects.

Eligibility for both groups was determined by an extensive phone screen with a physician (B.F.) and by

documentation of a positive Western blot assay for the LYD group. No children were accepted into the study if

there was a preexisting or pre-Lyme history of significant diagnosed medical, neurologic, psychiatric, or

learning problems (including, but not limited to, seizure disorder, head trauma, attention deficit disorders, learn-

ing disability, and conduct disorder). Healthy control subjects were not included if they presented with a sig-

nificant history of any of the following symptoms: arthralgias /arthritis, recurrent neck pain or headache,

marked fatigue, EM rash, or cranial /radicular neuropathies. Control subjects were not selected as “super-nor-

mals,” since we included all children unless there were marked medical or psychiatric problems.

All procedures were conducted at the New York State Psychiatric Institute, where parents and children gave

signed informed consent and were asked to avoid disclosing the diagnostic group of the child.

METHODS

Subjects

Children between 8 and 16 years of age were recruited. Twenty children with chronic LYD and 20 healthy con-

trol subjects were enrolled. Children with a history of LYD who were symptom-atic for 6 months to 3 years,

with persistent cognitive complaints including memory problems, distractibility, and school decline, were referred

by their pediatricians. The diagnosis of LYD was confirmed based on a) history of exposure to a Lyme-endemic area,

b) an illness course distinguished by symptoms characteristic of LYD, and c) either 1) history of a physician-documented

erythema migrans (EM) rash or unambiguous EM described by a parent, or 2) history of a positive whole-blood polymer-

ase chain reaction (PCR) test for Bb or a positive Western blot meeting explicit current Centers for Disease Control

and Prevention (CDC) criteria. The CDC criteria for the immunoglobulin G Western blot (IgG WB) were broad-

ened to recognize that the 31-kD and 34-kD bands represent the highly specific Osp A and B bands. Children

were accepted into the study only if LYD infection occurred after completion of a marking period in school.

This helped to establish good academic performance prior to the onset of LYD. Twenty healthy control subjects

with no history of LYD were included. An attempt was made to match the groups on gender, age, grade, and

socioeconomic status determined by using Hollingshead occupational codes.13 Healthy children were solicited through

the families of children with LYD, including siblings, friends, and relatives. In addition, control subjects were

recruited from flyers posted at Columbia Presbyterian Medical Center, although many of these self-referred

children were not eligible because they were not fluent in English. Negative enzyme-linked immunosorbent as-

say and Western blot tests were required for control subjects.

Eligibility for both groups was determined by an extensive phone screen with a physician (B.F.) and by

documentation of a positive Western blot assay for the LYD group. No children were accepted into the study if

there was a preexisting or pre-Lyme history of significant diagnosed medical, neurologic, psychiatric, or

learning problems (including, but not limited to, seizure disorder, head trauma, attention deficit disorders, learn-

ing disability, and conduct disorder). Healthy control subjects were not included if they presented with a sig-

nificant history of any of the following symptoms: arthralgias /arthritis, recurrent neck pain or headache,

marked fatigue, EM rash, or cranial /radicular neuropathies. Control subjects were not selected as “super-nor-

mals,” since we included all children unless there were marked medical or psychiatric problems.

All procedures were conducted at the New York State Psychiatric Institute, where parents and children gave

signed informed consent and were asked to avoid disclosing the diagnostic group of the child.

Cognitive Evaluation

All subjects were administered a neuropsychological battery selected in part to replicate a previous pediatric

LYD study.10 Tests were administered in a standardized manner and in a systematic order. The cognitive do-

mains assessed included 1) general intelligence, using the Wechsler Intelligence Scale for Children III (WISC-

III);14 2) short-term memory for visual and verbal material, using subtests of the Wide Range Assessment of

Memory and Learning (WRAML);15 3) learning of new verbal and nonverbal material, using subtests of the

WRAML; 4) attention, using the Conners’ Continuous Performance Test (CPT);16 5) executive functioning, us-

ing the Wisconsin Card Sorting Test (WCST)17; and 6) language, using the word association subtest of the

Clinical Evaluation of Language Fundamentals.18

Prior to testing, all children completed a Likert-type scale for physical symptoms, assessing fatigue, joint

pain, previous night’s sleep, appetite, headache, and other pain, as well as the Children’s Depression Inven-

tory (CDI)19 and the Youth Self-Report (YSR).20 Parents completed a general information question-

naire and a physical symptom checklist (rating symp- tom severity and frequency over the past year). Parents

rated learning and attention problems on the Conners’502 J Neuropsychiatry Clin Neurosci 13:4, Fall 2001

CHILDREN WITH LYME DISEASE Parent Rating Scale (CPRS-48)21 and psychopathology

on the Child Behavior Checklist (CBCL).20

Because the present study is not a longitudinal one, the children had no pre-Lyme cognitive assessment.

Given that limitation, school grades and standardized achievement test scores were used as an indirect way to

assess premorbid cognitive functioning. School records were obtained for the current year and all years starting

from the disease onset. Premorbid standardized achievement test scores were also obtained.

Statistical Methods

Statistical analyses were conducted by using SPSS 7.5. The continuous demographic variable of age was con-

trasted between the two groups by independent-sample t-tests. Demographic variables of socioeconomic class

and sex were analyzed between the groups by t-test and chi-square analysis. The neuropsychological test results

as well as the self- and parent-report questionnaires were compared by using independent-sample t-tests for

the various indices and subtests. Test performance between the groups was also analyzed by analysis of co-

variance to control separately for differences in Verbal Comprehension, depression, anxiety, and fatigue. Bon-

ferroni correction was applied separately to groups of indices and subtests of the measures to correct for mul-

tiple comparisons. Results before and after Bonferroni correction are presented for the reader ’s information.

The CPT’s overall assessment of the presence, absence, or possibility of attentional problems was compared be-

tween the groups by chi-square analysis. When available, analyses were done using standardized scores pro-

cured from published age-corrected normative data. All hypothesis-testing was two-tailed. A P-value of 􏰉0.05

was applied for significance.

RESULTS

Patient Characteristics

Twenty children were eligible for the study, and all agreed to participate. There were 13 females and 7 males

(mean age 13.83􏰅2.41 years; mean􏰅SD reported throughout). All children were Caucasian, fluent in En-

glish, and, consistent with the demographics of Lyme disease, all but one came from middle- or upper-class

families. The mean age at diagnosis was 11.90􏰅2.85 years. The mean number of physicians consulted before

the diagnosis of LYD was 3.80􏰅4.48. The mean time since diagnosis was 74.95􏰅68.04 weeks; from parent-

reported symptom onset until diagnosis, 47.28􏰅44.41 weeks; and from diagnosis to treatment, less than 1

week (0.30􏰅0.92). Thus, these children were symptomatic for many months before being diagnosed and

treated.

Of the 20 children with LYD, 16 (80%) had a fully reactive WB and 6 (30%) had a history of an unambig-

uous EM rash. Of the 4 without a reactive WB, 3 had both well-documented EM rashes and 4 /5 bands on an

IgG WB, and 1 had a positive whole-blood PCR for Bb DNA and frank arthritis.

All of the children had received oral antibiotics (mean􏰆23.21􏰅21.99 weeks), and 11 had received intra-

venous antibiotics (8.79􏰅16.10 weeks). All initially benefited from antibiotic therapy, but improvement was

sustained in only 10% (2 /20) after oral antibiotics and in 36% (4 /11) after IV antibiotics. At the time of testing,

7 children (35%) were being treated with oral antibiotics and 2 (10%) were being treated with IV antibiotics.

Based on physician assessment, the most common symptoms during LYD were marked fatigue (100%), ar-

thralgias (100%), frequent and severe headaches (100%), irritability /depression (94%), short-term memory prob-

lems (94%), schoolwork deterioration (94%), myalgias (88%), brain fog (88%), neck pain (88%), insomnia (82%),

distractibility (82%), word-finding problems (82%), and severe flu (80%). Arthritis was noted in only 38% of the

sample. On the more extensive parent-rated questionnaire, children were rated as having moderate to severe

sensory hyperacusis to sound (58%) and /or light (74%); insomnia (77%); word-finding problems (79%); and rad-

icular pains (56%).

Thirteen females and 7 males (mean age􏰆13.53􏰅2.67 years) were entered into the study as healthy control

subjects. Nine of these children were siblings of children in the LYD group, 6 were friends of children in the LYD

group, and 5 were recruited independently. All children were Caucasian and English-speaking. No significant

age, sex, or socioeconomic differences were found between the two groups.

Outcome Measures

Neuropsychological Testing: Performance of the groups on the neuropsychological measures was compared (see

Table 1). On two generally accepted measures of preserved premorbid intellectual functioning (Vocabulary

and Verbal Comprehension Index), the two groups were not significantly different. On other indices, however,

the LYD group had significantly lower scores: Full Scale IQ; Performance IQ; the Perceptual /Organization and

Freedom from Distractibility indices of the WISC-III; and the General Memory, Verbal Memory, and Visual

Memory indices of the WRAML. The LYD group had significantly lower scores on the digit span, picture com-

pletion, coding, and block design subtests of the WISC III. They had significantly lower scores on the design

TABLE 1. Neuropsychological measures and results in the Lyme disease and healthy control groups

Lyme Disease Healthy Control- [see link below]

memory, story memory, finger windows, sentence memory, and number /letter subtests of the WRAML. The

LYD group had significantly greater difficulty maintaining set on the WCST. The CPT data are available only

for a subset of the subjects because this version of the test was added mid-study. Despite the small n (9 LYD,

14 Healthy), there was a strong trend for the LYD group to have greater attentional difficulties. There was a sig-

nificantly greater frequency of definite attention problems in the LYD group than in the control subjects (9:1;

P􏰆0.007). After correction for multiple comparisons, Performance IQ, General Memory Index, Verbal Mem-

ory Index, and finger windows remained significant.

Premorbid Academic Achievement: School grades indicated children in the control group were functioning in

the above-average range. Pre-LYD school grades indicated children in the LYD group had been functioning in the

above-average range. Premorbid standardized achievement test scores were available for 14 children (70%) in the

LYD group. Eight of 14 children (57%) had scores greater than 90%, 3 (22%) in the 80%–89% range, 1 (7%) in

the 70%–79% range, 1 (7%) in the 60%–69% range, and 1 (7%) in the 50%–59% range. For the 6 who were missing

standardized tests, pre-Lyme report card grades of A’s and B’s indicated above-average functioning in school.

Physical Symptoms and Psychopathology: The LYD group had significantly elevated scores on all measures of

physical distress and parent /child-reported psychopathology. After controlling for multiple comparisons,

most scales remained significantly different (Table 2). Regarding depression, parents indicated that 41% (7 /

17) of children with LYD had suicidal thoughts and 11% (2 /18) had made a suicide gesture. On the child rating

(CDI), 40% (8 /20) had suicidal thoughts. The LYD group scored far worse on measures of learning prob-

lems and hyperactivity: almost 7 SD above the control subjects’ mean on the CPRS Learning Problems scale,

and 5 SD above the controls’ mean on the Hyperactivity Index scale.

Because affective disorders influence cognitive performance, the data were analyzed in an attempt to con-

trol these potentially confounding variables. Depression did not account for group differences in Perceptual /Or-

ganizational Index (P􏰆0.050), General Memory Index (P􏰆0.045), Verbal Memory Index (P􏰆0.021), digit span

(P􏰆0.045), coding (P􏰆0.002), design memory (P􏰆0.034), finger windows (P􏰆0.011), or number /let-

ter (P􏰆0.003). Parent-rated anxiety did not account for differences in Performance IQ (P􏰆0.027), Visual Mem-

ory Index (P􏰆0.049), coding (P􏰆0.038), finger windows (P􏰆0.005), or number /letter (P􏰆0.038). Self-ratings of

fatigue did not account for differences in digit span (P􏰆0.038), finger windows (P􏰆0.016), or number /let-

ter (P􏰆0.024). When we attempted to statistically control for depression, anxiety, and fatigue together, three

non-independent variables, group comparisons for many index and subtest scores failed to attain statistical

significance. However, finger windows (P􏰆0.022) and number /letter (P􏰆0.010), two important tests of visual

and auditory processing, continued to be significantly different between the groups.

DISCUSSION

In adults, LYD can cause significant cognitive deficits, specifically in the domain of memory. This is one of the

few controlled studies of the cognitive sequelae of LYD in children. We did not attempt to study the prevalence

of cognitive deficits in children with LYD. Rather, we have described a subgroup of children who developed

persistent neuropsychiatric complaints subsequent to the onset of LYD, despite having been premorbidly neu-

ropsychiatrically healthy. Thus, our LYD group was defined by their cognitive complaints. We were interested

to see if these children would have objective cognitive deficits as well. The LYD group was compared with

healthy control subjects and was found to have comparable premorbid intellectual functioning. The groups

were compared on multiple neuropsychologic, self-report, and parent-report measures. Our results indicated

that compared with control subjects, the Lyme sample had significantly more psychopathology and more ob-

jective cognitive deficits.

Our prior work11 indicated that children with chronic LYD had higher rates of anxiety, mood, and behavioral

disorders than children without LYD. Our current study specifically recruited patients with cognitive com-

plaints, not psychiatric ones, and hence may be less likely to suffer from a referral bias in the area of psy-

chopathology. Yet the children with LYD had significantly higher rates of psychopathology than control sub-

jects across various domains.

Both children and parents agreed that these children had difficulty with learning and focusing attention. The

self-report forms indicated that learning and attention problems, feelings of ineffectiveness, and mood prob-

lems were significantly greater for the LYD group compared with the control group. These findings are im-

portant because children with LYD who present with psychiatric problems may be misdiagnosed as having a

primary psychiatric problem such as an affective disorder, oppositional defiant disorder, or attention deficit

disorder.

In order to assess the meaning of our findings, we examined whether our children with LYD had premor-

bid cognitive abilities comparable to the control subjects. On the available standardized tests and school grades,

the two groups appeared comparable. The groups did not differ on the particular neuropsychological mea-

sures that tend to be least affected by brain injury (measures of vocabulary and verbal abstract reasoning).

Thus, the two groups appeared to have similar cognitive endowments.

On the neuropsychological measures of cognitive functioning, children with LYD had significantly lower

scores on certain measures. As with the self-report measures, the particular areas of deficits fell within a pat-

tern. On the standardized measure of intellectual functioning (WISC-III), the deficit in Performance IQ

TABLE 2. Self- and parent-reported physical symptoms and psychopathology in the Lyme disease and control groups

Lyme Disease Healthy Control

suggests a problem in overall perceptual and organizational abilities, and the lower Freedom from Distracti-

bility score suggests a problem with attention and concentration. Visual and auditory tracking or scanning

difficulties could account for these results.

On standardized tests of memory, deficits were noted in both visual and auditory primary processing as well

as visual memory. These deficits might mislead one to think that these children have primary memory prob-

lems. However, the two groups did not differ on the Learning Index, indicating intact ability to learn and re-

call /recognize both visual and auditory material over trials. In other words, children when presented with

complex information may initially “miss” some of it, but with repetition they can both learn and remember.

The data from the Continuous Performance Test are more difficult to interpret because of the small sample

size. However, the groups significantly differed on the percentage in each group who had attention problems

based on an overall categorical rating. The trend seen for the Lyme group to have higher scores on Attentive-

ness (d’) and Overall Index indicated that these children had difficulties in perceptual sensitivity—that is, in dis-

criminating the perceptual features of signals from nonsignals.

Taken as a whole, our study demonstrated that a group of children with LYD had a pattern of cognitive

deficits, as defined by both objective measures of cognitive functioning and self-report measures. Since these

children were included because of their cognitive complaints and we do not have any premorbid objective

cognitive assessments on the children with LYD, we cannot say for certain whether these cognitive deficits are

caused by LYD. However, the objective neuropsychological findings and the subjective parent and child re-

port measures all point to deficits in visual and auditory attention, or in working memory and mental tracking,

in children with cognitive problems associated with LYD. These particular functions tend to be very sensitive

to brain injury and disease. As noted above, these types of deficits may be incorrectly perceived by the patients

and others as memory impairments, since the new information is not attended to and processed and there-

fore will not be recalled. Consistent with this possibility are the reports by children and parents that the children

with LYD had increased short-term memory problems, such as forgetting homework assignments.

Our findings were consistent with the cases reported by Bloom et al.12 but differed from the findings of Ad-

ams et al.10 An important difference between the two studies is that Adams and colleagues’ sample was taken

from a clinic population of all LYD cases, in which only approximately 22% of the population presented with

mental status changes and neurological involvement. Their sample may be more reflective of a rheumatolog-

ical LYD population than a neurological LYD population.

This study has several limitations. First, because of the small sample size, only large differences can be detected

between groups. Second, it would be useful to know whether the control subjects and the patients were pre-

morbidly comparable on cognition. This would have been possible only if all children had been given iden-

tical standardized testing at a similar age. Such was not the case. Premorbid standardized achievement test

scores were available for only some of the Lyme group, and quantitative school grades were not available for all

children. Given the information available to us, how-ever, it does appear that the two groups were premor-

bidly comparable on academic performance.

Third, it would be useful to know whether the cognitive performance of our Lyme patients differed from that of other

chronically ill children who do not have a disease that affects the central nervous system, or of children who

have LYD without neurologic involvement. Only with such a comparison group can we be certain that the cog-

nitive profile of our patients reflects a disease process that actually affects the brain, as opposed to the non-

specific effects of a chronic illness.

CONCLUSION

Our study highlights the presence of attentional problems in a sample of children who develop persistent

cognitive symptoms after LYD. Published pediatric studies on LYD often include only children with either

early localized or early disseminated LYD. These children tend not to develop long-term problems, perhaps

because treatment was initiated early. In contrast, our study demonstrates that children whose diagnosis and

treatment are delayed may suffer considerable impairment. The present study, comparable to Belman et al.22

and Bloom et al.,12 indicates that children with chronic neurologic LYD can have significant neuropsychiatric

problems. Our study raises the question of whether a repeated course of antibiotics would be helpful. Only a

placebo-controlled treatment study can answer this question and determine whether neuropsychiatric prob-

lems are due to past damage or secondary to persistent infection.

Our findings have relevance to mental health professionals as well as educators working in Lyme-endemic

areas, who may be the first to recognize the possible underlying infectious origin of the neuropsychiatric dis-

order. Recognizing that LYD may present with neuropsychiatric symptoms can lead to timely diagnosis and

treatment. Furthermore, identification of children with persistent neuroborreliosis is imperative so that these

children can receive the most appropriate medical, psychological, and educational assistance.

This research was supported in part by a New York State Psychiatric Institute Research Support Grant to Dr. Tager

and by a grant from the Lyme Disease Association of New Jersey to Dr. Fallon. Portions of this work were presented at

the annual meetings of the Academy of Child and Adolescent Psychiatry (Anaheim, CA, October 1998), the International

Neuropsychological Society (Boston, February 1999), the American Psychiatric Association (Washington, DC, May

1999), and the International Conference on Lyme Borreliosis (Munich, Germany, June 1999).

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To see tables from the study

http://neuro.psychiatryonline.org/cgi/reprint/13/4/500