Comparison of Lipid Profiles in Pulmonary Tuberkulosis (TB)

Patients with and without Human Immunodeficiency Virus Infection

(HIV)

Novita Sari Tambunan1, Melati Silvanni Nasution2*

1
Student of Medical Faculty of Universitas Sumatera Utara
2
Department of Internal Medicine, Faculty of Medicine,University North Sumatra
H. Adam Malik Hospital, JalanBunga Lau No 17, Medan 20136, Indonesia.
*Correspondence: melatisilvanni@yahoo.com

Keywords : Pulmonary TB, HIV, Lipid Profile

Abstract : Pulmonary tuberculosis (TB) can co-occur with HIV. The inflammatory conditions that accompany
infection cause the release of free radicals and reactive oxygen species (ROS) which will affect the host
lipid profile (host) through increased lipid peroxidase. In patients who have TB and HIV infection there is a
decrease in serum LDL, HDL and total cholesterol concentrations. Meanwhile, low serum triglycerides were
found in TB and HIV positive patients compared to the control group. Hypocholesterolemia encourages the
development of TB while hypercholesterolemia leads to protection against TB with Mtb. This condition
needs to be considered because it can affect the prognosis of HIV coinfected TB. The purpose of this study
is to compare lipid profiles in TB patients with and without HIV infection This type of research is
comparatic analytic with cross sectional design. The data that will be used is secondary data taken from
medical records. The population of this study were all pulmonary TB tuberculosis patients with and without
HIV infection in HAM Medan General Hospital in January 2014 to October 2018 with 72 samples for each
group. Sampling using simple random sampling method. The data of this study were analyzed by
independent t test and Mann-Whitney U using statistical application. In this study it was found that
triglyceride levels were significantly higher in TB-HIV compared to TB and there were no significant
differences in LDL, HDL and total cholesterol.

1 INTRODUCTION Low total cholesterol, LDL and HDL

TB are susceptible to oxidative stress. In
pulmonary TB there is an increase in circulating
marker (marker) of free radical activity. Increased
ROS / Reactive Nitrogene Secondary Intermediate
occurs due to increased release of respiratory
phagocytes in the lungs. Increased ROS can
increase tissue injury and inflammation including
fibrosis of lung tissue. When tissue inflammation
occurs, inflammation will occur at the cellular
level. TG and LDL as the main components of cell
membranes, will be attacked quickly by ROS and
free radicals. TG and LDL that bind to cell
membranes will be catabolized by lipid peroxidase.
So that the loss of TG and LDL in this cell
membrane will be replaced by serum lipids. The
use of serum lipids will reduce serum lipid levels
as found in previous studies (Taparia et al., 2015).
concentrations were observed in active TB patients
compared to the control group in Etopia in line
with studies conducted in Turkey, Egypt and Benin
(Gebremicael et al., 2017). Infection with TB is
known to increase plasma TG levels by decreasing
the amount of circulating lipoprotein, a process
that is considered as a result of a reduction in
lipoprotein lipase (LPL) (Van der Geize et al.,
2007). The activity of the lipoprotein lipase
enzyme is also inhibited by increased production
of IFNγ, IL-6 and TNF α in fat tissue. While LPL
plays a role in the process of cleaning triglycerides.
So that through this process triglycerides increase.
This is in line with the research conducted by
Diani and Devi (2017), which found an increase in
triglycerides that form adipose tissue as the body's
most important fuel reserve.
In patients who have TB and HIV infection there is
a decrease in serum LDL, HDL and total
cholesterol concentrations. The lipid concentration
is lower compared to patients who only experience
TB. Meanwhile, low serum triglycerides were
found in TB-HIV compared to the control group.
However, the value is not much different from
serum triglyceride in TB (Gebremicael et al.,
2017).
Research shows that changes in lipid profile are a
consequence of TB disease and HIV infection, so
that if TB disease with HIV infection is treated
then the lipids will return to normal levels
(Mohamed and Hesham, 2012). But some studies
also suggest paying attention to lipid profiles. it is
known that hypercholesterolemia is a protective
factor of TB infection while hypocholesterolemia
can worsen the prognosis of TB, especially TB
with HIV infection (Wilson et al., 2003).
MATERIALS AND METHODS
This type of research is comparative analytic with
cross sectional design. The study was conducted at
the Adam Malik Haji Central Hospital with a study
population of all pulmonary TB patients with and
without HIV infection in HAM Medan Hospital in
January 2014 to October 2018. From all
populations, 72 samples met the inclusion criteria,
namely patients who have been diagnosed with
pulmonary TB with and without HIV infection and
have examined the lipid profile and exclusion
criteria, namely medical record data that does not
have a complete lipid profile examination results.
The research subjects were taken by simple
random sampling. The variables studied included:
1) patient characteristics (age, sex, education,
occupation); 2) lipid profile of TB patients with
and without HIV infection; 3) CD4; 4) ART used.
Statistical Analysis
Data were presented as mean ± SD. A statistical
analysis test was performed using the independent
T-test on data that were normally distributed (LDL
and total cholesterol) and Mann-Whitney U test on
data that were not normally distributed
(triglycerides and HDL) to assess the comparison
of lipid profiles in the TB and TB-HIV groups.
Two-sided p-values of less than 0.05 were
regarded as statistically significant. The data were
analyzed using SPSS software.
This research has received an Ethical Clearance
permit and was approved by the USU Medical
Faculty Ethics Commission.
RESULTS

Table 1. Distribution of frequency based on characteristics

TB-HIV TB
Sex n % n %
Man 50 69,4 53 73,6
Women 22 30,6 19 26,4
Age
15-19 1 1,4 1 1,4
20-29 13 18,1 2 2,8
30-39 21 29,2 10 13,9
40-49 15 20,8 18 25
≥50 22 30,6 41 56,9
Education
No school 1 1,4 1 1,4
Elementary school 5 6,9 9 11,1
Junior high school 9 12,5 8 12,5
High school 42 58,3 47 65,3
Bachelor 15 20,8 7 9,7
Job
Government employees 13 18,1 9 12,5
Private employees 9 12,5 5 6,9
Housewife 9 12,5 13 18,1
Student 1 1,4 0 0
Trader / Entrepreneur 20 27,8 27 37,5
 Etc 20 27,8 18 25
Total 72 100 72 100

Table 3. Comparison of mean lipid profiles in TB- though the average is in the optimal level. In
HIV and TB patients. addition, through the table above it is known that
the average lipid profile (LDL, HDL, total
Lipid Profile P cholesterol and triglycerides) in TB-HIV patients is
TB-HIV TB
(mg/dL) Value higher than TB. Based on the independent T test
LDL 102,22±41,48 94,96±43,61 0,308 LDL levels and total cholesterol were not
HDL 36,57±13,60 33,44±13,22 0,103
statistically different (p value> 0.05). While the
Total
cholesterol
159,35±47,61 149,99±51,47 0,259 Mann-Whitney U test on HDL and triglyceride
Triglycerides 131,28±68,74 109±57,01 0,026 levels found a significant difference in triglyceride
levels (p Value <0.05, p Value = 0.026) between
TB-HIV and TB patients. Triglyceride levels in
TB-HIV (131.28 ± 68.74) were significantly higher
Based on table 3 it can be seen that generally the compared with TB triglyceride levels (109 ±
lipid profile in TB-HIV or TB can be said to be 57.01). However, there was no significant
low even difference in HDL levels between TB-HIV and TB.

Table 4. Levels of lipid profile are based on absolute CD4 + value

Absolute
CD4+ (cell/ LDL HDL Total Cholesterol Triglycerides
(mg/dL) (mg/dL) (mg/dL) (mg/dL)

<200 100,88±42,48 32,08±11,62 154,62±52,81 124,04±60,72

200-349 85,36±35,52 34,73±14,74 146,36±52,78 126,45±38,41
350-499 98,38±38,91 37,5±18,23 158,38±54,08 119,88±51,07
≥500 115,55±46,29 44,91±11,79 176,18±37,30 190,45±116,89

Based on table 4 it can be seen that the increase in the average HDL and triglyceride levels is proportional to
the increase in CD4 + absolute. On average serum LDL and total cholesterol levels found an increase in serum
lipid levels in line with an increase in CD4 + at CD4 + ≥200.

Table 5. Level of lipid profile based on ART regiment.

Total
ART LDL HDL Triglycerides
cholesterol
Tenovofir+Lamivudine +Evafiren 94,42 33,63 150,42 105,42

Tenovofir+Emricitabin+Evafiren 115 40 149 52

Zidovudine+Lamivudine+Evafiren 116,71 42,86 181,71 132,29

Zidovudine+Lamivudine+Nevirapine 106,63 38,25 155 182,13

 Tenovofir+Lamivudine+Nevirapine 78,33
Based on table 5, it can be seen that the lipid profile of LDL, HDL and total cholesterol was the highest in the
use of Zidovudine, Lamivudine and Evafiren regimens of 116.71 mg/dL, 42.86 mg/dL, 181.71 mg/dL. The
highest lipid triglyceride profile was 182.13 mg/dL in the use of Zidovudine, Lamivudine and Nevirapine.
DISCUSSION
The results of this study indicate that men suffer
more from TB-HIV than women according to
research on the characteristics of TB-HIV patients
in the RSUP HAM in 2013-2015 conducted by
Talenta (2017). This is probably due to the large
number of men of productive age who work far
away from their families for quite a long time so as
to enable someone to be unfaithful to their partner.
This can be a risk factor that increases
transmission. The results of research conducted by
(Taparia et al., 2015) also showed the proportion
of male sex who suffered more TB compared to
women. According to (Kaur et al., 2013), the
diagnosis of TB in women is often late and the
attitude of women is less interested in going to
health services to check their health to be one of
the causes.
The most infected age group is the productive age
group (sexually active), which is 15-49 years. HIV
patients with a productive age are at high risk of co
infection because of their high mobility and
enabling contact with many people (Soemirat,
2011).
The proportion of TB patients is the most at the
senior secondary education level and the results of
this study are in line with the results of research
conducted by Apsari (2018). Research conducted
by Talenta (2017) also shows that the proportion of
TB-HIV is highest at the senior secondary level.
This study shows that TB infection and TB-HIV
can occur at all levels of education. Higher
education levels do not necessarily guarantee that
someone can take preventive measures against TB
and TB-HIV.
Low risk groups are housewives and students. This
is probably because a housewife is infected by a
man or her husband who has sex outside without
using a condom (Puspa, Y, 2010). Student groups
41,33 133 149
are also very likely to be exposed to TB-HIV and
TB because of their work and social environment.
This study is in accordance with previous studies
which found the most opportunistic infections
other than TB, namely oral candidiasis in patients
with HIV / AIDS in RSUP HAM (Yusri, A., 2012,
Elona, 2011). The high proportion of OC is caused
because this infection is the most common and
early manifestation as a sign of the onset of HIV
infection. Even stage 3 HIV infection has shown
symptoms of OC (Pohan, 2006). In addition, 50%
of the human oral cavity contains this fungus as a
normal microflora (Silverman, 2001).
Based on research data, it was also found that 30
(41.7%) patients had no opportunistic infections
other than TB. This does not mean that there is no
disease that accompanies HIV infection but
because the data taken is data on opportunistic
infections so that non-infectious diseases that
accompany TB-HIV are not included. In addition,
also because some TB-HIV patients have just been
diagnosed with HIV when retrieving data so that it
makes these patients experience opportunistic
infections because they are still in the early stages.
The results of this study show differences with the
research conducted by (Gebremicael et al., 2017).
The study showed significantly lower lipid profiles
(total cholesterol, LDL and HDL) in patients who
experienced TB-HIV than TB. While TB-HIV
triglycerides are higher than TB, but there is no
significant difference. The differences in the results
of this study with previous studies may be due to
the influence of the administration and duration of
use of drugs such as ART and OAT and
comorbidities where in the study by Gebremicael,
all of these criteria were excluded. While in this
study, researchers did not pay attention to
comorbidities and the average patient who entered
the study had received OAT and ART therapy.
Triglycerides and choleterol-LDL are the main
constituents of cell membranes (Liesuy and
Tomato, 1994). Cholesterol is needed by
lymphocytes in cytotoxic functions (Dabrowski et
al., 1980). The active lymphocyte subset recruits
macrophages and releases molecules such as
interferon, and tumor necrosis factors that make it
more efficient at killing Mtb (Kaul et al., 2004).
The inability of macrophages to phagocytose Mtb
due to the low cholesterol content in the cell
membrane further damages the body's defense
system against Mtb. The condition of
hypocholesterolemia and TB infection is very
related. In the study of Metwally and Raheem
(2012) found that Tuberculosis resulted in
hypocholesterolemia. This condition can increase
the severity of TB disease (Wilson, 2003).
The WHO in "Guidelines for Use of ART living
with HIV" suggests that fasting lipid profiles
should be examined at baseline, before patients
start ART. Then repeat checking fasting lipid
profiles in 3-6 months after ARV starts, and faster
for patients who have abnormal values at baseline.
Patients with normal lipid values must be re-
examined every year (faster if the ARV is
changed). Patients with dyslipidemia may require
more intensive monitoring (for example, every 4-6
weeks) until LDL goals are met, after which
monitoring every 4-6 months is sufficient.
Treatment of dyslipidemia usually involves a
multimodal approach, including diet and exercise
in all cases, drugs, lipid modification, and
consideration of changes in ARV treatment.
Research conducted by Kumar and Sathian (2011)
shows a strong correlation between CD4 + to
Triglycerides and LDL. LDL and triglyceride
levels increase with increasing CD4 +. But the
increase in HDL levels and total cholesterol is
inversely proportional to CD4 +. It seems that this
research is appropriate in terms of triglycerides and
LDL.
The Zidovudin + Lamivudin + Efaviren regimen
caused an increase in lipid profiles of LDL, HDL
and total cholesterol compared to other regimens.
WHO in the "Guidelines for the Use of ART living
with HIV" states that zidovudin-based regimens
can increase triglycerides and LDL and Efaviren
can increase triglycerides, LDL and HDL. This is
one of the factors that makes the Zidovudin +
Lamivudin and Efaviren regimens the highest
levels of lipid profiles (LDL, HDL and total
cholesterol) among the other regimens. In addition,
the effects of evafiren are almost similar to
nevirapine which can increase lipid profiles.
CONCLUSION
Low levels of lipid profiles (LDL, HDL, total
cholsterol and triglycerides) were found in groups
of TB-HIV and TB patients. There was no
significant difference in total cholesterol, HDL and
LDL in TB-HIV patients compared to TB (p
value> 0.05). However, triglycerides were
significantly higher in TB-HIV patients compared
to TB (p value = 0.026). The difference in lipid
profile may be due to the use of OAT, ART and the
duration of use of these drugs.
Conflict of Interests
The authors declare that there is no conflict of
interests regarding the publication of this paper.
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