Yorke et al. BMC Psychiatry          (2020) 20:143 
https://doi.org/10.1186/s12888-020-02570-8
RESEARCH ARTICLE Open Access
Comparison of neurocognitive changes
among newly diagnosed tuberculosis
patients with and without dysglycaemia
Ernest Yorke1*, Vincent Boima1, Ida Dzifa Dey1, Vincent Ganu2, Norah Nkornu3, Kelvin Samuel Acquaye4 and
C. Charles Mate-Kole3,5,6
Abstract
Background: Diabetes often occurs together with tuberculosis (TB) and both may affect each other negatively.
Diabetes may be associated with neurocognitive dysfunctioning in affected patients and may negatively impact
treatment adherence and outcomes. This study compared the neurocognitive status between newly diagnosed
smear positive tuberculosis patients with dysglycaemia and those with normoglycaemia.
Methods: The current study was a cross-sectional study involving one hundred and forty-six (146) newly diagnosed
smear positive TB patients. Oral glucose tolerance test (OGTT) was performed and the results were categorized as
either normoglycaemia, impaired glucose tolerance (IGT), impaired fasting glucose (IFG) or diabetes.
Neurocognitive functioning among study participants was assessed at the time of TB diagnosis using Cognitive
Failure Questionnaire (CFQ), Montreal Cognitive Assessment tool (MoCA), California Verbal Learning Test (CVLT), Brief
Symptom Inventory (BSI) and the Spitzer Quality of Life Index (QLI).
Results: The mean age of the participants (n = 146) was 38.7 years with 78.8% being males and 21.2% females.
Using the fasting blood glucose test, the prevalence of impaired fasting glucose and diabetes were 5.5 and 3.4%
respectively, both representing a total of 13 out of the 146 participants; whilst the prevalence of impaired glucose
tolerance and diabetes using 2-h post-glucose values were 28.8 and 11.6% respectively, both representing a total of
59 out of the 146 participants.
There were no significant differences in the mean scores on the neurocognitive measures between the
dysglaycaemia and normoglycamic groups using fasting plasma glucose (FPG). However, there were significant
differences in the mean scores between the dysglycaemia and normal groups using 2-h postprandial (2HPP)
glucose values on Phobic Anxiety (Normal, Mean = 0.38 ± 0.603; dysglycaemia, Mean = 0.23 ± 0.356; p = 0.045), and
Montreal Cognitive Assessment (MoCA) scores (17.26 ± 5.981 vs. 15.04 ± 5.834, p = 0.037).
Conclusion: Newly diagnosed smear positive patients with dysglycaemia were associated with significantly lower
mean cognitive scores and scores on phobic anxiety than those with normoglyacaemia. The latter finding must be
further explored.
Keywords: Tuberculosis, Smear positive, Dysglycaemia, Neuropsychological disorders
* Correspondence: pavlovium@yahoo.com
1Department of Medicine & Therapeutics, School of Medicine & Dentistry,
College of Health Sciences, University of Ghana, Legon, Accra, Ghana
Full list of author information is available at the end of the article
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Yorke et al. BMC Psychiatry          (2020) 20:143 Page 2 of 7
Background Methods
A lot of effort continues to be made to reduce the Study site and design
worldwide incidence, morbidity and mortality associated We conducted a hospital based cross-sectional study at
with tuberculosis (TB); however it continues to be a the Chest Clinic of the Korle-Bu Teaching Hospital,
deadly communicable disease. In 2015, 10.4 million new which is a tertiary care facility and the largest hospital in
cases and 1.4 million deaths due to TB were estimated Ghana. The Korle-Bu Chest clinic is the main referral
to have occurred by World Health Organisation (WHO) centre in southern Ghana for TB cases and other re-
[1]. Many reviews and meta-analysis have reported that spiratory conditions.
diabetes increases TB risk by between 1.5 to 7.8 fold [2, 3].
Since developing countries have the greatest burden of Participants and recruitment
TB, the expected increase in the prevalence of type 2 Inclusion criteria included TB patients who were newly
diabetes in these parts of the world would increase the im- diagnosed smear positive cases and were either initially
pact of diabetes on TB [1, 4]. Negative impact of comorbid diagnosed or referred for treatment at the Chest Clinic,
diabetes on TB include poor treatment outcomes [2], 18 years and above with no previous history of TB treat-
more severe disease and re-activation of dormant tubercu- ment. None of the patients had known pre-existing
losis foci [5]. diabetes. Excluded participants were those aged below
Tuberculosis (TB) like many chronic diseases is associ- 18 years, those with previous history of TB treatment,
ated with a high burden of psychological disorders which patients with smear negative TB, extra pulmonary TB,
may have a negative impact on the psychological health, those with previous history of psychological, psychiatric
treatment adherence and outcomes [6]. or neurological disorders or those who refused consent.
Common psychological disorders among TB patients We used a convenient sampling method to recruit about
especially around the time of diagnosis include depres- 3–4 participants on a weekly basis (week days only) who
sion, anxiety, in addition to poor quality of life [6]. The met the included criteria. A total of 160 participants
reasons for these changes include physiological and were recruited over a 12-month period.
physical impact of the disease, stigma and isolation, effects
of medications and rigours of keeping appointment and Measurements
other negative social impact including loss of income [6]. At enrolment, data on demographic and anthropometric
These problems may affect self-esteem and attitudes characteristics such as body mass index (BMI), waist cir-
towards disease management including compliance to cumference (WC), hip circumference (HC) and waist-
medications and eventually lead to poor disease out- hip-ratio (WHR) as well as medical history were col-
come [6]. The association of cognitive impairment lected using standardized questionnaire.
with pulmonary TB alone does not appear to be BMI (calculated) was categorized as obese, overweight,
strong, although this may be the case among patients normal and underweight with defined values of 30.0 or
with systemic spread [7–9]. However, cognitive dys- more, 25–29.9, 18.5–24.9-and less than 18.5 (Kg/m2) re-
function has been strongly associated with diabetes, spectively [13].
which may impair self-management activities in many Microscopy using Ziehl-Neelsen (ZN) stain was used
patients [10–12]. to determine the presence of acid fact bacilli (AFBs)
The negative impact of diabetes on TB, including po- [14]; whilst plasma glucose levels were determined using
tential cognitive impairment, coupled with the expected a 75 g oral glucose tolerance test (OGTT). After an over-
increases in the prevalence of both diseases is likely to night fast (8 h), ten millilitres (ml) of fasting blood
portend bad prognosis in the management of TB pa- sample was taken into fluoridated blood sample tubes
tients [1, 2, 4–6]. Unfortunately, developing nations have and centrifuged within 15 min of blood draw after being
limited healthcare budgets and resources to deal with kept on ice [15]. After 2 h of the administration of 75 g
the expected negative reciprocal impact of diabetes and glucose in 250 ml water a second blood sample was
TB on the affected population. taken into fluoride tubes for glucose determination. A
Despite the plethora of information on the potential commercial glucose oxidase reagent kits and controls
interaction and effect of diabetes on cognitive function (Diasys, GmBH, Germany) was used to determine
in general population, there is minimal published data plasma glucose; which were then categorized into nor-
about the potential cognitive impact of diabetes and dys- mal glucose levels, impaired glucose tolerance (IGT), im-
glycaemia on cognition among TB patients [2, 3, 5, 6]. paired fasting glucose (IFG) and diabetes.
This study examined and compared the neurocognitive A FPG and 2HPP values of 6.1–6.9 mmol/l and 7.8–
functioning among newly diagnosed smear positive tu- 11 mmol/l diagnosed impaired fasting and glucose toler-
berculosis patients at time of diagnosis with dysglycae- ance respectively; whilst FPG and 2HPP are > 7 mmol/l
mia and those without. and > 11.1 mmol/l respectively or a person on regular
Yorke et al. BMC Psychiatry          (2020) 20:143 Page 3 of 7
medication for diabetes was labelled a diabetic. Normal information. It was imported from Microsoft Excel ver-
plasma glucose values were defined by FPG and 2HPP sion 2010 following an initial cleaning.
values below 6.1 mmol/l and 7.8 mmol/l respectively Socio-demographic, anthropometric, medical history
[16]. Using fasting blood glucose values, dysglycaemia and glycaemic variables were summarised descriptively
was defined as those with IFG and/or diabetes whilst as means and standard deviations, frequencies and
using 2HPP values, it was defined as those with IGT percentages, For the purposes of analysis, dysglycaemia
and/or diabetes. All patients diagnosed with any form of (abnormal glucose level) was defined to include the
dysglycaemia were referred to diabetes specialists for combined prevalence of impaired fasting glucose and
continued care [16]. diabetes (using fasting glucose values) or those with im-
Neuropsychological measurement tools include the paired glucose tolerance and diabetes (using 2-h post-
Cognitive Failure Questionnaire (CFQ) [17], Montreal prandial values). Mean baseline scores of participants on
Cognitive Assessment tool (MoCA) [18], California neurocognitive measures tools were compared using an
Verbal Learning Test (CVLT) [19], Brief Symptom independent T-test at baseline between those with dys-
Inventory (BSI) [20] and the Spitzer Quality of Life glycaemia and those without using both FBS and 2HPP
Index (QLI) [21]. BSI assesses various psychological do- values. The statistical significance levels were set at 5%.
mains including depression, anxiety, somatization, para-
noid ideation, phobia anxiety, obsessive compulsive
behaviour, and interpersonal sensitivity [20]. For the pur- Results
poses of this study only depression, anxiety, somatization, One hundred and forty-six (146) participants (78.8%
phobia anxiety as well as the Global severity index (GSI) males and 21.2% females) with a mean age of 38.7 years
of the BSI [22] were analysed. GSI of the BSI is calculated were involved in the study. Majority (51.37%) of our par-
using the sums for the nine symptom dimensions plus the ticipants were single with 36.99% having education up to
four additional items not included in any of the dimension Junior High School (JHS) level (Table 1). Fasting blood
scores, and dividing by the total number of items to which glucose tests results showed 5.48% had impaired glucose
the individual responded. If no items were skipped the levels whilst 3.42% had diabetes (Table 1). 2-h postpran-
GSI will be the mean for all 53 items. The mean scores of dial results showed 28.77% had impaired glucose levels
the various domains including GSI are interpreted by whilst 11.64% had diabetes (Table 1).
comparison to age-appropriate norms [20]. The Spitzer Information on the prevalence of diabetes and dysgly-
Quality of Life Index (QLI) [21] rates patient’s well-being caemia in this study shown in Table 1 has been pub-
in the areas of health, activity, daily living, outlook and lished earlier and discussed extensively [23].
support. The QLI yields a score that ranges from a high of
10 to a low of 0. The higher one’s score on this measure,
the better his or her quality of life. Cognitive Failure Ques- Mean scores on neuropsychological testing
tionnaire (CFQ) [17] assesses self-reported cognitive The independent t-test conducted to compare the differ-
lapses in perception, memory and misdirected action. The ences in the scores on neurocognitive tests (CFQ,
total score on the scale is obtained by adding up the rat- MOCA, and CVLT) between dysglycaemia and those
ings of the 25 individual items, yielding a score from 0 to with normal glucose, using FBS showed no significant
100. Score ranges between 0 and 50 is within the average differences between the two groups.
scores and reflect normal functioning. Scores above 50 re- However, on the behavioural measures there were
flects clinically relevant problems. Montreal Cognitive As- significant differences between those with dysglycae-
sessment tool (MoCA) [18] is a widely used screening mia and those without using 2HPP scores, and the
assessment for detecting cognitive impairment. MoCA scores of Phobic Anxiety t (150) = 2.025, p = 0.045.
scores range between 0 and 30. A score of 26 or over is Participants’ with dysglycaemia had lower scores
considered to be normal. compared to those who had normal glucose values
CVLT is a measure of verbal learning and memory, (Normal, Mean = 0.38 ± 0.603; dysglycaemia, Mean =
which demonstrates sensitivity to a range of clinical condi- 0.23 ± 0.356), Table 2.
tions such as recall, cognition and encoding [19]. CVLT The scores on the Montreal Cognitive Assessment
short form was used; It consists 9 items and there are no (MOCA) tool showed a significant difference in the
cut-offs for normality, however the higher the scores (the mean scores between those with normal vs. dysglycae-
number of items one can recall) the better the memory. mia, t (105) =2.112, p = 0.037. Those with dysglycaemia
had lower mean scores (Mean = 15.04 ± 5.834) compared
Statistical analysis with those with normal glucose (Mean = 17.26 ± 5.981).
The Statistical software Stata version 15 was used for the There were no significant differences in the rest of the
analysis of data of 146 patients with complete OGTT mean scores for the other tests (Table 2).
Yorke et al. BMC Psychiatry          (2020) 20:143 Page 4 of 7
Table 1 Background Characteristics of newly diagnosed smear Discussion
positive tuberculosis patients at the Chest Clinic of the Korle-Bu In this study, using fasting glucose values, the prevalence
Teaching hospital in Accra, Ghana, 2017 of impaired fasting glucose and diabetes were 5.5 and
Frequency Percentage 3.4% respectively. Using 2-h post-glucose, the prevalence
Age (mean ± SD) 38.70 ± 13.97 of impaired glucose tolerance and diabetes were 28.8
Sex and 11.6% respectively. These prevalence findings have
Female 31 21.20 already been published and discussed extensively [23]
Male 115 78.80 with similar results compared to other studies [24–26].
Significantly, most of the patients (about 70%) were
Highest educational level
underweight. TB patients tend to come from low socio-
Tertiary 23 15.75 economic background and generally malnourished and
O-Level/A-level/SHS 32 21.92 underweight [27]. Weight loss among TB patients may
Middle School/ JHS 54 36.99 also be contributed to by the inflammatory response to
Primary 14 9.59 infection [28, 29] as well as nausea, loss of appetite and
None 13 8.90 vomiting.
Other 10 6.85
Marital Status Diabetes and cognition decline among TB patients
The 2-h post-glucose values revealed that TB patients
Single 75 51.37
with dysglycaemia had a significant lower mean score
Married 62 42.47 than those with normal glucose values on MOCA. This
Separated/Divorced 9 6.16 implies that dysglycaemia is associated with poorer
Employment status cognitive functioning compared to those with normal
Unemployed 38 26.03 glucose levels among TB patients. This finding supports
Employed 108 73.97 the conclusions from other studies that diabetes predis-
Alcohol intake poses to cognitive decline both in humans and animal
Yes 22 15.07 models [12, 30–33], and this finding also holds true for
our study cohort who had TB and dysglycaemia. Cogni-
No 124 84.93
tive decline may negatively affect compliance to the
Smoking strict requirements of TB treatment including adherence
Yes 10 6.85 to medications which can potentially worsen disease
No 136 93.15 outcomes [34].
Weight (mean ± SD) 52.74 ± 8.94 Whiles the pathophysiology of cognitive dysfunction in
Height (mean ± SD) 1.68 ± 0.08 diabetes mellitus is putative; hyperglycaemia, vascular
BMI disease, hypoglycaemia, and insulin resistance are
Above 30 (Obese) 1 0.68 thought to play important roles [35]. Altered cerebral in-
sulin and glucose homoeostasis may lead to widespread
25–29.9 (Overweight) 2 1.37
brain microangiopathy [36, 37]. Insulin resistance, a fea-
18.5–24.9 (Normal) 40 27.4 ture of diabetes and prediabetes, increases the formation
Below 18.5 (Underweight) 103 70.55 of Advanced Glycation End-products (AGE) leading to
Mean ± SD 18.49 ± 3.00 the overproduction of Reactive Oxygen Species (ROS)
2-HPP Glucose (mmol/L) which accelerate biological aging and subsequent cogni-
Diabetes (> 11.1) 17 11.64 tive decline [38]. The recognition of cognitive impair-
Impaired (7.8–11.1) 42 28.77 ment in the dysglycaemia group in a relatively younger
Normal (< 7.8) 87 59.59 patient cohort in our study (average age 38.7 years)
might suggest that cognitive impairment that occurs in
Mean ± SD 8.35 ± 3.44
patients with dysglycaemia and diabetes in TB patients
Fasting Plasma Glucose (mmol/L) probably occurs early on in the disease. This was
Diabetes (> 7.1) 5 3.42 supported by a study by Ruis et al. who found out that
Impaired (6.1–7) 8 5.48 early on in the course of type 2 diabetes, there is modest
Normal (< 6.1) 133 91.1 cognitive decline [39].
Mean ± SD 5.12 ± 1.52 The influence of pulmonary TB alone on cognitive de-
SD Standard deviation, DBP Diastolic Blood pressure, SBP Systolic Blood cline does not appear to be strong. A study published in
Pressure, 2HPP 2-h postprandial India in 2015 showed that cognitive impairment was sig-
nificantly higher among HIV patients with Pulmonary
Yorke et al. BMC Psychiatry          (2020) 20:143 Page 5 of 7
Table 2 Summary of Independent t-test for 2HPP and neuropsychological measures among newly diagnosed smear positive
tuberculosis patients at the Chest Clinic of the Korle-Bu Teaching hospital in Accra, Ghana, 2017
2HPP n M SD t df p
Cognitive Failures (CFQ) Normal 93 19.23 13.20 1.25 152 .202
Abnormal 61 16.61 11.86
Somatisation Normal 92 1.27 .81 −.38 152 .704
Abnormal 62 1.32 .77
Anxiety Normal 92 .55 .66 1.53 152 .106
Abnormal 62 .41 .48
Depression Normal 91 .52 .59 .68 151 .477
Abnormal 62 .46 .45
Phobic Anxiety Normal 92 .38 .60 2.03 149.7 .045
Abnormal 62 .23 .36
Perceived Psychological Distress (BSI-GSI) Normal 92 .65 .47 1.21 151.8 .229
Abnormal 62 .58 .30
Total Free Recall Normal 70 20.13 5.83 .87 105 .353
Abnormal 37 19.16 4.65
Short Delay Free Recall Normal 70 5.47 1.96 1.61 105 .120
Abnormal 37 2.12 1.61
Long Delay Free Recall Normal 68 4.76 2.02 1.03 102 .307
Abnormal 36 4.33 2.04
Cognitive Impairment (MOCA) Normal 84 17.26 5.98 2.10 132 .037
Abnormal 50 15.04 5.83
Quality of Life Normal 93 7.20 1.90 1.30 153 .197
Abnormal 62 6.82 1.59
p < .05 (2-tailed), Note: M Mean, SD Standard deviation, df Degree of freedom, BSI Brief Symptom Inventory, GSI Global severity index, MOCA Montreal Cognitive
Assessment, Abnormal Dysglyacaemia
Tuberculosis than in patients with HIV infection alone for diabetes, and 1.43 for having either prediabetes or
[40]. In the setting of non-clinically obvious systemic diabetes [44]. .Another study found modest cognitive de-
spread, especially among HIV patients, PTB may impact cline already present at the early stage of type 2 diabetes
on neurocognitive function [41, 42] through granuloma- [39]. The results of this study are preliminary and our
tous meningeal inflammation with the formation of ex- future study will employ more neuropsychological mea-
udate and adhesions, obliterative vasculitis, encephalitis sures and larger numbers to assess various domains of
or myelitis or hydrocephalus [7–9]. cognition, and compare any differences between those
with overt diabetes and prediabetes.
Prediabetes and cognitive decline
The dysglycaemia group included TB patients with pre- Phobic anxiety
diabetes who scored significant lower scores on cognitive Our study revealed that participants with dysglycaemia
tests. In a recent study published in 2017 [43], prediabe- had significantly lower scores on Phobic Anxiety com-
tes was associated with lower performance in memory in pared to those who had normal glucose levels. This
middle age and but a less steep decline in memory over means that participants with dysglycemia reported less
the follow-up period [43]. Also, the Confucius Home- phobic anxiety compared to those with normal glucose
town Aging Project, which was a cross-sectional study of levels. This finding however differs from other publica-
1528 participants conducted in Shandong province in tions, which found higher anxiety related symptoms in-
China, examined the association of diabetes and predia- cluding phobic anxiety associated with diabetes [45–47].
betes with cognitive impairment and depression among Differences in participant characteristics such as the
Chinese elderly people aged ≥60 years. Cognitive impair- relatively young age of subjects and a different setting of
ment and depression was found in 24.7 and 20.3% sub- the study may account for the observed differences in
jects respectively. The multiple adjusted odds ratio (OR) the findings. This must further be explored in subse-
of cognitive impairment was 1.61 for prediabetes, 1.38 quent studies.
Yorke et al. BMC Psychiatry          (2020) 20:143 Page 6 of 7
Future research Availability of data and materials
Future research must include extensive neuropsycho- The datasets used and/or analysed during the current study are available
from the corresponding author on reasonable request.
logical measures to assess various cognitive domains and
establish the severity and degree of cognitive decline that
Ethics approval and consent to participate
may impact treatment outcomes among TB patients. All patients provided written informed consent. Ethical and Protocol
Also since social, demographic and sanitary variables are approval for the study was sought from the College of Health Sciences
often implicated in psychological issues concerning TB Ethics and Protocol Review Committee of the University of Ghana with
reference number URF/9/ILG-076/2015–2016. It complied with the Helsinki
patients, these factors could be explored in the future Declaration of 1964 (Revised 2013) on human experimentation. Strict
studies as moderators/modulators of neurocognitive confidentiality of data and privacy for study participants were ensured. Data
function as well. was kept secured and was available only to the principal investigator.
Patients found to have dysglycaemia and/or psychological disorders were
referred for further assessment and possible treatment.
Conclusion
Our study is unique in examining the influence of dys- Consent for publication
Not applicable.
glyacaemia on cognitive performance among young
adults with TB. Newly diagnosed smear positive TB pa-
Competing interests
tients with dysglycaemia was associated with statistically The authors declare that they have no competing interests.
significantly lower mean cognitive scores than those with
normal glucose values. Also, patients with abnormal glu- Author details1Department of Medicine & Therapeutics, School of Medicine & Dentistry,
cose values was associated with statistically lower mean College of Health Sciences, University of Ghana, Legon, Accra, Ghana.
scores on phobic anxiety as compared to those who were 2Department of Medicine, Korle-Bu Teaching Hospital, Accra, Ghana.
3
normoglycaemic; and this finding must be further Department of Psychology, School of Social Sciences, College of
Humanities, University of Ghana, Accra, Ghana. 4Department of Social and
explored. Behavioural Sciences, School of Public Health, University of Ghana, Accra,
The study findings have implications TB management. Ghana. 5Department of Psychiatry, School of Medicine & Dentistry, College of
6
Among newly diagnosed smear positive patients, neuro- Health Sciences, Korle-Bu, Accra, Ghana. Centre for Ageing Studies, College
of Humanities, University of Ghana, Accra, Ghana.
psychological tests must be performed at diagnosis to ascer-
tain the presence or otherwise of any neuropsychological Received: 11 April 2019 Accepted: 25 March 2020
deficits. Any deficits identified should be promptly treated
to reduce its impact on the patient as well to improve treat-
ment outcomes. It is hoped that this will spur increased References
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