




































_____________________________________________________________________________________________________ 
 
*Corresponding author: E-mail: johnisa66@yahoo.com; 
 
 
 

Asian Journal of Immunology 
 
2(1): 18-25, 2019; Article no.AJI.52667 
 

 
 

 

 

Immunomodulatory Effects of Honey in Wistar Rats 
Infected with Salmonella typhimurium 

 
Justinah F. John-Isa1*, Tinuola T. Adebolu1 and Victor O. Oyetayo2 

 
1
Department of Microbiology, Federal University of Technology Akure (FUTA), P.O.Box 704, Akure, 

Ondo State, Nigeria.  
2
Department of Microbiology, Federal University of Technology, Akure, Nigeria. 

 
Authors’ contributions  

 
This work was carried out in collaboration among all authors. Author JFJI designed the study, 

performed the statistical analysis, wrote the protocol and wrote the first draft of the manuscript. 
Authors TTA and Author VOO managed the analyses of the study. Author TTA managed the literature 

searches. All authors read and approved the final manuscript. 
 

Article Information 
 

Editor(s): 
(1) Dr. Jaffu Othniel Chilongola, Department of Biochemistry and Molecular Biology, Kilimanjaro Christian Medical University 

College, Tumaini University, Tanzania. 
Reviewers: 

(1) Asma Bouasla, University Souk-Ahras, Algeria. 
(2) Oyiborhoro Onoriode, University of Medical Sciences, Nigeria. 

(3) Syed Umer Jan, University of Balochistan, Pakistan. 
Complete Peer review History: http://www.sdiarticle4.com/review-history/52667 

 
 
 
 

Received 10 September 2019 
Accepted 14 November 2019 
Published 19 November 2019 

 
 
ABSTRACT 
 

Aim: To evaluate the immunomodulatory effects of honey on Wistar rats infected with Salmonella 
typhimurium. 
Place and Duration of Study: Research laboratory of The Federal University of Technology Akure 
(FUTA), Ondo State, Nigeria between July, 2019 and September, 2019. 
Methodology: A total thirty – nine (39) apparently healthy Wistar rats, three (3) rats per group were 
used in this study. Twelve (12) out of the rats were used to determine the infectivity dose of S. 
typhimurium on the rats and twenty – seven (27) rats for infection and treatment assay. The rats 
were divided into nine (9) groups of 3 rats per group, the first 8 groups were infected with S. 
typhimurium and treated for seven (7) days with honey, augmentin and oral rehydration solution 
(ORS) (different treatment for different groups) except group 1 that was infected and not treated 
and group 9, that was not infected, not treated. The blood samples of all the rats was collected after 
treatment to study the effect of honey on the haematological parameters of the rats.  

Original Research Article 



 
 
 
 

John-Isa
 
et al.; AJI, 2(1): 18-25, 2019; Article no.AJI.52667 

 
 

 
19 

 

Results: Honey administered at 2ml and 3ml twice daily to the S. typhimurium infected rats exerted 
good therapeutic potential in combating diarrhoea in the animals. Also, in these group of rats, 
honey caused an increase in the PCV, RBC, HB and lymphocytes which displays honey to be a 
good immunostimulator and immunomodulator.   
Conclusion: Honey exerted therapeutic, haematinic and immunomodulatory potentials in rats 
infected with S. typhimurium. These findings therefore could be exploited in the treatment of 
diarrhoeal diseases caused by this bacterium.  
 

 

Keywords: S. typhimurium; wistar rats; honey; augmentin; Oral Rehydration Solution (ORS); 
immnuomodulation. 

 

1. INTRODUCTION  
 

Salmonella typhimurium is a Gram-negative, 
flagellated, aerobic (oxygen-consuming) 
bacteriium, the major cause of human 
salmonellosis [1], a type of gastroenteritis, or 
inflammation of the intestine [2]. S. typhimurium 
is also a frequent cause of acute, self-limiting 
food borne diarrhoea. It is spread primarily by 
contaminated food and drink, but it can come in 
contact with human via direct contact with an 
infected animal or pet [1]. Salmonella 
typhimurium induces a systemic infection in rats, 
so S. typhimurium-infected rats have been 
extensively used as models for the 
understanding of the immunological and 
antibacterial effect of honey. Diarrhoeal diseases 
are among the leading causes of morbidity and 
mortality in young children in developing 
countries [3]. It is characterized by frequent, 
loose and watery stool which may result in 
dehydration and in severe cases, death. Each 
year, an estimated 2.5 billion cases of diarrhoea 
occur among the children under five years of 
age, and estimates suggest that overall incidence 
has remained relatively stable over the past two 
decades. Although, diarrhoea is self-limiting 
however when it is as a result of bacterial 
infection, antibiotic therapy might be required but 
because of the high resistance rate of bacteria to 
available antibiotics, administration of antibiotics 
may not result in recovery of patients. Moreover, 
some of these antibiotics can also induce 
diarrhoea known as “antibiotic induced diarrhoea” 
[4]. Therefore, it becomes imperative to search 
for alternatives to conventional antibiotics to treat 
this disease. In most ancient cultures, honey has 
been used for both nutritional and medical 
purposes. The belief that honey is a nutrient, a 
drug and an ointment has been carried into our 
days, and thus, an alternative medicine branch, 
called ‘‘apitherapy’’, has been developed in 
recent years, offering treatments based on honey 
and other bee products against many diseases 
including bacterial infections. Honey has been 
reported to have immunomodulatory and 

antibacterial activity on bacteria found in wounds 
[5], responsible for food spoilage [6], common 
diarrhoeagenic bacteria such as S. typhimurium  
[7] and many other bacterial species. It becomes 
worthwhile therefore to investigate whether 
honey has therapeutic and immunostimulatory 
potentials in Wistar rats infected with S. 
typhimurium in addition to nits antibacterial 
potential. 
  

2. MATERIALS AND METHODS  
 

2.1 Location and Duration of the 
Research 

 

The research was carried out in the Graduate 
Research Laboratory of Department of 
Microbiology, Federal University of Technology, 
Akure, Ondo State, Nigeria between July and 
September, 2019.  
 

2.2 Honey Sample  
 

The honey sample used was collected from 
FUNAAB, Abeokuta Ogun State.  It’s of wild flora 
source.   
 

2.3 Test Organism 
 

The test organism used was Salmonella 
typhimurium. 
 

2.4 Isolation and Identification of the Test 
Organism 

 

S. typhimurium was isolated from poultry 
droppings, the droppings was serially diluted in 
sterile distilled water using the method of 
Boateng and Diunase [8]. The dilutions were 
plated on Salmonella - Shigella agar to isolate 
the bacterium and was identified based on 
morphological and biochemical characteristics 
according to the method of Rozanska [9]. 
 

2.5 Experimental Animals 
 

A total of 39 female Wistar rats of weight range 
60-90 g were used for the study.  The animals 



 
 
 
 

John-Isa
 
et al.; AJI, 2(1): 18-25, 2019; Article no.AJI.52667 

 
 

 
20 

 

were purchased at Animal Production and Health 
Dept. of Federal University of Technology Akure, 
Ondo State. They were brought to the animal 
house of Microbiology Department, FUTA       
and acclimatized for 7 days before the 
commencement of this work. The animals were 
fed with broiler starter and clean water twice 
daily. 

 
2.6 Determination of Infectivity Dose (ID) 

of Salmonella typhimurium 
 
A total of twelve (12) female apparently Wistar 
rats was used to determine infectivity dose. The 
rats were divided into four groups of 3 rats per 
cage. This was done using standard method 
described by Adebolu et al.  [10]. A colony of S. 
typhimurium of 24 hrs old was inoculated into 
100 ml of Nutrient agar, incubated at 37ºC for 18 
– 24 hrs. The cells were harvested by 
centrifuging at 3000 rpm for 15 minutes. The 
supernatant was decanted and 10ml of sterile 
normal saline was poured into the tube and was 
further centrifuged to wash the cells, this was 
done three times.  Serial dilution was carried on 
the harvested cells and 1ml was taken from each 
of the different concentrations already prepared 
to infect different groups of the experimental 
animals respectively. The dilution that produced 
the symptoms of illness in all of the animals was 
taken as the infectivity dose (ID) of the organism.  

 
2.7 Experimental Design 
 
A total of 27 female apparently healthy Wistar 
rats were assigned into nine (9) treatment groups 
designated as 1 – 9.  i.e. 3 rats per cage.   Rats 
in group 1 were infected with the ID of S. 
typhimurium  and not treated, rats in group 2 
were infected and treated with 1 ml raw honey 12 
hourly, group 3 infected and treated with 2 ml 
raw honey 12 hourly, group 4 infected and 
treated with 3ml raw honey 12 hourly,  group 5 
infected and treated with  0.5 ml Augmentin (30 
mg/kg/day) 12hourly, group 6 infected and 
administered honey – ORS 12 hourly,  group 7 
infected and administered 1ml commercial ORS 
12 hourly, group 8 infected and administered 1ml 
homemade ORS 12 hourly and group 9 not 
infected, not treated (control group). 

 
2.8 Infection of Rats with the ID of S. 

typhimurium 
 
The infection of the animals was done using the 
infectivity dose (ID) of the organism by 

orogastrically dosing them according to the 
method of Adebolu et al. [10]. The infectivity 
dose used in this study was calculated to be 1.5 
x10

8 
cfu/ml. 

 

2.9 Treatment of Infected Rats 
 
Treatment begins 24 hours after which infection 
has set in, specific volume of honey, augmentin, 
honey – ORS, ORS both commercial and home - 
made variants were administered to the           
infected rats for 7 days according to Oladunmoye 
[11].  
 

2.10 Isolation, Identification and 
Enumeration of S. typhimurium in 
the Faeces of Infected Rats 

 
One gram (1 g) of faeces of the infected rats 
were aseptically collected, serial dilution was 
done on them and plated on salmonella shigella 
agar in order to isolate the Salmonella 
typhimurium present in the rats and monitor         
their bacterial count throughout the experiment 
[12].  
 

2.11 Weighing of Animals 
 
The weight of the animals were taken throughout 
the pre and post ingestion period using the 
method of Momoh et al. [13]. 
 

2.12 Haematological Assay 
 

The blood of the infected and uninfected rats was 
collected weekly into EDTA bottles after which 
the Packed Cell Volume (PCV), Haemoglobin 
(HB), Red blood Cell (RBC), White Blood Cell 
(WBC) and differential leukocytes counts of             
the collected blood samples were evaluated 
according to the method described by Baker et 
al. [14]. 
 

2.13 Statistical Analysis 
 
All experiments were done in triplicates, Mean, 
Standard deviation were calculated for all data 
using Descriptive Statistics and difference 
between means was determined by  Duncan’s 
New  Multiple Range Test at p≤.05.   
 

3. RESULTS AND DISCUSSION 
 
All the rats infected with S. typhimurium and 
treated with honey recovered by the 3

rd
 day while 

those ones that was administered honey – ORS 



 
 
 
 

John-Isa
 
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21 

 

and the ones with homemade ORS recovered by 
day 4 and those treated with augmentin and 
those administered commercial ORS recovered 
by the 5

th
 day, those that were infected but not 

treated started to show signs of recovery by the 
6

th
 day. The recovery without treatment by the 6

th
 

day confirms that acute diarrhoea is self limiting 
according Chen et al. [15]. The mean recovery 
times of rats infected with Salmonella 
typhimurium and treated with honey –ORS was 
significantly reduced when compared with 

infected and not treated group (Table 1). This is 
agreement with the work of Beretta et al. [16]. 
There was no evidence of S. typhimurium in the 
faeces of rats treated with 1 ml, 2 ml, 3 ml of 
honey and administered 1 ml of honey –ORS 12 
hourly for 7 days (Fig. 1). 
 
There was no evidence of Salmonella 
typhimurium in the faeces of rats treated with 1 
ml, 2 ml, 3 ml of honey and administered 1 ml of 
honey – ORS 12 hourly for 7 days. (Fig. 1). 

 
Table 1. Physical observations of the wistar rats during infection with Salmonella typhimurium 

and treatment 
 

Group of 
rats 

Treatment Interval (Days) 

1 2 3 4 5 6 7 

1 Infected and  
not treated with 
honey 

RA, EL, 
UF,PM,SS 

RA, 
EL, UF, 
PM, SS 

RA, EL, 
UF, PM, 
SS 

RA, EL, 
UF, PM, 
SS 

RA, EL, 
UF, PM, 
SS 

A, EW, 
FS, NM, 
SF 

A, EW, 
FS, NM, 
SF 

2 Infected and 
treated with 1 
ml honey (12 
hourly) 

RA, EL, 
UF, PM, 
SS  

RA, 
EL, UF, 
PM, SS 

A, EW, 
FS, NM 

A, EW, 
FS, NM 

A, EW, 
FS, NM 

A, EW, 
FS, NM 

A, EW, 
FS, NM 

3 Infected and 
treated with 2 
ml honey (12 
hourly) 

RA, EL, 
UF, PM, 
SS 

RA, 
EL, UF, 
PM, SS 

A, EL, 
UF, PM, 
SS 

A, EL, 
FS, NM, 
SF 

A, EL, 
FS, NM, 
SF 

A, EW, 
FS, NM, 
SF 

A, EW, 
FS, NM, 
SF 

4 Infected and 
treated with 3 
ml honey (12 
hourly) 

RA, EL, 
UF, PM, 
SS 

RA, 
EL, UF, 
PM, SS 

A, EL, 
UF, PM, 
SS 

A, EL, 
FS, NM, 
SF 

A, EL, 
UF, NM, 
SF 

A, EW, 
FS, NM, 
SF 

A, EW, 
FS, NM, 
SF 

5 Infected and 
treated with 0.5 
ml Augmentin 
(12 hourly) 

RA, EL, 
UF, PM, 
SS 

RA, 
EL, UF, 
PM, SS 

RA, EL, 
UF, PM, 
SS 

RA, EL, 
UF, PM, 
SS 

A, EW, 
FS, NM, 
SF 

A, EW, 
FS, NM, 
SF 

A, EW, 
FS, NM, 
SF 

6 Infected and 
treated with 1 
ml Honey - 
ORS (12 
hourly) 

RA, EL, 
UF, PM, 
SS 

RA, 
EL, UF, 
PM, SS 

RA, EL, 
UF, PM, 
SS 

A, EW, 
FS, NM, 
SF 

A, EW, 
FS, NM 

A, EW, 
FS, NM, 
SF 

A, EW, 
FS, NM, 
SF 

7 Infected and 
treated with 1 
ml ORS (12 
hourly) 

RA, EL, 
UF, PM, 
SS 

RA, 
EL, UF, 
PM, SS 

RA, EL, 
UF, PM, 
SS 

RA, EL, 
UF, 
*PM, SS 

A, EW, 
FS, NM, 
SF 

A, EW, 
FS, NM, 
SF 

A, EW, 
FS, NM, 
SF 

8 Infected and 
treated with 1 
ml homemade 
(12 hourly) 

RA, EL, 
UF, PM, 
SS 

RA, 
EL, UF, 
PM, SS 

RA, EL, 
UF, PM, 
SS 

A, EW, 
FS, *PM, 
SS 

A, EW, 
FS, NM, 
SF 

A, EW, 
FS, NM, 
SF 

A, EW, 
FS, NM, 
SF 

9 Not infected 
and not treated 

A, EW, FS, 
NM, SF 

A, EW, 
FS, 
NM, SF 

A, EW, 
FS, NM, 
SF 

A, EW, 
FS, NM, 
SF 

A, EW, 
FS, NM, 
SF 

A, EW, 
FS, NM, 
SF 

A, EW, 
FS, NM, 
SF 

Key: A = Activeness, RA = Reduced activity, EL = Eating little, EW = Eating well, UF = informed stool,  
FS = Formed stool, SF = Smooth fur, SS = Scattered fur, PM = Presence of mucous,  

*PM = High presence of mucous, NM = No mucous 



 
 
 
 

John-Isa
 
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22 

 

 
 

Fig. 1. Total counts of S. typhimurium in the faeces of wistar faeces after infection and 
treatment 

Key: A = Infected and not treated, B = Infected and treated with 1 ml honey, C = Infected and treated with 2 ml 
honey, D = Infected and treated with 3 ml honey, E = Infected and treated with 0.5 ml augmentin, F = Infected 

and administered with 1 ml honey – ORS, G = Infected and administered with 1ml commercial ORS, H = Infected 
and administered with 1 ml homemade ORS, TM1 = Treatment day 1, TM2 = Treatment day 2. TM3 = Treatment 

day 3, TM4 = Treatment day 4 and TM7 = Treatment after day 7 

 
The infected rats lost weight as a result of the 
infection with S. typhimurium however, 
administration of honey to the infected rats 
caused a significant increase (p<0.05) in their 
weight but the infected and not treated rats 
recorded weight loss for a longer duration than 

those that were administered different volumes of 
honey (Fig. 2A-E). The observation that the 
infected and not treated rats did not gain back 
their body weight throughout the duration of the 
research is in agreement with the work of Momoh 
et al. [13]. 

 

  
 

A 
 

B 
  

0 

1 

2 

3 

4 

5 

6 

7 

24 h/TM1     48 h/TM2 72 h/TM3 96 h / TM4 168 h / TM7 

lo
g 

cf
u

/m
l 

Infection period (h)/Treatment 

A B C D E F G H 

0 

20 

40 

60 

80 

100 

120 

0 1 2 3 4 5 6 7 

w
ei

gh
t 

(g
) 

Period (Day) 

Infected and  not treated with honey 

Not infected and not treated 

0 

20 

40 

60 

80 

100 

120 

0 1 2 3 4 5 6 7 

w
ei

gh
t 

(g
) 

Period (Day) 

Infected and treated with 1ml honey 

Not infected and not treated 



 
 
 
 

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23 

 

  
 

C 
 

D 
 

 
 

E 
 
Fig. 2 A–E. Average weight of wistar rats before infection with S. typhimurium, at the onset of 

infection and after treatment with honey and augmentin 

 
Infection of rats with S. typhimurium caused a 
decrease in their PCV, HB and RBC and 
increase in their neutrophil counts, showing a 
sign of infection but after treatment with honey 
(between 2ml and 3ml), there was no significant 
difference in the PCV, WBC of the group of rats 
treated with honey and the group not infected, 

not treated (control) (Tables 2a and b). 
Administration of honey to apparently                
healthy rats (control) caused a significant  
(p<.05) increase in the PCV and lymphocytes              
of the rats. This shows that the honey has                
both haematinic and immunomodulatory 
potentials. 

 

0 

20 

40 

60 

80 

100 

120 

0 1 2 3 4 5 6 7 

w
ei

gh
t 

(g
) 

Period (Day) 

Infected and treated with 2ml honey 

Not infected and not treated 

0 

20 

40 

60 

80 

100 

120 

0 1 2 3 4 5 6 7 
w

ei
gh

t 
(g

) 
Period (Day) 

Infected and treated with 3ml honey 

Not infected and not treated 

0 

20 

40 

60 

80 

100 

120 

0 1 2 3 4 5 6 7 

w
ei

gh
t 

(g
) 

Period (Day) 

Infected and treated with 0.5ml Augmentin 

Not infected and not treated 



 
 
 
 

John-Isa
 
et al.; AJI, 2(1): 18-25, 2019; Article no.AJI.52667 

 
 

 
24 

 

Table 2a. Effect of honey on the haematological parameters of wistar rats infected with  
S. typhimurium 

 

Group PCV (%) HB (g/L) WBC (10
9
/L) RBC (10

12
g/L) 

1 32.50 ± 4.95
b
 10.85 ± 1.66

b
 12.70 ± 0.28

a
 3.00 ± 0.82

b
 

2 40.00 ± 2.83
ab

 13.50 ± 0.71
ab

 11.70 ± 0.28
ab

 3.20 ± 0.25
 ab

 
3 42.50 ± 2.12

 a
 14.14 ± 0.66

 a
 8.77 ± 0.49

 c
 4.04 ± 0.87

 ab
 

4 43.00 ± 4.24
 a
 14.30 ± 1.36

 a
 8.94 ± 0.42

 c
 4.29 ± 0.07

 a
 

5 40.33 ± 4.51
ab

 13.50 ± 1.51
ab

 10.86 ± 0.17
abc

 4.06 ± 0.30
 ab

 
6 35.50 ± 0.71

ab
 11.90 ± 0.28

 ab
 10.88 ± 0.05

abc
 3.66 ± 0.03

 ab
 

7 39.67 ± 4.51
ab

 13.19 ± 1.56
ab

 9.56 ± 1.92
bc

 4.07 ± 0.34
 ab

 
8 35.00 ± 6.00

ab
   11.64 ± 2.00

 ab
 9.83 ± 1.47

bc
 3.66 ± 0.53

 ab
 

9 42.33 ± 2.08
 a
 13.66 ± 0.35

 ab
 8.82 ± 1.06

c
 4.07 ± 0.58

 ab
 

Key: 1 = Infected and not treated, 2 = Infected and treated with 1ml honey, 3 = Infected and treated with 2ml 
honey, 4 = Infected and treated with 3ml honey, 5 = Infected and treated with 0.5ml augmentin, 6 = Infected and 
administered with 1ml honey – ORS, 7 = Infected and administered with 1ml commercial ORS, 8 = Infected and 

administered with 1ml homemade ORS, 9 =  Not Infected, not treated,  PCV = Packed cell volume, HB = 
Haemoglobin concentration,  WBC =  White blood cell and RBC = Red blood cell 

 
Table 2b.  Effect of honey on the haematological parameters of wistar rats infected with  

S. typhimurium contd 
 

Group Lymphocytes (%) Neutrophils (%) Monocytes (%) Eosinophils (%) Basophil (%) 

1 31.50 ± 0.71
f
 64.50 ± 0.71

a
 3.00 ± 0.00

a
 1.50 ± 0.71

a
 1.00 ± 0.00

a
 

2 37.50 ± 0.71
bc

 61.00 ± 1.41
ab

 2.50 ± 0.71
a
 2.00 ±1.41

a
 1.00 ± 0.00

a
 

3 40.00 ± 2.83
ab

 56.50 ± 0.71
b
 1.50 ± 0.71

a
 1.00 ±  0.00

a
 0.00 ± 0.00 

4 40.50 ± 0.71
a
 57.00 ± 1.41

b
 1.50 ± 0.71

a
 1.00 ± 0.00

a
 0.00 ± 0.00 

5 39.33 ± 150
abc

 56.00 ± 4.00
b
 1.67 ± 1.15

a
 1.00 ± 0.00

a
 0.00 ± 0.00 

6 37.00 ± 1.41
cd

 60.00 ± 2.83
ab

 2.00 ± 1.41
a
 1.50 ± 0.71

a
 0.00 ± 0.00 

7 32.67 ± 1.15
ef
 60.33 ± 3.79

ab
 2.00 ± 1.00

a
 1.67 ± 0.58

a
 0.00 ± 0.00 

8 34.67 ± 0.58
de

 60.67 ± 1.15
ab

 2.33 ± 0.58
a
 1.67 ± 0.58

a
 1.00 ± 0.00

a
 

9 40.00 ± 1.00
ab

 57.33 ± 1.15
b
 1.33 ± 0.58

a
 1.33 ± 0.58

a
 0.00 ± 0.00 

Key: 1 = Infected and not treated, 2 = Infected and treated with 1ml honey, 3 = Infected and treated with 2ml 
honey, 4 = Infected and treated with 3ml honey, 5 = Infected and treated with 0.5ml augmentin, 6 = Infected and 
administered with 1ml honey – ORS, 7 = Infected and administered with 1ml commercial ORS, 8 = Infected and 

administered with 1ml homemade ORS and 9 = Not infected, not treated 

 

4. CONCLUSION 
 

This study has shown that honey sample from 
FUNAAB (HF) caused enhanced immune 
response in the rats against S. typhimurium. This 
honey also has haematinic, immunomodulatory, 
and immunostimulatory potentials in rats infected 
with S. typhimurium. These findings therefore 
could be exploited in boosting the immune 
system and in the treatment of diarrhoeal 
diseases caused by this bacterium.  
 

CONSENT  
 
It is not applicable  
 

ETHICAL APPROVAL  
 
As per international standard written ethical 
approval has been collected and preserved by 
the author(s).  

ACKNOWLEDGEMENTS 
 

The authors appreciate the effort made by Mr 
Jimoh, Kabiru Ayobami for cross checking the 
statistical analysis.  
 

COMPETING INTERESTS 
 
Authors have declared that no competing 
interests exist. 
 

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© 2019 John-Isa

 
et al.; This is an Open Access article distributed under the terms of the Creative Commons Attribution License 

(http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, 
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