literature review on honey pdf

Honey and Health: A Review of Recent Clinical Research

Affiliations.

• 1 Department of Basic Medical Sciences, Neyshabur University of Medical Sciences, Neyshabur, Iran.
• 2 Department of Immunogenetics, BuAli Research Institute, Mashhad University of Medical Sciences, Mashhad, Iran.
• 3 Department of Neurosurgery, Mashhad University of Medical Sciences, Mashhad, Iran.
• PMID: 28539734
• PMCID: PMC5424551
• DOI: 10.4103/0974-8490.204647

Honey is one of the most appreciated and valued natural products introduced to humankind since ancient times. Honey is used not only as a nutritional product but also in health described in traditional medicine and as an alternative treatment for clinical conditions ranging from wound healing to cancer treatment. The aim of this review is to emphasize the ability of honey and its multitude in medicinal aspects. Traditionally, honey is used in the treatment of eye diseases, bronchial asthma, throat infections, tuberculosis, thirst, hiccups, fatigue, dizziness, hepatitis, constipation, worm infestation, piles, eczema, healing of ulcers, and wounds and used as a nutritious supplement. The ingredients of honey have been reported to exert antioxidant, antimicrobial, anti-inflammatory, antiproliferative, anticancer, and antimetastatic effects. Many evidences suggest the use of honey in the control and treatment of wounds, diabetes mellitus, cancer, asthma, and also cardiovascular, neurological, and gastrointestinal diseases. Honey has a potential therapeutic role in the treatment of disease by phytochemical, anti-inflammatory, antimicrobial, and antioxidant properties. Flavonoids and polyphenols, which act as antioxidants, are two main bioactive molecules present in honey. According to modern scientific literature, honey may be useful and has protective effects for the treatment of various disease conditions such as diabetes mellitus, respiratory, gastrointestinal, cardiovascular, and nervous systems, even it is useful in cancer treatment because many types of antioxidant are present in honey. In conclusion, honey could be considered as a natural therapeutic agent for various medicinal purposes. Sufficient evidence exists recommending the use of honey in the management of disease conditions. Based on these facts, the use of honey in clinical wards is highly recommended.

Summary: There are several evidence that suggesting the usage of honey in the management of disease. Therefore, honey in clinical wards is highly recommended. Abbreviations Used : WA: Water activity, RDI: Recommended daily intake, Si: Silicon, RB: Rubidium, V: Vanadium, Zr: Zirconium, Li: Lithium, Sr: Strontium, Pb: Lead, Cd: Cadmium, As: Arsenic, MIC: Minimum inhibitory concentration, PARP: Poly (ADP-ribose) polymerase, ROS: Reactive oxygen species, iNOS: Inducible nitric oxide synthase, NKcells: Natural killer cells, SCFA: Short-chain fatty acid, CRP: C-reactive protein.

Keywords: Antioxidant; flavonoids; honey; polyphenols; therapeutic agent; traditional.

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Properties of bee honeys and respective analytical methods

• Published: 04 March 2022
• Volume 15 , pages 1720–1735, ( 2022 )

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• Kamila Goderska   ORCID: orcid.org/0000-0003-4724-075X 1  

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The paper presents information concerning the beneficial and harmful effects of honey on human health. Selected therapeutic properties and components responsible for the antibiotic activity of honey are discussed, along with the impact of different factors and technological treatments on these properties. This paper also presents methods applied in the analyses of antioxidant and antibacterial properties of bee products. The purpose of the following study is to present a review of the health properties of honey and the effect of various factors on these properties. Honey is a valuable product because of its nutritional and health properties. It should be noted, however, that individual botanical varieties of honey exhibit different levels of nutritional and health properties, including antibacterial properties.

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Goderska, K. Properties of bee honeys and respective analytical methods. Food Anal. Methods 15 , 1720–1735 (2022). https://doi.org/10.1007/s12161-022-02243-0

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Received : 15 July 2021

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DOI : https://doi.org/10.1007/s12161-022-02243-0

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Honey: its medicinal property and antibacterial activity

Manisha deb mandal.

1 Department of Physiology and Biophysics, KPC Medical College and Hospital, 1F Raja S C Mallick Road, Jadavpur, Kolkata-700 032, India

Shyamapada Mandal

2 Department of Zoology, Gurudas College, Narkeldanga, Kolkata-700 054, India

Indeed, medicinal importance of honey has been documented in the world's oldest medical literatures, and since the ancient times, it has been known to possess antimicrobial property as well as wound-healing activity. The healing property of honey is due to the fact that it offers antibacterial activity, maintains a moist wound condition, and its high viscosity helps to provide a protective barrier to prevent infection. Its immunomodulatory property is relevant to wound repair too. The antimicrobial activity in most honeys is due to the enzymatic production of hydrogen peroxide. However, another kind of honey, called non-peroxide honey ( viz. , manuka honey), displays significant antibacterial effects even when the hydrogen peroxide activity is blocked. Its mechanism may be related to the low pH level of honey and its high sugar content (high osmolarity) that is enough to hinder the growth of microbes. The medical grade honeys have potent in vitro bactericidal activity against antibiotic-resistant bacteria causing several life-threatening infections to humans. But, there is a large variation in the antimicrobial activity of some natural honeys, which is due to spatial and temporal variation in sources of nectar. Thus, identification and characterization of the active principle(s) may provide valuable information on the quality and possible therapeutic potential of honeys (against several health disorders of humans), and hence we discussed the medicinal property of honeys with emphasis on their antibacterial activities.

1. Introduction

Antimicrobial agents are essentially important in reducing the global burden of infectious diseases. However, as resistant pathogens develop and spread, the effectiveness of the antibiotics is diminished. This type of bacterial resistance to the antimicrobial agents poses a very serious threat to public health, and for all kinds of antibiotics, including the major last-resort drugs, the frequencies of resistance are increasing worldwide [1] , [2] . Therefore, alternative antimicrobial strategies are urgently needed, and thus this situation has led to a re-evaluation of the therapeutic use of ancient remedies, such as plants and plant-based products, including honey [3] – [5] .

The use of traditional medicine to treat infection has been practiced since the origin of mankind, and honey produced by Apis mellifera ( A. mellifera ) is one of the oldest traditional medicines considered to be important in the treatment of several human ailments. Currently, many researchers have reported the antibacterial activity of honey and found that natural unheated honey has some broad-spectrum antibacterial activity when tested against pathogenic bacteria, oral bacteria as well as food spoilage bacteria [6] , [7] . In most ancient cultures honey has been used for both nutritional and medical purposes. The belief that honey is a nutrient, a drug and an ointment has been carried into our days, and thus, an alternative medicine branch, called apitherapy, has been developed in recent years, offering treatments based on honey and other bee products against many diseases including bacterial infections. At present a number of honeys are sold with standardized levels of antibacterial activity. The Leptospermum scoparium ( L. scoparium ) honey,the best known of the honeys, has been reported to have an inhibitory effect on around 60 species of bacteria, including aerobes and anaerobes, gram-positives and gram-negatives [8] . Tan et al [9] reported that Tualang honey has variable but broad-spectrum activities against many different kinds of wound and enteric bacteria. Unlike glucose oxidase, the antibacterial properties from Leptospermum spp. honeys are light- and heat-stable. Natural honey of other sources can vary as much as 100-fold in the potency of their antibacterial activities, which is due to hydrogen peroxide [6] , [10] . In addition, honey is hygroscopic, which means that it can draw moisture out of the environment and dehydrate bacteria, and its high sugar content and low level pH can also prevent the microbes from growth.

Based upon the extensive searches in several biomedical science journals and web-based reports, we discussed the updated facts and phenomena related to the medicinal property of honeys with emphasis on their antibacterial activities in this review.

2. Medicinal property

Honey is an ancient remedy for the treatment of infected wounds, which has recently been ‘rediscovered’ by the medical profession, particularly where conventional modern therapeutic agents fail. The first written reference to honey, a Sumerian tablet writing, dating back to 2100-2000 BC, mentions honey's use as a drug and an ointment. Aristotle (384-322 BC), when discussing different honeys, referred to pale honey as being “good as a salve for sore eyes and wounds”. Manuka honey has been reported to exhibit antimicrobial activity against pathogenic bacteria such as Staphylococcus aureus ( S. aureus ) and Helicobacter pylori ( H. pylori ) making this honey a promising functional food for the treatment of wounds or stomach ulcers [10] .

The honey has been used from ancient times as a method of accelerating wound healing [11] , and the potential of honey to assist with wound healing has been demonstrated repeatedly [12] , [13] . Honey is gaining acceptance as an agent for the treatment of ulcers, bed sores and other skin infections resulting from burns and wounds [14] , [15] . The healing properties of honey can be ascribed to the fact that it offers antibacterial activity, maintains a moist wound environment that promotes healing, and has a high viscosity which helps to provide a protective barrier to prevent infection [6] . There are many reports of honey being very effective as dressing of wounds, burns, skin ulcers and inflammations; the antibacterial properties of honey speed up the growth of new tissue to heal the wound [16] . The medihoney and manuka honey have been shown to have in vivo activity and are suitable for the treatment of ulcers, infected wounds and burns [6] , [17] .

The honey, when applied topically, rapidly clears wound infection to facilitate healing of deep surgical wounds with infection [18] . The application of honey can promote the healing in infected wounds that do not respond to the conventional therapy, i.e. , antibiotics and antiseptics [18] , including wounds infected with methicillin-resistant S. aureus [19] , [20] . Moreover, it can be used on skin grafts and infected skin graft donor sites successfully [21] .

The manuka, jelly bush and pasture honeys are capable of stimulating the monocytes, the precursors of macrophages, to secrete TNF-α [22] , [23] . On the other hand, glycosylated proteins can induce TNF-α secretion by macrophages, and this cytokine is known to induce the mechanism of wound repairing.Furthermore, the ability of honey to reduce ‘reactive intermediates release’ [23] may well limit tissue damage by activated macrophages during wound healing. Thus, the immunomodulatory property of honey is relevant to wound repair.

The support for using honey as a treatment regimen for peptic ulcers and gastritis comes from traditional folklore as well as from reports in modern times [24] . Honey may promote the repair of damaged intestinal mucosa, stimulate the growth of new tissues and work as an anti-inflammatory agent [24] , [25] . Raw honey contains copious amounts of compounds such as flavonoids and other polyphenols which may function as antioxidants [26] . Clinical observations have been reported of reduced symptoms of inflammation when honey is applied to wounds. The removal of exudate in wounds dressed with honey is of help in managing inflamed wounds [18] .

3. Antibacterial activity

3.1. potential antibacterial agent.

The use of honey as a traditional remedy for microbial infections dates back to ancient times [8] . Research has been conducted on manuka ( L. scoparium ) honey [27] , which has been demonstrated to be effective against several human pathogens, including Escherichia coli ( E. coli ), Enterobacter aerogenes , Salmonella typhimurium , S. aureus [6] , [27] . Laboratory studies have revealed that the honey is effective against methicillin-resistant S. aureus (MRSA), β- haemolytic streptococci and vancomycin-resistant Enterococci (VRE) [28] , [29] . However, the newly identified honeys may have advantages over or similarities with manuka honey due to enhanced antimicrobial activity, local production (thus availability), and greater selectivity against medically important organisms [6] . The coagulase-negative staphylococci are very similar to S. aureus [14] , [30] in their susceptibility to honey of similar antibacterial potency and more susceptible than Pseudomonas aeruginosa ( P. aeruginosa ) and Enterococcus species [14] .

The disc diffusion method is mainly a qualitative test for detecting the susceptibility of bacteria to antimicrobial substances; however, the minimum inhibitory concentration (MIC) reflects the quantity needed for bacterial inhibition. Following the in vitro methods, several bacteria (mostly multidrug resistant; MDR) causing human infections that were found susceptible to honeys are presented in Table 1 .

3.2. Zone diameter of inhibition

The zone diameter of inhibition (ZDI) of different honey samples (5%–20%) has been determined against E. coli O157: H7 (12 mm – 24 mm) and S. typhimurium (0 mm – 20 mm) [31] . The ZDIs of Nilgiris honeys were found to be (20–21) mm, (15-16) mm and (13–14) mm for S. aureus , P. aeruginosa and E. coli , respectively [32] . Agbagwa and Frank-Peterside [33] examined different honey samples: Western Nigerian honey, Southern Nigerian honey, Eastern Nigerian honey and Northern Nigerian honey, and compared their abilities to inhibit the growth of S. aureus , P. aeruginosa , E. coli and Proteus mirabilis ( P. mirabilis ) with an average of ZDIs (5.3–11.6) mm, (1.4–15.4) mm, (4.4–13.5) mm and (9.1–17) mm, respectively, and with honey concentrations of 80%–100%. The extracts of raw and processed honey showed ZDI (6.94–37.94) mm, against gram-positive bacteria viz. , S. aureus , Bacillus subtilis , Bacillus cereus , as well as gram-negative bacteria like E. coli , P. aeruginosa and S. enterica serovar Typhi [34] . Figure 1 represents the ZDIs for gram-negative and gram-positive bacterial strains due to ulmo and manuka honeys.

3.3. Minimum inhibitory concentration

The MIC assay showed that a lower MIC was observed with ulmo ( Eucryphia cordifolia ) honey (3.1% – 6.3% v/v) than with manuka honey (12.5% v/v) for MRSA isolates; for the E. coli and Pseudomonas strains equivalent MICs were observed (12.5% v/v) [35] . The MICs for Tualang honey ranged 8.75% - 25%, while those for manuka honey ranged 8.75% – 20% against many pathogenic gram-positive and gram-negative bacteria [9] . The MICs of manuka, heather, khadikraft and local honeys against clinical and environmental isolates of P. aeruginosa were recorded as 10% – 20%, 10% – 20%, 11% and 10% – 20%, respectively [36] . The MICs of A. mellifera honey ranged (126.23 – 185.70) mg/mL and of Tetragonisca angustula honey (142.87 - 214.33) mg/mL against S. aureus [37] . The Egyptian clover honey MIC was 100 mg/mL for S. typhimurium and E. coli O157:H7 [31] . The Nilgiri honey MICs were 25%, 35% and 40% for S. aureus , P. aeruginosa and E. coli , respectively [32] . MIC values of honey extracts were found in the range of (0.625–5.000) mg/mL, for S. aureus , B. subtilis , B. cereus , and gram-negative bacteria ( E. coli , P. aeruginosa and S. typhi [34] .

By visual inspection, the MICs of Tualang honey ranged 8.75% – 25% compared with those of manuka honey (8.75% – 20%) against wound and enteric microorganisms: Streptococcus pyogenes ( S. pyogenes ), coagulase-negative Staphylococci , MRSA, Streptococcus agalactiae , S. aureus , Stenotrophomonas maltophilia ( S. maltophilia ), Acinetobacter baumannii ( A. baumannii ), S. Typhi , P. aeruginosa , Proteus mirabilis , Shigella flexneri, E. coli , Enterobacter cloacae ( E. cloacae ) [9] . Six bacterial strains from burn- wound patients, namely, Aeromonas schubertii ( A. schubertii ), Haemophilius paraphrohaemlyticus ( H. paraphrohaemlyticus ), Micrococcus luteus ( M. luteus ), Cellulosimicrobium cellulans ( C. cellulans ), Listonella anguillarum ( L. anguillarum ) and A. baumannii had MICs of Cirtrus, Clover, Nigella and Eljabaly honeys 35%–40%, 35%–40%, 35%–40%, 25%–30%, respectively, as has been reported by Hassanein et al . The honeys were inhibitory at dilutions down to 3.6% – 0.7 % (v/v), for the pasture honey, 3.4% – 0.5% (v/v), and for the manuka honey, against coagulase-negative Staphylococci [10] . The MICs of various types of honeys for various pathogenic bacterial strains have been determined by many authors [39] ; in this article for oral bacterial strains and bacterial strains causing wound infections, honey MICs are depicted in Figure 2 and ​ and3 3 .

3.4. Time-kill study

The kill kinetics provides more accurate description of antimicrobial activity of antimicrobial agents than does the MIC [2] . In our earlier study, we explored the time-kill activity of autoclaved honey against E. coli , P. aeruginosa and S. Typhi in order to establish the potential efficacy of such local honey (not studied before) collected from a village of the West Bengal state, India [5] . Antibiotic susceptible and resistant isolates of S. aureus , S. epidermidis , Enterococcus faecium , E. coli , P. aeruginosa , E. cloacae , and Klebsiella oxytoca were killed within 24 h by 10%–40% (v/v) honey [40] . Thus, more studies are required to establish various local honeys based upon kill kinetics and their effective in vivo application against MDR infections.

4. Mechanism and factors affecting antibacterial activity

4.1. mechanism of antibacterial activity.

The beneficial role of honey is attributed to its antibacterial property with regards to its high osmolarity, acidity (low pH) and content of hydrogen peroxide (H 2 O 2 ) and non-peroxide components, i.e. , the presence of phytochemical components like methylglyoxal (MGO) [41] , [42] . The antimicrobial agents in honey are predominantly hydrogen peroxide, of which the concentration is determined by relative levels of glucose oxidase, synthesized by the bee and catalase originating from flower pollen [41] . Most types of honey generate H 2 O 2 when diluted, because of the activation of the enzyme glucose oxidase that oxidizes glucose to gluconic acid and H 2 O 2 , which thus attributes the antimicrobial activity [43] . But, in some cases, the peroxide activity in honey can be destroyed easily by heat or the presence of catalase.

Besides H 2 O 2 , which is produced in most conventional honeys by the endogenous enzyme glucose oxidase, several other non-peroxide factors have been found to be responsible for the unique antibacterial activity of honey [13] . Honey may retain its antimicrobial activity even in the presence of catalase (absence of glucose oxidase), and thus this type of honey is regarded as “non-peroxide honey” [8] , [13] . Several components are known to contribute the non-peroxide activity, such as the presence of methyl syringate and methylglyoxal, which have been extensively studied in manuka honey that is derived from the manuka tree ( L. scoparium ) [42] , [44] . Unlike manuka honey, the activity of ulmo honey is largely due to H 2 O 2 production: 25 % (v/v) solution of ulmo honey had no detectable antibacterial activity when tested in presence of catalase, while, at the same concentration the manuka honey retained its antibacterial activity in the presence of catalase (absence of H 2 O 2 ) [35] . Neither type of activity is influenced by the sterilizing procedure of gamma-irradiation [13] .

Honey is characteristically acidic with pH between 3.2 and 4.5, which is low enough to be inhibitory to several bacterial pathogens [45] ; Figure 4 depicts the pH values of different honeys. The minimum pH values for growth of some common pathogenic bacteria are: E. coli (4.3), Salmonella spp. (4.0), P. aeruginosa (4.4), S. pyogenes (4.5) [46] , and thus in undiluted honey the acidity is a significant antibacterial factor. The antibacterial property of honey is also derived from the osmotic effect of its high sugar content and low moisture content, along with its acidic properties of gluconic acid and the antiseptic properties of its H 2 O 2 [47] . A recent study examining the antimicrobial properties of honey in vitro found that H 2 O 2 , MGO and an antimicrobial peptide, bee defensin-1, are distinct mechanisms involved in the bactericidal activity of honey [48] .

4.2. Factors affecting antibacterial nature of honey

Molan and Cooper [49] reported that the difference in antimicrobial potency among the different honeys can be more than 100-fold, depending on its geographical, seasonal and botanical source as well as harvesting, processing and storage conditions. The antibacterial nature of honey is dependent on various factors working either singularly or synergistically, the most salient of which are H 2 O 2 , phenolic compounds, wound pH, pH of honey and osmotic pressure exerted by the honey. Hydrogen peroxide is the major contributor to the antimicrobial activity of honey, and the different concentrations of this compound in different honeys result in their varying antimicrobial effects [8] . It has further been reported that physical property along with geographical distribution and different floral sources may play important role in the antimicrobial activity of honey [50] . Several authors reported that different honeys vary substantially in the potency of their antibacterial activity, which varies with the plant source [6] , [7] , [51] . Thus, it has been shown that the antimicrobial activity of honey may range from concentrations < 3 % to 50 % and higher [6] , [10] , [51] . The bactericidal effect of honey is reported to be dependent on concentration of honey used and the nature of the bacteria [4] , [52] . The concentration of honey has an impact on antibacterial activity; the higher the concentration of honey the greater its usefulness as an antibacterial agent [31] . Taormina et al [50] reported that the concentration of honey needed for complete inhibition of S. typhimurium growth is <25%.

5. Conclusion

Microbial resistance to honey has never been reported [53] , which makes it a very promising topical antimicrobial agent against the infection of antibiotic-resistant bacteria ( e.g. , MDR S. maltophilia ) and in the treatment of chronic wound infections that do not respond to antibiotic therapy. Hence honey has been used as a last-resort medication. Manuka honey has been widely researched and its antibacterial potential is renowned worldwide. The potency of honeys, such as Tualang honey, against microorganisms suggests its potential to be used as an alternative therapeutic agent in certain medical conditions, particularly wound infection.

Lusby et al [6] reported that honeys other than the commercially available antibacterial honeys ( e.g. , manuka honey) can have equivalent antibacterial activity against bacterial pathogens. The growth of bacterial species that cause gastric infections, such as S. typhi , S. flexneri and E. coli , are inhibited by Tualang honey at the low concentrations. The Tualang honey has been reported to be effective against E. coli , S. typhi and S. pyogenes [54] , and thus, when taken orally in its pure undiluted form, this honey may help speed up recovery from such infections. Honey is effective when used as a substitute for glucose in oral rehydration and its antibacterial activity shortened the duration of bacterial diarrhoea.

Currently, the emerging antimicrobial resistance trends in burn wound bacterial pathogens are a serious challenge [55] . Thus, honey with effective antimicrobial properties against antibiotic-resistant organisms such as MRSA and MDR P. aeruginosa, Acinetobacter spp.. and members of the family Enterobacteriaceae , which have been associated with infections of burn wounds and in nosocomial infections, is much anticipated [55] , [56] .

Overall, the unpredictable antibacterial activity of non-standardized honey may hamper its introduction as an antimicrobial agent due to variation in the in vitro antibacterial activity of various honeys. At present a number of honeys are sold with standardized levels of antibacterial activity, of which the best known is manuka ( Leptospermum ) honey as well as Tualang ( Koompassia excelsa ) honey. The medical-grade honey (Revamil, medihoney), which has the potential to be a topical antibacterial prophylaxis because of its broad-spectrum bactericidal activity, or to be a treatment for topical infections caused by antibiotic-resistant as well as antibiotic-sensitive bacteria, should be considered for therapeutic use. Moreover, mountain, manuka, capillano and eco-honeys have exhibited inhibitory activity against H. pylori isolates at concentration 10% (v/v) [57] , demonstrating that locally produced honeys possess excellent antibacterial activity comparable to the commercial honeys. Therefore it is necessary to study other locally produced but yet untested honeys for their antimicrobial activities.

Conflict of interest statement: We declare that we have no conflict of interest.

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• Published: 08 February 2022

Honey authenticity: the opacity of analytical reports - part 1 defining the problem

• M. J. Walker   ORCID: orcid.org/0000-0002-4350-5549 1 ,
• S. Cowen 1 ,
• K. Gray 1 ,
• P. Hancock 1 &
• D. T. Burns 2  

npj Science of Food volume  6 , Article number:  11 ( 2022 ) Cite this article

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The composition of honey, a complex natural product, challenges analytical methods attempting to determine its authenticity particularly in the face of sophisticated adulteration. Of the advanced analytical techniques available, only isotope ratio mass spectrometry (IRMS) is generally accepted for its reproducibility and ability to detect certain added sugars, with nuclear magnetic resonance (NMR) and high-resolution mass spectrometry (HRMS) being subject to stakeholder differences of opinion. Herein, recent reviews of honey adulteration and the techniques to detect it are summarised in the light of which analytical reports are examined that underpinned a media article in late 2020 alleging foreign sugars in UK retailers’ own brand honeys. The requirement for multiple analytical techniques leads to complex reports from which it is difficult to draw an overarching and unequivocal authenticity opinion. Thus arose two questions. (1) Is it acceptable to report an adverse interpretation without exhibiting all the supporting data? (2) How may a valid overarching authenticity opinion be derived from a large partially conflicting dataset?

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Introduction

In November 2020, the Government Chemist, the UK statutory technical appellate function for food control 1 , was asked to provide an independent secondary expert opinion on the dataset of analytical results underpinning a UK media article. The story carried the headline “ Supermarket brands of honey are ‘bulked out with cheap sugar syrups made from rice and corn’ ” 2 ; similar media stories recur from time to time, e.g 3 , 4 , 5 , 6 , 7 , 8 . The dataset stemmed from the analyses of 13 own-brand honey samples of major UK retailers, commissioned by a South American bee-keeping organisation. The UK Foods Standards Agency, FSA, supplied three certificates of analysis (CoA), representative of the dataset 9 . Herein is presented the Government Chemist’s opinion.

A European Directive (‘EU Directive’) 10 defines honey as ‘the natural sweet substance produced by Apis mellifera bees from the nectar of plants or from secretions of living parts of plants or excretions of plant-sucking insects on the living parts of plants, which the bees collect, transform by combining with specific substances of their own, deposit, dehydrate, store and leave in honeycombs to ripen and mature’. The Codex Alimentarius definition 11 is similar, substituting ‘honey bees’ for the specific species as, worldwide honey may be collected from other honeybee species. The EU Directive was implemented in each of the then member states 12 . UK Ministerial policy responsibilities on honey are with the UK Department for Environment, Food & Rural Affairs 13 , 14 , while general food law enforcement policy is with the FSA 15 .

Nectar is composed primarily of water, sugars, such as fructose, glucose, and other oligo- and polysaccharides, and minor constituents, such as pollen, proteins, amino acids, aliphatic acid salts, lipids, and flavouring components. Bees process the collected material with enzymes, including diastase (amylase) and invertase (α-glucosidase). Thus, honey is primarily a concentrated aqueous solution of ‘invert’ sugar (the monosaccharides glucose and fructose) 16 and typically contains a wide range of saccharides, amino acids, proteins, organic acids, vitamins, minerals, enzymes, polyphenols and pollen. Some of these arise from honey maturation, others from the bees and some from the plants 17 . Honey composition depends on many factors including the botanical source, geographical origin, species of bee, year and season 18 . Codex and the EU Directive set certain compositional criteria. The EU Directive differentiates blossom honey (nectar honey in Codex) and honeydew honey, the latter from plant and insect secretions. Honeydew honey is also a concentrated aqueous solution of ‘invert’ sugar, albeit lower in fructose and glucose and typically darker than nectar honey; its chemical characteristics, such as pH, acidity, electric conductivity and other minor components including oligosaccharides are typically higher than in nectar honey 19 . Codex, the EU Directive, and national law stipulate various labelling options and requirements for honey in addition to general food labelling requirements to protect its authenticity 20 .

Data from the three CoA were grouped into (a) well-established traditional techniques, (b) well-established recent techniques (e.g. some forms of IRMS), and (c) other more recent techniques. CoA data were assessed in 5 categories: (1) those where a legislative limit applies, (2) non-legislative but generally agreed limits, (3) quality defect data, (4) authenticity data and (5) other general data.

Recent primary literature and review papers were identified by literature search (Google® Scholar, Scifinder, 28.01.2020, search terms honey, authenticity, review, and more specific terms as appropriate). All data generated or analysed during this study are included in this published article (and/or its supplementary information files).

Adulteration of honey and its detection

Anklam (1998) 17 reviewed honey authenticity methods finding no single parameter provided unequivocal information about botanical or geographical origins. Some potentially suitable methods were identified indicating a botanical origin from flavonoids, pollen, aroma and marker compounds, although deliberate addition of readily-available known markers and the loss of volatile markers on storage may vitiate detection. It was suggested profiles of oligosaccharides, amino acids and trace elements could be used to verify the claimed geographical origin. A combination of methods with statistical data evaluation was a promising approach. Anklam also noted carbon stable isotope ratio analysis can detect honey adulterated with C 4 sugars such as corn syrups or cane sugar (LoD 7%), particularly using the carbon isotope ratio of the honey protein fraction as an internal standard, but the addition of C 3 sugars such as beet could not be proved since nectar generally arises from C 3 plants. Of the 131 studies reviewed by Anklam, honey sample numbers tended to be small, generally below 30, with several up to 50 and only three between 90 and 100.

Types of adulteration

After Anklam 17 subsequent reviews, with variable coverage of the literature (Fig. 1 ) have expanded on types of adulteration (Fig. 2 ). The decline of bee populations has also been mentioned 21 as a driver.

Coverage of original papers by review papers considered herein, y -axis shows numbers of papers cited; clearly the reviews by Anklam, 17 Soares et al. 21 and Chin & Sowndhararajan 35 achieved more coverage that others.

Types of honey adulteration [Sources: Anklam 1998, 17 Soares et al., 2017, 21 European Commission 2018, 22 Ayton et al., 2019, 32 Se et al., 2019 34 and Chin & Sowndhararajan, 2020 35 ].

A European Commission expert stakeholder seminar of January 2018 confirmed ‘direct’ adulteration (addition of sugar/syrup) as the most frequent type of fraud. ‘Indirect’ adulteration is a term for deliberate inappropriate bee feeding with sugars when nectar is naturally available. Bee feeding is widespread and accepted when it is necessary in the absence of nectar and the expert stakeholder seminar recognised that if it does not stop when nectar becomes available it is more likely to be a malpractice rather than fraud. Adding pollen or other natural honey constituents, such as enzymes, to ultrafiltered honey and labelling it as a monofloral honey or the dilution of good quality honey with ultrafiltered honey were discussed. Synthetic resins are illegally used to remove unwanted substances (including antibiotics or pesticides) from honey, a potential health issue. Early removal of honey from the hive (immature honey) was also discussed and the Round Table report concluded “it was generally agreed that immature honey is not properly defined in legislation, and a guidance document is needed” 22 .

Views on immature honey particularly originating from certain parts of Asia are polarised. Many view systematic harvesting of immature honey followed by industrial moisture reduction as not complying with the Codex definition, since the honey is not matured by bees in the hive. 23 , 24 , 25 Others point to the nomadic lifestyle of Chinese beekeepers 26 , 27 , 28 and the high humidity of Asia necessitating periodic collection of immature honey for aggregation and moisture removal, to prevent fermentation. There are ongoing discussions on these issues 29 . Figure 2 illustrates the complexity of honey adulteration.

Analytical techniques for determining honey authenticity

Methods for the detection of honey adulteration have developed in a variety of ways. Zábrodská and Vorlová (2015) 30 considered inappropriate bee feeding difficult to detect, noting few successful studies e.g. using high-performance anion-exchange chromatography with pulsed amperometric detection, HPAEC-PAD with chemometrics, carbon isotope ratio mass spectrometry, IRMS, and gas chromatography-mass spectrometry, GC-MS. The latter identified markers such as fructosyl-fructose, although this marker has also been detected in honey from free-flying bees. One-dimensional and two-dimensional nuclear magnetic resonance spectroscopy, NMR, with multivariate analysis were regarded as effective (95.2% and 90.5% accuracy) in detecting bee feeding when applied to 63 samples of honey from various botanical sources and seven different sugar syrups marketed as specific bee-keeping products. Reviewing direct adulteration from a Czech perspective these authors 30 noted traditional analyses 31 and pollen analysis by microscopy (melissopalynology) are routinely applied. The latter is relatively time-consuming, although microscopy for the presence of starch grains may rapidly reveal crude addition of starch-derived syrups. Physicochemical investigations include analysis of phenolic and volatile compounds, protein, free amino acid content, colour, lactones, water activity, free fatty acids, sensory characteristics and antioxidant activity. Low honey prices in some countries with year-round production, very large broods and low labour costs are associated with honey quality indicators considerably different from those of traditional Czech honey but this may not necessarily mean lower quality. Fermentation which may occur when honey is harvested prematurely, may be obvious from the appearance or revealed by physicochemical and microbiological analyses. Pollen DNA by Polymerase Chain Reaction, PCR for botanical and geographical origins involves time-consuming and laborious DNA extraction, but one successful study was reported 30 .

Soares et al. (2017) 21 confirmed stable carbon IRMS as the most appropriate approach to detect C 4 sugar adulteration in honey and reviewed detection of C 3 sugar syrups noting chromatographic approaches for oligosaccharides and polysaccharide fingerprints and advances in spectroscopic techniques. Multi-elemental and trace analysis appeared to be the most promising approach to discriminate the geographical origin of honey. Again the need for use of at least two complementary techniques and large datasets from authentic samples was noted. These authors summarised Protected Designation of Origin (PDO) and Protected Geographical Indication (PGI) honeys registered with the European Commission as of 2017 and characteristic volatile compounds are described (2012 -2015) for different types of honeys. The presence of formic, oxalic and lactic acids in honey could be attributed to their use against the Varroa parasite as alternatives to synthetic acaricides. The effectiveness of nontargeted NMR, Raman spectroscopy and Infrared IR spectroscopy in combination with chemometrics was regarded as having been demonstrated, but more efforts were called for to validate and include them as official methods for honey authentication. Advances were reviewed in DNA analysis, including next-generation sequencing applied to botanical and entomological authentication of honey although it is inapplicable to filtered honeys 21 .

Negative media coverage in 2018 on the alleged presence of adulterated honey in Australian supermarkets prompted an Australian government review of the Australian honey industry 32 . The review discussed the strengths and weaknesses of analytical techniques with particular focus on elemental analysis IRMS, EA-IRMS, including the causes of unusual isotopic fractionation in Leptospermum honeys, NMR and other spectroscopic techniques (mid- and near-infrared (MIR, NIR) and Raman). The databases associated with NMR and other non-targeted spectroscopic approaches were assessed in some detail with concerns that, when used for Australian honey samples, “typical” ranges had been established with honeys from other countries, mainly in Europe and Asia not necessarily appropriate for Australian honey. The review made recommendations aimed at regaining consumer confidence in Australia honey. More recently, improvements in the protein precipitation procedure have been reported to eliminate the apparent failure of Australian honeys in EA-IRMS testing for C 4 sugars 33 .

Se et al. (2019) 34 reviewed honey adulterants and the advantages and disadvantages of 17 techniques including NMR and other spectroscopies, sensor-based methods, chromatography, and marker compounds. The EA-IRMS approach of AOAC Official Method 991.41 was reviewed noting that additional HPLC-IRMS and mean Δδ 13 C HPLC-IRMS data for individual sugars successfully detected C 3 sugar adulterants to a low level. Spectroscopic techniques with chemometrics are considerably more practical but also require correlation with traditional analytical methods and these authors recommend monitoring of honey quality via biosensor technology for the future 34 .

Chin and Sowndhararajan (2020) 35 gave a useful summary of authentication techniques and reported the number of samples and/or honey types analysed per technique by each study reviewed. Inspection of these data (graphed for ease of reference in Supplementary Fig. 1 ) confirms low numbers of samples in peer-reviewed published studies persists, other than perhaps in non-NMR spectroscopic studies. By contrast commercial NMR databases contain data on over 20,000 samples 32 .

A 2015/16 European-wide honey control exercise organised by the European Commission found a substantial proportion (about 20%) of the 2264 samples taken were non-compliant owing to indications by EA-LC-IRMS of foreign sugars. However of these a much lower proportion (about 5%) of the samples taken in the UK were non-compliant, owing to incorrect botanical source (4%) or presence of exogenous sugars (1%) 36 .

The above review papers and the report of the JRC ‘Round Table’ (European Commission 2018), 22 confirm analytical techniques to authenticate honey include the following.

Conventional physicochemical analysis, most of which is official and harmonised, and pollen analysis by microscopy.

Isotopic techniques, EA-IRMS and LC-IRMS.

Separation techniques, e.g. sugar profiling by LC or GC.

Spectrometric techniques, including LC-followed by high-resolution mass spectrometry (LC-HRMS), LC-MS/MS for marker detection and GC-MS for aroma profiling.

Spectroscopic techniques, including Fourier transform infrared (FTIR), NIR and NMR.

Trace elements profiling by inductively coupled plasma-mass spectrometry (ICP-MS).

Molecular biology, DNA barcoding and Next Generation Sequencing.

Statistical tools.

Other techniques such as the use of biosensors, electronic tongues and noses, and sensory analysis.

The UK Government Chemist convened a seminar on honey authenticity on 13 November 2019 on the determination of exogenous sugars by NMR. Fifty-seven stakeholders from across the UK honey supply chain, regulators (FSA, the Department for Environment, Food and Rural Affairs, Defra, and local authority enforcement), analytical service providers and expert scientific researchers attended. Whilst there was support for NMR as a diagnostic analytical tool, it was regarded by some as not yet suitable for the detection of exogenous sugars in honey for enforcement purposes, owing to lack of information on the databases underpinning interpretation of the method outputs. Others felt there was insufficient information on the results of inter-laboratory method comparisons and the scope of laboratory accreditation 37 . Suggestions made included continuing dialogue, training and guidance on the production and analysis of honey, and standardisation of the application and interpretation of NMR data for exogenous sugars in honey.

Assessment of supplied CoA data

As recommended in a number of review articles, complementary analytical approaches representing a range of analytical techniques were exhibited within the CoA provided. The methods were badged as ISO/IEC 17025 accredited, except for NMR which appeared to have been sub-contracted and for which no accreditation status was provided. Tables 1 – 4 summarise the data received, the opinions of the reporting laboratory and the present authors’ comments.

A summary page in each CoA provided overall opinions for 7 categories of results for each sample, 4 containing single parameters or a single technique and 3 containing two. For all but one of the 21 categories across the three CoA, the overall opinion was “noncompliant”, including for paired results one of which was “noncompliant” and the other “compliant”. In one instance a “compliant” opinion was given, although it was not possible to see why as the individual data did not differ appreciably from those in the other two CoA.

Table 1 exhibits the data for physicochemical parameters including major sugars for which legislative or commonly agreed limits exist. Each of the three samples, two described as ‘clear Honey’ and one as ‘set honey’ were apparently deficient in diastase activity. The provisions of the EU Directive require a product described as honey to exhibit a diastase activity of not less than 8 determined after processing and blending. There is a derogation for honey with a low natural enzyme content (e.g. citrus honey) to avail of which the hydroxymethylfurfural (HMF) content must be not more than 15 mg/kg. The samples were not described as citrus honey and contained more than 15 mg/kg HMF hence the diastase numbers for each were apparently deficient of the minimum required (However, time and storage conditions could have affected the results, see further commentary in Part 2 of this series (Honey authenticity: the opacity of analytical reports—part 2, forensic evaluative reporting as a potential solution). For one sample conflicting LC and NMR results were exhibited. Data for the amino acid proline were reported and while there are no legislative limits, a minimum threshold of 180 mg/kg proline has been proposed below which dilution with exogenous sugars might be suspected 38 . On that basis, samples 1 and 3 are compliant while sample 2 at ‘<150 mg/kg’ (i.e. less than the limit of detection of the method) is not. The reporting laboratory are tentative in their opinion flagging adulteration as “possible” for both samples 1 and 2 without citing a suggested limit and despite sample 1 containing more than 180 mg/kg proline.

Table 2 exhibits data related to fermentation based on glycerol concentrations. The results found are higher than literature data 39 and suggest incipient fermentation, for which harvesting of immature honey might be an explanation. Note however there is no supporting evidence from the ethanol 40 , 41 or 2,3-butandiol data, both of which arise from fermentation. Equally, no sensory properties (off-tastes), microbiology or microscopy for yeast cells have been reported.

Table 3 exhibits data relating to authenticity, some of which appear to show non-compliance. AOAC 998.12 ( 13 C IRMS) proved negative for C 4 sugars (cane sugar or corn syrups); the method has a LoD of 7% as C 4 sugars 42 and does not detect C 3 sugars. EA-LC-IRMS, capable of detecting C 3 sugar adulteration 34 , 43 , 44 was not carried out. HRMS screening was reported as positive for certain syrup markers which are untypical for honey. There was no disclosure of the identity of the markers and the reporting laboratory’s opinion appears tentative. NMR results were reported as positive for foreign sugars, but there was no disclosure of the identity of the foreign sugars. Ten individual sugars including mannose, a putative marker for syrups 45 and oligosaccharides, were reported without adverse comment. Caramel was reported as positive, a non-compliance possibly indicating the presence of added sugar syrup in all three CoA but no quantitative data were given. Psicose, an epimer of D-fructose rarely found in honey 46 was quantified in all three CoA.

Table 4 exhibits 35 data for each sample that did not excite any comment by the reporting laboratory and indeed are largely unremarkable.

On the face of it, to anyone lacking in-depth experience of honey analysis, the data in the CoA demonstrate non-compliance (for example apparent deficiency in diastase) or cast suspicion on the authenticity of the honey samples examined. This set of partially conflicting data reflects the tentative, and at times disputed, nature of much of the published work on honey authenticity, including reservations about the validity of databases. Moreover key data such as quantitative results, LoD and LoQ are in some instances missing and there is no reference to measurement uncertainty.

‘Untypical’ NMR profiles have reportedly been found in honeys derived from supply chains robustly audited as to their authenticity 32 , 37 giving rise to reservations that the NMR profiles in the databases do not take account of the full range of global honeys, nor adequately reflect other variables such as seasonality. To date, although UK industry-led work is in progress (see below), there is little published evidence examining, in the above context, the adequacy or otherwise of the databases. Divergent analytical results from HRMS, IRMS and NMR on the same samples have recently been described 47 . In a small (bee keeper-led) study 14 honey samples were sent to two different analytical service providers (‘ASP1’ and ‘ASP2’). By LC-HRMS, both ASP assessed 4 samples as possibly adulterated with sugar syrup. For a further 4 samples, LC-HRMS results differed between the ASP. EA-IRMS (presumed to be AOAC 991.41) in ASP1 failed to support the HRMS results for 4 samples, and NMR in ASP2 failed to support the HRMS results for 3 samples. No sample was returned as adulterated by all three techniques in both ASP 47 .

Conclusions

Challenges clearly remain for honey authentication and work is in progress to address these. Transparent validation of analytical methods for the determination of honey authentication, using quality assurance tools such as reference materials and proficiency testing schemes, are in development, although discrimination between industrially-dried immature honey and mature honey remains a difficult problem.

The JRC ‘Round Table’ 22 identified a need for internationally-agreed modern purity criteria for honey beyond the basic quality requirements of the current Codex and EU legislation. The ‘Round Table’ suggested a series of actions involving coordinated work from all stakeholders, including at an international level, the latter usually a lengthy process.

Progress has been made on the recommendations arising from the UK honey NMR seminar 37 , including training materials (which remain in development at the time of writing) and other aspects identified in a recent FSA publication 15 . Industry-led research is underway, including construction of a database of NMR spectra from samples relevant to the UK market. The work is said to include an investigation of NMR signals that with chemometrics differentiate honey by country of origin, and examination of changes in NMR spectra as a function of adulteration with sugar syrups 48 , 49 . Peer-reviewed publication of this industry-led work would add meaningfully to the collective ability to deal with the issues discussed herein.

Meanwhile polarised positions remain unresolved as illustrated in the press article 2 that prompted this study. There is consensus agreement that multiple approaches are needed to assess honey authenticity, leading inevitably to complex and data-rich certificates of analysis. These are difficult to interpret without further information and an in-depth knowledge of the techniques involved and hence are largely opaque to all but a small defined community of specialists. The summary opinion of the reporting laboratory in each of the CoA examined herein was unequivocally that the samples were noncompliant. However our critical examination of the CoA data reveals a much more nuanced picture from which it is currently difficult to draw a definitive opinion on the authenticity of the samples examined.

Many of the conventional, harmonised physicochemical methods underpinning limits in the EU Directive cannot identify sophisticated adulteration. Of the more advanced techniques, EA-LC-IRMS is well characterised and accepted with known and internationally validated performance characteristics, but there seems little immediate prospect of other reported analytical techniques becoming definitive and accepted.

Without further work and particularly further data disclosure the evidence in the examined CoA for adulteration, including with added sugars, is under-developed. This prompts two questions. (1) When reporting honey authentication data is it acceptable to give an interpretation, particularly an adverse one, without exhibiting all the supporting data? (2) How may a valid overarching opinion on authenticity be derived, from a large partially conflicting dataset? In Part 2 of this work we explore these questions and propose weighted, evidence-based appraisal of results of authenticity analyses by a forensic ‘evaluative reporting’ thought process.

Data availability

All data generated or analysed during this study are included in this published article (and/or its supplementary information files).

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Acknowledgements

The work described in this paper was funded in part (MW, SC, KG and PH) by the UK government Department for Business, Energy & Industrial Strategy (BEIS). MW is grateful to Queen’s University, Belfast for library facilities. Colleagues in FSA and Defra are thanked for helpful comments on the draft manuscript. The opinions herein represent the independent views of the UK Government Chemist Dr Julian Braybrook, to whom the authors are grateful for permission to publish this paper. Any view, information or advice given by LGC, the Laboratory of the Government Chemist, is formulated with care, but no responsibility can be taken for the use made of any view, information or advice given and should not be taken as an authoritative statement or interpretation of the law, as this is a matter for the courts.

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M.J.W. conceived the approach and experimental design, carried out the literature review, analysed the data and wrote the paper; S.C. analysed the data and contributed to the paper; K.G. analysed the data, verified accurate data transcription, was responsible for project administration and contributed to the paper; P.H. contributed to the paper; D.T.B. carried out the literature review, analysed the data and contributed to the paper. All authors have read and agreed the final version of the paper.

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Walker, M.J., Cowen, S., Gray, K. et al. Honey authenticity: the opacity of analytical reports - part 1 defining the problem. npj Sci Food 6 , 11 (2022). https://doi.org/10.1038/s41538-022-00126-6

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