Nutraceutical values of natural honey and its contribution to human health and wealth.
Journal: 2012/September - Nutrition and Metabolism
ISSN: 1743-7075
Abstract:
The use of natural honey (NH) as a nutraceutical agent is associated with nutritional benefits and therapeutic promises. NH is widely accepted as food and medicine by all generations, traditions and civilizations, both ancient and modern. The nutritional profiles, including its use in infant and children feeding reported in different literatures as well as health indices and biomarkers observed by various researchers are illustrated in this manuscript. The review documents folk medicine, experimentation with animal models, and orthodox medical practices shown by clinical trials. This covers virtually all human organs and body systems extensively studied by different workers. The sources and adverse effects of NH contamination, as well as the preventive methods are identified. This could promote the availability of residue free honey and a wholesome natural product for domestic consumption and international market. This could also help to prevent health problems associated with NH poisoning. In addition, apicultural practices and the economic importance of honey are well documented. This report also includes information about a relatively unknown and uncommon South American stingless bee species. We concluded this review by identifying important roles for Ethno-entomologists, other Scientists and Apiculturists in the development of stingless bees to boost honey production, consumption and economic earnings.
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Nutrition & Metabolism. Dec/31/2011; 9: 61-61
Published online Jun/19/2012

Nutraceutical values of natural honey and its contribution to human health andwealth

Abstract

Introduction

The use of natural honey as food and medicine by mankind has been in existence from timeimmemorial. In fact, records have it that raw honey is the most ancient sweetener, andit was noted to have been in use throughout the world several million years ago [1]. Natural honey (NH) is a sweet, flavourful liquid food of high nutritionalvalue [2,3], and immense health benefits [3,4]. NH is produced by honey-bees as blossom honey by secreting nectars offlowers, and honeydew honey (forest honey) by secreting the exudates of plant suckinginsects (Aphids). NH is widely embraced by all ages, and its use transcends the barriersof culture and ethnicity. The use of honey is even advocated and embraced by allreligious and cultural beliefs.

NH is a liquid spoken of by all religious books, and accepted by all generations,traditions and civilizations, both ancient and modern. The religion of Islam recommendedthe use of honey as food and medicine, and even named an entire chapter in the HolyQur'an called Surah al-Nahl meaning chapter of the Honey Bee [5]. In the book of hadith, Prophet Muhammad strongly advocated the use of honeyfor curative and healing purposes [6]. Furthermore, the Holy Qur'an explicitly encourages the consumption of NH asa highly nutritious and health promoting food in chapter 16 thus: “And your Lordinspired the bee(s), saying: "Take your habitations in the mountains and in the treesand in what they erect. Then, eat of all fruits, and follow the ways of your Lord madeeasy (for you)." There comes forth from their bellies, a drink of varying colour whereinis healing for men. Verily, in this is indeed a sign for people who think” [7]. In Christendom, there are references made to the importance of bees andhoney in the Bible, and these include the Books of Exodus, Judges, Mathew and Proverbs [8-11]. In accordance with this Christian holy book, the Bible, King Solomon wasquoted thus: “Eat honey my son, because it is good” [11]. In fact, it was reported in the Bible that John the Baptist actually thrivedon a diet including wild honey for a long period of time when he was in the desert areaor while travelling in the wilderness [10]. The other sets of people, sects, traditions and civilizations that attestedto the popularity of honey include Budhists, Jews, Hindus and Vedas [1,12].

The profile of honey in the health shopping list is rising. The reason for thisincreased demand for NH is attributable to its popularity due to several medicinal usesthat this substance has enjoyed throughout the history of mankind. It has been observedfrom time immemorial that NH is not only important for its medicinal attributes, butalso useful as food sweetener, complete food and natural beauty agent [1]. NH has been used severally by the Tradomedical practitioners for numeroushealth benefits, and researchers have also documented honey’s beneficial roles inmodern medicine, especially in wound treatments [13,14]. Several different surveys have been compiled on the nutritional and healthaspects of honey [14-18]. However, the nutritional value and medicinal properties of NH are toonumerous and highly inexhaustible to be comprehensively documented by these manuscripts.The records of honey as functional health food and uses of other honey-bee products arestill incipient. Thus, the need to review some relevant materials on natural honeybecomes imperative. This review documents the NH values as food and medicine, as well asenumerates the economic importance of NH production and other apicultural practices.

Honey as food

Nutritional profile

The composition of honey is mainly sugars and water (Table 1). In addition, it also contains several vitamins and minerals, includingB vitamins as shown in Table 2. The other constituents ofhoney are amino acids, antibiotic-rich inhibine, proteins, phenol antioxidants, andmicronutrients [2]. The sugars in honey are sweeter and give more energy than artificialsweeteners [2-4], and the most abundant sugar in honey is fructose (Table 1).

Table 1
Nutritional composition of honey*
Blossom honey
Honeydew honey
RangeMeanRangeMean
Water
15 – 20
17.2
15 – 20
16.3
Total sugars

79.7

80.5
Monosaccharides




fructose
30 – 45
38.2
28 – 40
31.8
glucose
24 – 40
31.3
19 – 32
26.1
Disaccharides




sucrose
0.1 – 4.8
0.7
0.1 – 4.7
0.5
others
2.0 – 8.0
5.0
1.0 – 6.0
4.0
Trisaccharides




oligosaccharides

3.1

10.1
erlose
0.5 – 6.0
0.8
0.1 – 6.0
0.1
melezitose

< 0.1
0.3 – 22
4.0
others
0.5 – 1.0
0.5
0.1 – 6.0
3.0
Minerals
0.1 – 0.5
0.2
0.6 – 2.0
0.9
Amino acids, proteins
0.2 – 0.4
0.3
0.4 – 0.7
0.6
Acids
0.2 – 0.8
0.5
0.8 – 1.5
1.1
pH value3.2 – 4.53.94.5 – 6.55.2

*Data in g/100 g of honey, Adapted from [2,3].

Table 2
Chemical elements found in honey*
MineralsAmount (mg/100 g)VitaminsAmount (mg/100 g)
Sodium (Na)
1.6 – 17
Thiamine (B1)
0.00 – 0.01
Calcium (Ca)
3 – 31
Riboflavin (B2)
0.01 – 0.02
Potassium (K)
40 – 3500
Niacin (B3)
0.10 – 0.20
Magnesium (Mg)
0.7 – 13
Pantothenic acid (B5)
0.02 – 0.11
Phosphorus (P)
2 – 15
Pyridoxine (B6)
0.01 – 0.32
Selenium (Se)
0.002 – 0.01
Folic acid (B9)
0.002 – 0.01
Copper (Cu)a
0.02 – 0.6
Ascorbic acid (C)
2.2 – 2.5
Iron (Fe)a
0.03 – 4
Phyllochinon (K)
0.025
Manganese (Mn)a
0.02 – 2


Chromium (Cr)a
0.01 – 0.3


Zinc (Zn)a0.05 – 2

*Adapted from [2,3]aHeavy metals.

These substances are of nutritional and health importance. Some of the vitamins foundin honey include ascorbic acid, pantothenic acid, niacin and riboflavin; along withminerals such as calcium, copper, iron, magnesium, manganese, phosphorus, potassiumand zinc. The detailed list of vitamins, minerals, other micronutrients and traceelements found in honey is given in Tables 2 and 3.

Table 3
Other chemical elements found in honey*
ElementAmount (mg/100 g)ElementAmount (mg/100 g)
Aluminium (Al)
0.01 – 2.4
Lead (Pb)a,b
0.001 – 0.03
Arsenic (As)a,b
0.014 – 0.026
Lithium (Li)
0.225 – 1.56
Barium (Ba)
0.01 – 0.08
Molybdenum (Mo)a
0 – 0.004
Boron (B)
0.05 – 0.3
Nickel (Ni)a
0 – 0.051
Bromine (Br)
0.4 – 1.3
Rubidium (Rb)
0.040 – 3.5
Cadmium (Cd)a,b
0 – 0.001
Silicon (Si)
0.05 – 24
Chlorine (Cl)
0.4 – 56
Strontium (Sr)
0.04 – 0.35
Cobalt (Co)a
0.1 – 0.35
Sulphur (S)
0.7 – 26
Fluoride (F)
0.4 – 1.34
Vanadium (V)
0 – 0.013
Iodide (I)10 – 100Zirconium (Zr)0.05 – 0.08

*Adapted from [2,3]aHeavy metals.

bToxic heavy metals listed amongst the first 20 top hazardoussubstances in the priority list compiled by ATSDR thus 1 : Ar, 2 : Pb, 7 :Cd; Presence and toxicity in NH can be due to contamination through humanerror or inimical practices.

The high nutritional profile of honey with wide range of nutrients (although inminute quantities), encourages its use as food. Due to the low quantities of some ofthe NH’s essential nutrients, it is advisable for adults to take it (NH) inlarge quantities (70 – 95 g daily) to get the full desirable nutritionaland health benefits [19-23].

Growth

Food is eaten for nourishment, metabolic activities, growth and healthy living.Regular consumption of natural honey gives all these benefits. In fact, honey is acomplete meal, as shown in Tables 13. It contains major components of a meal, and micronutrients thatwill enhance the digestion and absorption of these major dietary components, as wellas those required for metabolism and body functions. We recorded enhanced body weightgain by our rats fed blossom honey in two separate studies at different laboratoriesin Nigeria and South Africa [4,24]. In 2008, Chepulis and Starkey fed honeydew honey to 8-week old rats for52 weeks to assess weight gain. These workers show that the growth influence ofhoney in rodents is partly due to increased bone growth and mineralisation [25], probably due to the calcium content of honey. Our unpublished data fromvery recent study on NH supplemented rats confirmed this linear growth influence ofhoney. In his extensive review of the literature, Molan (2001) confirmed the growthstimulating property of honey [18]. He opines from his histological studies on wounds that stimulation ofcell growth by honey also enhances NH healing properties.

Source of antioxidants

The presence of free radicals and reactive oxygen species (ROS) is culpable in theprocesses of cellular dysfunction, pathogenesis of metabolic and cardiovasculardiseases (CVDs) as well as aging. The consumption of foods and substances rich inantioxidant can protect against these pathological changes and consequently preventthe pathogenesis of these and other chronic ailments. Researches indicate that NHcontains several important compounds, and these include antioxidants [26,27]. The qualitative and quantitative composition of honey (including theantioxidants constituent and the other phytochemical substances) is a reflection ofthe floral source as well as the variety of the particular honey. The colour of honeyalso influences its antioxidant content, as darker honeys are known to have higheramount than lighter honeys [28]. In their analysis of the phytochemical composition of monofloral Cubanhoneys, Alvarez-Suarez and co-workers, agreed with this submission and concluded thatCuban honeys contain important phenolic, flavonoid and carotenoid concentrations withhigh substantial antioxidant capacity [29]. Researchers in California also submitted that human beings can beprotected from the damaging effects of free radicals and ROS. The protection isthrough the absorption of the antioxidants from foods such as honey highly-rich inthis important substance called antioxidant. The report of their study in which twobuckwheat honey treatments were administered to 37 healthy human adults at the rateof 1.5 g/kg body weight, with corn syrup as control, show increased(p < 0.05) plasma total-phenolic content and plasma antioxidant. Thus,supporting the concept that phenolic antioxidants from processed honey arebioavailable, and they increase antioxidant activity of plasma. They advocated forthe substitution of honey in some foods as traditional sweetener for enhancedantioxidant defence system in healthy human adults [27].

Exercise and athletic performance

The consumption of energy giving substances before, during and after any form ofphysical exercise improves the individual’s performance and increases therejuvenation of muscles. This is also associated with dietary supplementation withNH, which provides up to 17 g of carbohydrates for every tablespoon consumed andgives the much needed energy, thus serving as an inexpensive substitute tocommercially available sporting activities enhancers. The data obtained from theSports Nutrition and Exercise Laboratory of one University show that honey can beused effectively instead of glucose for energy replenishment during physical exercise [30]. The physiological actions of NH observed during this performance were asignificant increase in heart frequency and a fairly constant blood glucose level.These suggest honey as a better substitute to glucose. Earnest and co-workersimproved on this preliminary investigation in another trial by administering low(honey) or high (glucose) glycaemic index (GI) carbohydrate gels on athletes, andtesting them on the performance of cyclists travelling a distance of about65 km [31]. The results of the cycling event show that both the low (honey) and thehigh (glucose) GI substances caused increase in performance. However, the effectproduced by eating NH surpassed that observed in the athletes fed with glucose. Thisaligns with other previous studies that NH consumption does not compromise metabolicand physical activities [4,25,26]. NH has been shown to decrease blood glucose level in hyperglycaemia suchas diabetic subjects [19,20,32-37], plausibly due to the beneficial effects of fructose [32,34-36], and more importantly honey’s several phytochemical constituents [2,37]. A very recent review of the hypoglycaemic effect of honey by some workersconclude that, the synergistic effect of fructose and glucose constituents of honeymight contribute to the low glycaemic response after a honey meal [38]. These experimental and clinical trials show that honey is awell-tolerated liquid food.

Furthermore, honey can be an effective carbohydrate source and a better substitute toglucose for exercise and athletic performance, due to its constituent of variousclasses of sugars. People favour slow-burning sugars for sustenance as energy sourceduring physical exercise. Honey is beneficial in this regard as it releases fructoseslowly into the blood stream to produce a sustained energy boost and maintainhomeostasis. The other major component of NH apart from fructose is glucose(Table 1). Fructose and glucose are ketose and aldosesugars respectively with chemical structural differences, and consequently differentpatterns of metabolism, despite both being monosaccharides with quick burningtendency. It is important to note that glucose is rapidly metabolized for absorptioninto the blood system for energy provision. On the other hand, fructose absorption isslow, and will continue to sustain the individual with energy, while the glucosemoiety burns out. The various phytochemical constituents of honey [2] also contribute to the progressive slow rate of fructose metabolism [39]. In addition, honey contains disaccharides such as sucrose andoligosaccharides as well as other trisaccharides (Table 1) that are slow burning sugars. These could facilitate energy replenishment,muscle recuperation and enhancement of performance in athletes nourished with honey,while those relying on glucose for an energy boost might have been exhausted.

Digestion and absorption

Natural honey contains several enzymes which enhance the digestion of food substancesespecially carbohydrates such as sugars and starch. The additional benefit of eatinghoney as a source of energy over the commonly used artificial sugar is that, themajor sugar constituents of NH are present as monosaccharides (simple sugars) [2]. Unlike the refined sugar (sucrose) which normally has to undergo theprocesses of digestion into simpler forms prior to their absorption, these sugarmolecules in NH are in pre-digested forms, and can be directly absorbed into thehuman system. Apart from giving nutrition, the use of honey as a sweetening agent insweets and desserts is also beneficial. As a sweetener, honey has nutritionaladvantages over sugar, providing some amount of small nutrients [2,3], which act to aid digestive processes in the body. The gastrointestinaltract (GIT) contains lot of essential and beneficial bacteria, especiallyBifidobacteria for the maintenance of life and good health. It has been suggestedthat one can increase the Bifidobacteria populations in the GIT by consuming foodswith rich supply of prebiotics such as natural honey [40,41]. Prebiotics are substances that facilitate the enhanced growth and thebiological activity of these good and beneficial bacteria. The consumption of honeyis important in human digestion, and this effect is produced by the honey’sconstituents of oligosaccharides [40-42]. Several experimental trials involving both in vitro and invivo studies have been documented on the importance of dietarysupplementation with natural honey on the growth of the beneficial bacteria(bifidobacteria and lactobacilli) and their prebiotic effects in the GIT [40-45]. One comparative study on natural (honey) and artificial (sucrose) sugarsshows that honey increased both in vitro the beneficial bacteria,lactobacilli, as well as in vivo (within the small and the large intestinesof experimental rats), while sucrose had no effect [46]. In some cases, the consumption of relatively large amounts of NH (between70 to about 95 g) can produce a mild laxative effect in people with fructosemalabsorption or inadequate absorption [47,48]. Generally, honey has a laxative effect on the digestive system ofindividuals. Another nutraceutical function of honey is provision of calcium. Honeyconsumption provides calcium, which is readily absorbable and strengthen bone massdevelopment. This can help reduce the risk of osteoporosis or low bone mass(causative agent of fractures) in old individuals. Research in animal models showthat calcium absorption increased correspondingly with increased honey intake [49].

Children nutrition

There are anecdotal evidences encouraging the feeding of honey to new born babies bysome customs and traditions. It is now an established fact that feeding honey toinfants will improve memory and growth, reduce anxiety and enhance thechildren’s performance in later life. In 2009, Chepulis and co workers gavescientific credence to this beneficial practice in their New Zealand behaviouralstudy in animals [50]. They fed 8 weeks old rats with diet supplemented with eitherhoneydew honey or sucrose, and control group with sugar-free diet (all dietspatterned after typical New Zealand human diet). These workers noted improved spatialmemory and reduced anxiety in the honey-fed rodents better than the other groups overthe twelve months trial period. The authors concluded that early introduction ofhoney diet is beneficial and can improve memory loss and cognitive decline associatedwith aging [50].

The application of honey in human infant nutrition also revealed some interesting andbeneficial observations. The palatability of honey for infants was investigated byRamenghi and others in 2001, and these workers reported that honey was well toleratedand significantly reduced the crying phases of babies than sterile water [51]. In a review on the importance of honey relative to sucrose inchildren’s nutrition, honey fed infants were found to have improvedhaematological profiles and calcium uptake, no digestion problem, lighter and thinnerfaeces, better skin colour, less susceptibility to diseases, and steady weight gain [52]. These beneficial effects produced by NH when included in infant formulaare attributable to its effects in enhancing the gastrointestinal function whichinclude the digestion process. The possible cause is the effect of the carbohydrateconstituents, oligosaccharides in NH on intestinal flora of these children [53]. One will be doing well to children by giving honey to replace sweets andother sugary substances they are often inclined to eat.

Medicinal properties of honey

Haematology and immunity

Honey has been found to be beneficial to people suffering from anaemia. Ajibola etal. (2007) reported enhanced blood profiles in floral honey-fed adult rats [4]. The study recorded improved haemoglobin concentration (iron constituentof NH played an important role in this), increased erythrocyte count and elevatedhaematocrit in the honey eaters. In another laboratory, Chepulis (2007) alsodocumented enhanced haematology and immune response in rats fed 10% honeydew honeysupplemented diet [54]. The author noted higher lymphocyte count and increased neutrophilphagocytosis in NH-fed rats than control. This aligned with previous research thatprebiotics can enhance immune function [55,56] and NH is known to contain the prebiotics, oligosaccharides [4,40,57]. Human subjects administered with two honey treatments in a Californianstudy show that honey eaters have the benefit of haematoprotection in addition toblood proliferation [27]. The researchers observed that the aqueous portion of the blood (plasma)is protected by honey. This is in agreement with the fact that most of theantioxidant components in processed honey are water soluble. In summarizing the factsthat honey can be considered to be a satisfactory immuno-nutrient, some workers opinethat the oral administration of natural honey can stimulate and increase theproduction of antibody during primary and secondary immune responses against theT-cells of the thymus-dependent as well as the thymus independent antigens [58].

Oral health

The use of NH can promote oral health and wellness. Molan opines that honey with highlevel of antibacterial activity has the potential to reduce the risk of dental caries [59]. In addition to the carioprotective effect of New Zealand manuka honey (avery potent antimicrobial honey), Molan and co-workers have shown from his extensivework on the influence of honey on oral health that honey prevents dental plaque,gingivitis, periodontics [60]. Other workers in different laboratories have also shown that honey isnon-cariogenic or less cariogenic than sucrose [61-64]. The carioprotective effect of honey has been adduced to its antibacterialproperty, which prevents the growth of the bacteria that can cause dental caries [59,62]. In one electron microscopy study, honey consumption was found to be saferand less inimical to oral health than drinking fruit juice [65]. There was a report of the tooth enamel being eroded just ten minutesafter the consumption of fruit juice, while honey ingestion delayed this observationtill half an hour after the intake of NH, and this erosion of teeth was not even asprominent or visible as that observed in the fruit juice eaters. The plausibleexplanation for the less cariogenic effect of honey is the protective role of NHconstituents which include calcium, fluoride, phosphorous and other colloidal honeycomponents. In summary, it can be concluded that honey has constituents withcario-protective effect.

Gastroenterology

Anecdotal evidences advocate the medicinal use of NH as therapeutic agent against theailments of the GIT in the past [6,66-69]. These are presently being supported by the global medicinal use of NH forthe prevention, cure and the treatments of some GIT disorders such as ulcers,gastritis and gastroenteritis [70-77]. Honey has been shown to be a gastroprotective agent. Its potency ininhibiting the activity of Helicobacter pylori, that causes gastritis andpeptic ulcers have been well documented [78-80]. In experimental rats, NH mitigated gastrointestinal assaults caused byalcohol, ammonia, aspirin and indomethacin [70,71,74,75]. Two mechanisms have been proposed to be responsible for this protectiveaction of honey. The first suggests that this effect is due to the antioxidantproperties of honey. NH was found to maintain or enhance the level of non-proteinsulfhydyl substances (such as glutathione) in gastric tissue subjected to factorsinducing ulceration [70-73]. Similar observation was made when Anzer honey pre-treatment was used toprevent N-ethylmaleimide (NEM) -induced liver damage in rats [81]. The findings imply that depletion of glutathione concentration plays anaetiological role in NEM-induced liver injury, and that the hepatoprotective effectof Anzer honey may be mediated through the sulfhydryl sensitive processes. Theauthors concluded that honey possess antioxidant properties.

According to some authors, the second mechanism of action being proposed shows thathoney intake stimulates the sensory nerves in the stomach, and this proprioceptiveeffect is in response to capsaicin [70,73]. This mechanism involves the reduction of ulcer index, vascularpermeability, and muscular activity of the stomach [77]. Other authors also explained this phenomenon by reporting the mitigatingeffect of dandelion honey intake against gastric juice acidity by more than 50% [82]. One study reported a slower passage rate of gastric content ofsaccharides after the intake of NH than that after ingestion of a mixture simulatinghoney that is glucose and fructose mixture [83], and thus, mitigating diarrhoea. The clinical uses of honey in infants andchildren revealed shorter duration of diarrhoea caused by bacteria. In the same vein,NH also reduced the pathogenesis and duration of viral diarrhoea unlike thatassociated with the use of conventional antibacterial therapy [84]. Honey was also found to be beneficial in maintaining blood-sugar levels.In honey, there is little water available to promote the growth of bacteria andyeast. In addition, honey's natural acidity inhibits some pathogens, as it has anamount of hydrogen peroxide and other substances contributing to its antibacterialeffect [18].

Ophthalmology

The use of honey in the treatment of eye diseases is well documented. The ancientpeople used honey from Attica [85], and Indian lotus honey [86] as curative substances for eye disorders. The Indian locals still use NHas eye drops to cure eye disease till today [87-89]. The Malian people used NH as a tradomedicinal therapeutic agent againstmeasles. The NH was usually applied on the eyes to prevent the scarring effect of thecornea which occurs as a complication of the measles infection [90]. There was an astounding success reported from NH application in clinicaltrials of 102 patients with different ophthalmological disorders such as(blepharitis, conjunctivitis and keratitis), hitherto not responding to conventionaltreatment [91]. After the NH application under the lower eyelid like an eye ointment,improvement was seen in 85% of the cases, with no deterioration seen in any of theother 15%. However, a transient stinging sensation and redness of the eye wasobserved soon after putting honey in the eye, but not enough to halt the treatment inall the 102 cases in the trial. The use of NH application in ophthalmology in Asiaand Eastern Europe has also been reported by Molan in the review on NH use inophthalmology [16]. In one Indian Medical College, an Ophthalmic Surgeon successfully treatedbacterial caused corneal ulcers with the topical application of NH [92]. The same paper documented Meier referring to NH being used for thetreatment of eyes discharging pus [92]. Molan (1999) also cited Russian authors, Mozherenkov and Prokof'eva thatdocument a review on the use of honey in ophthalmology [16]. The Russian authors observed antibacterial, antifungal andanti-inflammatory actions with the honey application to the eye under the lowereyelid [93]. It has been used for the treatment of burns to the eye caused by chemicaland thermal agents, as well as conjunctivitis, and corneal infections. This isusually done by the topical application of the undiluted NH on the affected eyes, oralternatively as a solution containing about 50% water, without any loss of potency [16].

Metabolic and cardiovascular effects

It has been shown that honey intake ameliorates risk factors of metabolic andcardiovascular diseases in patients and healthy individuals at risk. Unlike refinedsugars, diabetic patients can safely and harmlessly eat this natural and sweetestsugar (fructose)-containing product, natural honey. According to Costa-Neto (1999)reported by Santos and Antonini, the Pankararé tribe of Brazil even recommendedhoney’s use for the treatment of diabetes mellitus, bronchitis, mycosis, andthroat aches amidst other ailments [94,95]. Recently in our laboratory, we fed male and female rats with NH or sugar(golden syrup, GS) supplemented diet for 12 weeks from 7 days of age tocompare their metabolic response, and see if NH is protective against metabolicsyndrome (MetS). This MetS is a condition characterized by abdominal obesity,hyperglycaemia, hypertension and dyslipidaemia, and thus increased susceptibility todiabetes, kidney and heart diseases [96,97]. In male rats, GS significantly increased (p < 0.05) bloodlevels of metabolic substrates (glucose and triglycerides, TGs); and caused enhanced(p < 0.001) visceral adiposity, hypercholesterolemia,hyperinsulinemia, hepatomegaly and fatty liver. These CVDs and metabolicdiseases’ risk factors were not observed in the NH-fed rats in this trial. Weconcluded that honey is cardio-protective, and its (NH) consumption could not induceMetS [unpublished results]. These results confirmed the conclusion drawn from earlierstudy that substituting honey for refined carbohydrates was beneficial [40]. Earlier researches from other laboratories and clinical trials furtheraffirmed the metabolic and cardiovascular health significance of eating honey byrecording some health profiles. These were reduction in the plasma levels of riskfactors which include total cholesterol [19,20]; low density lipoprotein (LDL)-cholesterol [19,20,98]; TGs [19,24,31]; glucose in normal and diabetic patients [19,20]; C-reactive protein [19,20]; while the health indices elevated in the blood were high densitylipoprotein (HDL) cholesterol [19,20,25,40]. In addition, other workers recorded higher plasma antioxidants levels inrats nurtured with natural honey relative to fructose-fed rats, and consequently lowsusceptibility of these subjects to CVDs [40].

Chemotherapy and wounds management

Honey has antiseptic properties, good for treating burns, infected surgical woundsand ulcers. Glenys Round, a Cancer Specialist and Julie Betts in Waikato Hospital,New Zealand reported excellent results of the therapy from patients with fungatingwounds, recalcitrant leg ulcers and pressure sores using the Unique Manuka Factor(UMF)-containing honey known as manuka honey [99]. According to the Specialist, the application of honey dressings was usedin these patients (including those with cancer broken through the skin), afterfailure of healing from conventional treatments which include radiation therapy.Another Researcher successfully treated experimental surgical wounds in NigerianDwarf goats with blossom honey. He observed epithelialisation and significantlyhigher contraction of the NH treated wounds relative to untreated wounds [13]. Other several workers had also used honey for the same purpose in humansurgical wards and on experimental animals [100-105]. A comprehensive review of effect of honey on wounds is availableelsewhere [16].

Antimicrobial activity

Natural honey is a very potent broad spectrum antibiotic which most multi-resistantbacteria are found sensitive to (Table 4). Alvarez-Suarezand co-workers confirm this in their report and opine that antimicrobial activity ispresent in all types of honey [106]. The workers suggest that hydrogen peroxide formation may play animportant role as antibacterial natural products for minimizing the invasive effectsof bacterial infections in the native monofloral Cuban honeys analysed. Although, theCuban honeys varied in their chemical constituents’ values, all still exhibitantimicrobial activity against both Gram-positive and Gram-negative bacteria whichinclude Bacillus subtilis, Pseudomonas aeruginosa, Staphylococcus aureus andEscherichia coli[106]. The bacteria and other micro-organisms infections responsive to NHtreatment are listed in Table 4.

Table 4
List of Bacteria and other Organisms found to be sensitive to honey*
Actinomyces pyogenesPseudomonas aeruginosa
Bacillus anthracis
Rubella virus
Campylobacter coli
Salmonella cholerae-suis
Campylobacter jejuni
Salmonella typhi
Candida albicans
Salmonella typhimurium
Corynebacterium diphtheria
Serrata marcescens
Echinococcus parasite
Shigella species
Enterococcus avium
Staphylococcus aureus
Enterococcus faecalis
Streptococcus agalactiae
Enterococcus faecium
Streptococcus dysgalactiae
Enterococcus raffinosus
Streptococcus faecalis uberis
Epidermophyton floccosum
Streptococcus mutans
Escherichia coli
Streptococcus pneumonia
Haemophilus influenza
Streptococcus pyogenes
Helicobacter pylori
Streptococcus uberis
Klebsiella pneumonia
Serrata marcescens
Leishmania parasite
Shigella species
Microsporum canis
Trichophyton mentagrophytes
Microsporum gypseum
Trichophyton mentagrophytes var.
Mycobacterium tuberculosis
Trichophyton tonsurans
Nocardia asteroids
Trichophyton rubrum
Proteus speciesVibrio choleriae

*Adapted from [18,107,108].

In their various studies with about 200 New Zealand (Manuka and non-Manuka) honeys,Molan and co-workers are of the opinion that differences exist in the antibacterialand antifungal activities, although all exhibit potency [107-110]. Other pathogenic microbes reported to be susceptible to honey treatmentare Candida albicansRubella virus, Trichophytonmentagrophytes, and Leishmania parasites [109,111-113], as shown in Table 4.

Adverse effects

NH like any other natural foods can also be exposed to contamination by antibiotics,pesticides, heavy metals and other toxic compounds [114]. These poisonous substances can result from disease control, accidentalexposure, environmental hazards and inimical human practices [115,116]. It was reported that European health authorities found lead (Pb) in honeybought from India in early 2010 [115]. The presence of contaminants in Indian honeys was confirmed a year laterin a test by the Indian Export Inspection Council. The findings showed the presenceof lead and at least two antibiotics in almost 23% of the 362 test samples of honeymeant for export [115]. The antibiotics could have been the residual effect of treatment andcontrol of infection in honey-bees. A link to this hypothesis is the almostsimultaneous, coincidental control of the bacterial epidemic of foulbrood disease inbee hives by Chinese beekeepers, with the use of several antibiotics manufactured inIndia for animal use, including chloramphenicol [115]. Medical researchers had shown that treatment of children withchloramphenicol as an antibiotic can cause susceptibility to DNA damage andcarcinogenicity. The amount of chloramphenicol found in NH although minute, accordingpublic health experts, could cause a severe, fatal reaction such as aplastic anaemiain about one out of 30,000 people [115]. This led to the ban placed on honeys originating from China by the UnitedStates of America agency, Food and Drug Administration (FDA).

The high concentration of heavy metals in honey can be a source of illness to humanbeings. Heavy metals are chemical elements with a specific gravity that is at leastfive times the specific gravity of water. The heavy metals that are of concern in NHproduction and apicultural practices are listed in Tables 2 and 3. In small quantities, some heavy metals arenutritionally essential for a healthy life. These are referred to as the traceelements, and are listed under minerals in Table 2. Thenon-essential elements associated with NH are often absent or present in very minuteand insignificant levels. These heavy metals of no biological and chemicalsignificance identified in Table 3 are cobalt, molybdenumand nickel. However, there are certain heavy metals present in honey abovepermissible levels by pollution standards leading to toxicity [116]. The poisoning is due to these heavy metals’ inability to bemetabolized by the body, thus leading to their being accumulated to toxic levelswithin the human or animal soft tissues without being degraded or destroyed. It hasbeen reported that Pb can cause damage of brain, kidney, nervous system and red bloodcells. The other health problems caused by heavy metals toxicity include headache,metabolic abnormalities, respiratory disorders, nausea and vomiting [117].

The use of agrochemicals in growing of flowers causes contamination of nectar withheavy metals [2], such as arsenic (As), cadmium (Cd) and Pb. These three heavy metals (As,Cd, Pb) have been identified in the priority list of top 20 hazardous substancescompiled by an agency of the United States of America Department of Health and HumanServices, known as The Agency for Toxic Substances and Disease Registry (ATSDR) in2001. [118]. According to ATSDR, As is the most hazardous and toxic substance, beingthe first on the Agency’s priority list, closely followed by Pb as second,while Cd ranked seventh on the list. Arsenic poisoning could result fromenvironmental contamination through the use of pesticides and paints manufacturing [118]. The limited sources of As pollution might be the reason for lack of Ascontaminated honey cases being reported, despite the severity of its hazard. Cdcontaminated honey could be as a result of its (Cd) use in Pb and zinc (Zn) mining;use of pesticides; and improper handling and disposal of old, used Cd batteries.Nonetheless, Cd concentration in NH is 0 to 0.0001 mg/100 g honey(Table 3), probably due to its similar limited sourcesof environmental pollution like arsenic, and legislation on protection againstoccupational health [118]. These showed that this natural food (NH) can be said to be safe from twoof the three most hazardous contaminants. However, it is known that heavy metalpoisoning results from long term low level exposure to contaminants [114,118]. Hence, no effort should be spared at ensuring the availability ofwholesome NH devoid of toxic heavy metals especially Pb, which is the most commonlyencountered top hazardous substance of the three identified by ATSDR as beingassociated with NH.

The other factors causing metal contamination of NH are the methods of honeyharvesting, processing and storage. Most small scale local beekeepers use low costmetallic containers due to low purchasing power [115]. Thus, the acidic nature (pH 3.2 – 4.5) of NH (Table 1) corrodes the metal containers [115,119]. Lead is the most documented of all heavy metals causing honeycontamination [114-116], due to the various health problems it causes. The possible reason for itspresence in different types of honey from several geographic locations could be as aresult of the high concentration of Pb in the air due to oil extraction andautomobile exhaust emissions [116]. Another environmental factor causing high Pb presence in honey could bedue to poor waste disposal of paints, printing materials such as ink, as well as useddry batteries in some places [114]. The other heavy metals of public health importance found in NH apart fromAs, Cd and Pb are chromium (Cr) and zinc (Zn) (Table 3).The contact of honey with stainless steel surfaces during honey production can alsogenerate a high Cr content, due to the corrosive effect of honey acidity. It has alsobeen documented that NH storage in galvanized containers can be a source of Zncontamination [114,120]. Therefore it is important to take into account the type and quality ofequipment used to produce and store honey after harvesting as the possible sources ofhoney contamination with heavy metals. In addition, the increasing overwhelmingdemand of this natural product necessitates the promotion of all feasible activitiestowards ensuring quality [115]. This would increase the production of residue-free and wholesome honeyfor domestic and international consumption [121]. The safety of consumers and the high global demand for quality honey makeinternational legislation on the food imperative.

The concern of Paediatricians, microbiologists, nurses, Care-givers in health centresand maternity homes as well as other health professionals for infants is in regard tothe presence of toxic bacteria, Clostridium (Cl.)botulinum in natural honey. Since this bacterium may be present innatural foods, and honey mostly being a non-sterilized packaged food, the risk ofcontamination cannot be ruled out. In order to avoid the exposure of infants withimmature GIT to the risk of contamination with Cl. botulinum and itstoxin-producing spores, it is advisable not to feed infants that are below one yearold with raw honey. However, in order to alleviate the concern of introducingClostridial infection through this natural product, honey can be sterilized by gammairradiation without any loss of NH’s properties [60]; thus, preventing contamination without reducing its nutraceutical valueand potency.

Honey and wealth

NH Production and consumption

Natural honey production is of high economic importance globally. The cost of honeyproduction is minimal compared with the high returns on the investment. It has beenestimated that the global market for wound care annually is between two to sixbillion US dollars. If part of this huge sum is used to procure the recentlydeveloped hi-tech honey dressings, it will go a long way to improve honey production.However, little attention is given to this high-yielding enterprise known asapicultural practice. According to the information on honey production andconsumption available at http://www.apiservices.com/, the present annualworld honey production is about 1.2 million tons, which is less than 1% of the totalsugar production. The consumption of honey differs strongly from country to country.The major honey exporting countries China and Argentina have small annual consumptionrates of 0.1 to 0.2 kg per capita. NH consumption is higher indeveloped countries, where the home production does not always meet the marketdemand. In the European Union, which is both a major honey producer and importer, theannual consumption per capita varies from medium (0.3 – 0.4 kg)in Denmark, France, Great Britain, Italy and Portugal to high consumers (1.0 –1.8 kg) in Austria, Germany, Greece, Hungary and Switzerland. In countries suchas Australia, Canada and United States of America, the average per capitaconsumption is 0.6 to 0.8 kg/year [122]. According to FAO (Food and Agriculture Organization of the UnitedNations) reports of 2005, China is the world largest producer of honey. Other topproducers of natural honey are Argentina, Turkey and the United States of America [123]. The significant regional producers of honey include Turkey (ranked thirdworldwide) and Ukraine (ranked fifth worldwide) [7,124]. Mexico is also known as an important NH producer, providing about 10% ofthe world's supply. There is urgent need to increase NH production by all countriesworldwide to meet the high global demand of honey, which is adjudged an importantsubstitute of refined sugars and conventional medicaments.

Apicultural practices

Apiculture is the practice of keeping honey bees (Apis indica, Apismellifera) for its products such as NH, wax, propolis, pollens, cerume (amixture of wax and propolis) etc. It has been shown that NH and its by-products arenatural resources, yet to be taken full advantage of as economic earner of littleinvestment with huge returns [121-125]. However, apart from honey and its by-products used for nourishment andmedicine, the honey-bees and larvae also serve as source of protein for some people [94,95,125]. These communities harbour stingless bees, a South American speciesrestricted to Brazil, Paraguay, and Columbia [95]. According to Bertoni reported by [95] this species are the best honey producer, but the honey is always somewhatacidic [126], good as an antibiotic. Ethno-entomologists should exploit the trait ofhoney prolificacy of this species, and also control the acidity of their product (foruse as food). This will afford production of more honey, devoid of undesirablequality. Apicultural practices can improve economic earnings of most countriesespecially in the sub-Sahara African countries and other parts of the globe withforest reserves. Previous studies have shown that bees are integral inseparable partof the ecosystem. According to Costa-Neto 1998, 1999, there are no forests withoutbees, and there are no bees isolated from the forests [94,126]. Bee keeping can improve small scale and cottage industries, boost foreignearnings from export especially by sub Saharan African countries with vast expansesof unused land spaces and forest reserves.

Conclusion

The intake of honey as food and medicine resulted in high nutritional benefit andtherapeutic promise. The botanical origin plays prominent roles on the bioavailabilityof NH phytochemical compounds, which consequently has effects on the biological activityof honey. However, irrespective of the floral source, variety and number (mono,polyfloral or blended); honey type (blossom or honeydew honey, Manuka or non-Manuka);concentration (diluted or undiluted); bee (sting or stingless), all contain antioxidantsand exhibit various degree of biochemical activities attributable to NH’s potencyand value as a nutraceutical agent. The sources and adverse effects of NH contaminationidentified should be prevented. This could promote the availability of residue-freehoney and a wholesome natural product for domestic consumption and international market.This would also help to prevent health problems associated with NH toxicity, especiallythe most commonly encountered Pb poisoning. Apicultural practices should be encouragedand beekeeping increased especially in countries with avalanche of forests. This willincrease NH production worldwide and boost the availability of honey, which is adjudgedan important substitute of refined sugars and conventional medicaments. Furthermore,this will facilitate NH’s use as a cheap source of energy nutrient, and as analternative and economical medicament for most ailments. The stingless bees hithertorestricted to Brazil could be introduced to other parts of the world. TheEthno-entomologists, other Scientists and Apiculturists have roles to play in thisdevelopment. This will improve apicultural practices especially among people who aresceptical of harm from sting honey bees. The cost of honey production will reduce, anddomestic consumption as well as income from export will increase.

Abbreviations

As, Arsenic; ATSDR, Agency for Toxic Substances and Disease Registry; Cd, Cadmium; Cr,Chromium; CVDs, Cardiovascular diseases; GI, Glycaemic index; GIT, Gastrointestinaltract; GS, Golden syrup; HDL, High density lipoprotein; LDL, Low density lipoprotein;MetS, Metabolic syndrome; NEM, N-ethylmaleimide; NH, Natural honey; Pb, Lead; ROS,Reactive oxygen species; TGs, Triglycerides; UMF, Unique Manuka Factor; Zn, Zinc.

Competing interests

The authors declare that they have no competing interests.

Authors’ contributions

KHE mooted the idea of the review; AA carried out the literature search; and AA, KHE andJPC wrote the paper. All authors read and approved the final manuscript.

Authors’ information

AA, Senior Lecturer, Department of Physiology, Faculty of Basic Medical Sciences,Olabisi Onabanjo University, Ikenne campus, Ikenne 121002, Ogun State, Nigeria. KHE,Associate Professor, School of Physiology, Faculty of Health Science, University of theWitwatersrand, 7 York Road, Parktown 2193, South Africa. JPC, Senior Lecturer,Department of Veterinary Anatomy and Physiology, Faculty of Veterinary Science,University of Pretoria, Onderstepoort, South Africa.

Acknowledgements

The Doctoral study that led to this review was supported by grants from the EducationTrust Fund (ETF), Abuja Nigeria; and the University of the Witwatersrand,Johannesburg, South Africa.

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