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Journal of Nutrition & Intermediary Metabolism
journal homepage: www.elsevier.com/locate/jnim
Beneficial effects of an aqueous ginger extract on the immune system cells
and antibodies, hematology, and thyroid hormones in male smokers and
non-smokers
Sawsan Hassan Mahassni
∗
, Oroob Abid Bukhari
Department of Biochemistry, Faculty of Science, King Abdulaziz University, Jeddah, Saudi Arabia
HIGHLIGHTS
•Extract had different effects on immune components in smokers and non-smokers.
•Smokers and non-smokers benefited from enhancement of the thyroid gland.
•Enhancement of RBC counts and hemoglobin levels in smokers. Thus, ginger may be beneficial for smokers with anemia.
•Non-smokers had enhanced IgM levels. This may lead to a stronger antibody response against infections.
•Therefore, the extract had benefits for both smokers and non-smokers.
ARTICLE INFO
Keywords:
Aqueous ginger extract
Immune system cells
Antibodies
Thyroid hormones
C-reactive protein
Thyroxine
Triiodothyronine
Thyroid-stimulating hormone
Hematology
Smokers
Non-smokers
Males
ABSTRACT
The ginger rhizome is widely used for the treatment of diseases and conditions, such as inflammatory and
respiratory ailments, which are prevalent in smokers. This study is the first study of the effects of an aqueous
ginger extract on the immune system cells and antibodies, thyroid hormones, and hematology in smokers
compared to non-smokers. An aqueous ginger extract was administered to 68 male Saudi healthcare workers (33
smokers and 35 non-smokers) daily for 21 days. Blood samples were collected before and after the experimental
period to determine the complete and differential blood counts; and concentrations of C-reactive protein, IgG,
IgM, and thyroid hormones. Results showed that before consumption of the extract, smokers had a significantly
lower mean neutrophil count and higher mean red blood cell (RBC) count compared to non-smokers. At the end
of the experimental period, compared to non-smokers, smokers had a significantly higher mean lymphocyte and
RBC counts, and hemoglobin concentration; and a significantly lower mean neutrophil count, and IgM and
thyroid stimulating hormone concentrations. In conclusion, the extract had different effects on cells and anti-
bodies of the immune system in smokers and non-smokers, although both benefited from enhancement of the
thyroid gland. Smokers experienced increases in mean RBC counts and hemoglobin levels, thus ginger may be
beneficial for smokers with anemia. Non-smokers had increased mean IgM levels, which may lead to a stronger
antibody response, or humoral immunity, against infections. Therefore, the aqueous ginger extract had benefits
for both smokers and non-smokers.
1. Introduction
Tobacco use is estimated to kill more than 7 million active and
passive smokers annually, mainly in middle- and low-income countries
[1]. Cigarette smoke is known to have thousands of toxic and carci-
nogenic compounds that affect nearly all systems of the body and lead
to increased mortality and risk for heart diseases, stroke, pulmonary
diseases, cardiovascular diseases, dyslipidemia, blood vessel diseases,
lung cancer and other types of cancers [2]. The immune system is one of
the systems affected in smokers as evidenced by the fact that smokers
are more prone to infections and tend to have more severe symptoms
when sick [2]. Findings of studies [3–5] on the effects of smoking on the
immune system are contradictory, with some studies showing inhibi-
tion or enhancement of certain functions or components of the immune
system, while other studies showing no effects. Additionally, many
studies [4,6] have found increased levels of inflammatory cells, such as
https://doi.org/10.1016/j.jnim.2018.10.001
Received 16 July 2018; Received in revised form 17 October 2018; Accepted 17 October 2018
∗
Corresponding author.
E-mail address: sawsanmahassni@hotmail.com (S.H. Mahassni).
Journal of Nutrition & Intermediary Metabolism 15 (2019) 10–17
Available online 18 October 2018
2352-3859/ © 2018 Published by Elsevier Inc. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/BY-NC-ND/4.0/).
neutrophils, lymphocytes, and others, in smokers compared to non-
smokers.
Many studies have been done on the role of natural foods, nutrients,
herbs, and vitamins in strengthening the immune response and coun-
teracting the effects of stress and unhealthy lifestyles such as smoking.
Many diseases and conditions, such as inflammation, cancer, arthritis,
atherosclerosis, and many others, may be modulated or influenced by
different foods and nutrients. Therefore, it is worthwhile to find foods
that help decrease the damaging effects of smoking on smokers. Ginger
is known to contain many very beneficial components with enhancing
effects on respiratory ailments, health in general, and the immune
system, thereby leading to a stronger resistance to infections and an
enhanced response to diseases [7].
The ginger (Zingiber officinale Roscoe, Zingiberaceae) rhizome con-
tains many bioactive substances, including minerals, nutrients, vita-
mins, and antioxidants that are responsible for its many health-related
effects. Ginger is very widely consumed worldwide as a food condiment
and it has been used for thousands of years in folk, alternative, and
ayurvedic medicines. Many studies have shown ginger to be safe to
consume in both humans and animals with no harmful side effects and
no increased mortality [8], although neither its mode of action nor its
safety in the body is fully known [9,10]. Some uses of ginger and its
components are in the treatment or inhibition of many ailments and
conditions, such as inflammation, platelet aggregation, vomiting,
swelling, pain, hypertension, dyslipidemia, cardiovascular diseases,
oxidative damage, diabetes, nausea, colds, asthma, allergies, migraines,
arthritis, hypertension, and some cancers [11–14]. It has also been re-
ported to help with thyroid function and disease, and to have anti-in-
flammatory and antioxidant properties, which are linked to many dis-
eases and explain the ability of ginger to treat inflammation and
inflammation-related ailments and conditions [13,14].
Saudi Arabia is a major importer of tobacco products and has a high
prevalence of tobacco use. Saudi healthcare workers and medical and
healthcare students have a surprisingly high prevalence of smoking
[15–17]. Although many smokers are aware of the harmful effects of
cigarettes, they continue to smoke. Ginger is recommended and is
commonly used locally, among other uses, as a natural agent for alle-
viating the negative effects of smoking on the lungs and the immune
system, although this has not been proven scientifically.
Therefore, the aims of this study were to use an aqueous ginger
extract as a natural approach to attempt to mitigate the harmful effects
of smoking in male hospital healthcare workers and to clarify its effects
on the immune system and thyroid hormones in smokers compared to
non-smokers. An extensive search in the internet showed no research
studies on the effects of aqueous ginger extracts on the immune system
and thyroid hormones in smokers compared to non-smokers. Therefore,
this study is the first one to study these effects in smokers versus non-
smokers. The effects of an aqueous ginger extract on cells of the innate
(neutrophils, eosinophils, basophils, and monocytes) and acquired
(lymphocytes and antibodies) immunities, thyroid hormones (thyroxine
(T4), triiodothyronine (T3), and thyroid-stimulating hormone (TSH)),
C-reactive protein (CRP), red blood cells (RBC), hemoglobin, and pla-
telets in the blood of smoker and non-smoker male healthcare workers
were determined. This may help in clarifying the effects of ginger on the
immune system, inflammatory cells (WBCs and their types), markers of
inflammation (CRP and WBCs), thyroid hormones, and general health
of male smokers compared to non-smokers.
2. Materials and methods
2.1. Subjects
Subjects recruited for this study were 68 Saudi males working at
King Abdullah Medical Complex and living in Jeddah, Saudi Arabia
with an age range of 24–38 years. All subjects were healthy and none of
them were suffering from any allergies or chronic, hereditary, or
immune diseases nor taking any medications on a regular basis.
Subjects signed a consent form and they were instructed to fill a daily
follow-up schedule to confirm that they took the ginger extract daily for
21 days. Ethical approval for the study was provided by the King
Abdullah Medical Complex.
2.2. Preparation and administration of the ginger extract
The aqueous ginger extract was prepared according to the method
used locally. Ginger root (4 kg) was peeled, grated, and then boiled in
water (15.75 L) for 45 min. Subsequently, the extract was left overnight
at room temperature. The extract was then filtered to remove the grated
ginger, after which the extract was frozen as cubes of 8.3 g each at
−18 °C.
Each participant was instructed to ingest one cube of ginger extract
at the same time daily for 3 weeks, by thawing the cube in any warm
drink, such as tea, coffee, or warm water.
2.3. Blood sampling and processing
Blood samples were collected from all subjects the day before the
beginning of the experiment and the ingestion of the first ginger dose
(initial sample), and on the day after the last dose and the end of the
experiment (final sample). Blood samples were collected in EDTA va-
cutainer tubes for the differential CBC analysis, and in plain vacutainer
tubes for the determination of thyroid hormones and antibodies con-
centrations. Blood samples collected in plain tubes were allowed to
form a clot after which serum was obtained by centrifugation at
5000 rpm for 10 min. Serum was stored, for a maximum of one week, at
−40 °C for use later. Lithium heparin tubes were used for the CRP
concentrations, where whole blood was left for some time, after which
the tubes were centrifuged at 1500 rpm for 10 min. These samples were
stored at −20 °C until the analysis was performed.
2.4. Differential and complete blood count
The differential and complete blood counts (CBC) were done on an
ADVIA 2120i Hematology System with Autoslide (Siemens Company,
Phnom Penh, Cambodia) at the King Abdullah Medical Complex,
Jeddah, Saudi Arabia. The chemicals used were the 1850 CBC/Difftests
(Blue Opportunity Medical Company, Phnom Penh, Cambodia) as
specified for the instrument.
2.5. Determination of T3, T4, and TSH concentrations
The concentrations of T3, T4, and TSH were determined on a Cobas
e 411 Analyzer (Hitachi High-Technologies Corporation, Tokyo, Japan)
at King Fahad Hospital Jeddah, Saudi Arabia. The reagents used were
the Roche Diagnostic reagents (Mannheim, Germany) as recommended
for the instrument used.
2.6. Determination of IgG, IgM, and CRP concentrations
The serum concentrations of IgG and IgM antibodies, and CRP were
determined by using the ARCHITECT c8000 System (Abbott
Laboratories Inc., IL, USA) at King Fahad Hospital, Jeddah, Saudi
Arabia. The reagents used for the determination of the antibodies
concentrations were the Immunoglobulins G and M assays (Abbott,
Green Oaks, Illinois, USA) which were used according to the manu-
facturer's instructions. For the determination of CRP concentrations, the
MULTIGENT CRP Vario assay (Randox Company, Milan, Italy), which is
a latex immunoassay, was used according to the manufacturer's in-
structions.
S.H. Mahassni, O.A. Bukhari Journal of Nutrition & Intermediary Metabolism 15 (2019) 10–17
11
2.7. Statistical analysis
The Megastat statistical program (version 9.4) was used to obtain
descriptive and analytical statistics for the data. The minimum and
maximum values, mean, standard deviation ( ± SD), and standard error
of the mean ( ± SE) were determined for all parameters. The P value
was calculated to determine the significance of the differences between
smokers and non-smokers, using the t-test for the normally distributed
parameters and the Mann-Whitney Utest for the none normally dis-
tributed parameters. As for the comparison between the initial and final
samples for smokers and non-smokers, separately, the paired t-test was
used for the normally distributed parameters and the Wilcoxon t-test
was used for the none normally distributed parameters. A significant
difference is a P value less than 0.05 and a highly significant difference
is a P value less than 0.01.
3. Results
3.1. Subjects of the study
Of the 68 subjects recruited for the study, 33 were smokers and 35
were non-smokers. The median age for smokers was 30 years and for
non-smokers 29 years.
3.2. Comparing smokers and non-smokers for the initial and final blood
samples
3.2.1. Differential and complete blood counts
For the initial blood samples (Table 1), the mean WBC, lymphocyte,
monocyte, eosinophil, basophil, and platelet counts; and the mean he-
moglobin concentrations for smokers compared to non-smokers were
not significantly different. On the other hand, smokers had a sig-
nificantly lower mean neutrophil count and a highly significantly
higher mean RBC count compared to the respective means in non-
smokers.
As for the final blood samples (Table 2), there were no significant
differences between smokers and non-smokers for the mean WBC,
monocyte, eosinophil, basophil, and platelet counts. On the other hand,
smokers had a significantly lower mean neutrophil count, significantly
higher mean lymphocyte count, and highly significantly higher mean
RBC count and hemoglobin concentration compared to the respective
means in non-smokers.
3.2.2. Concentrations of IgG and IgM antibodies, CRP, and thyroid
hormones
For the first blood samples (Table 3), there were no significant
differences between smokers and non-smokers for the mean IgG, IgM,
CRP, TSH, T4, and T3 concentrations. As for the final blood samples
(Table 4), there were no significant differences between smokers and
non-smokers for the mean IgG, CRP, T4, and T3 concentrations. On the
other hand, compared to non-smokers, smokers had a highly sig-
nificantly lower mean IgM and TSH concentrations.
3.3. Comparing the initial and final blood samples in smokers and non-
smokers
3.3.1. Differential and complete blood counts
There were no significant differences between the initial and final
blood samples for smokers for the mean hemoglobin concentrations;
and the mean counts for the differential and complete WBC, RBC, and
platelets (Table 5).
There were no significant differences in non-smokers between the
initial and final blood samples for the mean WBC, monocyte, neu-
trophil, lymphocyte, basophil, RBC, and platelet counts; and the mean
hemoglobin concentration. On the other hand, the mean eosinophil
count in non-smokers (Table 6) increased highly significantly after
consumption of ginger compared to the mean count before extract
consumption.
3.4. Concentrations of IgG and IgM antibodies, CRP, and thyroid hormones
The initial and final blood samples for smokers were not sig-
nificantly different for the mean IgG, IgM, CRP, T4 and T3 concentra-
tions (Table 7). On the other hand, the mean TSH concentration for
smokers after extract consumption decreased highly significantly
compared to before consumption of the extract.
For non-smokers, the mean IgG, CRP, T4, and T3 concentrations
(Table 8) for the initial and final samples were not significantly dif-
ferent. On the other hand, after consumption of the extract, the mean
IgM concentration showed a highly significant increase and the mean
Table 1
Descriptive statistics and test of significance for the differences between smokers and non-smokers for the differential complete blood counts for the initial blood
samples (before consumption of the extract).
Parameter Group n Min Max Mean ± SD ± SE P value
WBC
b
(X10
9
/L) Smokers 33 1.20 12.57 4.77 2.82 0.49 0.074
NS
Non-smokers 35 1.23 30.49 7.10 6.27 1.06
Neutrophils
a
(X10
9
/L) Smokers 33 16.6 90.2 43.4 16.7 2.9 0.045
S
Non-smokers 35 21.9 95.1 53.2 22.1 3.7
Lymphocytes
a
(X10
9
/L) Smokers 33 0.7 63.8 36.4 16.0 2.8 0.232
NS
Non-smokers 35 0.0 53.2 31.5 17.5 3.0
Monocytes
b
(X10
9
/L) Smokers 33 2.7 22.5 8.2 4.7 0.8 0.668
NS
Non-smokers 35 1.6 36.2 8.8 6.2 1.0
Eosinophils
a
(X10
9
/L) Smokers 33 0.0 19.9 8.1 5.1 0.9 0.092
NS
Non-smokers 35 0.0 29.6 5.9 5.8 1.0
Basophils
a
(X10
9
/L) Smokers 33 0.0 9.6 3.5 2.2 0.4 0.051
NS
Non-smokers 35 0.0 9.4 2.4 2.4 0.4
RBC
a
(X10
12
/L) Smokers 33 3.94 6.78 5.48 0.73 0.13 0.007
HS
Non-smokers 35 2.98 6.34 4.88 1.00 0.17
Platelets
a
(X10
9
/L) Smokers 33 71 315 198 53 9 0.166
NS
Non-smokers 35 39 692 233 137 23
Hemoglobin
a
(g/L) Smokers 33 104 189 153 18 3 0.129
NS
Non-smokers 35 72 186 143 34 6
NS: Not significant (P ≥0.05), S: significant (P < 0.05), HS: Highly significant (P < 0.01).
Max: Maximum, Min: Minimum, n: number of subjects.
a
T-test was used for the significance test.
b
Mann-Whitney Utest was used for the significance test.
S.H. Mahassni, O.A. Bukhari Journal of Nutrition & Intermediary Metabolism 15 (2019) 10–17
12
Table 2
Descriptive statistics and test of significance for the differences between smokers and non-smokers for the differential complete blood counts for the final blood
samples (after consumption of the extract).
Parameter Group n Min Max Mean ± SD ± SE P value
WBC
b
(X10
9
/L) Smokers 33 1.53 14.17 4.64 2.52 0.44 0.492
NS
Non-smokers 35 1.01 16.65 5.66 3.79 0.64
Neutrophils
a
(X10
9
/L) Smokers 33 20.1 85.7 42.0 15.8 2.8 0.040
S
Non-smokers 35 19.4 86.7 51.0 19.2 3.2
Lymphocytes
a
(X10
9
/L) Smokers 33 1.0 64.0 38.1 16.8 2.9 0.017
S
Non-smokers 35 0.0 60.7 27.8 17.7 3.0
Monocytes
b
(X10
9
/L) Smokers 33 2.7 41.0 9.3 6.5 1.1 0.329
NS
Non-smokers 35 2.6 48.8 10.6 9.9 1.7
Eosinophils
a
(X10
9
/L) Smokers 33 0.4 16.8 7.2 3.8 0.7 0.327
NS
Non-smokers 35 0.1 29.6 8.5 6.5 1.1
Basophils
a
(X10
9
/L) Smokers 33 0.2 10.6 3.7 2.1 0.4 0.519
NS
Non-smokers 35 0.1 9.4 3.2 3.1 0.5
RBC
a
(X10
12
/L) Smokers 33 3.57 7.30 5.58 0.68 0.12 0.000
HS
Non-smokers 35 2.66 6.30 4.80 0.97 0.16
Platelets
a
(X10
9
/L) Smokers 33 76 582 199 83 14 0.079
NS
Non-smokers 35 90 459 237 96 16
Hemoglobin
a
(g/L) Smokers 33 88 183 153 20 4 0.003
HS
Non-smokers 35 79 170 134 29 5
NS: Not significant (P ≥0.05), S: significant (P < 0.05), HS: Highly significant (P < 0.01).
Max: Maximum, Min: Minimum, n: number of subjects.
a
T-test was used for the significance test.
b
Mann-Whitney Utest was used for the significance test.
Table 3
Descriptive statistics and test of significance for the differences between smokers and non-smokers for the concentrations of antibodies and hormones for the initial
blood samples (before consumption of the extract).
Parameter Group n Min Max Mean ± SD ± SE P value
IgG
a
(g/L) Smokers 17 3.6 27.8 14.0 6.5 1.6 0.099
NS
Non-smokers 17 1.5 18.6 10.8 4.5 1.1
IgM
a
(g/L) Smokers 17 0.25 3.16 1.17 0.82 0.20 0.464
NS
Non-smokers 17 0.35 3.82 1.41 0.99 0.24
CRP
a
(mg/L) Smokers 14 1.2 6.9 4.1 2.2 0.6 0.982
NS
Non-smokers 14 1.6 8.3 4.1 1.7 0.5
TSH
b
(Mmol/L) Smokers 33 0.98 5.47 2.34 1.10 0.19 0.377
NS
Non-smokers 35 0.55 6.33 2.18 1.28 0.22
T4
a
(Mmol/L) Smokers 33 12.36 33.57 21.44 4.80 0.83 0.719
NS
Non-smokers 35 12.81 29.86 21.83 4.02 0.68
T3
a
(Mmol/L) Smokers 33 4.40 10.05 6.56 1.14 0.20 0.579
NS
Non-smokers 35 4.21 8.81 6.41 1.13 0.19
NS: Not significant (P ≥0.05).
Max: Maximum, Min: Minimum, n: number of subjects.
a
T-test was used for the significance test.
b
Mann-Whitney Utest was used for the significance test.
Table 4
Descriptive statistics and test of significance for the differences between smokers and non-smokers for the concentrations of immunoglobulins and hormones for the
final blood samples (after consumption of the extract).
Parameter Group n Min Max Mean ± SD ± SE P value
IgG
a
(g/L) Smokers 17 7.0 27.6 13.9 5.9 1.4 0.222
NS
Non-smokers 17 2.5 18.3 11.7 4.2 1.0
IgM
a
(g/L) Smokers 17 0.25 3.20 1.18 0.83 0.20 0.005
HS
Non-smokers 17 0.82 4.56 2.19 1.05 0.25
CRP
a
(mg/L) Smokers 14 1.2 6.8 3.8 2.1 0.8 0.906
NS
Non-smokers 14 1.3 7.0 3.8 1.6 0.4
TSH
b
(Mmol/L) Smokers 33 0.81 4.70 1.64 0.80 0.14 0.000
HS
Non-smokers 35 0.54 4.54 1.78 1.05 0.18
T4
a
(Mmol/L) Smokers 33 12.11 29.75 21.06 4.27 0.74 0.342
NS
Non-smokers 35 12.92 28.65 22.01 3.91 0.66
T3
a
(Mmol/L) Smokers 33 4.80 7.92 6.41 0.94 0.16 0.358
NS
Non-smokers 35 4.66 9.61 6.64 1.11 0.19
S: significant (P < 0.05), NS: Not significant (P ≥0.05), HS: Highly significant (P < 0.01).
Max: Maximum, Min: Minimum, n: number of subjects.
a
T-test was used for the significance test.
b
Mann-Whitney Utest was used for the significance test.
S.H. Mahassni, O.A. Bukhari Journal of Nutrition & Intermediary Metabolism 15 (2019) 10–17
13
TSH concentration showed a highly significant decrease compared to
the respective levels before consumption of the extract.
4. Discussion
Many research studies have shown cigarettes to have stimulatory
and/or inhibitory effects on the body. Smoking may lead to cellular
damage and effects on most systems and organs of the body, which may
lead to many deleterious changes [3–5,18]. These changes may include
changes in counts of blood cells and concentrations of secreted hor-
mones. For the past few decades, there has been an extensive interest by
the public and many researchers to discover and determine the roles
and effects of natural foods in treating, preventing or reducing diseases
or their symptoms. Ginger is one of the more popular foods that have
been studied and used extensively for its many beneficial effects, al-
though many of these effects have not been proven scientifically. For
many natural components, it is essential to consume the natural whole
food rather than the active ingredient alone since the active compo-
nents may need the synergy or influence of other components in the
whole food. Thus, in this study, the whole ginger aqueous extract was
used rather than using the individual active substances. Another reason
for using the whole extract is that it was our goal to assess the effects of
ginger as used locally and in other parts of the world to treat different
ailments.
The effects of the ginger extract on the immune system and general
health of male smokers and non-smokers were determined by mea-
suring the complete and differential blood counts; and levels of thyroid
hormones (T3, T4, and TSH), IgG and IgM antibodies, and C-reactive
protein. An extensive search of the literature available on the internet
showed no other studies on the effects of ginger aqueous extracts on the
parameters measured in the current study in smokers and non-smokers.
Thus, this is the first study of its kind, which meant that we were not
able to compare our results for the blood samples collected at the end of
the experiment with other studies.
The aqueous ginger extract was prepared according to the method
Table 5
Descriptive statistics and test of significance for the differences between the
initial and final blood samples for the differential complete WBC counts in
smokers.
Parameter Blood
sample
n Min Max Mean ± SD ± SE P value
WBC
b
(X10
9
/L) Initial 33 1.20 12.57 4.77 2.82 0.49 0.796
NS
Final 33 1.53 14.17 4.64 2.52 0.44
Neutrophils
a
(X10
9
/L)
Initial 33 16.6 90.2 43.4 16.7 2.9 0.704
NS
Final 33 20.1 85.7 42.0 15.8 2.8
Lymphocytes
a
(X10
9
/L)
Initial 33 0.7 63.8 36.4 16.0 2.8 0.683
NS
Final 33 1.0 64.0 38.1 16.8 2.9
Monocytes
b
(X10
9
/L)
Initial 33 2.7 22.5 8.2 4.7 0.8 0.249
NS
Final 33 2.7 41.0 9.3 6.5 1.1
Eosinophils
a
(X10
9
/L)
Initial 33 0.0 19.9 8.1 5.1 0.9 0.380
NS
Final 33 0.4 16.8 7.2 3.8 0.7
Basophils
a
(X10
9
/L)
Initial 33 0.0 9.6 3.5 2.2 0.4 0.755
NS
Final 33 0.2 10.6 3.7 2.1 0.4
RBC
a
(X10
12
/L) Initial 33 3.94 6.78 5.48 0.73 0.13 0.276
NS
Final 33 3.57 7.30 5.58 0.68 0.12
Platelets
a
(X10
9
/
L)
Initial 33 71 315 198 53 9 0.960
NS
Final 33 76 582 199 83 14
Hemoglobin
a
(g/
L)
Initial 33 104 189 153 18 3 0.767
NS
Final 33 88 183 153 20 4
NS: Not significant (P ≥0.05); Max: Maximum, Min: Minimum.
a
Paired t-test was used for the significance test.
b
Wilcoxon test was used for the significance test.
Table 6
Descriptive statistics and test of significance for the differences between the
initial and final blood samples for the differential complete WBC counts in non-
smokers.
Parameter Blood
sample
n Min Max Mean ± SD ± SE P value
WBC
b
(X10
9
/L) Initial 33 1.23 30.49 7.60 6.27 1.10 0.196
NS
Final 33 1.01 16.65 5.66 3.80 0.60
Neutrophils
a
(X10
9
/L)
Initial 33 21.9 95.1 53.2 22.1 3.7 0.638
NS
Final 33 19.4 86.7 51.0 19.2 3.2
Lymphocytes
a
(X10
9
/L)
Initial 33 0.0 53.2 31.5 17.5 3.0 0.357
NS
Final 33 0.0 60.7 27.8 17.7 3.0
Monocytes
b
(X10
9
/L)
Initial 33 1.6 36.2 8.8 6.2 1.0 0.599
NS
Final 33 2.6 48.8 10.6 9.9 1.7
Eosinophils
b
(X10
9
/L)
Initial 33 0.2 29.6 5.9 5.8 1.0 0.008
HS
Final 33 0.1 29.6 8.5 6.5 1.1
Basophils
a
(X10
9
/L)
Initial 33 0.1 9.4 2.4 2.4 0.4 0.095
NS
Final 33 0.1 9.4 3.2 3.1 0.5
RBC
a
(X10
12
/L) Initial 33 2.98 6.34 4.88 1.00 0.17 0.707
NS
Final 33 2.66 6.30 4.80 0.97 0.16
Platelets
a
(X10
9
/
L)
Initial 33 39 692 233 137 23 0.884
NS
Final 33 90 459 237 96 16
Hemoglobin
a
(g/
L)
Initial 33 72 186 143 34 6 0.112
NS
Final 33 79 170 134 29 5
NS: Not significant (P ≥0.05), HS: Highly significant (P < 0.01).
Max: Maximum, Min: Minimum.
a
Paired t-test was used for the significance test.
b
Wilcoxon test was used for the significance test.
Table 7
Descriptive statistics and test of significance for the differences between the
initial and final blood samples for the concentrations of antibodies and hor-
mones in smokers.
Parameter Blood
sample
n Min Max Mean ± SD ± SE P value
IgG
a
(g/L) Initial 17 3.6 27.8 14.0 6.5 1.6 0.706
NS
Final 17 7.0 27.6 13.9 5.9 1.4
IgM
a
(g/L) Initial 17 0.25 3.16 1.10 0.82 0.20 0.601
NS
Final 17 0.25 3.20 1.10 0.82 0.20
CRP
a
(mg/L) Initial 14 1.2 6.9 4.1 2.2 0.6 0.097
NS
Final 14 1.2 6.8 3.8 2.1 0.6
TSH
b
(Mmol/L) Initial 33 0.98 5.47 2.34 1.10 0.19 0.000
HS
Final 33 0.80 4.70 1.64 0.80 0.14
T4
a
(Mmol/L) Initial 33 12.36 33.57 21.44 4.80 0.83 0.634
NS
Final 33 12.11 29.75 21.06 4.27 0.74
T3
a
(Mmol/L) Initial 33 4.40 10.05 6.56 1.14 0.20 0.500
NS
Final 33 4.80 7.92 6.41 0.94 0.16
HS: Highly significant (P < 0.01), NS: Not significant (P ≥0.05).
Max: Maximum, Min: Minimum.
a
Paired t-test was used for the significance test.
b
Wilcoxon test was used for the significance test.
Table 8
Descriptive statistics and test of significance for the differences between the
initial and final blood samples for the concentrations of antibodies and hor-
mones in non-smokers.
Parameter Blood
sample
n Min Max Mean ± SD ± SE P value
IgG
a
(g/L) Initial 17 1.5 18.6 10.8 4.5 0.8 0.052
NS
Final 17 2.4 18.3 11.7 4.2 0.7
IgM
a
(g/L) Initial 17 0.34 3.82 1.41 0.99 0.17 0.000
HS
Final 17 0.82 4.56 2.19 1.05 0.18
CRP
a
(mg/L) Initial 14 1.6 8.3 4.1 1.7 0.3 0.130
NS
Final 14 1.3 7.0 3.8 1.6 0.3
TSH
b
(Mmol/L) Initial 33 0.55 6.33 2.18 1.28 0.22 0.003
HS
Final 33 0.54 4.54 1.78 1.05 0.18
T4
a
(Mmol/L) Initial 33 12.81 29.86 21.83 4.02 0.68 0.825
NS
Final 33 12.92 28.65 22.01 3.91 0.66
T3
a
(Mmol/L) Initial 33 4.21 8.81 6.41 1.13 0.19 0.302
NS
Final 33 4.66 9.61 6.64 1.11 0.19
NS: Not significant (P≥0.05), HS: Highly significant (P < 0.01).
Max: Maximum, Min: Minimum.
a
Paired t-test was used for the significance test.
b
Wilcoxon test was used for the significance test.
S.H. Mahassni, O.A. Bukhari Journal of Nutrition & Intermediary Metabolism 15 (2019) 10–17
14
used locally, and the subjects were instructed to mix it with a hot liquid,
as is advised by folk medicine for best results. None of the subjects
reported any adverse symptoms due to the consumption of the extract
during the entire experimental period. All the parameters were de-
termined for both the initial (before the consumption of the ginger
extract) and final (after the consumption of the extract) blood samples.
There was no significant difference between mean ages for smokers and
non-smokers as reported previously [19] using the same groups of
smokers and non-smokers. In addition, the median ages for smokers and
non-smokers (30 and 29 years, respectively) were very close to each
other.
The complete and differential blood counts for the initial blood
samples showed no significant differences (P ≥0.05) between smokers
and non-smokers for the mean WBC, lymphocyte, monocyte, eosino-
phil, and basophil cell counts. As for the final blood samples, the mean
WBC, monocyte, eosinophil, and basophil cell counts for smokers were
not significantly different from the respective mean counts for non-
smokers. Therefore, the only significant differences between smokers
and non-smokers were significantly lower (P = 0.045, and P = 0.040,
respectively) mean neutrophil counts for both the initial and final
samples for smokers (Mean ± SD: 43.4 ± 16.7, and 42.0 ± 15.8,
respectively) compared to the respective counts in non-smokers
(53.2 ± 22.1; and 51.0 ± 19.2, respectively), and a significantly
higher (P = 0.017) mean lymphocyte count for the final sample for
smokers (38.1 ± 16.8) compared to the mean count for non-smokers
(27.8 ± 17.7). Comparing the complete and differential blood counts
before and after the consumption of the ginger extract in smokers and
non-smokers each, neither WBC nor its types showed any significant
differences, with the exception of a highly significant increase
(P = 0.008) in the mean eosinophil count in non-smokers after extract
consumption (8.5 ± 6.5) compared to before extract consumption
(5.9 ± 5.8).
The findings of the first blood samples do not support previous re-
search studies that demonstrated significantly higher WBC, neutrophil,
lymphocyte, monocyte, eosinophil, and basophil counts [20–28] and
lower lymphocyte counts [26] in smokers compared to non-smokers.
Other studies that agree with the results of the current study showed no
significant differences between smokers and non-smokers for lympho-
cyte, eosinophil, basophil [24], and monocyte counts [24,26]nor for
counts of granulocytes in general [28]. As for the results after con-
sumption of ginger, there are no published studies on the effects of
ginger on WBC and their types in smokers, as mentioned above, for
comparison with the current results. A study done on healthy rats given
different doses of ginger extract [29] resulted in significantly lower
WBC counts and higher neutrophil counts compared to the control rats
that did not consume ginger. These findings contradict our findings of
no significant differences for WBC and neutrophil counts between the
initial and final blood samples in non-smokers.
Increased counts of white blood cells and their subtypes are in-
dicators of infection, diseases, or an unhealthy lifestyle. Therefore, it is
interesting that the ginger extract led to a higher mean lymphocyte
count for smokers or, in other words, it led to a lower mean lymphocyte
count for non-smokers. On the other hand, neutrophils remained sig-
nificantly lower for smokers at the end of the experimental period. In
addition, WBC and their types did not change significantly for smokers
after the consumption of the extract. Lymphocytes are important in
both humoral and cellular acquired immunities while neutrophils are
important in innate immunity and infections, and both cells are linked
to inflammation. Thus, it may be concluded that ginger enhances ac-
quired immunity in smokers compared to not non-smokers, through the
increase in the lymphocyte cell count but it does not enhance innate
immunity since neutrophils remained low in smokers and the remaining
types of WBC did not change.
The mean RBC counts for both the initial and final blood samples
were highly significantly higher (P = 0.007, and P = 0.000, respec-
tively) for smokers (5.48 ± 0.73, and 5.58 ± 0.68, respectively)
compared to non-smokers (4.88 ± 1.00, and 4.80 ± 0.97, respec-
tively). The mean platelet count and hemoglobin concentration for the
first blood samples did not show significant differences between the two
groups (P > 0.05). For the final blood samples, the mean platelet
counts were not significantly different between smokers and non-smo-
kers, while the mean hemoglobin concentration for the smokers group
(15.3 ± 2.0) was highly significantly higher (P = 0.003) than for the
non-smokers group (13.4 ± 2.9). As for the comparison between the
mean RBC and platelet counts and mean hemoglobin concentrations
before and after the extract in smokers and non-smokers, there were no
significant differences.
The findings for the initial blood samples agree with other studies
[22,24,25,29] that found higher RBC counts in smokers compared to
non-smokers. On the other hand, these results disagree with studies that
found higher hemoglobin levels [22,24,25,28,30–32] in smokers com-
pared to non-smokers. The findings of the present study of no differ-
ences in platelet counts between smokers and non-smokers are con-
sistent with the findings of other research studies [22,23,25,33].
The only other study on the effects of ginger extract consumption in
health, done on healthy rats, on RBC and platelet counts, and he-
moglobin concentrations was the study by Tende et al. [29], mentioned
previously. The ginger extract resulted in significantly lower he-
moglobin concentration and higher RBC counts. This contradicts the
current results of no differences in these parameters between after
consumption of the extract and before. In addition, since the mean RBC
counts for both the initial and final blood samples were higher for
smokers compared to non-smokers, therefore there were no ginger-
specificeffects on the subjects. As for hemoglobin, ginger led to a sig-
nificantly higher hemoglobin concentration for smokers compared to
non-smokers, or, alternatively, a significantly lower hemoglobin con-
centration for non-smokers compared to smokers. The lower he-
moglobin level in non-smokers agrees with the findings of Tende et al.
[29] mentioned above, but the result of a lower RBC count in non-
smokers does not.
An explanation [29] for the higher RBC counts in smokers for both
blood samples is that the carbon monoxide in cigarette smoke binds to
hemoglobin in RBC more successfully than oxygen. This leads to less
hemoglobin to carry oxygen and a lower release rate of oxygen carried
by hemoglobin. Therefore, to provide the body with the needed amount
of oxygen, carried by RBC, the body produces more RBC to compensate.
Our findings agree with this explanation since before the consumption
of ginger smokers had higher RBC than non-smokers. This held true
after consumption of ginger, but now, in addition, smokers had higher
hemoglobin concentration compared to non-smokers. Therefore, the
ginger extract led to a beneficial effect on smokers where the increased
hemoglobin concentration may counteract the reduced amount of he-
moglobin available to bind oxygen in smokers.
The results for the mean IgG and IgM concentrations before con-
sumption of the extract did not show any significant differences
(P > 0.05) between smokers and non-smokers. After consumption of
ginger, the mean IgG concentrations for smokers and non-smokers were
not significantly different, whereas the mean IgM concentration for
smokers (1.18 ± 0.83) was highly significantly lower (P = 0.005) than
the mean IgM concentration for non-smokers (2.19 ± 1.05).
Additionally, the mean IgG and IgM concentrations for smokers before
and after extract consumption were not significantly different. As for
non-smokers, mean IgG levels were not significantly different before
and after extract consumption while the mean IgM level after extract
consumption (2.19 ± 1.05) increased highly significantly (P = 0.000)
compared to before extract consumption (1.41 ± 0.99). These results
are in disagreement with the findings of other studies of significantly
lower IgG levels [34–37] and increased IgG and IgM levels [38] in ci-
garette smokers compared to non-smokers. Research work done on
healthy fish and sows administered ginger extract showed increased
IgM [39], and IgG concentrations [40], which may suggest an enhanced
immune system. This agrees with the current result of a significantly
S.H. Mahassni, O.A. Bukhari Journal of Nutrition & Intermediary Metabolism 15 (2019) 10–17
15
higher IgM level for non-smokers after the consumption of the ginger
extract, but disagrees with the results for IgG levels that did not show
any significant differences in all comparisons. Thus, it may be that the
extract enhances humoral immunity in non-smokers specifically, but
not smokers, through higher IgM levels. On the other hand, decreased
levels of antibodies lead to a weaker humoral response, which may be
partially to blame for the increased susceptibility of smokers to infec-
tions and more severe symptoms of infections and diseases.
Mean CRP concentrations did not show any significant differences
(P > 0.05) between smokers and non-smokers for both the initial and
final blood samples, nor before and after ginger extract consumption for
smokers and non-smokers. These findings are contradictory to previous
studies [20,21,27,38,41] that showed that smokers have a significantly
higher CRP level compared to non-smokers. No studies on the effect of
ginger or its extract on CRP levels in smokers were found. CRP, im-
portant in both the innate and humoral acquired immunities, is used as
a marker for inflammation, increasing in inflammatory diseases, such as
cardiovascular disease, trauma, infections, and lifestyle choices and
conditions that lead to inflammation, such as obesity and smoking.
Therefore, it was expected that smokers would have significantly higher
CRP levels compared to non-smokers.
The mean thyroid hormones (TSH, T4, and T3) concentrations were
not significantly different between smokers and non-smokers
(P > 0.05) for the initial and final blood samples, with the exception of
the mean TSH concentrations after extract consumption which were
highly significantly lower (P = 0.000) for smokers (1.64 ± 0.80)
compared to non-smokers (1.78 ± 1.05). Additionally, the mean T4
and T3 concentrations before and after extract consumption were not
significantly different in smokers and non-smokers. On the other hand,
the mean TSH concentrations after extract consumption for smokers
and non-smokers each (1.64 ± 0.80, and 1.78 ± 1.05, respectively)
decreased highly significantly (P = 0.000, and P = 0.003, respectively)
compared to the levels (2.34 ± 1.10, and 2.18 ± 1.28, respectively)
before extract consumption by smokers and non-smokers, respectively.
Studies conducted by other researchers agree with the current results of
no effects of smoking on the serum levels of TSH [42], T3 [42–45], and
T4 [43–45]. On the other hand, the findings of the current study do not
support other previous research findings that observed that smokers
have significantly lower serum TSH levels [46–50] and higher T4 and
T3 levels [46,47,49,50] compared to non-smokers. No studies on the
effects of ginger or its extracts on thyroid hormones were found.
The thyroid gland, one of the larger glands in the body, regulates
growth, energy expenditure, metabolism, and the function of many
systems and hormones. The blood concentrations of the major thyroid
hormones T3, and T4 are regulated by the blood concentration of TSH,
which is produced by the pituitary gland. The TSH stimulates the
thyroid to produce more T3 and T4. Therefore, the lower TSH in
smokers after consumption of the extract indicates enhanced activity of
the thyroid gland and that may result in higher T3 and T4 concentra-
tions if the experimental period were prolonged.
It is noteworthy that the mean TSH levels for smokers and non-
smokers were both lower after ingestion of the ginger extract compared
to before the beginning of the experiment. Thus, the extract leads to
enhancement of thyroid gland function and this would lead to increased
T3 and T4 concentrations in both smokers and non-smokers with pro-
longed consumption of the ginger extract. This effect may be more
pronounced in smokers since their mean TSH level was decreased more
than for non-smokers.
5. Conclusions and recommendations
In conclusion, before extract consumption, smokers had a sig-
nificantly lower neutrophil count and higher RBC count compared to
non-smokers. After consumption of the ginger extract, these differences
remained, but now smokers also had significantly higher lymphocyte
count and hemoglobin concentration, and significantly lower IgM and
TSH concentrations compared to non-smokers. On the other hand, after
consumption of the extract, smokers had significantly decreased TSH
levels compared to before consumption of the extract. Non-smokers had
significantly increased eosinophil count and IgM concentration, and
significantly decreased TSH levels than before consumption of the ex-
tract. Therefore, it is clear that the extract leads to enhancement of the
thyroid gland function in both smokers and non-smokers since TSH
levels were decreased in both smokers and non-smokers. In addition,
the extract did not counteract the effects of smoking, since the low
neutrophil count and high RBC count in smokers remained unchanged
at the end of the experimental period. However, smokers benefited
from a higher lymphocyte count and hemoglobin concentration com-
pared to non-smokers, although non-smokers had a higher eosinophil
count and IgM concentration. Thus, the extract has different effects on
the immune system cells and antibodies in smokers and non-smokers,
although both benefited from enhancement of the thyroid gland.
Smokers had variable effects on the immune system cells but had en-
hancement of RBC counts and hemoglobin levels. Non-smokers had
enhanced IgM levels, which may lead to a stronger antibody response,
or humoral immunity, against infections.
The increased hemoglobin concentration after ginger consumption
in smokers may be beneficial for compensating for the reduced he-
moglobin molecules available for binding oxygen due to cigarette
smoke, as explained above. Therefore, ginger may be beneficial for
smokers with anemia. It is recommended that similar studies on smo-
kers be done using more subjects and studying both females and males
to determine any gender-specificeffects.
Funding
This research study was partially funded by a grant (grant number
P-S-37-1938) provided by the King Abdulaziz City for Science and
Technology, Saudi Arabia.
Author contributions
Contribution of author SHM: Was responsible for the con-
ceptualization of the research study, data analysis, funding acquisition,
writing of the initial draft, and revising of the initial and subsequent
drafts.
Contribution of author OAB: Was responsible for the con-
ceptualization of the research study, data analysis, data collection,
sample analysis, data analysis, funding acquisition, writing of the initial
draft, and revising of the initial and subsequent drafts.
Compliance with ethical standards
Conflicts of interest
Both authors declare that they have no conflicts of interest.
Human subjects
Ethical approval for the study was provided by the King Abdullah
Medical Complex.
“Informed consent was obtained from all individual participants
included in the study.”
“All procedures performed in the study were in accordance with the
ethical standards of the institutional and/or national research com-
mittee and with the 1964 Helsinki declaration and its later amendments
or comparable ethical standards.”
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://
doi.org/10.1016/j.jnim.2018.10.001.
S.H. Mahassni, O.A. Bukhari Journal of Nutrition & Intermediary Metabolism 15 (2019) 10–17
16
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