International Journal of Food Properties

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Rheology and crystallization kinetics of honey:

Present status

Bhesh Bhandari , Bruce D'Arcy & Camilla Kelly

To cite this article: Bhesh Bhandari , Bruce D'Arcy & Camilla Kelly (1999) Rheology and
crystallization kinetics of honey: Present status, International Journal of Food Properties, 2:3,
217-226, DOI: 10.1080/10942919909524606

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INTERNATIONAL JOURNAL OF FOOD PROPERTIES, 2(3), 217-226 (1999)

RHEOLOGY AND CRYSTALLIZATION KINETICS OF HONEY: PRESENT

STATUS

Bhesh Bhandari1,*, Bruce D'Arcy1, and Camilla Kelly2

1
Food Science and Technology, School of Land and Food, University of Queensland, Gatton
QLD 4345, Australia (Tel: +61-7-5460 1196, Fax: +61-7-5460 1171, and E-mail:
bb@burger.uqg.uq.edu.au)
2
Department of Chemical Engineering, University of Queensland, St. Lucia
QLD 4072, Australia; 'Corresponding author

ABSTRACT

Crystallization property of honey is a matter of interest for beekeepers, honey handlers and
processors. Honey is basically a sugar syrup with about 16-18% moisture content (wet
basis). The composition and rheology are some of the important parameters that influence the
crystallization behavior of honey. At present, most of the crystallization prediction methods
are based on the composition considering honey as a glucose-fructose-water system. This
review paper presents current methods used to predict honey crystallization and puts forward
a hypothesis based on viscosity and glass transition temperature.

COMPOSITION OF HONEY

The composition of honey is influenced by the floral source, climate and environmental
conditions, and beekeeper skills. Therefore, in every region of the world, the composition of
the honeys is different (Table 1). Honey is a solution of various sugars and is frequently
supersaturated at normal temperatures with respect to glucose. Glucose and fructose (invert
sugars) are the principal sugars in honey, accounting for 33-35% and 38-40% respectively.
Fructose content is normally higher than glucose, although some exceptions have been
reported (Sanz et al., 1994). These two reducing sugars constitute above 65% (w/w) of
honey. The minimum amount of reducing (invert) sugars in honey set by the Australian Food
Standards Code is 60% (w/w) (ANZFA, 1998). In addition, there are other minor sugars
present in honey, mainly sucrose and maltose, which can vary from 1-5% each. Several
trisaccharides and higher oligosaccharides in minor amounts are also present at various
proportions in honeys (Swallow and Low, 1990; White, 1978), which are not individually
described in this paper. The amount of higher sugars (such as maltose) is reported to
increase at the expense of monosaccharides during honey storage, depending on storage

217

Copyright © 1999 by Marcel Dekker, Inc. www.dekker.com

218 BHANDARI, D'ARCY, AND KELLY

Table 1. Variability in the composition of honey*

Ingredients (%, wet basis**)

Glucose 22-41
Fructose 27-44
Sucrose 0.25-8
Maltose 3-16
Higher sugars 0.13-8.5
Water 13-23
pH 3.42-6.1
Total acid (as gluconic) 0.2-1.2
Ash 0.02-1.0

•Sources: White (1978); Crane (1980)

** (kg/kg sample) x 100

conditions. This is caused by two mechanisms: enzyme activity and acid reversion (Crane,
1980).
Moisture in honey normally ranges from 16 to 18% (wet basis). The moisture content
in various varieties of honey may be as low as 13% (White, 1978) and as high as 29%
(Junzheng and Changying, 1998). Honey is an intermediate moisture food with a water
activity of about 0.6; therefore, it is self stable for a reasonable period of time. Low water
activity and high osmotic environment do not support microbial growth. The fermentation of
honey may occur by some osmophilic yeast if the moisture content is high, but honeys with
moisture contents less than 18.5% are unlikely to ferment (Chandler et al., 1974). The
Australian standard specifies moisture content in honey of not more than 20% (w/w)
(ANZFA, 1998).

CRYSTALLIZATION

Glucose is the least soluble component of all the sugars of honey and is supersaturated in
nearly all honeys (White, 1978). Bonvehi (1989) reported that the coefficient of
supersaturation of glucose in honey varies from 1.8 to 2.6. The coefficient of supersaturation
is the ratio of concentration of solute (w/w) in water at a given temperature to the
concentration of solute in a saturated solution at the same temperature. Under certain
conditions glucose in honey crystallizes as glucose-monohydrate form. Crystallization of
honey is an undesirable property in handling, processing and marketing (Hanaa et al., 1991).
On the other hand, this property might be a desirable for certain purpose such as in the
production of creamed honey. Crystallization of honey is a matter of interest for many
beekeepers and processors. The reason is that each variety of honey crystallizes differently.
Some of them never crystallize, some crystallize very slow, some very quickly, some have
fine crystals and some have bigger crystal grains. This has created a handling and processing
uncertainties for the honey handlers and processors. In addition, crystallization of honey
affects the keeping quality (yeast growth) as the non-crystallized portion will contain a
greater amount of water which results from the rejected water from crystals (Wilson and
Marvin, 1931). Consequently, the top liquid layer in a container of a crystallized honey will
RHEOLOGY AND CRYSTALLIZATION KINETICS OF HONEY 219

contain more water than the bottom crystallized portion. This makes the top liquid layer
vulnerable to yeast growth. Hanaa et al. (1991) also found crystallization of producer honey
samples due to moisture loss during storage in plastic containers. It is interesting to note that
in normal circumstances, honey does not crystallize in the comb. According to Crane (1980),
in the capped cell of the comb, honey crystallization is inhibited due to the fact that the comb
provides an environment that is protected from moisture, dust and other contaminants.
In the processing, honey is normally heated to 70-75°C for some 5-10 minutes to
ensure melting of glucose crystals. After melting all the crystals and nuclei, even the most
crystallisable honey can remain liquid for many months (Gupta et aL, 1992; White, 1978).
Several literature reports mentioned that heating to temperatures below 55°C is not effective
in melting some microscopic nuclei, which eventually results in faster crystallization (Sethi
1995). The primary crystallization nuclei can only be detected by using polariscope (Bonvehi,
1989). In many circumstances, crystallization is a problem during storage.
The velocity of crystallization and nucleation, and the types of crystal is obviously
influenced by composition and temperature (Lupano, 1997; Bonvehi, 1989; Wilson and
Marvin, 1931). Impurities (dust, dirt), air bubbles, pollen grains, the wall of the honey
container, contamination with previous glucose crystals present in the collecting containers,
and beeswax particles have been reported to influence nucleation of honey (Crane, 1980;
Hanaa et al., 1991; White, 1978). According to the stage of growth, honey crystals may be
needle shaped, flat plate or star shaped (White, 1978; Dyce, 1978). The flat plate form of the
crystals is characteristics of fine granulation, which gives smooth feel to the tongue. At slow
crystallization rate many crystals grow from the base of each crystals, forming larger star-
shaped masses, which give honey a gritty texture (Dyce, 1978). This type of crystal is
observed in jars of liquid honey in supermarket shelves. White (1978) mentioned that the
natural crystallization in raw honey is usually fine grained, while heated honey crystallizes
slowly and is coarse grained. Additionally, Lupano (1997) also found that honey stored at
20°C produced coarse.grain, while that stored at -20°C produced fine-crystals, and a mid
temperature range (4-10°C) produced mixed size crystals. This observation indicates that the
rate of nucleation and crystal growth is dependent on temperature, with lower temperatures
producing smaller crystal sizes due to the limited mobility of the molecules (Lupano, 1997;
Wilson and Marvin, 1931).
As honey is a complex solution of several sugars, it is difficult to predict the
crystallization of glucose in this complex situation. This is due to the fact that the solubility
and crystallization are positively or negatively affected by other sugar components. Several
experimental methods have been used to characterise the crystallization behavior of honey by
considering it as a glucose-fructose-water system (White, 1978; Sanz et al. 1994; Bonvehi,
1989; Chandler et al., 1974; Hanaa et al., 1991; Mohamed et aL, 1982). Some of the most
common approaches to predicting the crystallization behavior are listed in Table 2.
All of the factors listed in Table 2 have been used to characterize the crystallization
(Bonvehi, 1989). However, many studies have reported that the value for G/W
(glucose/water) is more reliable than any other method. For a given composition, a variation
of 1% moisture in liquid honey can influence the rate of crystallization (Townsend, 1975). In
several reports, a value of G/W of <1.7 has been associated with non-granulating honey
while a value of 2.2 or more indicates rapidly granulating honeys (White, 1975). However,
Chandler et al. (1974) reported that none of the three common formulas (G/W, F/G or G-
W/F) were accurate for 25 varieties of Australian honeys. They assumed that this is because
of the presence of dextrins, which increase the solubility of glucose and prolong the stability
of supersaturation state of glucose. On the other hand, Sanz et aL (1994) found the ratio F/G
to be a good predictor of crystallization of some Spanish honeys, though no method could
predict with 100% confidence. Tabouret (1979) suggested a novel method in prediction of
220 BHANDARI, D'ARCY, AND KELLY

Table 2. Various crystallization indicators used for honeys*

Indicators No granulation Fast granulation

G/W ratio <1.70 >2.16

F/G ratio >1.33 <1.11
(G-W)/F ratio <0.30 >0.49
% Glucose <27.7 >35
Coefficient of
supersaturation of glucose <1.8 >2.6
Tabouret index <9.8 >12.6

* Source: Bonvehi (1989)

crystaUization based on G/W ratio and water activity (Equation 1):

_G_
I=T: rr 0)

where, I is the Tabouret index, G is glucose content (% wet basis), W is water content (%
wet basis), aw is water activity, and power n depends upon the moisture of the honey (n=l for
moisture>17%, and n=2 for water content<17%). There are not many publications, which
validate this index method. However, Bonvehi (1989) found this index method relatively
more accurate than other methods. Most of the published reports indicate that all of the
predictive methods for crystallization are not sufficiently accurate and further investigation is
needed in this area.

METHODS TO CONTROL CRYSTALLIZATION

There are several artificial methods studied and proposed to stop crystaUization of honey.
Some of them are storage at freezing temperature (-40°C), heat treatment to dissolve crystals
and crystal nuclei, removal of air bubbles, dust and pollen particles by filtration, filling at
higher temperatures (>45°C) to avoid air bubbles incorporation during filling, addition of
inhibitors such as isobutyric acid and sorbic acid, adjusting the glucose to fructose ratios or
the water content (Gupta et aL, 1992; Lupano et aL, 1997; White, 1978; Lower, 1987;
Hanaa, 1991). Use of additives are not permitted in various countries (including Australia),
hence, heating or blending of various honeys with known composition are some of the
common ways to control the crystallization. Heating of honey delays the crystaUization, but if
seeded they can crystallize in about the same way as freshly extracted honeys (Dyce, 1975).

RHEOLOGY OF HONEY

Viscosity is one of the important properties of honey. This property is particularly critical
during storage, handling and processing (White, 1978, AssU et aL, 1991). The flow
RHEOLOGY AND CRYSTALLIZATION KINETICS OF HONEY 221

properties of honey are influenced by several factors such as composition, temperature, and
amount and size of crystals. One of the predominant factors is the moisture content. In
normal circumstances, higher moisture levels result in a reduction in the viscosity. Other
factors influencing viscosity of honey are the composition of individual sugars, and the
amount and type of colloids present in honey. Honey is basically sugar syrup and the
viscosity characteristics can be governed by the molecular chain length of sugars present in
the honey. For the same mass fraction, disaccharides contribute to a higher viscosity than
monosachharides in a solution system (Chirife and Buera, 1997). The viscosity of some
Australian (Bhandari et aL, 1999) and Chinese (Junzheng and Changying, 1998) honeys are
presented in Table 3. The relatively lower viscosity of Chinese honey as compared to
Australian honey might be due to the higher moisture content in Chinese honey.
In most of the published works, honey is reported to be a Newtonian fluid (White,
1978; Kokini, 1997; Junzheng and Changying, 1998; Bhandari et aL, 1999). Munro (1943)
reported that the presence of colloids (0.18-0.8%) in some honeys (such as buckwheat,
heather, and white clover) contributed to their thixotropic, or time dependant, behavior.
Removal of colloids (possibly protein) by heat coagulation from the sample resulted in the
loss of this thixotropy and a permanent increase in viscosity. Other honeys that are reported
to be thixotropic are Manuka from New Zealand and Karvi from India (Crane, 1980). Some
honeys are reported to be shear-thickening (dilatancy) such as honeys from some Eucalyptus
sp. This effect was attributed to the presence of the polysaccharide dextran with a molecular
weight of 1250 000 range (Rao, 1977; White, 1975).
Temperature has a most significant role on the viscosity of honey. Munro (1943)
showed that the temperature effect on viscosity is greatest at temperatures below 15°C, and
heating above 30°C has an effect of little practical importance. The temperature dependence
of honey viscosity is supposed to follow an Arrhenius relationship (Equation 2), a similar
property noted for other sugar-rich liquid foods such as fruit juice concentrates and sugar
syrups (Manohar et al., 1991, Khalil et aL, 1989).

H = Ho exp (E/RT) (2)

where, (l is the viscosity (Pa s), fio is the pre-exponent constant, Ea is the activation energy
(J/g-mole), R is the gas constant (8.14 J/kg K), and T is temperature (K). The slope of a
linear plot of In (|i) versus (1/T) gives the activation energy (Ea).
A non-Arrhenius behavior of some honeys has been reported but without any detail (White,
1975). Bhandari et al. (1999) found Newtonian behavior for some seven varieties of
Australian honeys at a range of temperatures between 4-30°C (Figure 1). The temperature
dependence of these honeys was described by tl.e Arrhenius relationship with activation
energies ranging from 1250 to 1850 J/g-mole. All of these reports indicate that the varietal
factor also affects the flow behavior of honey. There is very little updated information
available on the rheology of honey at present.

GLASS TRANSITION TEMPERATURE (Tg)

In terms of physical state, liquid honey is a viscous glass where all the sugars are present in
an amorphous state. The viscosity of the solution increases as the temperature is reduced. If a
solution is cooled fast, it is vitrified at a viscosity of around 1012Pa.s (Downton et al., 1982).
This behaves like a solid at this state. All the physical and chemical reactions are extremely
slow at this viscosity. When this solid solution is warmed up slowly, at a certain temperature
it starts to flow at around the viscosity of 107 Pa.s. At this viscosity, the molecular mobility is
222 BHANDARI, D'ARCY, AND KELLY

Table 3. Viscosity of some Australian and Chinese honeys*

Honey type Moisture (wet basis, %) Viscosity at 20cC (Pa.s)

Australian:
Yellow box 17.6 39.9
Tea tree 16.9 33.4
Strawberry clover 17.1 43.5
Iron bark 16.8 33.3
Red gum 17.3 70.0
Leatherwood 17.2 43.8

Chinese:
Acacia 29.0 0.3
Chaste 22.5 2.3
Rape 19.8 6.3
Linden 27.4 0.5
Chinese astralagalus 21.5 3.0
Locust 26.2 0.8

•Sources: Bhandariet al. (1999), Junzheng and Changying (1998)

1000 2400
IRON BARK
•«" 800
ra

0 5 10 15 20 25 30 0 5 10 15 20 25 30 35

Temperature (°Q Temperature (°C)

Figure 1. Viscosity of honey as a function of temperature (• observed, — predicted

using Arrhenius model) (Bhandari et al., 1999)
RHEOLOGY AND CRYSTALLIZATION KINETICS OF HONEY 223

regained and the reaction rates are quickly increased. This particular temperature is termed
the glass transition temperature (Tg). Though limited information is published, the glass
transition temperature of honey is reported between -40 to -50°C (Rubin et al., 1990). The
knowledge of this temperature is of practical importance in honey processing and storage.
The reason is that the crystallization phenomenon is completely inhibited when honey is
cooled below glass transition temperature. The crystallization only takes place above glass
transition temperature due to regain of molecular mobility. This phenomenon is well known
for synthetic polymers, where the quantity Tg +T is commonly used to give some indication
as to the rate of development of crystallinity (Fried, 1995).
Temperature and viscosity of honey influence the crystallization rate. Viscosity of a
particular honey is again a function of temperature. In several published reports it has been
found that the crystallization rate for honey is maximum at around 10-15°C while the rate is
decreased above and below this temperature (White, 1978; Dyce, 1975). Above 30°C, honey
crystallization will not occur due to the increased solubility of glucose. The crystallization
rate is increased below room temperature due to increased supersaturation of glucose. On
lowering temperature, the increase is viscosity counteracts supersaturation effects. At about
10-15cC, the effect of supersaturation is more dominating than the viscosity effect. As
mentioned previously, the viscosity of honey is least affected above this temperature range.
However, below this optimum temperature the crystallization phenomenon is viscosity
limited. The crystallization will be completely seized below glass transition temperature when
the molecular mobility is almost null. This hypothesis is depicted in Figure 2. Similar type of
crystallization behavior has also been reported for various polymers (Sperling, 1992).

CRYSTALLIZATION RATE OF A SUGAR SYSTEM

The crystallization rate of a glassy sugar solution below room or subzero temperatures is a
matter of practical as well as academic interest. The rate of crystallization may be
hypothetically related to the mobility, hence the viscosity of the honey as a glass. The
mechanical properties of a material, at temperatures above the glass transition temperature
(T>Tg, e.g.Tg+100K), such as the characteristic relaxation time, and the viscosity can be
predicted by William-Landel-Ferry (WLF) equation (Roos and Karel, 1991a; Reid et al.,
1994; Wallack and King, 1988; Rahman, 1995). When the property is viscosity or
crystallization behavior, the WLF equation is described by:

JJ^ C,(TT,)
l0gl =
>g C2+(T-Tg)

U_ - C , ( T - T t )
1OSl0
tg=C2+(T-Tg)

where, \i is the viscosity, [i$ and tg are the viscosity and isothermal crystallization time at
glass transition temperature Tg, repectively, T and tc are the temperature and isothermal
crystallization time at temperature T respectively, and Ci and C2 are "universal" constants
(17.44 and 51.6 K respectively). Roos and Karel (1991c) found Equation 3 using such
"universal" constant values valid for an amorphous sucrose-lactose-water system. Soesanto
and Williams (1981) also validated the WLF relationship (Equation 3) for an amorphous
224 BHANDARI, D'ARCY, AND KELLY

Viscosity limited Saturation limited

.2

Tg Temperature
Tg+T

Figure 2. Hypothetical crystallization rate of honey with respect to the temperature (Tg
is glass transition temperature, and T is temperature of honey at any instance)

sucrose-fructose-water system. As crystallization is directly related to the viscosity and the

molecular mobility of the glass, Roos and Karel (1991b) found the applicability of Equation 4
(analogous to Equation 3) for the crystallization of amorphous lactose and sucrose. Although
the use of WLF model has been criticised in a complex food system (Peleg, 1996), honey
being relatively a simple food system (sugar-water system) use of this model can be a
practical approach. The Tg embraces the influence of all sugars in an aqueous system.
Therefore, use of Tg can also be a useful tool to predict crystallization behavior of honey.

CONCLUSIONS

Honey is a mixture of several sugars in a water system. Glucose is the principal component
that crystallizes in honey as it exists in a supersaturated state. The solubility of glucose is
influenced by other components in honey. Therefore, the crystallization behavior is
dependent on the proportions of other components in honey. Most of the crystallization
prediction methods are based on glucose, fructose and water content. The predictability of
current methods is still poor. There is no single method which embraces the effect of all the
components in honey. In conclusion, there is a need for further research to find a method
which will accurately predict the crystallization behavior of honey.

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(Received March 9, 1999; revised March 29; accepted April 6, 1999)