viruses

Article
Subjective and Objective Cognitive Impairments in
Non-Hospitalized Persons 9 Months after
SARS-CoV-2 Infection
Inge Kirchberger 1,2, * , Daniela Peilstöcker 1 , Tobias D. Warm 3 , Jakob Linseisen 1,2 , Alexander Hyhlik-Dürr 3 ,
Christine Meisinger 1 and Yvonne Goßlau 3

1 Epidemiology, Faculty of Medicine, University of Augsburg, University Hospital of Augsburg,

Stenglinstraße 2, 86156 Augsburg, Germany
2 Institute for Medical Information Processing, Biometry and Epidemiology—IBE, LMU Munich,
81377 Munich, Germany
3 Vascular Surgery, Faculty of Medicine, University of Augsburg, 86156 Augsburg, Germany
* Correspondence: [email protected]

Abstract: Studies on cognitive problems of persons with mild COVID-19 courses are still lacking.
This study aimed to determine the frequency and associated factors of subjective and objective
cognitive problems after COVID-19 in non-hospitalized persons. Study participants were examined
at the University Hospital of Augsburg from 04/11/2020 to 26/05/2021. The Wechsler Adult
Intelligence Scale (WAIS) IV digit span, Stroop Color and Word Test (SCWT), Regensburger verbal
fluency test (RWT) and, subjective ratings of memory and concentration were applied. Of the 372
participants (mean age 46.8 ± 15.2 years, 54.3% women, median time after infection 9.1 months),
24.9% reported concentration and 21.9% memory problems. Overall, 55.6% of the participants had at
least a mild negative alteration in any cognitive test. The strongest impairments were found regarding
memory functions (41.1% mild alterations, 6.2% distinct impairments) and verbal fluency (12.4% mild
alterations, 5.4% distinct impairments). SCWT showed negative alterations in no more than 3.0% of
the participants. Level of school education, age, and depressiveness emerged as significantly related
Citation: Kirchberger, I.; Peilstöcker,
to the cognitive tests. The number of complaints and depressiveness were significantly associated
D.; Warm, T.D.; Linseisen, J.;
with subjective memory and concentration problems. It is important to identify mild cognitive
Hyhlik-Dürr, A.; Meisinger, C.;
Goßlau, Y. Subjective and Objective
impairment in non-hospitalized COVID-19 patients early to offer them effective interventions.
Cognitive Impairments in
Non-Hospitalized Persons 9 Months Keywords: outpatients; cognition; memory; depression; COVID-19; long COVID; post COVID
after SARS-CoV-2 Infection. Viruses
2023, 15, 256. https://doi.org/
10.3390/v15010256
1. Introduction
Academic Editors: Juan-Manuel
Anaya and Rüdiger E. Scharf Since December 2019 the novel severe acute respiratory syndrome coronavirus 2
(SARS-CoV-2) that causes coronavirus disease (COVID-19) has reached approximately 514
Received: 7 December 2022 million cases, with about 25 million of them in Germany [1]. Although the majority of
Revised: 11 January 2023
the persons infected with SARS-CoV-2 recover within 3–4 weeks, a number of patients
Accepted: 13 January 2023
experience persisting symptoms beyond the acute phase of infection [2].
Published: 16 January 2023
Neurological manifestations have been recognized as part of the SARS-CoV-2 infec-
tion [3]. The underlying mechanisms by which SARS-CoV-2 affects the brain may include
processes related to inflammation, neuroinvasion, microvascular injury, and hypoxia [4].
Copyright: © 2023 by the authors.
Emerging evidence has revealed that the olfactory bulb, thalamus, and brain stem are
Licensee MDPI, Basel, Switzerland. infected by the virus through a trans-synaptic transfer [5]. The excessive release of inflam-
This article is an open access article matory signals such as cytokines and chemokines, and infection of the astrocytes induce
distributed under the terms and neuroinflammation and neuronal death and may result in further neurodegenerative com-
conditions of the Creative Commons plications [5].
Attribution (CC BY) license (https:// The most frequent neurological manifestations are headache, myalgias and an im-
creativecommons.org/licenses/by/ paired sense of smell and taste [6]. In addition, current systematic reviews and meta-
4.0/). analyses suggested an overall high frequency of cognitive impairment after COVID-19 [7–9].

Viruses 2023, 15, 256. https://doi.org/10.3390/v15010256 https://www.mdpi.com/journal/viruses

Viruses 2023, 15, 256 2 of 13

However, most of the available studies focus on cognitive impairment shortly after the
acute disease or hospital discharge, hospitalized patients, and have only small sample
sizes [7,9–12]. For instance, from 22 studies included in the systematic review by Tavares-
Junior et al. [7], only two studies had a follow-up time exceeding 6 months and both had
mixed samples of hospitalized patients and out-patients [13,14]. Since only a small propor-
tion of COVID-19 patients have a severe course of disease and require in-hospital treatment
(approximately 5% in Germany) [15,16], information regarding the long-term cognitive
impairments following a mild COVID-19 infection is needed, but evidence is still lack-
ing [8,17]. Furthermore, it has been proposed that the development of long-term cognitive
decline depends on COVID-19 risk factors such as advanced age and comorbidities as well
as pulmonary, vascular and neurologic pathological processes and treatment course [18].
However, studies which have analyzed associated factors of cognitive impairment also in
persons with mild COVID-19 are scarce [19,20]. Overall, comprehensive knowledge on the
long-term cognitive consequences of COVID-19 is of utmost importance, since cognitive
impairments have been shown to negatively affect working ability and health-related
quality of life [21]. Thus, future studies should promote the identification of individuals
susceptible to the development of cognitive impairments after COVID-19 in order to offer
appropriate interventions [22].
Therefore, this study aimed to investigate the frequency, severity and associated
factors of objective and self-reported cognitive difficulties post COVID-19, using data from
a prospective observational study in Augsburg, Germany.

2. Material and Methods

2.1. Design and Study Population
The present study used data from the Corona Thrombosis Study (COVID-T), a prospec-
tive single-center observational study evaluating the consequences of COVID-19 on the
vascular system and carried out in Augsburg, Germany. The study sample was recruited
from the population living in the city and the county of Augsburg. The public health depart-
ments identified eligible persons with past COVID-19 confirmed by positive polymerase
chain reaction (PCR) testing and sent out a total of 1600 postal invitations for study partici-
pation between 21 October 2020 and 6 November 2020. The potential study participants
were invited for clinical examinations and further assessments that were performed at the
University Hospital of Augsburg from 4 November 2020 to 26 May 2021. From the 1600
invited persons, a total of 525 (32.8%) participants could be enrolled in the study. Of these,
89 participants with a follow-up (FU) time of less than three months, 56 hospitalized partic-
ipants, 4 participants with a history of stroke and one participant who had not completed
any cognitive test were excluded, leaving 372 participants for the statistical analysis.
The study was approved by the ethics committee of the Ludwig-Maximilians Univer-
sität Munich and was performed in accordance with the Declaration of Helsinki. Written
informed consent was obtained from all participants.

2.2. Survey Data

Data was collected using a self-reporting questionnaire on a tablet personal computer.
The survey included information on socio-demographics, disease history, comorbid condi-
tions as well as symptoms during the acute COVID-19 infection and persisting symptoms.
The participants were asked to complete a self-developed list of 42 symptoms, rating
them for their occurrence in the acute COVID-19 phase as well as for the 14 days before
the FU examination. If the symptom was currently present, a rating of its severity was
requested. Furthermore, the participants were asked to compare the current symptom
frequency and severity with the symptom burden experienced in the acute COVID-19 phase.
The symptom list covered a number of neurological symptoms, including concentration and
memory problems, an impaired sense of smell and taste, headache, vertigo, and sleeping
problems.
Viruses 2023, 15, 256 3 of 13

In addition, standardized questionnaires were used to assess depression, post-traumatic

stress disorder (PTSD), and health-related quality of life (HRQOL). Depressive symptoms
were assessed with the depression module of the Patient Health Questionnaire (PHQ).
The PHQ-9 consists of nine items with response options on a scale from 0 to 3 (never to
nearly every day), resulting in a score ranging from 0 to 27. A score less than five can be
interpreted as the absence of depressiveness. Values between 5 and 10 constitute a mild
degree of depressiveness. Values of 10 and higher can be subdivided into moderate (10 to
14), moderately severe (15 to 19), and severe (20 to 27) depressiveness [23].
PTSD was measured using the revised Impact of Event Scale (IES-R). The IES-R
consists of three subscales made up of 22 items. Based on a weighted summation of the
subscale scores, a total score can be calculated which indicates the likelihood of a suspected
diagnosis of PTSD. A score of 0 or below indicates no suspected diagnosis of PTSD, whereas
scores above 0 suggest a suspected PTSD diagnosis [24].
To assess HRQOL the Veterans RAND 12-Item Health Survey (VR-12) was used. The
VR-12 consists of 12 items assessing physical and mental HRQOL with two subscales. The
scores range between 0 and 100 with higher values indicating better HRQOL [25].

2.3. Cognitive Assessments

Cognitive evaluation covered memory and executive cognitive functions. The cog-
nitive tests were conducted by trained study nurses. To test the working memory (WM)
the subtests “forward, backward and sequential digit span” from the Wechsler Adult
Intelligence Scale (WAIS) IV were used [26]. To assess the ability to inhibit cognitive in-
terference, the Stroop Color and Word Test (SCWT) with the subtests “word” (W), “color”
(C) and “color-word” (CW) was applied [27]. The semantic verbal fluency test is a subtest
of the Regensburger verbal fluency test that aims to assess divergent thinking. The study
participants were asked to name as many animals as possible within 2 minutes [28].

2.4. Data Analysis

Descriptive statistics were used to present the demographic, psychosocial, and clinical
characteristics and the cognitive test results. The frequency and severity of cognitive im-
pairments was determined by comparing patients’ cognitive performance with normative
test data derived from different populations available from the respective test manuals.
The raw values from the WAIS-IV were transformed into age-corrected standardized value
points. A normal distribution with a mean of 10 and standard deviation of 3 was assumed.
Cut-off points were 7 for mild or borderline negative alteration of the working memory and
4 for impairment of the working memory. Values higher than 7 indicate no negative alter-
ation [26]. The raw values of the SCWT were transformed into t-standardized age-corrected
values, assuming a normal distribution with a mean of 50. The standard deviation of cut-off
points were 40 for mild or borderline negative alteration of the inhibition of cognitive
interference and 30 for impairment of the inhibition of cognitive interference. Values larger
than 40 can be interpreted as no negative alteration [29]. Raw values of the Regensburger
verbal fluency test were transformed and age-corrected into percentage ranks with 16%
as the cut-off point for a mild or borderline negative alteration of divergent thinking and
2% for an impairment of divergent thinking. Values equal or higher than 17 indicate no
negative alteration [28].
Five multiple linear regression models were fitted to determine the association between
working memory, cognitive interference, semantic verbal fluency and a number of possible
demographic, psychosocial and clinical covariables. In addition, the association between
the subjective ratings of present problems with concentration or memory and demographic,
psychosocial and clinical covariables was determined by two multiple logistic regression
models. The covariables included in the models were selected based on current literature [7–9].
The assumptions for multiple linear regression analyses were tested using scatterplots
and Q-Q plots to confirm the linearity of associations, normal distribution of the residuals
and homoscedasticity. Cook’s distances and leverage diagnostic plots were used to check
Viruses 2023, 15, 256 4 of 13

for leveraging outliers. Variance inflation factors were used to identify multicollinearity
and Durbin–Watson tests were calculated to determine autocorrelation.
For statistical tests, an alpha level of 0.05 was defined. The statistical analyses were
performed using SAS-Studio.

3. Results
3.1. Demographic Characteristics
The demographic and clinical characteristics of the participants are shown in Table 1.
The mean age of the enrolled participants was 46.8 ± 15.2 years with 170 (45.7%) men and
202 (54.3%) women. The median time between SARSCoV-2 infection and FU examination
was 9.1 months.
Among the participants, 156 (43.0%) had at least one comorbidity. The most common
comorbidity was hypertension (n = 71, 19.1%), followed by depression (n = 32, 8.6%)
and autoimmune disease (n = 30, 8.1%). The most common symptom was tiredness or
exhaustion with a prevalence of 83.8% in the acute phase and 34.0% at FU. Headaches,
sleeping problems and disturbance of taste or smell were reported by more than 20% of the
participants at the FU examination. At the FU examination, mild depressiveness was found
in 103 participants (27.7%), whereas 48 (12.9%) had moderate to severe depressiveness.
Furthermore, 15 participants (4.1%) showed a suspected diagnosis of PTSD.

Table 1. Demographic and clinical characteristics of the study sample (n = 372).

Demographic Characteristics
Age (years) (mean (SD), MIN–MAX) 46.8 (15.2), 18–87
Sex
Female 202 (54.3%)
Male 170 (45.7%)
School education
≤ 9 years 63 (17.0%)
> 9 years 308 (83.0%)
Marital status
Married 246 (66.5%)
Single 98 (26.5%)
Divorced 20 (5.4%)
Widowed 6 (1.6%)
Smoking
Never-smoker 203 (54.6%)
Current smoker 29 (7.8%)
Former smoker 140 (37.6%)
Clinical characteristics
Comorbidities (yes)
Hypertension 71 (19.1%)
Coronary heart disease or angina pectoris 17 (4.6%)
Heart attack 9 (2.4%)
Diabetes 14 (3.8%)
Cancer 17 (4.6%)
Depression 32 (8.6%)
Anxiety Disease 22 (6.0%)
Chronic Bronchitis 21 (5.7%)
Autoimmune Disease 30 (8.1%)
Sum comorbidities
None (0) 213 (57.0%)
At least one (≥1) 156 (43.0%)
FU time (months) (median (Q1-Q3)) 9.1 (6.0–11.3)
≥ 3–≤ 6 95 (25.5%)
> 6–≤ 9 88 (23.7%)
> 9–≤ 12 111 (32.8%)
> 12–≤ 15 67 (18.1%)
Viruses 2023, 15, 256 5 of 13

Table 1. Cont.

Clinical characteristics
Neurological symptoms
Headache
Acute COVID-19 phase 244 (65.8%)
FU examination 80 (21.6%)
Disturbance of sense of taste
Acute COVID-19 phase 233 (62.8%)
FU examination 60 (16.3%)
Disturbance of smell
Acute COVID-19 phase 228 (61.5%)
FU examination 75 (20.3%)
Vertigo
Acute COVID-19 phase 130 (35.1%)
FU examination 34 (9.2%)
Sleeping problems
Acute COVID-19 phase 108 (29.2%)
FU examination 87 (23.5%)
Coordination of movements
Acute COVID-19 phase 53 (14.3%)
FU examination 16 (4.4%)
Tiredness or exhaustion
Acute COVID-19 phase 310 (83.8%)
FU examination 126 (34.0%)
Depressive mood
Acute COVID-19 phase 97 (26.2%)
FU examination 61 (16.5%)
Anxiety or panic
Acute COVID-19 phase 80 (21.6%)
FU examination 28 (7.6%)
Sum of complaints
Acute COVID-19 phase (median, (Q1–Q3)) 13 (9–19)
FU examination (median, (Q1–Q3)) 3 (1–7)
Depressiveness (PHQ-9) (median (Q1–Q3)) 4 (2–7)
<5: 221 (59.4%)
≥ 5–<10: mild depressiveness 103 (27.7%)
≥ 10–<15: moderate depressiveness 38 (10.2%)
≥ 15–<20: moderately severe depressiveness 8 (2.2%)
≥ 20: severe depression 2 (0.5%)
Post-traumatic stress disorder (IES-R total score)-
0: no suspected diagnosis 353 (95.9%)
>0: suspected diagnosis 15 (4.1%)
Physical HRQOL (VR-12) (median (Q1–Q3)) 52.7 (45.6–55.8)
Mental HRQOL (VR-12) (median (Q1–Q3)) 50.9 (43.8–56.3)
FU: Follow-up; PHQ-9: Patient Health Questionnaire; IES-R: Impact of Event Scale revised; HRQOL: Health-
related quality of life; VR-12: Veterans RAND 12-Item Health Survey.

3.2. Cognitive Impairments

Results of the evaluation of subjective and objective cognitive problems are shown
in Table 2. A total of 164 participants (44.2%) stated having had difficulties concentrating
during the acute COVID-19 infection, and 92 participants (24.9%) reported having had
difficulties with concentration in the two weeks prior to the FU examination, with the
majority having either slightly (n = 38, 41.8%) or moderately (n = 20, 22.0%) severe problems.
Memory problems during the acute COVID-19 infection were reported by 90 participants
(24.3%). A total of 81 participants (21.9%) reported having had memory problems in the
two weeks prior to the FU examination, with the majority having either slightly (n = 31,
38.3%) or moderately (n = 21, 25.9%) severe memory problems. Compared with at the time
of the acute COVID-19 infection, most of the participants rated their current concentration
problems as being equally severe/frequent (n = 20 (25.6%) or even more frequent/severe
Viruses 2023, 15, 256 6 of 13

(n = 28, 35.9%). Similarly, memory problems were considered as being persistent by 10

participants (19.6%) or more frequent/severe by 20 participants (39.3%).

Table 2. Cognitive evaluation: results of subjective ratings of concentration and memory problems,
and standard cognitive tests.

Subjective Ratings
Difficulties Concentrating
Acute COVID-19 phase (yes) 164 (44.2%)
FU examination (yes) 92 (24.9%)
Severity at FU (n = 91)
No impairment 3 (3.3%)
Slightly impaired 38 (41.8%)
Moderately impaired 20 (22.0%)
Fairly impaired 17 (18.7%)
Severely impaired 13 (14.3%)
Frequency/severity at FU compared with acute COVID-19 phase (n = 78)
Much less often/weaker (−3) 9 (11.5%)
−2 11 (14.1%)
−1 10 (12.8%)
Equal frequency/severity (0) 20 (25.6%)
+1 6 (7.7%)
+2 12 (15.4%)
Much more often/stronger (+3) 10 (12.8%)
Memory problems
Acute COVID-19 phase (yes) 90 (24.3%)
FU examination (yes) 81 (21.9%)
Severity at FU (n = 81)
No impairment 6 (7.4%)
Slightly impaired 31 (38.3%)
Moderately impaired 21 (25.9%)
Fairly impaired 11 (13.6%)
Severely impaired 12 (14.8%)
Frequency/severity at FU compared to acute COVID-19 phase (n = 51)
Much less often/weaker (−3) 7 (13.7%)
−2 4 (7.8%)
−1 10 (19.6%)
Equal frequency/severity (0) 10 (19.6%)
+1 6 (11.8%)
+2 9 (17.7%)
Much more often/stronger (+3) 5 (9.8%)
Cognitive tests
WAIS-IV: median, (Q1–Q3) 8 (6–9)
≥8: normal 196 (52.7%)
>4–≤7: mild/borderline negative alteration 153 (41.1%)
≤4: impairment 23 (6.2%)
RWT: median, (Q1–Q3) 63 (28–87)
≥17: normal 302 (81.2%)
>2–≤16: mild/borderline negative alteration 47 (12.6%)
≤2: impairment 23 (6.2%)
SCWT–W: median, (Q1–Q3) 54 (50–60)
≥41: normal 358 (97.0%)
>30–≤ 40: mild/borderline negative alteration 10 (2.7%)
≤30: impairment 1 (0.3%)
SCWT–C: median (Q1–Q3) 55 (50–62)
≥41: normal 361 (97.1%)
>30–≤ 40: mild/borderline negative alteration 6 (1.6%)
≤30: impairment 1 (0.3%)
SCWT–CW: median (Q1–Q3) 56 (53–62)
≥41: normal 363 (98.6%)
>30–≤ 40: mild/borderline negative alteration 4 (1.1%)
≤30: impairment 1 (0.3%)
FU: Follow-up; WAIS-IV: Wechsler Adult Intelligence Scale; RWT: Regensburger Wortflüssigkeitstest (verbal
fluency); SCWT: Stroop Color and Word Test, word (W), color (C), color words (CW).

Among the participants, 23 (6.2%) obtained a score signaling impairment in the WAIS-
V test, and 153 (41.1%) showed a mild/borderline negative alteration in terms of memory
function. In 23 participants (6.2%), an impairment was observed, and in 47 (12.6%) a
 SCWT–C: median (Q1–Q3) 55 (50–62)
≥41: normal 361 (97.1%)
>30–≤ 40: mild/borderline negative alteration 6 (1.6%)
Viruses 2023, 15, 256 ≤30: impairment 1 (0.3%)
7 of 13
SCWT–CW: median (Q1–Q3) 56 (53–62)
≥41: normal 363 (98.6%)
mild/borderline >30–≤ 40: mild/borderline
negative negative
alteration of the alteration
verbal fluency was observed on the4 RWT
(1.1%)test.
≤30: impairment
Fewer participants showed impairment or negative alterations in the SCWT1tests,(0.3%)
with
one Follow-up;
FU: participant (0.3%) who
WAIS-IV: hadAdult
Wechsler an impairment, and up
Intelligence Scale; to Regensburger
RWT: 10 participants (2.7%) with
Wortflüssigkeit-
stest (verbal fluency);
mild/borderline SCWT:alterations.
negative Stroop Color and Word Test, word (W), color (C), color words (CW).

3.3. Variables Associated with Cognitive Impairments

The multivariable
multivariable linear
linear regression
regressionmodels
modelsfor
forthe
thecognitive
cognitivetests
testsare
areshown
shownininFigure
Figure1
1and
andSupplementary
SupplementaryTable
TableS1.S1.All
Allfive
fivemodels
modelsincluded
included the
the same
same independent variables:
independent variables:
sex, age,
sex, age, education,
education, FU
FU time,
time, sum
sum of
of complaints, concentration problems
complaints, concentration problems atat FU,
FU, memory
memory
problems at FU, depression, PTSD, mental HRQOL, and neurological
problems at FU, depression, PTSD, mental HRQOL, and neurological symptoms at symptoms at FU
FU
(disturbance of smell or taste, headaches, vertigo, sleep problems).
(disturbance of smell or taste, headaches, vertigo, sleep problems).

Figure 1. Multivariable linear regression models for the cognitive

cognitive tests
tests Wechsler
Wechsler Adult Intelligence
Scale (WAIS-IV); Regensburger Wortflüssigkeitstest (verbal fluency) (RWT);
Scale (WAIS-IV); Regensburger Wortflüssigkeitstest (verbal fluency) (RWT); and and Stroop
Stroop Color
Color and
and
Word Test (SCWT), word (W), color (C), color words (CW). Directions of triangles correspond
Word Test (SCWT), word (W), color (C), color words (CW). Directions of triangles correspond to the to
the directions of estimates. Triangles outlined in red represent significant p-values. The color and
directions of estimates. Triangles outlined in red represent significant p-values. The color and size
of triangles are based on the p-values (i.e., large dark blue triangles represent low p-values and vice
versa).

These variables explained 8% (adjusted R2 ) of the WAIS-IV variance. Participants

with equal or less than 9 years of school education had significantly lower WAIS-IV scores
(indicating more memory problems) compared with participants with more than 9 years
Viruses 2023, 15, 256 8 of 13

school education (β = −1.38, p < 0.0001). In addition, women were more likely to have
memory problems than men (ß = −0.62, p = 0.0125).
The regression model for verbal fluency showed 13% explained variance of the RWT
scores. Besides years of school education, a higher age (β = 0.71, p < 0.0001), and higher
depression scores (PHQ-9) (ß = 1.51, p = 0.0332), worse mental HRQOL (VR-12) (ß = 0.57, p
= 0.0266) and lower PTSD scores (IES-R) (ß = −3.76, p = 0.0297) were associated with lower
RWT scores, indicating impaired verbal fluency.
The linear regression model for SCWT–W has an adjusted R2 of 14%. Lower age (β =
0.16, p < 0.0001), school education equal or less than 9 years (β = −3.10, p = 0.0016) and worse
mental HRQOL scores (β = 0.14; p = 0.0113) were significantly associated with lower SCWT–W
scores. The model for SCWT–C has an adjusted R2 of 2%. Similar to the SCWT–W results,
participants with school education equal or less than 9 years had significantly lower SCWT–C
scores than participants with longer school education (β = −2.81, p = 0.00311). In addition,
higher depression scores (ß = 0.48, p = 0.0191) were significantly associated with lower SCWT–C
scores. The regression model explaining the variance of SCWT-CW has an adj. R2 of 4%. The
variables age (β = 0.05, p = 0.0398), school education equal or less than 9 years versus more than
9 years (β = −2.14, p = 0.0370), higher depression score (ß = 0.32, p = 0.0442) and lower PTSD
scores (ß = 2.35, p = 0.0441) were significantly related with lower SCWT–CW scores, whereas
women (β = 1.97, p = 0.0108) had significantly higher SCWT–CW scores than men.
Results of the multivariable logistic regression models for self-reported difficulties
concentrating and memory problems at FU are shown in Figure 2 and in Supplementary
Table S2. Participants reporting concentration difficulties at FU were significantly younger
(OR = 0.97, p = 0.0142), had significantly more complaints (OR = 1.59, p < 0.0001), higher
depression scores (OR = 1.15, p = 0.0452) and were less likely to report smell disturbance
(OR = 0.23, p = 0.0186) than participants without concentration difficulties. Moreover,
participants
Viruses 2023, 15, x FOR PEER REVIEW who reported concentration problems during acute COVID-19, 10 ofhad
15 an almost
12-fold odds of having concentration problems at FU (OR = 11.81, p < 0.0001).

Figure Figure 2. Multivariable logistic regression models for the dependent variables concentration prob-
2. Multivariable logistic regression models for the dependent variables concentration problems
lems and memory problems at follow-up. Odds Ratios (OR) and 95% confidence intervals.
and memory problems at follow-up. Odds Ratios (OR) and 95% confidence intervals.
Similarly, the presence of memory problems in the COVID-19 acute phase was the
main predictor of memory problems at FU (OR = 7.09, p < 0.0001), and more complaints
(OR = 1.32, p < 0.0001) as well as higher depression scores (OR = 1.25, p = 0.0010) were
significantly associated with self-reported memory problems.

3.4. Sensitivity Analyses

Viruses 2023, 15, 256 9 of 13

Similarly, the presence of memory problems in the COVID-19 acute phase was the
main predictor of memory problems at FU (OR = 7.09, p < 0.0001), and more complaints
(OR = 1.32, p < 0.0001) as well as higher depression scores (OR = 1.25, p = 0.0010) were
significantly associated with self-reported memory problems.

3.4. Sensitivity Analyses

For the cognitive test results and subjective cognitive problems, regression models
were modified by including the neurological symptoms reported in the acute COVID-19
phase instead of 14 days before FU examination. The results, however, were very similar
(see Supplementary Tables S3 and S4).

4. Discussion
The present study examined cognitive functions based on objective tests and self-
reported problems in 372 participants at an average of 9 months following a mild COVID-
19 infection. Overall, 24.9% and 21.9% of the participants reported having concentration
problems and memory problems, respectively. Cognitive test results revealed that 55.6%
of the participants had at least a mild negative alteration in any tested cognitive function.
The strongest impairments were found regarding memory functions, where 41.1% of the
study participants showed mild/borderline negative alterations compared with population
norms, and distinct impairments were found in 6.2% of the participants. In terms of
word fluency, 12.4% of the study participants had mild/borderline negative alterations
and 5.4% had distinct impairments. In contrast, cognitive interference, as tested by the
SCWT, was negatively affected in no more than 3.0% (depending on the subtest) of the
study participants. Level of school education, age and depressiveness emerged as the most
important predictors of cognitive test results. Self-reported memory and concentration
problems at follow-up were mainly explained by the presence of these problems in the
acute phase. In addition, the number of reported complaints at follow-up and the level of
depressiveness were significantly associated with the report of memory and concentration
problems.
Overall, it is difficult to compare the results from the present study with previous
results, since available studies considerably differ regarding the assessment of cognitive
functions, the cut-offs for defining impaired functions, the time between acute COVID-19
and examination, and the clinical severity of COVID-19.
In terms of self-reported cognitive difficulties, the findings from the present study
are in line with the results of studies reporting memory problems in 19.5–34.0% and
attention difficulties in 24.4–28.0% of the participants 4–15 weeks post COVID-19 [30,31]. A
smaller number of cognitive problems was found in a study from Mattioli et al. [32], with
attention difficulties reported by 11.6% and memory difficulties by 6.6% of 120 persons 4
months after mild to moderate COVID-19. The present study suggests that self-reported
cognitive problems tend to persist and even deteriorate over time. This finding may be
partly explained by the ongoing restraining measures due to COVID-19, including social
distancing, social isolation and restriction of movements, which the entire population was
exposed to [33]. In contrast, Del Brutto et al. [34] found an improvement in cognitive
impairments over 1.5 years in patients with mild COVID-19.
In terms of objective cognitive tests, with the exception of Mattioli et al. [32], most prior
studies reported cognitive impairments post COVID-19 [21,35]. Jaywant et al. [36] found
mild to severe cognitive impairment in 81% of 57 COVID-19 patients 7 days after diagnosis.
Similar to the present study, working memory was the cognitive function most strongly
affected. Mazza et al. [37] found that 78% of 226 patients showed poor performance in at
least one cognitive domain 3 months after hospital discharge; 24% had poor performance
in working memory and 32% in verbal fluency. Albu et al. [35] and Miskowiak et al. [21]
both reported a cognitive impairment in 59–65% of their participants 2–4 months after
hospital discharge. However, the validity of these studies is limited by the small sample
sizes, n = 30 and n = 29, respectively. Lower prevalences of cognitive deficits were reported
Viruses 2023, 15, 256 10 of 13

by Rass et al. [38] (23% of 135 participants 3 months post COVID-19), Negrini et al. [39]
(33.3% of 9 participants 44 days after hospital admission) and Almeria et al. [40] (5.7–11.4%
(depending on the specific test) of 35 participants 26 days after hospital discharge).
Although a recent systematic review indicated that cognitive impairment can be also
found in mild or asymptomatic cases of COVID-19, studies which focus on non-hospitalized
persons are rare [8]. Hampshire et al. [18] found significant cognitive deficits in 326 non-
hospitalized COVID-19 cases compared with controls. The only study which compared
cognitive function of asymptomatic COVID-19 subjects (n = 93) with healthy controls found
significantly more cognitive dysfunction in the domains of fluency, visuoperception and
naming in the COVID-19 group [41].
Of interest is that the regression analysis of the cognitive tests revealed no variables
which were consistently and independently associated with cognitive impairments, except
poor education level. Since poor education may adversely affect cognition via low cognitive
reserves, future studies should be conducted on this specific patient group [5]. In contrast
to the results from Almeria et al. [40], the presence of neurological symptoms was not
consistently associated with cognitive functions in the present study. Only disturbance of
smell function was found to be related with the persons’ subjective rating of concentration
problems and worse scores on the SCWT-CW test. However, Almeria et al. [40] also
included hospitalized persons, and the cognitive tests were performed shortly after hospital
discharge.
In contrast, depression was significantly associated with impairments of executive
cognitive functions as well as with subjective memory and concentration problems. It is well
known that people with depressive disorders suffer from cognitive impairments; however,
the association between depression and cognitive problems is so far rarely investigated
in studies on COVID-19 [20,40]. Of interest is that, similar to other studies [35,40,42],
subjective cognitive problems were not significantly associated with test results in the
present study. Subjective cognitive problems were, however, strongly related with the
number of post-COVID-19 complaints and depressiveness, indicating relevant risk groups
for post-COVID-19 cognitive impairment. In addition, the failure to objectify subjective
cognitive impairments by means of standard cognitive tests underscores the need to define
a standard test battery applicable for COVID-19 survivors.
Furthermore, the present study showed that the independent variables included in
the regression models explained only a low percentage of the cognitive test variance. Con-
sequently, other factors are suggested to be associated with cognitive impairment after
COVID-19. These could include pre-COVID-19 cognitive problems or consequences of the
COVID-19 inflammation process, such as pulmonary hypoxaemia and neuroinflamma-
tion [18]. Thus, further studies are needed in order to specify the factors contributing to the
development of cognitive dysfunction after COVID-19.

5. Strengths and Limitations

To the best of our knowledge, the present study is the first which investigated both
subjective and objective cognitive functions in a large sample of non-hospitalized persons
with COVID-19. Further strengths of this study are the median follow-up time of nine
months and the inclusion of participants with confirmed COVID-19 in a defined study
region.
However, this study has several limitations. Firstly, the study was lacking a healthy
control group. Comparison of test results was based on the published norming populations.
Secondly, the participants reported their symptoms during the acute COVID-19 infection
phase retrospectively. These statements are, therefore, subject to a possible recall bias. In
addition, information on previous cognitive impairments was missing. Furthermore, a
selection bias cannot be excluded, since persons with a large disease burden may be more
likely to participate in a study than persons without any health impairments after COVID-
19. Therefore, the cognitive impairments found in the present study may be overestimated.
The variance explained by the independent variables in the regression models of cognitive
Viruses 2023, 15, 256 11 of 13

tests was small, indicating that relevant predicting factors may be missing. Finally, the
study participants were infected with the early SARS-CoV-2 variants of concern, and the
results may not be transferrable to later virus variants.

6. Conclusions
In conclusion, the present study consisting of participants with mild COVID-19 course
highlights the need to consider screening for post COVID-19 cognitive impairment also
in this large group of affected people. Whether cognitive problems after COVID-19 con-
siderably impair the daily life activities and other domains of quality of life of the affected
persons should be investigated in future studies. Such results may support the estimation
of treatment needs. Furthermore, since no clear predictors of cognitive impairments could
be identified in the present study, the role of neuroinflammation should be further investi-
gated in order to find suitable preventive strategies and specific therapeutic approaches.
Meanwhile, people who suffer from post-COVID-19 cognitive problems can be supported
by established cognitive trainings. Given the prevalence of COVID-19, digital interven-
tions, which can be widely disseminated, might be a useful approach for those with mild
cognitive impairments [16]. For more severely affected individuals, extended cognitive
diagnostics and treatment may be provided within in- or out-patient rehabilitation or in
specialized post-COVID outpatient clinics.

Supplementary Materials: The following supporting information can be downloaded at: https:
//www.mdpi.com/article/10.3390/v15010256/s1, Table S1: Multivariable linear regression models
for the cognitive tests WAIS-IV, RWT, SCWT-W, SCWT-C and SCWT-CW; Table S2: Multivariable
logistic regression models for the dependent variables concentration problems and memory problems
at follow-up; Table S3: Multivariable linear regression models for the cognitive tests (with acute
symptoms as covariables); Table S4: Multivariable logistic regression models for the dependent
variables concentration problems and memory problems (with acute symptoms as covariables).
Author Contributions: Conceptualization, C.M. and Y.G.; Methodology, C.M. and I.K.; Formal Analy-
sis, I.K. and D.P.; Investigation, Y.G., T.D.W. and C.M.; Resources, J.L. and A.H.-D.; Writing—Original
Draft Preparation, I.K. and D.P.; Writing—Review and Editing, C.M., J.L., Y.G., T.D.W. and A.H.-D.;
Supervision, C.M., J.L. and A.H.-D.; Project Administration, Y.G. and T.D.W.; Funding Acquisition,
Y.G. and C.M. All authors have read and agreed to the published version of the manuscript.
Funding: This work was funded by the Bavarian state funding for SARS-CoV-2 research projects
2020.
Institutional Review Board Statement: The study was conducted in accordance with the Declaration
of Helsinki and approved by the Ethics Committee of the Ludwig-Maximilians-Universität, Munich
(No. 20-735, date of approval: 15 December 2020).
Informed Consent Statement: Informed consent was obtained from all subjects involved in the
study.
Data Availability Statement: The datasets generated during and/or analyzed during the cur-
rent study are not publicly available due to data protection requirements but are available in an
anonymized form from the corresponding author on reasonable request.
Acknowledgments: The authors wish to thank all members of the University Hospital Augsburg,
Chair of Vascular Surgery and Chair of Epidemiology, who were involved in the planning and
conduct of the study as well as the local public health departments who enabled the recruitment of
study participants. Finally, we express our appreciation to all study participants.
Conflicts of Interest: The authors declare no conflict of interest.

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