Archives of Orthopaedic and Trauma Surgery (2023) 143:2189–2197

https://doi.org/10.1007/s00402-022-04445-x

HIP ARTHROPLASTY

Chronic pain in osteoarthritis of the hip is associated with selective

cognitive impairment
Murteza Ali Kazim1 · André Strahl1 · Steffen Moritz2 · Sönke Arlt2 · Andreas Niemeier1,3

Received: 5 January 2022 / Accepted: 10 April 2022 / Published online: 5 May 2022
© The Author(s) 2022

Abstract
Introduction Chronic pain of various origin is known to be associated with selective cognitive impairment. Osteoarthritis
(OA) of the hip is one of the leading causes of chronic pain in the adult population, but its association with cognitive perfor-
mance has not been evaluated. Here, we investigate the effect of chronic pain due to unilateral OA of one hip and no further
source of chronic pain on cognitive performance.
Materials and methods A neuropsychological test battery, consisting of the Mini-Mental State Examination, Rey–Osterrieth
complex figure test, Rivermead behavioural memory test, d2 test of attention, and F-A-S test was applied in 148 patients and
82 healthy pain-free control individuals. The influence of potentially confounding factors such as depression and anxiety
was examined.
Results Patients with OA of the hip showed decreased performance in specific neuropsychological tests. Performance in
verbal and visual short-term and long-term memory and selective attention tests was significantly poorer compared to healthy
controls. Whereas the executive functions “updating”, “set shifting”, “response inhibition” and “reflection” appear intact,
“problem solving” and “planning” were impaired. None of the confounders showed any influence on cognitive performance
in both study groups.
Conclusion We conclude that chronic pain secondary to end-stage hip OA is associated with selective cognitive impairment.
Future studies are required to investigate the effect of total hip arthroplasty on cognitive performance.

Keywords Chronic pain · Hip osteoarthritis · Hip replacement · Cognitive impairment

Introduction negative impact on cognitive performance. Jones [2] first

described the impairment of episodic memory in patients
Chronic pain represents a crucial factor of direct, indi- with chronic pain in 1957. Since then, several studies have
rect, and intangible costs to society, economy, and affected shown that chronic pain of various aetiologies, including
patients with a reported prevalence of 19% in the European musculoskeletal pain in conditions such as chronic back
population [1]. It is well known that chronic pain has a pain, rheumatoid arthritis, and others [3–10] can affect cog-
nitive abilities, in particular working memory, attention, and
executive functions. Many of these studies did not consider
* Murteza Ali Kazim the influence of potential confounders such as depression
[email protected] and anxiety. Furthermore, the individual functional areas of
1 cognition were investigated separately.
Division of Orthopaedics, Department of Trauma
and Orthopaedic Surgery, University Medical Center To the best of our knowledge, there are no studies exam-
Hamburg-Eppendorf, Martinistraße 52, 20246 Hamburg, ining all cognitive functional areas and considering potential
Germany confounders for a specific cause of chronic pain. Prakash
2
Department of Psychiatry and Psychotherapy, University et al. [11] showed that memory and pain activate the same
Medical Center Hamburg-Eppendorf, Martinistraße 52, central nervous pathways including the anterior cingulate
20246 Hamburg, Germany cortex, prefrontal cortex, hypothalamus, island, hippocam-
3
Department of Biochemistry and Molecular Cell Biology, pus, and amygdala. This finding supports the relationship
University Medical Center Hamburg-Eppendorf,
Martinistraße 52, Hamburg, Germany

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2190 Archives of Orthopaedic and Trauma Surgery (2023) 143:2189–2197

between the decrease of gray matter in different brain announcements, flyers placed in general practitioners' offices
regions and chronic pain of various aetiologies [12–19]. and through invitations to residents of senior citizen housing
Regarding OA of the hip, we have previously demon- facilities. All study participants were informed about data
strated that gray matter is reduced in patients with chronic protection regulations before the start of the study. Prior to
pain in the anterior cingulate cortex, orbitofrontal cortex, study participation, written declaration of consent of all par-
dorsolateral prefrontal cortex, island, and operculum [13, ticipants was signed and archived. The study conforms to the
17]. Interestingly, despite these findings, the cognitive per- principles of the Declaration of Helsinki, was approved by
formance in patients with hip OA has not been examined the local research ethics committee (PV5016) and registered
in detail yet. One single study in the literature analyzed the with ClinicalTrials.gov (NCT02997891).
physical limitation in hip OA and its interactions with body
function, comorbidities, and cognition [8]. This study pri- Demographic and clinical data
marily focused on physical limitation and the results were
not compared to standard values or to a control group (CG). Demographic and clinical data including age, gender,
Although the prevalence of hip OA is > 7% within the age employment, comorbidities, pain medication and pain inten-
group of 60–90 years [20], and thus represents one of the sity in the last 7 days using the visual analog scale (VAS)
leading causes of chronic pain [21], further studies focusing were collected. Hip function was recorded by the Harris Hip
on cognition in patients with hip OA are lacking. Score (HHS) only in the CPG.
Since depression is associated with cognitive impairment
[22], and the rate of depression is increased in patients with Neuropsychological tests
chronic pain, we hypothesize, that these two factors (depres-
sion and pain) may both be associated with cognitive impair- The Mini-Mental State Examination (MMSE) was per-
ment and may reinforce each other regarding the impact on formed to detect dementia and exclude patients and controls
cognition. We further hypothesize that also anxiety may add with a score of 24 and below. The distinct cognitive dimen-
to cognitive impairment in patients with chronic hip OA sions were investigated by the following neuropsychological
pain, since there is an association of anxiety disorders and tests:
cognitive impairment, especially in the elderly [23].
The primary objective of the present study was to investi- Rey–Osterrieth complex figure test (ROCFT) [24]
gate the cognitive performance in chronic pain patients due
to unilateral hip OA in comparison to a healthy CG. The The participant is requested to draw a complex figure with
secondary goal was to evaluate the effect of depression and a total of 18 items, afterwards the figure must be drawn
anxiety on the relationship between pain and cognition. from memory and after another 30 min again. The ROCFT
measures the visual construction and the visual memory
performance.
Methods
Rivermead behavioral memory test (RBMT) [25]
Population and study design
The RBMT is a diagnostic test consisting of eleven tasks
This study was performed as a single institution prospective to identify memory problems. We used the sub-test “story”
clinical trial. The inclusion criterion for the chronic pain to examine verbal short- and long-term memory. A short
group (CPG) was chronic pain caused by end-stage unilat- story is read aloud, and the test person is asked to give a
eral hip OA, scheduled for elective total hip replacement verbatim report of it (immediate recall). After 30 min, the
surgery. Based on patient´s symptoms, orthopedic exami- participant is asked to repeat the story again (delayed recall).
nation, and radiograph images the diagnosis of end-stage Each reproduced item was awarded with points for verba-
OA was confirmed. The severity of the OA was described tim or analogous items reproduction. Conclusions about the
by the Kellgren–Lawrence grade. Exclusion criteria were executive functions “problem solving” and “planning” were
chronic pain of further origin, bilateral hip osteoarthritis, drawn of the results.
dementia, substance-related addiction (including alcohol,
psychotropic intoxicants, or medication), current psychiatric d2 test of attention [26]
treatment, untreated visual or hearing impairment or lack of
German language skills. The same criteria were applied to The participant must mark any letter "d" in 14 lines with two
the healthy CG, with the only difference being chronic pain marks around above or below it in any order. The patient has
of any origin as an exclusion criterion. The CG consisted 20 s per line to mark all items between wrong items. From
of healthy volunteers recruited by word-of-mouth, e-mail the correct, incorrect, and omitted markings, scores can be

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formed, of which the “concentration performance” (CONC) high practical importance) were calculated for each t-test
is derived. CONC describes the number of correctly detected [33]. The effect size illustrates the practical relevance of
target items minus the number of errors of commission. The statistically significant results. To evaluate the second-
test is suitable for the examination of selective attention. ary goal, confounding effect of depression and anxiety,
Furthermore, the evaluation of “wrong marking errors” mediator analyses with multiple regressions were con-
allows conclusions about the executive function "response ducted for each neuropsychological test. This method can
inhibition". be used to examine potentially significant indirect effects
of depression and anxiety on the relationship between
Trail making test (TMT) [27] pain and cognition. This relationship is described by the
Pearson correlation (r). Since age has a possible influ-
The TMT part A comprises numbers from 1 to 25, which ence on neuropsychological test results partial correlations
must be connected in ascending order as quickly as possible. ­( r partial) were calculated to exclude the influence of this
In part B, letters are mixed in between, and the participant variable if necessary. Additionally, descriptive statistics
must alternately combine numbers and letters in sequence were calculated to present demographic data by means,
(1–A–2–B–3–C… 13–J). The time required for the two standard deviations, and percentages. Any differences in
parts represents a measure of attention and executive func- sociodemographic parameters were analyzed by t-tests
tion "updating" and "set shifting". Psychomotor speed and for continuous data and Chi-square tests for categorical
visual perception exert a significant influence. By subtract- data. Data analyses were performed with SPSS statistical
ing A from B, the influence of psychomotor speed can be software version 25 (IBM Corp., Armonk, NY, USA) and
reduced [28]. JASP (Version 0.14) [34]. P values ≤ 0.05 were considered
statistically significant.
Verbal fluency F‑A‑S test [29]

The task of the F-A-S test is to enumerate as many words

as possible with the initial letter "s" in 60 s. Personal names Results
and words with the same word stem are not validated. The
total number of words was not only used for the short-term The study enrolled 148 patients with unilateral OA of the
memory, but also for the evaluation of the executive func- hip into the CPG out of a total of 575 respondents who
tion [30]. “Set shifting” and “updating” play a decisive role were screened for participation. In the CG, 83 participants
completing this task. out of a total 114 respondents were included. One partici-
pant of the CG had to be excluded from the study due to a
Confounding factors MMSE result < 25. Demographic and clinical data, includ-
ing outcomes of depression and anxiety scores, are listed
The potentially confounding factors depression and anxiety in Table 1. There were no significant differences between
were determined by means of questionnaires. The Patients the two groups in age, sex, occupation, and number of
Health Questionnaire (PHQ-9) [31] and Generalized Anxi- comorbidities. Pain assessment by the visual analog scale
ety Disorder (GAD-7) [32] questionnaire include items (VAS) showed a highly significant difference (p < 0.001) in
about depression and anxiety, covering core DSM-IV crite- pain between CPG (mean 6.1 ± 2.1) and CG (0.9 ± 1.3). No
ria of depressions and generalized anxiety disorders. Both neurological comorbidities, such as brain trauma, stroke or
scores differentiate between four levels from mild to severe epilepsy were reported. A synopsis of means and standard
depression/anxiety disorder. deviates of the neuropsychological test results are presented
in supplementary Table 1.
Statistical analysis

The primary outcome, differences in cognitive perfor- Memory

mance, was evaluated using independent t-tests for con-
tinuous data to determine whether significant differences The impairment of the visual, spatial, and verbal short-term
exist between CPG and CG. To analyze whether these dif- and long-term memory was tested by ROCFT and RBMT.
ferences are also clinically relevant effect sizes according In both tests, the results of the CPG were significantly
to Cohen (d-values between 0.2 and 0.5 represent a small lower with medium to large effect sizes (“ROCFTmemory”
effect without practical significance, d-values between 0.5 p < 0.001, d = 0.62; “ROCFTmemory quotient” p = 0.001,
and 0.8 represent a medium effect with moderate practical d = 0.51; “RBMTrecall” p < 0.001, d = 0.80; “RBMTdelayed
significance, all values above 0.8 have a large effect with recall” p < 0.001, d = 1.15; (Figs. 1 and 2).

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Table 1  Demographic and Chronic pain group Control group p value

clinical characteristics of the
study cohorts Age in years (mean, SD) 68.0 (9.9) 66.8 (7.8) 0.306
Sex (N, %) 78 females (52.7%) 44 females (53.7%) 0.889
Pain intensity (mean, SD)
6.1 (2.1) 0.9 (1.3) < 0.001
Pain medication (N, %)
Opiates + non-opiates 11 (7.8%) 2 (2.9%)
Non-opiates 61 (43.6%) 6 (8.7%) < 0.001
No pain medication 68 (48.6%) 61 (88.4%)
(8 missings) (13 missings)
Depression (N, %)
Minimal 50 (38.5%) 63 (81.8%)
Mild 62 (47.7%) 12 (15.6%)
Moderate 13 (10.0%) 1 (1.3%) < 0.001
Severe 5 (3.8%) 1 (1.3%)
(18 missings) (5 missings)
Anxiety (N, %)
Minimal 91 (70.0%) 66 (85.7%)
Mild 33 (25.4%) 10 (13.0%)
Moderate 4 (3.1%) 1 (1.3%) 0.01
Severe 2 (1.5%) 0 (0%)
(18 missings) (5 missings)
Occupation (N, %)
Full time 25 (19.4%) 20 (26.0%)
Half time 18 (14.0%) 6 (7.8%) 0.282
Unemployed/pension 86 (66.6%) 51 (66.2%)
(19 missing) (5 missing)
Number of comorbidities (mean, SD)
1.0 (± 0.9) 1.0 (± 1.2) 0.957
HHS (mean, SD) 58.2 (± 13.9) – –
Kellgren–Lawrence score
0 0 (0.0%) – –
1 0 (0.0%)
2 10 (6.8%)
3 95 (64.2%)
4 43 (29.1%)

HHS Harris hip score, SD standard deviation

Attention inhibition". There was no evidence for a significant dete-

rioration of “response inhibition” in the CPG (p = 0.234).
Selective attention, measured by d2 test, was significantly According to the results of TMTB and the.
lower in the CPG with medium effect sizes (“total marks” F-A-S test (“TMTB” p = 0.09; “TMTB–A” p = 0.296;
p < 0.001, d = 0.55, “total marks – mistakes” p < 0.001, “F-A-S “ p = 0.129), “set shifting", "updating" and “com-
d = 0.53, “concentration performance” p = 0.004, d = 0.42). plex executive functions” did not indicate significant
The investigation of split attention (TMTB) bordered on sig- differences between the groups (Figs. 4 and 5). On the
nificance (p = 0.09; Figs. 3 and 4). contrary, considering the results of the ROCFT executive
function such as “planning” and “problem solving” seem
Executive function to be impaired.

Wrong markings from the d2 test were used as a meas-

urement value for the executive function "response

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­r partial =  – 0.262, p < 0.001; “d2concentration performance”

­r partial =  – 0.194, p = 0.01), visual memory (“ROCFT-
memory” ­r partial =  – 0.322, p < 0.001; “ ROCFTmemory
quotient” ­r partial =  – 0.266, p < 0.001) and verbal memory
(“RBMTrecall “ ­rpartial =  – 0.268, p < 0.001; “RBMTdelayed
recall “ r­ partial =  – 0.396, p < 0.001) but not for psychomotor
speed (“TMTA” p = 0.066, “TMTB” p = 0.17, “TMTB–A”
p = 0.497).
To evaluate the potential indirect effects of depression
and anxiety as confounding variable on these significant
relationships, a multivariate mediator analysis was per-
formed. All analyses revealed no significant confounding
influence of depression and anxiety (Table 2).

Fig. 1  The memory A and memory quotient B scores of the Rey– Discussion
Osterrieth complex figure test (ROCFT) reveal a significant impair-
ment of the memory in the chronic pain group (CPG) as compared to To the best of our knowledge, this is the first study to inves-
the control group (CG). **p < 0.001 tigate cognition in patients with chronic pain caused by OA
of the hip. We analyzed various facets of cognitive perfor-
mance (selective/shared attention, verbal/visual memory,
and executive functions) and the impact of potential con-
founding factors (depression and anxiety) on cognitive per-
formance in 148 patients with chronic pain due to end-stage
unilateral hip OA. We compared the results to a CG of 82
free of chronic pain of any cause. The major finding is that
chronic pain due to hip OA is associated with significantly
worse test results with high effect sizes in neuropsycho-
logical tests measuring verbal/visual short-term, long-term
memory and selective attention. Executive functions are only
partially impaired, with lower scores for “problem solving”
and “planning”, while “updating”, “set shifting”, “response
inhibition”, and “reflection” appeared intact. In a follow
up study of this patient collective, Strahl et al. [35] dem-
onstrated the improvement of cognition, measured by the
same neuropsychological test battery, six months after total
Fig. 2  The Rivermead behavioral memory test (RBMT) reveals a sig-
nificant impairment of behavioral memory in the chronic pain group hip arthroplasty. The potential confounders do not appear to
(CPG) as compared to the control group (CG) in both recall (A) and have measurable impact on cognition in the hip OA popula-
delayed recall (B) qualities. **p < 0.001 tion. Since the neuropsychological test battery used in this
study is available in many languages, reproducing these tests
and findings in an English-speaking population is possible.
Influence of depression and anxiety
on the relationship between pain and cognition Cognitive functions

Significant small to moderate correlations (p < 0.001) Regarding memory and attention (measured by ROCFT and
between r = 0.225 and r = 0.446 were found between age RBMT), the present findings do correspond to previously
and all but one neuropsychological test parameter. The published results on cognitive impairment in patients with
sum of errors of the d2 test showed no significant corre- chronic pain of other etiology [3–10, 36–40].
lation with age (p = 0.691). Taken the effect of age into Regarding executive function, the effect of chronic pain
account, partial correlations between VAS pain intensity is more diverse. Executive functions are a set of cognitive
and neuropsychological test parameters demonstrated sig- processes that are necessary for cognitive control of behav-
nificant correlations for selective attention (“d2total marks” ior. Some executive functions are clearly impaired in hip
­r partial =  – 0.268, p < 0.001; “d2total marks – mistakes” OA such as “planning” and “problem solving” (measured

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Fig. 3  The d2 test reveals sig-

nificant differences in the total
marks (A), total marks minus
mistakes (D) and concentration
performance (E) indicating an
impairment of selective atten-
tion and executive function in
the chronic pain group (CPG) as
compared to the control group
(CG). Omit mistakes (B) and
wrong marks (C) displayed
no significant differences.
**p < 0.001

Fig. 4  A, B, C The Trail Mak-

ing Test (TMT) does not reveal
differences in the executive
functions set shifting and updat-
ing between the chronic pain
group (CPG) and the control
group (CG). These functions
appear to be unaffected by hip
OA

by ROCFT), while others do not seem to be altered in pain conditions. Specifically, “set shifting” was shown
patients with chronic hip OA pain. For example, “response to be impaired in patients with fibromyalgia [19, 41] and
inhibition” (measured by wrong markings in the d2 test), chronic pain conditions due to visceral, musculoskeletal,
“reflecting” (measured by F-A-S), “set shifting” and “updat- and neuropathic pain [42]. We believe that cognitive aging
ing” (measured by TMTB and TMTB–A) did not show any is the reason for this discrepancy [43]. The average age
difference. of patients in the present was 68.0 years while the aver-
Interestingly, some of these qualities, which are age age of the previously published work ranged from
not affected by chronic hip OA, have been previously 48.1 years to 53.6 years. Therefore, it is conceivable that
described to be altered in patients with other chronic a significantly younger study group with hip OA may also

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in a complex, not a uniform, manner. The extent of cogni-

tive impairment appears to depend on the cause of chronic
musculoskeletal pain, pain intensity, pain progress and
pain localization. Further delineating specific interactions
of the various qualities of the CNS cognitive function with
various chronic OA pain qualities from, e.g., knee, hip, and
shoulder, may help counseling patients regarding the options
and expected benefits of elective joint replacement surgery
beyond pain control.

Potential confounders

In the present study, there was no significant influence of

depression or anxiety on cognition (Table 2). This is consist-
Fig. 5  The verbal fluency test F-A-S does not reveal any differences ent with published literature in that depression and anxiety
in the executive functions set shifting and updating between the secondary to chronic pain of different causes were not asso-
chronic pain group (CPG) and the control group (CG) ciated with impaired cognition [5, 42, 45, 46], while primary
depression or anxiety disorders were related to cognitive
impairment [22, 23, 41, 47–49]. Obviously, when depression
present impaired “set shifting” as compared to an CG of or anxiety is secondary to pain, their effect on cognition is
the same age. run over by a dominant effect of pain on cognition.
Other qualities such as “planning” and “problem solving”
have previously been shown to remain unaffected in patients Pain severity
with rheumatoid arthritis compared to a healthy CG [44].
Taken together, the present results and previously pub- Increasing pain severity has been demonstrated to be asso-
lished work demonstrate that cognitive functions are sub- ciated with decreased cognitive performance in patients
ject to change in patients with chronic musculoskeletal pain with chronic back pain, visceral, musculoskeletal, and

Table 2  Multivariate mediator analysis for indirect effects of depression and anxiety on the relationship between pain and cognition

Indirect effects of depression Estimate SD error z-value p value 95% confidence

interval
Lower Upper

VAS pain → PHQ → ­d2total marks 0.275 1.426 0.193 0.847 – 2.519 3.070
VAS pain → PHQ → ­d2total marks-mistakes 0.482 1.278 0.377 0.706 – 2.024 2.988
VAS pain → PHQ → ­d2concentration performance 0.425 0.593 0.717 0.473 – 0.737 1.588
VAS pain → PHQ → ­ROCFTmemory – 0.207 0.214 – 0.966 0.334 – 0.626 0.212
VAS pain → PHQ → ­ROCFTmemory quotient – 0.647 0.599 – 1.081 0.280 – 1.820 0.526
VAS pain → PHQ → ­RBMTrecall 0.010 0.044 0.223 0.823 – 0.076 0.096
VAS pain → PHQ → ­RBMTdelayed recall 0.009 0.042 0.203 0.839 – 0.074 0.092
Indirect effects of anxiety Estimate SD error z-value p value 95% confidence
interval
Lower Upper

VAS pain → GAD → ­d2total marks 0.527 0.687 0.768 0.443 – 0.819 1.873
VAS pain → GAD → ­d2total marks-mistakes 0.597 0.619 0.964 0.335 – 0.616 1.811
VAS pain → GAD → ­d2concentration performance 0.337 0.290 1.161 0.246 – 0.232 0.906
VAS pain → GAD → ­ROCFTmemory 0.025 0.102 0.250 0.802 – 0.174 0.225
VAS pain → GAD → ­ROCFTmemory quotient 0.003 0.286 0.011 0.991 – 0.558 0.564
VAS pain → GAD → ­RBMTrecall – 0.003 0.021 – 0.150 0.881 – 0.045 0.038
VAS pain → GAD → ­RBMTdelayed recall 0.008 0.020 0.386 0.700 – 0.032 0.047

SD error Delta method standard mistakes: Estimate = ML estimator, PHQ Patient Health Questionnaire, GAD generalized anxiety disorder scale

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2196 Archives of Orthopaedic and Trauma Surgery (2023) 143:2189–2197

neuropathic pain [46, 50, 51]. Our results also confirm these as you give appropriate credit to the original author(s) and the source,
findings for pain due to hip OA. First, we found weak to provide a link to the Creative Commons licence, and indicate if changes
were made. The images or other third party material in this article are
moderate significant correlations between pain intensity and included in the article's Creative Commons licence, unless indicated
our neuropsychological parameter. Second, our CG with a otherwise in a credit line to the material. If material is not included in
low level of pain showed significantly higher neuropsycho- the article's Creative Commons licence and your intended use is not
logical test results as the CPG. permitted by statutory regulation or exceeds the permitted use, you will
need to obtain permission directly from the copyright holder. To view a
copy of this licence, visit http://​creat​iveco​mmons.​org/​licen​ses/​by/4.​0/.

Limitation
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