Honey: Nature’s natural sweetener

A review of recent scientific literature linking consumption

with health benefits

September 2012

Introduction

Honey has a long history of human consumption and through history has been used in a number of ways as a sweetener in foods and beverages. Its sweetness, whilst similar to that of granulated sugar, is brought about by a different composition of sugars and in addition honey typically has a distinct flavour, resulting in part to other components present. This taste separation is highly dependent on the sources of the original nectar used by the bees to make the honey. These additional components have, in folk law, often been associated with direct health benefits. With the increased popularity in recent years of some specialist honeys such as New Zealand Manuka, which seek to exploit health attributes, there has been increased interest from the research community to see if there is any scientific basis for these. This short review gives some background on the nutritional properties of honey and highlights some of recent scientific research exploring health benefits. History Honey has a long and varied relationship with humans which in many cases goes beyond its nutritional attributes but which, for example in religions such as Hinduism and Buddism ,has other meanings1. Honey has been collected by humans for at least 8000 years and cave paintings found in Spain2 depict people gathering honey and honey combs from wild bees’ nests. Honey formed an important dietary and medical component of civilisations across the globe including Egypt and the Middle East, China, Mesoamerica (Mayan) and Rome. This role has continued throughout the ages into modern times. General Characteristics The honey consumed by humans is generally formed by wild or cultivated honey bees although other species of bees and some other insects are known to produce similar substances. Bees collect nectar from flowering plants and store it as a primary food source for their colony. Nectar is transformed into honey by the action of the bees. Honey’s main components are sugars and generally honey comprises approximately a mixture of the monosaccharides fructose (38.5%) and glucose (31%). Sucrose, a disaccharide of fructose and glucose, most commonly found in granulated sugar, comprises only around 1%. Total disaccharides, including maltose, isomaltose and maltulose comprise around 7% of the composition with the remaining component mainly water. Honey is a natural product and there is wide variation in content depending on the type of flora that were used to produce it. This contributes to the exact ratios of carbohydrate composition and to the characteristics of individual products. Table 1 summarises some typical carbohydrate characteristics.

Table 1 Typical carbohydrate composition of Honey 4

Carbohydrate Average Content Range

Fructose 38.38% 30.91-44.26

Glucose 30.31% 22.89-40.75

Reducing Sugars 76.65% 61.39-83.72

Sucrose 1.31% 0.25-7.57

Fructose/Glucose Ratio 1.23 0.76-1.86

This variation in composition leads to a wide variation in physical characteristics. As gathered honey is a supersaturated solution (ie contains more sugar than should be dissolved in water at normal temperatures) and at room temperature this becomes a supercooled liquid in which the glucose present can precipitate as solid particles (or crystals). The melting point of crystallised honey varies between 40°C and 50°C depending on composition. As a result at room temperature honey can become metastable (will not crystallise until a seeding crystal has been added) or more commonly labile and self seeding. Crystallisation occurs fastest between 13 and 17°C and below 5°C honey does not freeze5. As a supercooled liquid honey does not freeze solid but becomes an increasingly viscose liquid, flowing at increasing slower rates until at temperatures below -42°C to-51°C it enters the glassy state becoming an amorphous solid6. Viscosity is affected both by the relative sugar content and amount of water. Some honeys, notably Manuka, show thixotropic behaviour becoming liquid when stirred but gel like when motionless. Honey is hygroscopic, ie absorbs water from the air. Levels of water absorbed are affected by the relative humidity and temperature of the surroundings. The water content affects the refractive index of honey and this can be used to estimate the water content. Honey is also affected by polarised light, rotating the polarising plane. Fructose rotates the plane negatively whilst glucose gives a positive rotation. This can be used to estimate the relative composition of the honey. Honey is around 1-1.5 times sweeter than granulated sugar (based on dry weights) and approximately equivalent as a liquid. Fructose imparts a stronger sweet taste than glucose, sucrose or other disaccharides and as a result high fructose honeys generally have a sweeter taste. The disaccharides present also play an important role in the functionality of honey including moisture retention, shelf life and processing7. The ratio of fructose/glucose and glucose/water play an important role in predicting the tendency for honey to crystallise and those with low glucose/water ratios crystallise less easily. Basic Nutritional Composition Honey is a natural product whose composition depends on the environment from which the original nectar was collected. This includes the varieties of plants involved, seasonal and geographic variations. As indicated previously the major nutritional components are sugars (mainly fructose and glucose) and water. As a result of the environmental factors honey also contains a number of micronutrients and other components derived from plants which may have health impacts on consumers. Table 2 shows an indicative nutritional composition for a typical honey

Table 2 Typical nutritional compositions data for Honey (per 100g)

Energy 1272 kJ( 304kcal)

Carbohydrate 82.4g

Of which Sugars 82.12g

Protein 0.3 g

Fat 0 g

Water 17.10g

Fibre 0.2 g

Vitamin B2( Riboflavin) 0.038mg

Vitamin B3(Niacin) 0.121mg

Vitamin B5(Pantothenic Acid) 0.068mg

Vitamin B6 0.024mg

Vitamin B9(folate) 2µg

Vitamin C 0.5mg

Calcium 6mg

Iron 0.42mg

Magnesium 2mg

Phosphorous 4mg

Potassium 52mg

Sodium 4mg

Zinc 0.22mg

Depending on its type and origin some honeys also contain other trace elements such as boron, cobalt, manganese, chromium and selenium in small quantities. Honey also contains choline and acetylcholine in variable amounts. Choline is important in vascular health, brain function and cellular membrane repair whilst acetylcholine has a function in neuro transmission.

Honey Types Honey can be classified in a number of ways.:

Monofloral or Floral source: This is based on the floral source of the nectar from which the honey was made. This can be as a single flower type or be comprised of a specific post collection blend. In each case pollen in the honey will have a unique profile and can be used to help track authenticity. Monofloral honey will typically have a distinct flavour, colour and texture profile linked to that source. If it is sourced from a geographically restricted plant it may also show seasonal variations in colour and texture. Production of monofloral honey can be problematic for beekeepers if the flowering season is short or if there are other nectar rich species within the flying range of the bees. Poly floral: This is based on nectar collected from an unspecified range of flowers, which may be extensive, typically in a geographic region or across a season. It is

sometimes known as ‘ Wildflower Honey’ although not necessarily derived from wildflowers. The taste and texture of the honey will be dependent on the breadth of the species from which the nectar has been gathered and local geography. It will also vary from season to season. Blended: This forms the majority of high volume commercial honey sold and comprises a mixture of two or more honeys with different floral and often geographic origins. The blend is typically made to create a consistent colour, flavour and physical characteristics profile. It is generally linked with strong commercial brands where consistency is key.

Honey contains a wide range of different tastes and colours depending on the botanical origin. High fructose content honey (such as Acacia) are sweeter compared to high glucose variants (such as rape). Aroma will depend on a number of factors but is typically linked primarily to the types and amounts of amino acids present( derived from the bees). The system is complex and recent research8 has shown that there are more than 500 different volatile compounds responsible for contributing to the aroma profile. Honeys also contain a range of polyphenols, typically around 50-500mg/kg. These are typically flavenoids (eg quercitin, luteolin, kaempferol, apigen, and chrysin), phenolic acids and phenolic acid derivatives9 which are known to be antioxidants. It has been argued9 that this complex map could also form a tool for provenance and authenticity verification. The main polyphenols are flavenoids and their higher presence has been linked to hotter and dryer production regions 10. In addition to source post harvest processing can further influence classification based on the form in which the honey is finally presented to the customer. Some examples include:

Comb, where the honey is still in the intact honeycomb, possibly including the wooden frame in which the comb sits, Raw, in which honey has been minimally processed from the honeycomb. It may contain small amounts of pollen and wax from the comb. Strained, in which the honey has been filtered through a mesh to remove large particulates (including wax) but in which smaller particulates such as pollen remain. Filtered, in which honey is more rigorously filtered to remove all particles (including pollen) and remove trapped air. To speed the process filtering is often undertaken at temperatures similar to those for pasteurisation with associated impacts (see later). Filtered honey is slower to crystallise and this brings benefits in pouring and commercial uses. Ultra sound treated, where exposure to a burst of ultrasound is used to destroy any yeasts present (that might stimulate fermentation). The process also impacts on crystallisation and as a result can help with liquefaction of honey in subsequent processing or use. Crystallised, in which some or all of the liquid honey has spontaneously crystallised or has been induced to crystallise. Set Honey, where crystallisation has been controlled to produce a large number of small crystals in the liquid matrix. These small crystals prevent formation of larger

ones and produce a product with an extended texture profile and one which has consistent properties for spreading. Pasteurised, in which raw honey has been taken through a pasteurisation process. In addition to reducing microbial spoilage (which as a result of the high sugar content is in any case low) the process can be used to reduce crystallisation but can promote colour, taste and fragrance changes, reduce enzyme activity and lead to production of other chemical species11.

Links with Health In addition to its role as a natural sweetener honey has, since it was first consumed, been linked to health benefits. Some of these benefits may derive from the structure and composition of the sugars present. Others may derive from the presence of other materials, largely as a result of the action of the bees collecting and making the honey. The health benefits of honey have historically been linked with folk remedies and alternative medicines. In recent years there has been increased research to understand the scientific basis of many of the potential health benefits and a number of useful general review papers have been published12, 13, 14, 15. The health benefits can be grouped into a number of broad areas: Antimicrobial, antiviral and anti-parasitic activity There is evidence to show that honey inhibits the growth of microorganisms classed as gram-positive bacteria. A number of these organisms are linked with disease. Table 3 summarises some of the bacteria affected, A more comprehensive list can be found in the review paper written by Bogdanov et al12.

Table 3 Some bacteria known to be sensitive to honey

Bacteria Related infection

Haemophilius influenzae Respiratory infections

Helicobacter pylori16 Gastric ulcers

Pseudomonas aerugonisa25 Urinary infections , wound infections

Salmonella sp diarrhoea

Salmonella typhimurium Wound infections24,29

Streptococcus faecalis Urinary infections

Streptococcus mutans26 Dental caries

Streptococcus pneumoniae Ear infections, sinusitis

Streptococcus pyogenes27 Throat infections, wound infections

The bacteriological effect depends on the structure of the honey which is linked to its origins. At a macro level low water activity inhibits growth. Enzymes such as glucose oxidase produce hydrogen peroxide17 which has an antimicrobial effect but production is limited by other enzyme activity. Peroxides are however destroyed by heat treatment and to maintain potential activity honey must be processed and stored with care.

Other substances present are also believed to contribute to the antibacterial activity. Manuka honey is for example believed to be high in aromatic acids and phenolic compounds and flavenoids, which in addition to their antioxidant properties show antimicrobial activity18, 19, 20, 21. Similar results have been reported for some other geographic honeys22. Recent data suggests that peptides present may also contribute to antibacterial properties particularly in treatment of antibiotic resistant bacteria strains28. Antioxidant Effects Oxidative stress or the in balance between production of free radicals and antioxidant protection is now generally recognised to be linked to the progression of chronic disease30. There is evidence that honey contains a number of compounds shown to have antioxidant capacity. The most important of these are the polyphenols and there is evidence to suggest that the phenolic content of honey is linked directly to its oxidative protection characteristics. Human intervention studies31,32 have, for example, used volunteers fed honeys having different antioxidant capacities (using sugar as a control ) and measures of oxidative capacity have been assessed using biomarkers. Honey showed increased levels of antioxidant protection linked to composition. Antioxidant markers such as glutathionine reductase and uric acid were increased. In each case the authors were though quick to note that the antioxidant capacity of the honey was highly dependent on the botanical and geographic source35. Honeys used in the study had been previously benchmarked for antioxidant capacity using in vitro and chemical tests such as ORAC (oxygen radical absorbance capacity)33. Some typical ORAC data taken from Bogdanov 12 are shown in Table 4.

Table 4 ORAC antioxidant capacity and phenol content data for some honeys

Honey ORAC capacity Total Phenolics ( mg/kg)

Buckwheat(Illinois) 16.95 796

Buckwheat ( New York) 9.75 456

Clover 6.05 128

Acacia 3.00 46

Recent data has indicated that whilst processing may not affect antioxidant levels storage can in some cases lead to reductions in levels with time34. Cancer Cancers develop through mutation of the genetic structure of tissues. This mutation is promoted by chemicals and other stimuli, some of which can be nutritionally based. For example it is generally accepted that heterocyclic amines and nitrosamines formed during roasting and frying of food can promote such activity. There is evidence that suggests that some compounds found in honey may slow or prevent such activity. For example Wang et al tested a number of different monofloral honeys and showed that they all had antimutagenic properties36. Work in mice models 37 suggests that honey may stimulate the immune system and the researchers speculated that consumption prior to tumour formation might slow of prevent disease progression. The study did not however offer evidence for this speculation.

Anti-inflammatory Honey has been shown to have anti-inflammatory effects in humans consuming around 70g/d 38. Key markers of inflammation such as thromboxane and PGE(2) showed reductions at 1,2 and 3 hours after ingestion. There is also evidence in mice models that honey has a positive effect in models of IDB and colitis40. Researchers are still working to understand which active compounds are responsible. Comparison to the effects of honey in burns and wound healing39 , which also show inflammatory behaviour,has though suggested that active compounds prevent formation of free radical release in inflamed tissues as well as having a direct anti-inflammatory effect.

Oral health There has been considerable speculation about the role of honey in oral health. There is though conflicting data concerning dental caries with some reports suggesting a protective effect41 whilst others liken the effects to sucrose42. These seemingly conflicting observations may reflect the dependence of functional characteristics on the origin of the honey. It is likely though that the antibacterial activity of honey highlighted above may influence the growth of bacteria and that this may be responsible for the protective effect. Certainly one study43 using Manuka honey, known to have strong antimicrobial activity, has shown positive effects against formation of dental plaque and the onset of gingivitis. Whilst these observations have been made it should always be remembered that the main constituents of honey are sugars, which are strongly linked with poor oral health and thus results need to be considered with some caution. Digestive and Gut Health Honey has been linked with digestive health since ancient times. Early civilisations such as the Romans and Arabic empires used honey as part of their treatments for gastro intestinal disorders. There is research evidence44, for example, that honey inhibits growth of Helicobacter pylori, the bacteria associated with development of gastric ulcers. Recent work has highlighted the potential antibiotic effect of honey with a number of intestinal pathogens 47. The mechanisms for this remain unclear but it is believed that either components in honey stimulate sensory nerves in the stomach 45 or the action is linked to an antioxidant effect. Again some work has shown dependence on floral and geographic origins as a key factor in activity. There have been health links associated with oligosaccharides present in honey with some evidence of prebiotic effects similar to fructo-oligosaccharides more commonly used. An example is a study 46 which showed particular effects on the functionally important bacteria bifidobacteria and lactobacilli. Vascular health/ Diabetes There is evidence to suggest that micro components in honey have a positive effect on markers of heart health. For example one study48 compared ingestion of a fructose/glucose mixture with consumption of honey on various heart biomarkers. The study showed honey to have positive effects on a number of biomarkers of vascular health. Other research has shown positive vascular effects in diabetic patients postulating that this could be used in the

management of the condition49,50,52 . As in other areas the origin of the effect remains uncertain however one group 51 has suggested that it could be due oligosaccharides present .A second has suggested that the effect is linked to stimulation of increased energy expenditure54. Nitric oxide (NO) metabolites can be present in honey. NO is a known marker of heart disease and elevated levels of metabolites may be evidence of a protective function53. NO metabolites levels vary with honey variety, storage and processing. Conclusions Honey has played an important role in nutrition since man’s earliest days. The perceived potential health benefits of consumption have been exploited in many cultures for almost as long but it is not until recently that scientists have sought to understand if there is evidence to support this. Honey is a complex mixture of substances, the composition of which is dependent upon a wide range of natural and man-made variables. For a single flora sourced honey composition will be highly dependent on the floral source, season and geographic factors as well as the action of the bees that collect the primary nectar. Further complexity is added where bees have access to multiple floral sources and individual honeys are combined or blended by producers. The way in which honey is processed and stored can also be important in ensuring native health impacts remain intact. There is an ever growing body of scientific literature showing evidence for a number of health related impacts from consumption or even application to the body of honey. However in reviewing this data some caution is needed. Very few of the observed effects are linked simply with honey as a whole. Rather scientists have identified specific health impacts linked with honeys showing strong provenance to floral and regional characteristics. For some, such as Manuka from New Zealand, there is a strong and growing portfolio of information. For others such as UK honeys scientists are only beginning the journey of understanding and we still lack some basic information on the composition of specific honeys and information on the potential bioactives present. Data is needed from different floral and regional origins before we can fully assess and compare specific health impacts. As in New Zealand much of this will need to be done at a local level but armed with this information Scottish and UK producers can begin to look at developing their own healthy messages.

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September 2012 Nutrition and Health Foresighting Functional Ingredients Free From Reformulation