Biological Trace Element Research

https://doi.org/10.1007/s12011-018-1305-2

Determination of Quality Criteria that Allow Differentiation

Between Honey Adulterated with Sugar and Pure Honey
Cevat Nisbet 1 & Filiz Kazak 2 & Yuksel Ardalı 3

Received: 27 July 2017 / Accepted: 8 March 2018

# Springer Science+Business Media, LLC, part of Springer Nature 2018

Abstract
This study used various parameters of honey to develop a potentially more robust approach to the detection of adulterated honey. For
this purpose, 25 multifloral, natural honey samples and 20 samples of adulterated honey produced by bees that had been fed
supplementary sucrose syrup were analysed. The mean total phenolic content of the natural honeys was considerably higher than
in the adulterated honeys at 157 ± 13 and 35.2 ± 7.3 mg GAE/100 g, respectively. Similarly, considerable variation was determined
between natural and adulterated honeys in terms of total flavonoids (3.3 ± 0.3 and 2.1 ± 0.4 mg QE/100 g, respectively), antiradical
activity (87.9 ± 12 and 163 ± 11 mg/mL, respectively) and proline content (202 ± 26 and 71.1 ± 21.6 mg/kg, respectively.) The
potassium, phosphorus, calcium and magnesium contents of natural honeys were also higher than in adulterated honeys (P < 0.01).
In conclusion, the determination of the proline level, phenolic content, antioxidant activity and mineral profile may collectively provide
a more holistic method approach to the differentiation of natural and adulterated honey, and also for comparing their food values.

Keywords Adulterated honey . Antioxidant . Honey composition . Trace elements

Introduction proteins [5]. Honey also contains small amounts of amino

Honey bees produce honey from the nectar of flowers, plant
exudates and the secretions of plant-sucking insects [1].
Honey is an esteemed food that has also been used as a med-
ical product for millenia. It is widely consumed as a therapeu-
tic product due to its anti-inflammatory, antimicrobial, antiox-
idant, antiviral and probiotic qualities [2–4]. It contains about
180 substances, those in the highest amounts are sugars (glu-
cose, fructose, maltose and sucrose), water, minerals and
* Cevat Nisbet
cnisbet@omu.edu.tr
Filiz Kazak
filizkazak@mku.edu.tr
Yuksel Ardalı
yuksel.ardali@omu.edu.tr
1
Department of Biochemistry, Faculty of Veterinary Medicine,
Ondokuz Mayis University, 55220 Samsun, Turkey
2
Department of Biochemistry, Faculty of Veterinary Medicine,
Mustafa Kemal University, 31060, Antakya, Hatay, Turkey
3
Department of Environment Engineering, Faculty of Engineering,
Ondokuz Mayis University, 55220 Samsun, Turkey
acids, vitamins, flavonoids, phenolic acids, enzymes and or-
ganic acids [3]. However, the composition of natural honey
varies widely, depending mostly on the combination of nectar
sources, and its quality varies according to the climatic condi-
tions of the region of production, production techniques, han-
dling conditions and storage methods [4, 6].
The adulteration of honey is a serious, widespread problem
that has a substantial economic impact and negative impacts on
the nutrition and health of consumers [7, 8]. The most common
type of adulteration is the addition of different sugar syrups
during or after its production [6]. Various types and combinations
of syrups have been used in the adulteration of honey. The
inverted syrup, rice syrup, starch-based sugar syrups, high-
fructose corn syrup, glucose syrup and saccharose syrups used
to adulterate honey are sometimes diluted with water before
addition, or are added directly [8–10]. These procedures change
the biochemical composition of honey, particularly the proline,
vitamin, mineral and enzyme content [11]. Therefore, it is crucial
that a comprehensive method be developed to detect adulterated
honey to ensure the quality, safety and credibility of the product.
A number of different chemical parameters, including pro-
line, mineral and nitrogen content; carbohydrate composition;
pollen and amino acid profiles; enzyme content and stable
carbon isotopes, have been used to distinguish between

natural and adulterated honey [1, 8, 12, 13]. This differ-
entiation is a complex, time-consuming and expensive
task because there are various sugar syrups and the
profiles of sugar syrup blends can be easily modified
to approximate the profiles of natural honey [9]. In ad-
dition, the current methods have several limitations [8,
9]. Honey has a considerable number of nutritional,
healing and prophylactic qualities that are directly attrib-
utable to its chemical constitution. To maximise its ben-
eficial effects, honey must not contain contaminating
and adulterating substances [19]. Therefore, there is a
pressing need to identify convenient markers that allow
honeys to be differentiated in terms of their authenticity
and quality. In that context, the aim of the present study
was to assess a number of potentially definitive charac-
teristics of natural honey, namely proline, protein, min-
eral, antioxidant, total flavonoid content and phenolic
content, that may clearly differentiate it from honey de-
liberately adulterated for financial gain.
Materials and Methods
Honey Samples In this study, 45 samples of honey were tested.
Samples of honey collected directly from 45 different bee-
keepers there. They included 20 natural honey samples
(Group I) from environments with considerable floral diversity
in eastern Anatolia (Erzurum), Turkey. The other 25 honey
samples (Group II) were purchased from beekeepers in eastern
Anatolia (Erzurum) who had produced honey from bees fed
with supplementary saccharose syrup in different combinations
and concentrations. Erzurum Province in north-eastern Turkey,
which has a diverse landscape and floral diversity, has a pasture
area of 1,545,869 ha. In this mixed pasture, among the com-
mon, nectar-producing plants are Anthemis tinctoria L.,
Centaurea solstitialis L., Astragalus spp., Carduus nutans L.,
Carum carvi L., Centaurea triumfettii All., Cirsium arvense (L.)
Scop., Cotoneaster horizontalis Decne.,Crataegus tanacetifolia
(Lam.) Pers., Crataegus monogyna Jacq., Crataegus orientalis
Pallas ex Bieb., Duacus carota L., Diospyros lotus L., Echium
italicum L., Echium plantagineum L., Epilobium angustifolium
L., Euphorbia macroclada Boiss., Heliotropium suaveolens
Bieb., Lamium spp., Lythrum salicaria L., Marrubium
astracanicum Jacq. subsp. astracanicum Jacq., Medicago sativa
L., Onobrychis spp., Rubus canescens Dc. Salix spp., Salvia
spp., Satureja hortensis L., Solidago virgaurea L. subsp.
Alpestris. and Taraxacum officinale [20].
Types of Honey The bees in Group I only exploited natural
flora. Group II bees, besides gathering nectar from floral
sources, were supplied about 10 kg of sugar syrup per hive.
Honey yield from Group II bees was reported to be about 30%
higher than for Group I bees
Nisbet et al.
Determination of Total Phenolic and Flavonoid
Contents
Phenolic compounds were extracted from the honey accord-
ing to the method described by Dimins et al. (2010) [14]. The
total concentration of phenolic compounds was estimated
spectrophotometrically by using the reagent, Folin–
Ciocalteu, with gallic acid used as the standard. A five gram
(5 g) subsample of the honey sample was diluted to 50 ml in
distilled water and filtered through a Whatman No. 1 paper.
Half a millilitre (0.5 mL) of this honey solution (10%) was
mixed with 2.5 mL of 0.2 N Folin–Ciocalteu reagent and
2.0 mL of 7.5% sodium carbonate (Na2CO3). After incubation
at room temperature for 2 h, the absorbance of the mixture was
measured in a spectrophotometer (OPTİMA SP-3000 PLUS
model) at 760 nm against a methanol blank. The calibration
curve was plotted with gallic acid (0–200 mg/mL) employed
as the standard, with the result calculated as the gallic acid
equivalent per 100 g of honey (GAE mg/100 g of honey).
The total flavonoid concentration in the honeys was deter-
mined with the Meda method [15], a procedure that involves
the use of aluminium chloride (AlCl3). Five millilitres (5 mL)
of 2% AlCl3 in methanol was mixed with the same volume of
a 10% honey solution in deionised water. After 10 min of
incubation at room temperature, the absorbance was measured
in a spectrophotometer at 415 nm against a blank sample
consisting of a 5-mL honey solution dissolved in 5 mL meth-
anol but not including AlCl3. The total flavonoid concentra-
tion was determined from a standard curve with quercetin
(Sigma-Aldrich) (0–50 mg/L) employed as the standard. The
results were expressed as milligrams of quercetin equivalent
(QE) per 100 g of honey.
Determination of Total Antioxidant Content
and Radical Scavenging Activity
The scavenging activity of honey samples for the radical 2,2-
diphenyl-1-picrylhydrazyl (DPPH) was determined with the
method of Velazquez et al. (2003) [16], with some slight changes
[15]. DPPH is a stable, free radical widely used for the determi-
nation of antioxidant activity. Honey samples were dissolved in
methanol at different concentrations (25–100 mg/mL), and
0.75 ml of each sample was then mixed with 1.5 mL of DPPH
dissolved in methanol (0.02 mg/mL). After 15 min of incubation
at room temperature, the absorbance of the reaction mixture was
recorded at 517 nm against a reference methanol blank. Radical
scavenging activity was calculated as per the following formula:
[(Absorbance of Blank – Absorbance of sample)/Absorbance of
Blank] × 100. The IC50, the concentration causing 50% inhibi-
tion in each honey sample, was determined from the graphed
relationship between the concentration of the sample and the
percentage of the DPPH radical that was inhibited.
Determination of Quality Criteria that Allow Differentiation Between Honey Adulterated with Sugar and Pure...

Proline Content Five grams (5 g) of each honey was placed in a porcelain

The proline concentration was determined with a method
adapted from that of Meda et al. (2005). A half millilitre
(0.5 mL) solution of honey (5 g/100 mL of distilled water)
was mixed with 1 ml of formic acid (80%) and 1 mL of 3%
ninhydrin solution in ethylene glycol monomethylether, and
then vortexed for 15 min. The mixture was placed in a 70 °C
water bath for 15 min. Five millilitres of a solution of 2-propanol
in deionised water (50% concentration) was then added. The
mixture was cooled for 45 min and the absorbance determined
by spectrophotometric analysis (OPTİMA SP-3000 PLUS mod-
el, Japan) at 510 nm. For comparison purposes, deionised water
and a 0.032 mg/ml solution of proline were used as the blank
and standard solutions, respectively. The proline concentration
in mg/kg of honey was calculated as follows [15]:
Proline (mg/kg) = (Es/Ea) × (E1/E2) × 80, where
Es = absorbance of the sample solution;
Ea = absorbance of the proline standard solution;
E1 = amount of proline in the standard solution (mg);
E2 = weight of honey (gr) and
80 = dilution factor.
Protein Analysis
crucible of known weight and then heated. The resulting white
ash was weighed, dissolved in 3 mL of concentrated nitric acid
(65% v/v) and diluted with deionised water in a 25-mL cali-
brated flask. The solution was used to determine potassium
(K), calcium (Ca), magnesium (Mg), iron (Fe) and zinc (Zn)
concentrations with the direct air-acetylene flame method [19].
In addition, the phosphate concentration was determined by
photometric analysis, namely the phosphomolybdenum blue
(PMB) method. The method is analogous to EPA 365.2 + 3,
APHA 4500-P E and DIN EN ISO 6878 analysis. Results for
all minerals were expressed as mg/kg of honey [21].
Statistical Analysis
To compare the natural and adulterated honey groups, the
post-hoc test was used for the determination of uniformity
within samples. The descriptive statistics were calculated as
means ± SE values, with the coefficient of variation CV (%)
and min-max values employed in the assessment of uniformi-
ty. To compare the means of the honey groups, the Mann-
Whitney non-parametric test procedure was used due to the
heterogeneity of variances [22]. All calculations and analyses
were conducted by using SAS (2014).

The protein content of the honey samples was determined by

spectrophotometry at 595 nm, utilising the Bradford method
(1976), with minor modification introduced by Azeredo et al.
(2003). Initially, 5 mL of Coomassie Brilliant Blue was added
to a 0.1 mL suspension of honey. After a 2-min incubation
period, the absorbance was measured against bovine serum
albumin (BSA), which is universally used as the standard
protein (10–100 mg/0.1 mL), in 0.15 M NaCl, for the deter-
mination of protein content [17, 18].
Mineral Analysis
An atomic absorption spectrophotometry (AAS) device
(Unicam 929) was used for the analysis of mineral content.
Results and Discussion
To guarantee the authenticity of honey and protect consumers
from fraudulent practices, the quality of honey must be
checked analytically. This study was concerned with the in-
vestigation of parameters, namely protein, mineral and proline
content; radical scavenging activity and total phenolic and
flavonoid contents, for their usefulness in the discrimination
of natural and adulterated honey (Tables 1 and 2).
The total flavonoid content of honey normally ranges between
2 and 10 mg/100 g [16, 23]. A considerable body of research has
shown that the botanical origin and flavonoid profiles of a honey
are correlated. This relationship suggests that flavonoid analysis

Table 1 Mean and standard error (mean ± SE) values for T. protein, proline, T. flavonoids, T. phenolics and antioxidant concentrations in natural and
adulterated honey samples.

Factor Natural honey Adulterated honey P value

Mean ± SE CV (%) Min-max Mean ± SE CV (%) Min-max

T. flavonoids (mg QE/100 g) 3.3 ± 0.3a 9.9 1.3–5.9 2.1 ± 0.4b 19.4 0.8–5.0 0.0002
T. phenolics (mg GAE/100 g) 157 ± 13a 2.0 56.9–230.1 35.2 ± 7.3b 9.0 2.5–84.5 0.0001
Antioxidants (g/mL) 87.9 ± 12b 3.6 41.4–156.5 163 ± 11a 1.9 102.5–25 0.0001
Total protein (mg/g) 36.9 ± 1.5a 8.5 29.5–55.3 31.5 ± 2.5b 10.0 18.2–41.3 0.0001
Proline (mg/kg) 202.2 ± 26.1a 12.9 69.8–407.3 71.1 ± 21.6b 30.4 11.6–221.1 0.0001

Different letters in the same row indicate a significant difference between means (p < 0.05)
 Nisbet et al.

Table 2 Mean and standard error

(mean ± SE) values (ppm) for Ca, Minerals Natural honey Adulterated honey
Mg, K, P, Zn and Fe
concentrations in natural and Mean ± SE (mg/kg) CV (%) Min-max Mean ± SE CV (%) Min-max P value
adulterated honey samples (mg/kg)

Ca 43.3 ± 5.5a 7.3 22–63 34.9 ± 4.7b 9.1 19–73 0.0001

a
Mg 26.1 ± 5.4 12.1 5–34 17.9 ± 4.8b 17.6 10–50 0.0001
K 1114 ± 178a 0.3 330–1839 309 ± 32b 1.0 107–521 0.0001
P 190 ± 30a 1.7 79–277 83.1 ± 9.0b 3.8 47–160 0.0001
Zn 7.5 ± 2.2b 29.3 3–19 10.2 ± 4.8a 47.0 0.2–19 0.0001
Fe 3 ± 0.2a 6.7 2–4 2.9 ± 0.2a 6.9 1–4 0.623

Different letters in the same row indicate a significant difference between means (p < 0.05)

could be useful in the determination of the origin of honey [24,
25]. In addition, there is remarkable variation in the DPPH scav-
enging activity and total concentration of phenols in honey, de-
pending on the botanical origin of the various nectars contribut-
ing to its production [26]. In the present study, the mean total
flavonoid concentration in the natural and adulterated honeys
was 3.3 ± 0.3 and 2.1 ± 0.4 mg/100 g, respectively (P < 0.01)
(Fig. 1). This substantial difference may offer a genuine oppor-
tunity to discriminate between authentic and adulterated honeys.
The total phenolic content of the honey samples was also
analysed by spectrophotometry, coupled with coulometric detec-
tion. The mean total phenolic content of 157 ± 13 mg/100 gin
natural honeys was significantly higher than the 35.2 ± 7.3 mg/
100 g in adulterated honeys (P < 0.01) (Fig. 1). The differentia-
tion of natural and adulterated honeys was therefore shown to be
possible by the substantial difference in the concentration of total
phenols. Our study also revealed that the natural and adulterated
honeys had 50% inhibitory concentrations of 87.9 ± 12.0 and
163 ± 11 mg/mL, respectively (P < 0.01) (Fig. 1), and that the
most potent DPPH scavengers were among the natural honey
samples. Therefore, both the total phenolic content and antioxi-
dant activity of honey may be useful indicators for the determi-
nation of the naturalness of honey and by inference, the manage-
ment practices of honey producers [24–27].
200
The protein content of honey varies according to the species
of the honeybee; the honeys produced by Apis cerana and Apis
mellifera contain from 0.1 to 3.3% protein, and from 0.2 and
1.6% protein, respectively [28]. The protein and amino acid
content of honey depends on the combination of floral sources
and the fluids and modified nectar secretions from the salivary
glands and pharynx of honeybees [29–32]. A small fraction of
the proteins present in honey are enzymes, including acid phos-
phatase, catalase, diastase, glucose oxidase and glucosidase,
which are produced by the bees themselves or originate in the
nectar [29, 33]. In the current experiment, the mean total protein
content (36.9 ± 1.5 mg/g) of the natural honeys (Group I) was
significantly higher than that of the adulterated honeys (Group II)
(31.5 ± 2.5 mg/g) (P > 0.01) (Fig. 2). In addition, analysis also
showed that the CV% value for total protein is more uniform in
natural honey. The present study therefore demonstrated that the
protein content of honey is a factor that can be reliably used for
the detection of adulterated honey with < 30% added sugar.
All honey contains about 50–300 mg/kg of amino acids,
with the most abundant amino acid being proline, which rep-
resents 50–85% of the amino acid total. Especially, certain
ratios between concentrations of proline (minimum value of
180 mg/kg) could be used to separate natural and adulterated
honey [31, 34]. In the present experiment, the mean proline
contents of the natural and adulterated honeys were 202 ± 26

180
250
163 202
157
160
200
140

120
150
100 87,9 Natural Honey
Natural Honey
80 Adulterated Honey
100 71,1 Adulterated Honey
60

40 35,2
50 36,9 31,5
20
3,3 2,1
0
Total Flavonoid (mg Total Phenolic (mg Anoxidant (mg/ml) 0
QE/100 g) GAE/100 g) T. Protein (mg/g) Proline (mg/kg)
Fig. 1 The observed levels of mean total phenolic content, flavonoid and Fig. 2 Mean and standard error values for protein and proline
radical scavenging activity of natural honeys and adulterated honeys concentrations in experimental groups (mean ± SE)
Determination of Quality Criteria that Allow Differentiation Between Honey Adulterated with Sugar and Pure...
and 71.1 ± 21.6 mg/kg honey, respectively (P < 0.01) (Fig. 2).
This very substantial difference suggests that the proline con-
tent may be a more suitable indicator than protein content for
the differentiation of natural and adulterated honeys.
Studies have revealed that the mineral content of honey
varies, depending on both the species of the plant and the type
of soil in which is growing [30, 35–37]. Therefore, the macro-
mineral content of honeys can therefore provide essential infor-
mation for consumers about the quality of honey [35]. Calcium,
potassium, sodium, phosphorus, magnesium, sulphur and sili-
con are the most abundant elements in honey, representing
more than 97% of the total mineral content [36, 38]. In our
study, for the pure and adulerated honeys, the mean potassium
contents were 1114 ± 179 and 309 ± 32 mg/kg, the mean phos-
phorus contents were190 ± 30 and 83.1 ± 9.0 mg/kg, the mean
calcium contents were 43.3 ± 5.5 and 34.9 ± 4.7 mg/kg and the
mean magnesium contents were 26.1 ± 5.4 and 17.9 ± 4.8 mg/
kg, respectively. In four cases, the amount of these four min-
erals (K, P, Ca, Mg) in the natural honeys was much higher than
in the adulterated honeys (P < 0.01) (Table 2). The mean zinc
concentrations of 7.5 ± 2.2 and 10.2 ± 4.8 mg/kg in the natural
and adulterated honeys, respectively, were significantly differ-
ent (P < 0.01). However, there was no significant difference
between the pure and adulterated honeys for Fe level (P =
0.623). These results indicate that K, P, Ca and Mg may be
suitable indicators for the authentication of natural honeys.
Conclusions
This study investigated parameters that are potentially useful in
differentiating between pure honey samples and honey samples
adulterated with less than 30% of sugar syrup. Results indicate
that the proline level; total phenolic content; antioxidant activity
and potassium, calcium, magnesium and phosphate mineral
concentrations are potentially useful in the differentiation of pure
and adulterated honey. The determination of the values of single
parameters of honey cannot be relied upon to detect the adulter-
ation of honey but the analysis of the profiles of particular com-
ponents may be suitable for this purpose. Therefore, multi-
component analysis, which involves a suite of parameters that
facilitate discrimination, appears to be a suitable approach for
quality control, and by inference, the authentication of honeys.
Acknowledgments The authors thank Dr. Serhat Arslan for editing the
content of this manuscript related to the statistical analysis and Gregory T.
Sullivan (School of Earth and Environmental Sciences, University of
Queensland, Brisbane, Australia) for editing the English in an earlier
version of this manuscript.
Compliance with Ethical Standards
Conflict of Interest The authors declare that they have no conflicts of
interest.
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