ANTIBACTERIAL ACTIVITY AND CHARACTERISATION OF SOME EGYPTIAN HONEY OF DIFFERENT FLORAL ORIGIN
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Bulgarian Journal of Veterinary Medicine, 2019 ONLINE FIRST
ISSN 1311-1477; DOI: 10.15547/bjvm.2019-0066
Original article
ANTIBACTERIAL ACTIVITY AND CHARACTERISATION OF
SOME EGYPTIAN HONEY OF DIFFERENT FLORAL ORIGIN
A. G. HEGAZI1, F. M. AL GUTHAMI2, A. F. M. AL GETHAMI2,
E. A. FOUAD3 & A. M. ABDOU3
1
Department of Zoonotic Diseases, National Research Centre, 12622 Dokki, Giza,
Egypt; 2Al Guthami Foundation, Saudi Arabia; 3Department of Microbiology and
Immunology, National Research Centre 12622 Dokki, Giza, Egypt
Summary
Hegazi, A. G., F. M. Al Guthami, A. F. M. Al Gethami, E. A. Fouad & A. M. Abdou, 2019.
Antibacterial activity and characterisation of some Egyptian honey of different floral origin.
Bulg. J. Vet. Med. (online first).
The aim of the current study was to evaluate the antibacterial activity and to analyse the physico-
chemical properties of some Egyptian honey of different botanical origin in comparison with Manuka
honey from New Zealand. Antibacterial activity of Egyptian honey of different floral origin was
evaluated against five reference bacterial strains including both Gram-positive and Gram-negative
bacteria using well diffusion method. Pollen analysis was used to confirm the floral origin of honey.
Meanwhile, the physicochemical parameters including total phenolic and total flavonoid contents
were measured to assess the quality of honey. Some honey types including Flowers, Aashab, Barda-
kosh, and Black seed honey showed significant antibacterial activity against Staphylococcus aureus
(ATCC 25923) when compared with clindamycin. The same types of honey, except Black seed honey
exhibited significant antibacterial activity against Citrobacter diversus (ATCC 13315). The total phe-
nolic and total flavonoid contents ranged from 130.5±9.0 to 175.3±11.3 mg GAE/100 g honey and
22.3±1.7–30.9±2.6 mg RE/100 g honey, respectively. The results indicated that Egyptian honey is a
promising natural product that can be potentially used as an alternative to synthetic antibiotics. Au-
thentication of honey through the investigation of its physicochemical characteristics is a very impor-
tant determinant of its biological activity. Separation and investigation of the antimicrobial activity of
each of the active compounds of honey will provide more information on the efficacy and the mecha-
nism of its biological activity. Further studies are still needed to identify and standardise protocols for
the use of honey either in the protection against or the treatment of microbial infections.
Key words: antibacterial activity, Egyptian honey, physicochemical parameters, total phe-
nolic, total flavonoid
INTRODUCTION
Honey was recognised for its safe and ancient times. It contains several organic
effective use in alternative medicine since and inorganic compounds exhibiting vari-Antibacterial activity and characterisation of some Egyptian honey of different floral origin
ous biological activities including antibac- MATERIALS AND METHODS
terial, antiviral, antifungal, anti-inflam-
matory, antitumor and antioxidant activity Bacterial strains
(Hegazi & Abd El-Hady, 2009; Hegazi, Five pathogenic bacterial strains including
2011; Hegazi & AbdAllah, 2012; Hegazi Staphylococcus aureus (ATCC 25923)
et al., 2014; Khan et al., 2018). The bio- representing Gram positive bacteria and
logical effect of each honey type is a re- Escherichia coli (ATCC 35218), Proteus
flection of its composition which is af- vulgaris (ATCC 13315), Citrobacter di-
fected by different factors including pol- versus (ATCC 13315) and Salmonella
len composition, climate, environmental enterica (ATCC 700931) representing
conditions, harvesting, handling, and Gram negative bacteria were used in this
processing (Alvarez-Suarez et al., 2014; study.
Pasias et al., 2018). The floral source of
honey, which provide nectar and pollen, is Honey samples
one of the natural factors which greatly A total of 6 fresh Egyptian honey types of
affect the physicochemical characteristics different floral origin and Manuka honey
of honey (Warui et al., 2019). Physico- were used in this study (Table 1). Five
chemical properties of honey including samples were collected from each type of
pH, acidity, moisture, sugars and protein honey. Before and during the analyses,
content as well as sensorial characteristics samples were stored in glass containers,
including colour, texture, aroma and fla- transferred to the laboratory and main-
vour can be used as indicators of both tained at 4 oC until the time of the experi-
quality and origin of honey (Kumar et al., ment. Egyptian honey samples were col-
2018). The therapeutic activity of honey lected during the harvesting and flowering
including its antioxidant activity is mainly season period by local suppliers between
due to the presence of phenolic com- April and June 2017 from six different
pounds such as phenolic acid and flavo- geographical regions. Manuka honey from
noids (Cianciosi et al., 2018). New Zealand was used as the standard
In the current study, the antibacterial authorised honey type .
activity, pollen analysis, physicochemical
characteristics, total phenolic and total Pollen analysis
flavonoid contents of some Egyptian A total of 10 mL of honey were mixed
honey types were determined in compari- with 20 mL of distilled water. The mixture
son with Manuka honey from New Zea- was centrifuged at 5000 rpm for 10 min.
land. The supernatant was removed and 10 mL
Table 1. List of honey types and their floral origin
Honey name Floral origin/place
1 Sahrawy Desert plants/ south desert near Matroh Governorate
2 Zater Thyme herb: Thymus vulgaris
3 Flowers different flowers
4 Bardakosh Origanum majorana
5 Black seeds Nigella sativa
6 Aashab wild herbs
7 Manuka Manuka tree/ New Zealand
2 BJVM, ××, No ×A. G. Hegazi, F. M. Al Guthami, A. F. M. Al Gethami, E. A. Fouad & A. M. Abdou
of glacial acetic acid was added and the the honey solution and incubated for an-
mixture was allowed to stand for 5 min. other 2 h at 25 oC. After incubation, the
The mixture was then centrifuged and absorbance of the solution was measured
decanted. A total of 1 mL of 10% potas- at 765 nm by using a UV-Visible spectro-
sium hydroxide was added to the sediment photometer (Perkin-Elmer Lambda 25,
and boiled on a water bath at 70 oC for 5 Waltham, MA, USA). Gallic acid (0–
min. The mixture was then centrifuged to 1000 mg/L) was used as a standard
remove potassium hydroxide and the chemical for calibration curve prepara-
sediment containing pollen was mounted tion. The TPC was reported as a mean
in glycerin jelly on a glass slide. The slide value of triplicate assays and expressed as
was covered by a cover slip and the sam- milligram of gallic acid equivalent (GAE)
ples were observed under microscope with in the gram of honey (Isla et al., 2011).
400× magnification to identify the type of
Total flavonoid content (TFC)
pollen through the comparison with the
pollen source catalogues of flowers in the A total of 5 mL of honey solution with the
study area (Rosdi et al., 2016). concentration of 0.1 g/mL was mixed with
5 mL of 2% aluminum chloride (AlCl3).
Physicochemical analysis and sugar
The mixture was then incubated for 10
composition of honey
min at 25 oC. The absorbance of the
The physicochemical analysis of honey formed complex was measured at 415 nm
samples was carried out to determine by using UV-Visible spectrophotometer.
moisture content, hydroxymethylfurfural, Rutin with the concentration of 0–100
diastase activity and acidity. Sugar com- mg/L was used as a standard chemical for
position including glucose and fructose calibration curve preparation. The TFC
concentration was also determined was reported as a mean value of triplicate
(Ng’ang’a et al., 2013; Manzanares et al., assays and expressed as milligram of rutin
2014; 2017). equivalent (RE) in the gram of honey (Isla
et al., 2011; Chua et al., 2013).
Determination of mineral elements
Antibacterial activity of honey
The mineral composition including Fe,
Mn, Zn, Cu, Ca and Mg were determined A suspension of each bacterial strain
in honey samples by atomic absorption Staphylococcus aureus, Escherichia coli,
spectrometry (Silva et al., 2017). Proteus vulgaris, Citrobacter diversus
and Salmonella enterica was freshly pre-
Total phenolic content (TPC)
pared by inoculating fresh stock culture
The total phenolic content (TPC) of honey from the tested reference strain into broth
samples was analysed by using Folin- tube containing 7 mL of Muller Hinton
Ciocalteu reagent, based on the method Broth. The inoculated tubes were incu-
described by Beretta et al. (2005) with bated aerobically at 37 °C for 24 h. Serial
some modification (Bertoncelj et al,. dilutions were carried out for each strain
2007; Chua et al., 2013). Honey solution and dilution matching with 0.5 McFarland
(0.5 mL) was mixed with 2.5 mL of Folin- scale standard was selected for the screen-
Ciocalteu reagent (2N) and incubated for ing of antimicrobial activities. Antimicro-
5 min. Subsequently, 2 mL of sodium bial susceptibility of honey was deter-
carbonate solution (75 g/L) was added to mined using well diffusion method. A
BJVM, ××, No × 3Antibacterial activity and characterisation of some Egyptian honey of different floral origin
volume of 100 μL of cell culture suspen- samples indicated that not only the ex-
sion matching with 0.5 McFarland of tar- pected pollen type based on the known
get strains was spread onto Muller Hinton source of nectar, but also pollen from
agar plates. To investigate the antibacte- some other plants and flowers was present
rial activity, 50 μL of each honey sample (Table 2). The pollen content of Sahrawy
was added in individual wells. A well con- honey was of Ocimum basilicum (basil),
taining 50 μL of clindamycin (30 mg/mL) Citrullus colocynthis (bitter-apple), Ar-
was used as positive control. The plates temisia judaica and wildflowers. Mean-
were left for 1 h at 25 °C to allow a period while, pollen content of Zater (thyme) was
of pre-incubation diffusion in order to of Thymus bovei, Tilia cordata, and wild-
minimise the effect of variation in time flowers. Also, the pollen types found in
between the applications of different solu- flowers honey were of Acacia senegal,
tions. The plates were then incubated Ocimum basilicum, Artemisia judaica,
aerobically at 37 °C for 24 h to allow bac- and wild flowers. Bardakosh honey car-
terial growth. After incubation, the plates ried pollen of Origanum majorana and
were observed and the zones of inhibition wildflowers. Black seed honey carried the
were measured to evaluate the antibacte- pollen of Nigella sativa and wild flowers.
rial activity for each of the tested honey Finally, the pollen types found in the
samples. The experiment was carried out Aashab honey were of Ocimum basilicum,
in triplicates for statistical relevance and Citrullus colocynthis, Artemisia judaica
the mean± standard deviation (SD) of the and wildflowers.
results was calculated (Hegazi et al., The results of the determination of the
2014). physicochemical properties of honey sam-
ples indicated that all samples including
Statistical analysis
Manuka honey were comparable in mois-
All assays including the antibacterial ac- ture, glucose, fructose, and diastase en-
tivity of honey samples were conducted in zyme contents, but there were some sig-
triplicates. The data (mean± standard de- nificant differences in sucrose, HMF and
viation; SD) were then subjected to statis- acidity (Table 3). Sucrose contents of all
tical analysis (SPSS Ver. 21 (IBM, New types of the Egyptian honey were signifi-
York, US). Pearson’s correlation coeffi- cantly higher than sucrose content of
cient test (r) was employed to determine Manuka honey. Sucrose contents of Sah-
the strength of linear relationships be- rawy, Zater, Flowers, Bardakosh, Black
tween the variables. Duncan Test of Post seed, and Aashab honey were 4.5±1.5,
Hoc Multiple Comparisons in one-way 5±1.3, 4.8±2.1, 4.7±2.3, 4.6±3.3, and
ANOVA was applied for comparison be- 4.3±1.2 g/100 g respectively as compared
tween and within the groups. A probabi- with 1±0 g/100 g for Manuka honey.
lity value PTable 2. Pollen content of different honey types
BJVM, ××, No ×
Pollen type
Thymus Origanum Nigella Acacia Ocimum Tilia Citrullus Artemisia Wild
Honey type/
bovei majorana stevia senegal basilicum cordata colocynthis Judaica flowers
Sahrawy + + + +
Zater (Thyme) + + +
flowers + + + +
Bardakosh + +
Black seed + +
Aashab + + + +
Table 3. Physicochemical properties of different honey types (mean±SD; n=5)
Honey types Moisture Glucose Fructose Fructose/ Sucrose Diastase HMF Acidity
(g/100 g) (g/100 g) (g/100 g) Glucose (g/100 g) (oGothe) (mg/kg) (meq/kg)
Manuka 14±2 32±2 36±2 1.13±0.01 1±0 11±2 25±1 36±2
Sahrawy 15±2 31±1 37±2 1.19±0.03 4.5±1.5* 18±1 45±3* 30±1
Zater (Thyme) 17±1 34±1 32±1 0.94±0.00 5±1.3* 19±2 53±1* 31±3
Flowers 19±2 33±3 30±3 0.91±0.01 4.8±2.1* 16±2 33±2 22±2*
Bardakosh 18±1 31±2 33±2 1.06±0.00 4.7±2.3* 19±1 36±3 35±1
Black seed 16±3 35±1 36±2 1.03±0.03 4.6±3.3* 20±1 41±4* 39±3
Aashab 14±2 32±4 35±1 1.10±0.11 4.3±1.2* 22±2 22±3 28±2
* PAntibacterial activity and characterisation of some Egyptian honey of different floral origin
wers honey (22±2 meq/kg) was signifi- g/100 g respectively). Fructose to glucose
cantly lower than that of Manuka honey ratios (F/G) for all honey samples were
(36±2 meq/kg). The moisture content of comparable with values of 1.13±0.01,
the analysed honey samples ranged from 1.19±0.03, 0.94±0.00, 0.91±0.01, 1.06±
14±2–19±2 g/100 g indicating compara- 0.00, 1.03±0.03and 1.10±0.11 for Manu-
ble results for moisture contents of both ka, Sahrawy, Zater, Flowers, Bardakhosh,
Egyptian honey types and Manuka honey. Nigella sativa and Aashab respectively.
Fructose content of all honey samples The diastase numbers of the examined
was from 30±3 to 37±2 g/100 g. Glucose honey samples were comparable and
contents of all types of honey did not ranged from 11±2 to 22±2 °G.
show significant differences. The Egyp- The mineral content of all honey sam-
tian Black seed honey recorded the high- ples including iron, manganese, zinc, cal-
est glucose content: 35±1 g/100 g, fol- cium, magnesium and copper were meas-
lowed by Zater 34±1 g/100 g, while the ured in mg/kg (Table 4). The iron contents
lowest content was recorded in Sahrawy in Black seed, Bardakosh, and Zater types
and Bardakosh honey (31±1 and 31±2 of honey (5.1±1.1, 4.9±06, and 4.8±1.0
Table 4. Mineral elements (mean±SD; n=5) of different honey types (mg/kg)
Honey types Fe Mn Zn Ca Mg Cu
Manuka 3.7±0.3 1.6±0.2 1.7±0.6 61.0±3.5 30.1±3.1 1.22±0.2
Sahrawy 3.5±0.5 1.5±0.6 1.8±0.5 50.8±6.4 25.1±3.4 1.11±0.1
Zater (Thyme) 4.8±1.0* 1.7±0.2 1.6±0.6 56.1±5.7 25.2±2.0 0.91±0.2
Flowers 3.6±0.2 1.3±0.5 1.4±0.4 43.3±4.7 26.1±4.1 0.94±0.2
Bardakosh 4.9±0.6* 1.6±0.3 1.9±0.6 59.3±7.5 24.7±2.6 1.16±0.4
Black seed 5.1±1.1* 1.6±0.5 2.1±0.5 66.2±3.8 24.6±3.5 1.14±0.1
Aashab 3.5±0.4 1.4±0.7 1.5±1.0 45.9±6.6 20.3±2.2 0.89±0.3
* PA. G. Hegazi, F. M. Al Guthami, A. F. M. Al Gethami, E. A. Fouad & A. M. Abdou
Table 5. Antibacterial activity of different honey types compared with clindamycin (mean±SD; n=5)
Bacterial strains
Honey types/ S. aureus E. coli P. vulgaris C. diversus S. enterica
antibiotic (ATCC (ATCC (ATCC (ATCC (ATCC
25923) 35218) 13315) 13315) 700931)
Clindamycin 30 mg 2.2±0.3 1.9±0.2 1.8±0.1 1.5±0.3 1.6±0.1
Manuka 2.8±0.5 2.3±0.1 2.0±0.4 1.9±0.1 1.9±0.1
Sahrawy 2.7±0.1 2.0±0.1 2.4±0.2 2.5±0.1 2.4±0.1
Zater (Thyme) 3.1±0.1 2.0±0.2 2.2±0.1 2.3±0.5 2.3±0.1
Flowers 3.8±0.1* 2.0±0.2 2.2±0.5 2.8±0.1* 2.4±0.4
Bardakosh 3.4±0.2* 2.0±0.4 2.4±0.3 2.5±0.1* 2.1±0.1
Black seed 3.3±0.1* 2.2±0.2 2.3±04 2.4±0.2 2.1±0.3
Aashab 3.5±0.2* 2.1±03 2.1±01 2.6±03* 2.2±01
* PAntibacterial activity and characterisation of some Egyptian honey of different floral origin
bial compounds (Ayaad et al., 2012; Fyfe is currently used in clinical applications
et al., 2017; Hegazi et al., 2017; Hussain, (Vatansever et al., 2013).
2018). Adulteration of honey either by Moisture content of honey is one of
adding cheap sugar syrup or by feeding the most important parameters. Low mois-
the bees on sugar solutions is a major ture content elongates honey shelf life
worldwide problem that leads to the loss while high moisture levels promote the
of many biological properties of honey process of fermentation during storage.
including its effective antimicrobial activi- Moisture content of Egyptian honey sam-
ty. Therefore, the selection of fresh and ples were comparable to the moisture con-
authentic honey based on the physico- tent of Manuka honey and within the ac-
chemical characteristics is a very impor- cepted range of moisture content which, in
tant step towards the potential use of spe- general, should not exceed 20% (Oroian
cific types of honey as candidate antibac- & Sorina, 2017; Se et al., 2019). The
terial agents. moisture content of the honey is affected
Around 200 compounds have been re- by the temperature and relative humidity
ported in honey (da Silva et al., 2016). in the geographical origin during honey
Honey is produced through the digestive production by bees. Although some ex-
processing of nectar collected from flow- ceptions may apply for the moisture con-
ers (Cornara et al., 2017). In the current tent of some types of honey, similar re-
study honey samples were of multifloral sults were documented earlier for honey
origin as they were rich in different pollen samples of different origin including
types indicating that nectar was collected Egyptian, Yemeni, Saudi and Kashmiri
from different plant sources. Although honey (El-Sohaimy et al., 2015).
unifloral honey is usually more expensive Sugar content of honey is one of the
and appreciated than multifloral honey parameters which are used to assess the
(Dias et al., 2015; Di Rosa et al., 2018), authenticity of honey and the evaluation
the last was reported to have diverse of its overall quality. Mixing the honey
classes of volatile compounds due to the with other cheaper sugar syrups is a
diversity of its floral origin (Devi et al., worldwide problem of honey adulteration
2018), which could be the cause of more (Salvador et al., 2019). Sugar analysis of
potent biological activity and medical honey is a good indication of whether the
importance. In the current study, we used honeybees were fed naturally on flowers
Manuka honey produced from the nectar nectar or they were fed on sugar solution.
of manuka tree as the standard honey. In When the glucose content of honey is
spite of its monofloral origin and the mul- much higher than its fructose content this
tifloral origin of the Egyptian honey sam- indicates the use of sugar solution to feed
ples; Manuka honey was used for com- honeybees (El-Sohaimy et al., 2015).
parison due to its trusted source and gua- Sugar contents of Egyptian honey samples
ranteed quality. The Ministry of Primary were comparable to the sugar content of
Industries in New Zealand approved a 5 Manuka honey. The sum of glucose and
test analysis since 5 January 2018 to pre- fructose, which measures the content of
vent adulteration and to ensure the authen- reducing sugars in honey, was within the
ticity of Manuka honey (Anonymous, accepted range to prove the authenticity of
2018). Furthermore, Manuka honey is honey. Fructose and glucose were the
considered as medical grade honey which most dominant sugars in honey samples
8 BJVM, ××, No ×A. G. Hegazi, F. M. Al Guthami, A. F. M. Al Gethami, E. A. Fouad & A. M. Abdou
and the fructose to glucose ratios (F/G) The mineral composition of honey is an
indicated the natural feeding of honey- important factor to determine the nutri-
bees. Meanwhile, sucrose content in all tional value of honey and it also affects
samples did not exceed 5% which is the the colour and the flavour of honey (Kadri
accepted level to prove the authenticity of et al., 2017; Silva et al., 2017). The simi-
honey. Higher content of sucrose may larity of mineral contents between differ-
indicate adulteration or artificial feeding ent types of Egyptian honey could be due
of bees on some types of sugar syrup to the similarity in soil and climate as al-
(Salvador et al., 2019). most all honey types were collected from
Both diastase activity and hydroxy- areas around The Nile River and Delta
methylfurfural content are also two impor- with almost the same soil contents and the
tant parameters used to prove the authen- same climate.
ticity and freshness of honey and as indi- The total phenolic content of different
cation of adulteration. Many factors are types of honey in our study were
affecting diastase activity including the 130.5±9.0 to 175.3±11.3 mg GAE/100 g
age of bees, nectar collection period, the honey which is higher than the results
physiological period of the colony and the found in honey, especially monofloral
quantity of nectar and its sugar content. honey, from other countries including
The maximum level for the 5-HMF con- India (47–98 mg GAE/100 g honey)
tent in honey was established by the Co- (Saxena et al., 2010), Argentina (18.730–
dex Alimentarius of the World Health 107.213 mg GAE/100 g honey) (Isla et
Organization and the European Union to al., 2011), Burkina Faso (32.59–114.75
be 40 mg/kg but in case of honey from mg GAE/100 g honey) (Meda et al.,
countries with tropical ambient tempera- 2005), Portuguese (30.87 to 87.27 mg
tures the HMF content should not exceed GAE/100 g) (Gonçalves et al., 2018), and
80 mg/kg (Anonymous, 2001; Pasias et al. Romania (2–125 mg GAE/100 g honey)
2017). In our study all samples were (Al et al., 2009).
within the accepted range for diastase Variable levels of total phenolic con-
number and HMF content as an indication tents were reported in different honey
of the authenticity and freshness of all types. This variability was associated with
samples which was achieved by collecting the floral origin of honey and multifloral
honey samples during the flowering sea- honey was found to have higher phenolic
son, preventing their exposure to heat and contents than monoforal honey. Multiflo-
shortening the storage time before the ral honey was also higher in its flavonoid
experiment. contents than monolfloal honey. The phe-
Acidity of all honey samples was nolic compounds, especially flavonoids,
found to be within the accepted range. of honey are a major determinant of its
The presence of organic acids, particularly antioxidant, antimicrobial, antiviral, anti-
the gluconic acid, was found to affect fungal, and anti-inflammatory activity. It
honey flavour, texture, shelf life and sta- is worth mentioning that, the quality of
bility (Warui et al., 2019). polyphenols is more important than their
The source of honey, the geographical quantity (Pasupuleti et al., 2007; Isla et
origin and the type of both plants and soil al., 2011).
are the most important parameters to de- In our study, most types of honey were
termine the mineral composition of honey. comparable in their antibacterial activity
BJVM, ××, No × 9Antibacterial activity and characterisation of some Egyptian honey of different floral origin
which may be attributed to the narrow cols for the use of honey either in the pro-
ranges of their total phenolic contents, tection against or the treatment of micro-
total flavonoid contents, and sugar con- bial infections.
tents. Although there was a positive corre-
lation between TPC and antibacterial ac-
ACKNOWLEDGEMENTS
tivity of both Bardakosh and Black seed
honey, there was a negative correlation The authors are grateful for the financial sup-
between TPC and antibacterial activity of port by the National Research Center of Egypt
Flowers honey. A significant correlation under registration number 12/5/1 and Al
between TPC and antibacterial activity Guthami Foundation, Saudi Arabia.
against P. aeruginosa was reported earlier
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