ПАРАЗИТОЛОГИЯ, 2020, том 54, № 6, с. 504-513.
УДК 576.895.2 / 576.32/.36
LEVEL OF IFN-Γ, TNF-Α, AND IL-10 AMONG SUDANESE
INFECTED BY MALARIA PARASITE
© 2020 S. E. A. Al Sayeda,*, A. H. Malika, H. A. Musab
a Department of Medical Parasitology, Faculty of Medical Laboratory Sciences,
The National Ribat University Khartoum, Sudan
b Department of Microbiology, Faculty of Medicine, The National Ribat University,
Khartoum, Sudan
* e-mail: alshoag333@yahoo.com
Received 22.08.2020
Received in revised form 12.10.2020
Accepted 19.10.2020
Malaria still remains one of the oldest documented diseases of humans in the world. This study
was aimed to measure the concentration of cytokine levels (IFN-γ, TNF-α, IL-10) in Sudanese malarial
patients in serum specimens. 148 malaria positive patients were included in this study. The specimens
were collected from three different areas: Kosti, Al-Greif Sharq, and El-Jayli Area. All specimens
were examined using both blood films and ICT Pf/Pan. The overall mean of parasite counts were 22.36
x 109 parasite/L. After 14 days 54 of the participants returned back for follow up after completion
of the anti-malarial treatment and the same previous tests were repeated again. 70 participants were
selected to measure the concentration of cytokines according to the inclusion and exclusion criteria
of the study. They were classified into two groups endemic and non-endemic and compared to their
corresponding control groups and to the treated participants. The mean levels of IFN-γ, TNF-α, and
IL-10 in serum of malarial patients from non-endemic area, was 59.94 pg/mL, 42.78 pg/mL, and
109.87 pg/mL respectively. The mean level of IFN-γ, TNF-α, and IL-10 in the serum of the malarial
patients from the endemic area, was 14.26 pg/mL, 52.26 pg/mL, and 131.99 pg/mL respectively.
IFN-γ and IL-10 showed a higher concentration when compared to a healthy control group (IFN-γ:
E: p = 0.040/NE: p < 0.000; IL-10: p < 0.000 for both areas). Also showed higher concentrations
when compared to the treated groups in both areas (IFN-γ: p = 0.010; IL-10: p < 0.000; TNF-α: E: p =
0.760/NE: p = 0.650). In the opposite TNF-α showed a significant difference with lower concentration
when compared to the healthy group in both areas (p < 0.000). In this study both pro-inflammatory
(IFN-γ, TNF-α) and anti-inflammatory (IL-10) cytokines for both endemic and non-endemic areas
were elevated during infection and both decreased after treatment.
Keywords: Malaria, IFN-γ, TNF-α, IL-10, cytokines, Sudan, ICT Pf/Pan
DOI: 10.31857/S1234567806060048
504
Malaria is one of the most common diseases in the world. More than half the world
population lives in malaria infected areas specially in Sudan where the latest WHO data
published in 2017, reported that the number of malaria cases was 1305000 and the number
of deaths reached 3,471 (Malaria in Sudan, 2017). Although it is a treatable disease, it has
severe and may be deadly complications like cerebral malaria if doesn’t treated (Centers for
Disease Control…, 2015). There are many reviews about the relation between the clinical
symptoms that caused by malaria parasite and the imbalance between cytokines that can
lead to serious complications with regard to the main function of them by activating the
effective molecules that kill malaria parasite (Perlmann, Troye-Blomberg, 2002; Nmorsi et
al., 2010; Perera et al., 2013). However sometimes the over production of certain cytokines
may lead to a serious deadly complications (Mandala et al., 2017). This concept can be
used to minimize the complication of malaria by using them in vaccine, immunotherapy,
or as diagnostic markers (Angulo, Fresno, 2002). In order to determine how cytokines vary
with disease severity and syndrome, a study enrolled in the year 2017 in Malawian children
presenting with cerebral malaria (CM), severe malarial anaemia (SMA) and uncomplicated
malaria (UCM), with healthy controls. They analyzed serum cytokines concentrations in acute
infection, and in convalescence. With the exception of IL-5, cytokine concentrations were
highest in acute CM, followed by SMA, and were only mildly elevated in UCM. Cytokine
concentrations had fallen to control levels when re-measured at one month of convalescence
in all three clinical malaria (Mandala et al., 2017). In endemic area of Brazil there was
study that aimed to characterize alterations in haematological patters and circulating plasma
cytokines and chemokine levels in patients infected with Plasmodium vivax or Plasmodium
falciparum during the acute and convalescent phases of infection whom compared with
a healthy control. Thrombocytopenia, eosinopaenia, lymphopaenia and an increased number
of band cells were observed in the majority of the patients during acute phase which returned
to normal values at convalescent phase. This study was found a significantly higher for both
P. vivax and P. falciparum patients of interleukin (IL)-6, IL-8, IL-17, interferon gamma
(IFN-γ), tumour necrosis factor alpha (TNF-α), macrophage inflammatory protein-1β and
granulocyte-colony stimulating factor levels than controls during acute phase which maintained
high levels during the convalescent phase. IL-10 was detected at high concentrations during
the acute phase, but returned to normal levels during the convalescent phase (Rodrigues-
da-Silva et al., 2014). In Nigeria Nmorsi et al. (2010) examined the array of some pro- and
anti-inflammatory cytokines, namely, interleukin-4 (IL-4), interleukin-10 (IL-10), interferon-γ
(IFN- γ), interleukin-5 (IL-5), interleukin-6 (IL-6), interleukin-12 (IL-12) and tumor necrosis
factor-α (TNF- α) concentrations in some Nigerians with falciparum malaria. They concluded
that IL-4, IL-5, IL-6, IL-10, IL-12, TNF-α, and IFN-γ are involved in the immune-pathology
and immune-regulation of uncomplicated and complicated malaria infections. IL-6, IL-12,
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IFN-γ and IL-10 depressed in complicated/severe malaria may not provide any protective
immunity and may be indicators of poor prognosis in Plasmodium falciparum infected
Nigerian children. In this study is meant to look for the levels of some cytokines in the
serum of Sudanese.
MATERIALS AND METHODS
This is a case control study conducted in three famous areas known to have a high prevalence of
malaria. The study was approved by the Ministry of Health and The National Ribat University ethical.
One hundred forty eight malaria positive patients recruited from the medical center in Aljraif East (n =
40), the medical center in El-Jayli (n = 23) area (Non-endemic areas/NE), and malaria center in Kosti
(n = 85) (Endemic area/E) during period 2015 to 2018. Ninety four of the participants were males
and fifty four were females. All samples were collected under special criteria: patients diagnosed as
having malaria, permanent resident in the study area, not taking anti-malarial drug at least 2 weeks,
free from other common infectious diseases, and willing to be involved in the study by signing a
consent form. All specimens were diagnosed by both Giemsa stained thick-thin blood film (10 % v/v)
and ICT Pf/Pan (Healgen Malaria Pf/Pan One Step Rapid Test). The parasite density was determined
per µL of blood by counting the asexual form of them against TWBCs.
Serum was obtained the collected blood in plain vacutainer tube to measure the cytokines. The levels
of cytokines (TNF-α, IFN-γ, and IL-10) were measured by sandwich ELISA kit (biolegend/ ELISA
MAX™ Deluxe Sets). Each cytokine included with standard curve as directed by the manufacture
that started from top standard concentration (IFN-γ: 500 pg/mL, TNF-α: 500 pg/mL, and IL-10 250
pg/mL) then six two fold serial dilutions of these top standard which run by ELISA parallel with the
specimens. The absorbance of the ELISA was read by spectrophotometer at 450 nm within 15 minutes.
Using Graph Pad Prism 7 program the standard curve was plotted with analyte concentration on the
x-axis and absorbance on the y-axis. After 14 days all the steps of diagnosis were repeated for the
0.050 as significant values using Microsoft Office Exel 2007.
RESULTS
The overall mean of parasite counts were 22.36 x 109 parasite/L. The mean of parasites
count in endemic area was 30.46 x 109 parasites/L and in the non-endemic area 13.28 × 109
parasites/L. The most prevalent Plasmodium species was P. falciparum 93.24 % (n = 138),
then mixed infection of P. falciparum + P. malariae as 3.38 % (n = 5), and both P. vivax
alone and mixed infection of P. falciparum + P. vivax with the same percentage 1.35 %
(n = 2), and finally P. malariae alone was 0.68 % (n = 1) (fig. 1).
After fourteen days 54 of the participants returned back for follow up after completion
of the anti-malarial treatment and the same previous tests were repeated again. 85.19 %
(n = 46) of participants were free of malaria parasite and the parasiteamia of 14.81 % (n =
8) was decreased significantly to 0.03 × 109 parasite/L (p < 0.000).
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Figure 1. The percentages of the detected Plasmodium species: P. f - Plasmodium falciparum,
P. m - P. malariae, P. v - P. vivax.
Seventy participants were selected to measure the concentration of cytokines (IFN-γ,
TNF-α, IL-10) in serum according to the inclusion and exclusion criteria of the study. They
were classified into two groups according to the endemicity of malaria parasite at these
areas (endemic and non-endemic) and compared to their corresponding control groups and
to the treated participants.
The group from non-endemic area was thirty three that compared to twenty participants
of control group and twelve of the treated participants. The mean levels of IFN-γ, TNF-α,
and IL-10 in serum of patients from non-endemic area before anti-malaria treatment was
59.94 pg/mL, 42.78, and 109.87 pg/mL respectively. All values of the cytokines in the
serum of the malaria infected group showed significant difference when compared to the
control group. The levels of the cytokines in the control group as follows: IFN-γ 6.57 pg/mL
(p < 0.000), TNF-α 70.22 pg/mL (p < 0.000), and IL-10 1.16 pg/mL (p < 0.000). After anti-
malarial treatment the level of the cytokines showed variations as follow: IFN-γ decreased
significantly to 9.99 pg/mL (p = 0.010), TNF-α decreased insignificantly to 41.88 pg/mL
(p = 0.650), and IL-10 decreased significantly to 5.02 pg/mL (p < 0.000) (table 1).
The group from endemic area was thirty seven that compared to twenty four participants
of the control group and eighteen as a group of after treatment. The mean level of the IFN-γ,
TNF-α, and IL-10 of the patients from the endemic area before anti-malarial treatment
was 14.26 pg/mL, 52.26 pg/mL, and 131.99 pg/mL respectively. The mean level of the
507
cytokines of the control group (IFN-γ, TNF-α, IL-10) was 9.62 pg/mL, 117.06 pg/mL, 1.51
pg/mL respectively. There was a significant difference between the patients and the control
group as follows: IFN-γ (significant, p = 0.040), TNF-α (significant, p < 0.000), and IL-10
(significant, p < 0.000) (table 2).
After the anti-malarial treatment the cytokines showed variations as follow: IFN-γ was
decreased significantly (7.90 pg/mL, p = 0.010), TNF-α was decreased insignificantly (51.84
pg/mL, p = 0.760), and IL-10 was decreased significantly (3.91 pg/mL, p < 0.000) (table 3).
There is a significant difference between cytokines of endemic and non-endemic sera
of healthy control as follows: IFN-γ: p = 0.010, TNF-α: p < 0.000, and IL-10: p = 0.010
(table 4).
Table 1. Mean of cytokines levels in the non-endemic area
Patients
Control (n = 20)
Cytokines
Before treatment
After treatment
P-vales
Cytokines
P-vales
(n = 33)
(n = 12)
level
IFN-γ
59.94
9.99
0.010
6.57
< 0.000
TNF-α
42.78
41.88
0.650
70.22
< 0.000
IL-10
109.87
5.02
< 0.000
1.16
< 0.000
Table 2. Comparison of the mean cytokines levels (pg/ml) in the serum between the patients
and controls in the endemic area
Cytokines
Patients (n=37)
Control (n=24)
P-vales
IFN-γ
14.26
9.62
0.040
TNF-α
52.26
117.06
< 0.000
IL-10
131.99
1.51
< 0.000
Table 3. The difference in the mean cytokines levels in serum (pg/ml) after treatment
in the endemic area
Cytokines
Before treatment (n=37)
After treatment (n=18)
P-vales
IFN-γ
14.26
7.90
0.010
TNF-α
52.26
51.84
0.760
IL-10
131.99
3.91
< 0.000
Table 4. Comparison of the mean cytokines levels in serum of healthy control among
non-endemic and endemic areas
Cytokines
Non-Endemic Areas
Endemic Areas
P-value
IFN-γ
6.57
9.62
0.010
TNF-α
70.22
117.06
<0.000
IL-10
1.16
1.51
0.010
508
DISCUSSION
Malaria is one of the most common diseases in Sudan. The World Health Organization -
WHO published data in 2017 reporting the rate of total death due to malaria was 1.30 %
(Malaria in Sudan, 2017). Now a days there are many trials to eradicate this disease and their
complications permanently (Pan American Health Organization / World Health Organization —
PAHO/WHO, 2018; WHO, 2018). These complications are shared between parasites and/or
immune responses where the cytokines are one of them (Medina et al., 2011). This study
aimed to measure the concentration of cytokines levels (IFN-γ, TNF-α, IL-10) in Sudanese
malarial patients in serum samples.
During infection there are several pro-inflammatory cytokines like IFN-γ and TNF-α
induced by many inflammatory cells like Th1 cells, CD8+ cells, NK cells, and macrophage.
These cytokines are stimulated by malarial antigens leading to elimination of parasite or
immuno-pathological effects in case of persistent response (Goldsby et al., 2002; Khan, 2008;
Medina et al., 2011). In contrast the anti-inflammatory cytokines like IL-10 which induced
by Th2 cells mainly and other inflammatory cells inhibit the pro-inflammatory cytokines
(Couper et al., 2008; Akdis et al., 2016). As seen in this study both pro-inflammatory (IFN-γ,
TNF-α) and anti-inflammatory (IL-10) cytokines in serum for both endemic and non-
endemic areas were elevated during infection and both were decreased after cure maintaining
the balance between them (pro/anti-inflammatory) as reported by Rodrigues-da-Silva et al.
(2014) to avoid any immuno-pathological effects that mentioned by Medina et al. (2011).
These cytokines showed significant difference to IFN-γ and IL-10 (endemic IFN-γ: p = 0.040;
non-endemic IFN-γ: p < 0.000; IL-10: p < 0.000 for both areas) with higher concentrations
when compared to healthy control group which agreed with Mandala et al. (2017), Medina
et al. (2011), and Tatfeng, Agbonlahor (2010). Also the concentrations were higher when
compared to the treated group in both areas (IFN-γ: p = 0.010; IL-10: p < 0.000) which
agreed again with Mandala et al. (2017). TNF-α showed insignificant difference with higher
concentration when compared to treated group (endemic area: p = 0.760; non endemic-area:
p = 0.650) which agreed with a previous studies in elevation but not in significance. But
this result agreed with Gandapur, Malik (1996) where the difference between the levels
of TNF-α cytokine showed insignificant higher concentration in severe malaria than mild
one and suggested that the population has some degree of immunity. Also they reported
that the young trophozoite may be microscopically undetectable which support the positive
correlation between parasite count and concentration of TNF-α in their study. TNF-α showed
significant difference with lesser concentration in healthy group in both areas (p < 0.000)
which disagreed with previous studies, where the TNF-α as pro-inflammatory cytokines
should be increased during infection for protection to be higher than healthy one. But the
inhibition of production of TNF-α is reported by many authors to be due to many possible
509
factors that act as anti-TNF-α during infection. Some microbes can act as immunosuppressive
by enhancing production of IL-10 leading to decreasing in neutrophil counts and tumor
necrosis factor α level (Hellgren et al., 2009). Another reason for this concept, the co-infection
with some helminthes can modulate the immune response to malarial parasites by making
more anti-inflammatory cytokines (IL-10) (Hartgers et al., 2009). Also the co-infection with
Gram negative enteric bacilli can inhibit the production of TNF-α. This organism may be
related to counter regulatory activities of IFN-induced increased nitric oxide (NO) that down
regulate nitric oxide synthase (NOS) inducing cytokines, such as TNF-α, through a feedback
mechanism (Davenport et al., 2016). The co-infection with HIV leading to depletion in CD4,
CD8 and lowered serum levels of immunological mediators (Tatfeng, Agbonlahor, 2008).
There are some foods which naturally inhibit the production of TNF-α like fatty fish, red
fruits, tomatoes, red meat, nutritional yeast, honey, caffeine, dates, lactoferrin, ginger, Hibiscus
sabdariffa (Karkadι) (Fakaye, 2008; Isa et al., 2008; Cohen, 2018). Beside that there are
certain drugs can suppress TNF-α like aspirin, artemisinin, erythromycin, and paracetamol
(Brandts et al., 1997; Schultz et al., 1998; Wang et al., 2011; Lutgen, Munyangi, 2018).
During the disease the rate of consumption of patients may be reduced leading to reduction
in expression of mRNA of TNF R2 in muscle (Hofmann et al., 1994). Finally the presence
of certain genes can inhibit the expression of TNF-α (Mendonça et al., 2014). Beside that,
there are other factors which increase production of TNF-α as seen in healthy control people
like a long exposure to sun-light which contain UV-A irradiation that induces synthesis of
IL-6 and TNF-α (Avalos-Diaz et al., 1999). Also the consumption of large amount of caffeine
(coffee) can increase the level of TNF-α; and insufficient ingestion of fruit or vegetables
may increase the TNF-α (Cohen, 2018). The continuous exposure of the immune system to
malaria parasite leads to a high concentration of cytokines. That was obvious in the detected
levels of the cytokines from the healthy candidates in the endemic area when compared to
those from the non-endemic one. The difference was significantly higher in those from the
endemic area (IFN-γ: p = 0.010, TNF-α: p < 0.000, IL-10: p = 0.010). Also this was true
about parasite counts (endemic area: 30.46 × 109 parasites/L; non-endemic area: 13.28 ×
109 parasites/L) which agreed with Wroczyńska et al. (2005).
CONCLUSION
In this study both pro-inflammatory (IFN-γ, TNF-α) and anti-inflammatory (IL-10)
cytokines in serum for both endemic and non-endemic areas were elevated during infection
and both decreased after cure maintaining the balance between them (pro/anti-inflammatory)
to avoid any immuno-pathological effects.
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ACKNOWLEDGEMENT
We are grateful to The National Ribat University and Prof. Moawia M. Mukhtar from
The Institute of Endemic Diseases-Khartoum University for providing some facilities for
this work. We would also like to acknowledge the personnel in the health centers for their
great help in the collection of the specimens.
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УРОВЕНЬ ЦИТОКИНОВ IFN-γ, TNF-α, and IL-10 В КРОВИ СУДАНЦЕВ,
ИНФИЦИРОВАННЫХ МАЛЯРИЙНЫМ ПАРАЗИТОМ
Аль Сайед С. Е. А., Малик А. Х., Муса Х. А.
Ключевые слова: малярия, IFN-γ, TNF-α, IL-10, цитокины, Судан, ICT Pf/Pan тест
РЕЗЮМЕ
Малярия по-прежнему остается одной из старейших зарегистрированных в мире болез-
ней человека. Целью предлагаемого исследования является измерение уровней концентрации
цитокинов (IFN-γ, TNF-α, IL-10) в образцах сыворотки крови у больных малярией пациентов
в Судане. Всего было изучено 148 больных малярией пациентов. Образцы сыворотки были
собраны в трех различных регионах Судана: г. Кости, Аль-Грейф Шарк и территория возле
г. Эль-Джайли. Все образцы были изучены с использованием как мазков крови, так и мето-
да иммунной хроматографии (тест Pf/Pan). Среднее число паразитов в образцах составило
22.36 × 109 паразитов на 1 л. Через 14 дней 54 пациента, лечившихся от малярии, были вновь
исследованы с применением вышеописанных методов. 70 пациентов были отобраны для изме-
рения концентрации цитокинов согласно критериям включения и исключения, использованных
в работе. Эти пациенты были разделены на две группы (из эндемичных и не эндемичных по
малярии районов), данные по которым сравнивали с соответствующими контрольными груп-
пами и с данными по пациентам, подвергавшимся лечебным процедурам. Средний уровень
концентрации цитокинов IFN-γ, TNF-α и IL-10 в сыворотке крови больных малярией из не
эндемичных районов составили соответственно 59.94 пг/мл, 42.78 и 109.87 пг/мл. Средний
уровень концентрации цитокинов IFN-γ, TNF-α и IL-10 в сыворотке крови больных малярией
из эндемичных районов составили соответственно 14.26 пг/мл, 52.26 и 131.99 пг/мл. IFN-γ
и IL-10 характеризовались более высоким уровнем концентрации в сравнении с контрольной
группой здоровых пациентов (IFN-γ: E: p = 0.040/NE: p < 0.000; IL-10: p < 0.000, для обоих
регионов). Более высокую концентрацию наблюдали и при сравнении с группами лечившихся от
малярии пациентов из обоих регионов (IFN-γ: p = 0.010; IL-10: p < 0.000; TNF-α: E: p = 0.760/
NE: p = 0.650). Кроме того, цитокин TNF-α достоверно отличался более низкой концентрацией
при сравнении с группой здоровых пациентов в обоих регионах (p < 0.000). Согласно нашим
данным, концентрация как про-воспалительных (IFN-γ, TNF-α), так и противовоспалительных
(IL-10) цитокинов у пациентов из эндемичных и неэндемичных регионов повышалась при за-
ражении малярией и понижалась после проведения лечебных процедур.
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