Part 12. Honey, Propolis, Fungi and Mushrooms, Uncommon Allies in Dental Healthcare and Humanity? A Reflective Personal and Professional Journey.

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I can remember the moment that I discovered the beautiful truth of mushrooms. Upon a mound of grassed earth, about 5 metres square was a huge ancient oak tree, perched next to a minor road that led from the railway station to the leafy suburbs of the rich and well-healed. This was a relatively innocent spot when every late-Spring to mid-Autumn when the environmental conditions lend themselves, the fruiting bodies of the Boletus Edulis mushroom appeared. This they do with grateful regularity, along with other less gastronomic varieties, being ignored by all and sundry, ignorant of the identity these fungi fruiting bodies, and the free gift from nature herself. Dear friends of ours, David and Rachel, had the same epiphany, but of the honey bee kind. They have found common purpose, collaboration, well-being, and began to care bees and their production of honey. They had both found peace and greater common interest, teaching and motivating others to the cause. Bees, however, are in crisis and for many reasons.

“Bees do have a smell, you know, and if they don’t they should, for their feet are dusted with spices from a million flowers”. Ray Bradbury

The Woodland Trust, a tree planting, and ancient woodland protecting UK organisation, is acutely aware of the necessity of the bee. They state “bees have been around for millions of years, pollinating our plants and producing the sweet, golden syrup we call honey.” The trees and woods are essential to filter our air but bees are vital for pollinating about a third of our food and 80 percent of the trees and flowers of our wildlife habitat.

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New Zealand has 28 native species of bees and 13 introduced species. As the native bees don’t make honey non-native species do the job in their absence collecting pollen from 224 native plant species. Despite this obvious benefit, the native bees are under threat by the honey-producing bees as they take their food sources, possibly threatening indigenous biodiversity.

However, bees are globally declining in numbers due to many threats, and saving them goes hand in hand with saving the trees and ancient woodlands. Habitat loss, caused by urban development, intensive farming methods alongside pesticides are the greatest threats to them. Climate changes, altering seasonal timings affect the flowering calendar, and extremes of weather contribute too, disrupted bee nesting behaviour. Parasites and diseases are another big threat, the Varroa mite clings to the back of the honey bee, passing diseases and viruses to it, thus draining its strength. These and other invasive species cause havoc to native species.

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The recently released documentary film Fantastic Fungi, a “time-lapse journey into the mysterious and magical world”, details the power of fungi to heal, sustain and contribute to the regeneration of life on Earth beginning some 1.5 billion years ago. Fungi feature actively in foods as diverse as beer, wine, and cheese. Fungi is neither animal or vegetable, there are over 1.5 million species, 6 times more than plants. They can break down complex organic matter and are responsible for the generation of soil. Fungi extend in vast networks that span hundreds of miles underfoot. They use electrolytes and electric pulses to communicate through mycelial networks, vaster than our own brain neural networks. Trees use these incredibly complex natural communication pathways recognising, protecting, and nurturing their own kind and kin. My hero, Paul Stamets, a mycologist with a mission, has an uncanny knack and passion powered presence regarding all things fungal. Hearing his podcasts with famous talking head Joe Rogan has three dimensionalised my mushroom learning journey. Initially, I was emotionally recruited into being mycophile because of its alternative and historical context. I liked the notion that critical knowledge could surpass that of the power of danger, but Paul’s pervading and persuasive sermons bring cruciality to the messages that a variety of medicines, conventional and alternative, can be created from fungi to ultimately saving the plant and humans by saving the bees.

“A day without a friend is like a pot without a single drop of honey left inside.” Winnie the Pooh

Honey is composed of many things, primary Fructose (38%) then Glucose (31%) followed by water (17%). Other components include minerals, amino acids, proteins, and acids. Sugar composes about 95% of honey dry weight. The acidity and pH of honey are lesser than the balanced level of 7, blossom honey is lower ranging between 3.3 to 4.6. Honeydew honey, due to its higher mineral content, has a higher pH value varying between 4.5 to 6.5. Honey, having a very concentrated sugar solution has a high osmotic pressure which makes it impossible for the growth of any microorganisms.

The oldest civilisation known, the Sumerians, from Mesopotamia, historically renowned for their innovations in language, governance, and architecture were also well acquainted with bee-keeping and honey. They worshipped a honey bee goddess and fashioned pottery, was making special jars for honey. There are biblical references to honey and are mentioned in scrolls from the Talmud and the Koran. The Egyptians and the Romans applied honey to wounds, and English Kings and Queens fermented it into drinkable mead.

Honey has both therapeutic and pharmacological properties, osmolarity, acidity, hydrogen peroxide system (inhibin), phytochemicals, and methylglyoxal. All have healing properties as expectorants, anti-cough, anti-constipation, liver detoxification, and alleviating digestive disorders like peptic ulcers. Honey is also considered both a probiotic and prebiotic and can be classed, as a result as a symbiotic, being contained in one product.

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Honey and its associated products have been also researched in the oral health context. Ahuja and Ahuja (2006) examined Apitherapy, specifically looking at the inhibitory effects on bacteria including aerobic and anaerobic gram-positive and gram-negative flora, the significant antimicrobial, antiviral and antifungal properties of flavonoids, and phenolic acids. Honey, having a high fructose and glucose content, would be expected to be very cariogenic, additionally presenting a lower pH too. Various studies (George et al 1978, Shumon et al 1979 and Nizel 1973) have determined it to be equal, or worse (Kong 1967) than sucrose, with one, by Decaix, (1976) surprising finding it less so! The diversity of outcomes demonstrates a degree of confusion, perhaps detailed observations of the differing methodologies, funding, and biases of the research, and researchers might add clarity. It may also be that selected honey having higher antibacterial activity and better-balanced pH, like honeydew, are less harmful to teeth by inhibiting cariogenic bacteria. Further research, if deemed necessary, may reveal more beneficial evidence.

Propolis, a resinous (55-60%), lipophilic material is waxy (30-45%), sticky, yellow-brown to dark brown, with aromatic oil and pollen (5-10%). It is collected from tree buds, sap flows, shrubs, or other botanical sources is used to protect and seal unwanted open spaces in the hive. Propolis is rich in chemicals like flavonoids, phenolics, and aromatic compounds being antioxidant and anti-inflammatory to name but a few. The main benefits come from two propolis products, the first is the Ethanolic Extract of Propolis (EEP). It is a rich source of phenolic acids and flavonoids. EEP and its phenolic compounds have been known for various biological activities including immunopotentiation, chemo preventive, and antitumor effects. It is highly effective against strains of Bacteroides and Pepto streptococcus.

Secondly, Propolis contains Caffeic Acid Phenethyl Ester (CAPE), a versatile therapeutically active polyphenol, and an effective adjuvant of chemotherapy for enhancing therapeutic efficacy and diminishing chemotherapy-induced toxicities. It is acquired from propolis obtained through extraction from honeybee hives. This bioactive compound displays anti-inflammatory and anti-oxidative properties, enhancing the production of cytokines IL4 and IL10 and decreasing the infiltration of monocytes and neutrophils.

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Propolis has been shown to inhibit cariogenic microorganisms, slow down the synthesis of insoluble glucans, and inhibit glucosyltransferase enzymes, essential for Streptococcus mutans to become sticky and adherent. Cariostatic effect of propolis is assisted by its fatty acids, slowing down the production of acids by Streptococcus mutans, and decrease the tolerance of microorganisms to acid pH. Also, A study assessed, in vitro, antibacterial effect of Iranian propolis on oral microorganisms concluded that ethanol extract of propolis is effective in the control of oral biofilms and dental caries development.

“Mushrooms were the roses in the garden of that unseen world because the real mushroom plant was underground. The parts you could see – what most people called a mushroom – was just a brief apparition. A cloud flower.” Margaret Atwood, The Year of the Flood

A large variety of mushrooms have been utilised traditionally in many cultures for health purposes, prevention, and treatment of diseases. Over 100 medical functions have been found in mushrooms and fungi. They range from antioxidant, anticancer, antiparasitic, antifungal, detoxification and hepatoprotective. The bioactive properties are found in fruiting bodies, cultured mycelium, and broths which contain polysaccharides (most important in modern medicines), proteins, fats, minerals, phenolics, flavonoids, carotenoids, folates, lectins, and enzymes. Beta-glucan is the next most versatile metabolite from the mushroom kingdom. It has a wide spectrum of biological activity, related to the immune system, especially regarding antitumor benefits.

A critical review on health-promoting benefits of edible mushrooms was undertaken by Jayachandran et al in 2017. They looked into the role of mushrooms as prebiotics in improving the host’s health. They have substances that induce the growth of or the action of microorganisms that contribute to the host’s well-being. Importantly they play a vital role in immune regulating pneumococcal pneumonia and antitumor activities. In particular button mushrooms increase microbial diversity in gut flora. Other mushroom types have been reported to reduce obesity, gut dysbiosis, improve antioxidant status via microbial alterations.

Specific cultivated and wild mushroom species have been researched for their potential application in human health. The Shiitake mushroom, Lentinula edodes, cultivated since the Sung dynasty in 1100 AD, is one of the most popular mushrooms worldwide, prized for their rich, savoury taste. It has a variety of biologically active compounds like erythritol. It is suggested Shiitake possess anti-oxidative and anti-atherosclerotic potential, with regular consumption improving human immunity. A study was undertaken in 2015 (Dai et al) looking at 52 subjects between the ages of 21 – 41 consuming 5g -10g daily. Their blood pictures after 4 weeks revealed reductions in C reactive protein (CRP) and an increase in IgA immune function activity. The cytokine pattern also differed before and after indicating immune improvement also, demonstrating less inflammation than that which existed before. A culinary favourite, the Cep or Penny Bun (Boletus edulis) has a polysaccharide profile, tested in laboratory mice, that demonstrated reduced pro-inflammatory and increased anti-inflammatory responses.

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Erythritol is responsible for anti-microbial activity in dental health, being seen to detach cariogenic bacteria from tooth structure, altering the cell surface hydrophobicity, and disrupting signals transmitted in Streptococcus mutans. Studies into Shiitake extract mouthwash was compared to a chlorhexidine rinse in an artificial mouth model. Eight key taxa of the oral health community were investigated over time. The results indicated the Shiitake extract lowered pathogenic bacterial numbers without affecting the taxa associated with health, whereas the commercial rinse affected all.

The symbiotic healing relationship between bees and fungi is becoming more understood. Fungi have an important role as providers of powerful medicine in fighting honey bee viruses. There have been waves of highly infectious viruses contributing to a massive decline in honey bee health. However, it has been recently noted that bees forage on mushroom mycelium. This suggests that they may be deriving medicinal as well as nutritional value from fungi. The wide range of chemicals that mushrooms possess include some that may benefit, antimicrobially, honey bees. They are particularly affected by two viruses, Lake Sinai Virus (LSV) and Deformed Wing Virus (DWV). Research undertaken by Stamets et al (2018), determined that extracts of Omadou and Reishi mushrooms reduced DWV 79 fold and LSV 45,000 fold compared to control colonies and they, understatedly, may gain health benefits from fungi and their antimicrobial contents. Besides the continuing work of Stamets and co-workers beyond fungi, where they are disseminating three-dimensional printing diagrams for the greater public to produce bee feeder platforms. These are simple measures we can all immediately do to meaningful help in real-time. This includes filling your garden with bee-friendly flowers, stopping the use of pesticides, and using 1 tablespoon of water with 2 tablespoons of white granulated sugar to make an energy drink, placing it nearby busy bees.

To conclude I am pleased that a passion project of mine, mycology, can be researched in my clinical field, albeit unorthodox but very relevant in my social context. I am aware that honey, propolis, and fungi will probably never see the mainstream light of day in my practice but will be able to engage, with knowledge, clients who are interested or associated with them. I am more the wiser and sympathetic towards those who have tried through research to bring their benefits to the fore, their work is worthy of examination. Furthermore the future of the human race is aligned with the future of bees and the environment. Greater attention to them and their habitat, be they fungi or bees should be invested in. It is time for man to provide more action and resources to protect them and understand our mutual environmental and sustainable needs.

Resources

A critical review of health-promoting benefits of edible mushrooms through gut microbiota Jayachandran et al, 2017. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5618583/

Propolis in Dentistry and Oral Cancer Management. Kumar, 2014. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4083525/

Propolis: A natural biomaterial for dental and oral healthcare. Khurshid et al, 2017. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5768961/

Extracts of polypore mushroom mycelia reduces viruses in honey bees. Stamets et al, 2018. https://www.nature.com/articles/s41598-018-32194-8

In vitro assessment of Shiitake mushroom (Lentinula edodes) Extract for its anti-gingivitis activity. Ciric et al, 2011. https://www.hindawi.com/journals/bmri/2011/507908/

Apitherapy – A sweet approach to dental diseases – Part I : Honey. Ahuja & Ahuja https://static.webshopapp.com/shops/035143/files/056059908/2012-a-sweet-approach-to-dental-diseases-part-i-ho.pdf

Apitherapy – A sweet approach to dental diseases. Part II: Propolis. Ahuja & Ahuja, https://journals.sagepub.com/doi/pdf/10.1177/2229411220110201
Does Propolis Help to Maintain Oral Health? Włodzimierz et al, 2013. https://www.hindawi.com/journals/ecam/2013/351062/

Health from the Hive: Potential Uses of Propolis in General Health. Eshwar, Shruthi, & Suma, 2012. https://www.scirp.org/html/1-2100265_19381.htm

Propolis: A natural biomaterial for dental and oral healthcare. Khurshid et al, 2017.
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5768961/

Effectiveness of Propolis on Oral Health: A Meta-Analysis. Hwu et al, 2014.
https://journals.lww.com/jnrtwna/fulltext/2014/12000/Effectiveness_of_Propolis_on_Oral_Health__A.3.aspx
Honey for Nutrition and Health: A Review. Bogdanov et al, 2008.
https://www.tandfonline.com/doi/full/10.1080/07315724.2008.10719745?casa_token=ZYitv9nW1OcAAAAA%3A9gwW1hMAieQCF4W0RyzPZh-ZA7wyql9koKB9op9EvblPoMIEHxOwiz4Qo8yWYjHrHp_5oK6XPg2A7g

Novel Insights into the Health Importance of Natural Honey. Ajibola, 2015.
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5295738/

Anti-inflammatory effects of Boletus edulis polysaccharide on asthma pathology. Wu et al, 2016. https://www.ncbi.nlm.nih.gov/pubmed/27830033

Edible Mushrooms: Improving Human Health and Promoting Quality Life. Valverde, 2014. https://www.hindawi.com/journals/ijmicro/2015/376387/

Lentinula edodes (shiitake mushroom): An assessment of in vitro anti-atherosclerotic bio-functionality. Rahman et al, 2018.
https://www.sciencedirect.com/science/article/pii/S1319562X16000231#!

Consuming Lentinula edodes (Shiitake) Mushrooms Daily Improves Human Immunity: A Randomized Dietary Intervention in Healthy Young Adults. Dai et al, 2014.
https://www.tandfonline.com/doi/full/10.1080/07315724.2014.950391?casa_token=IV08HJ-q8JAAAAAA%3AkI7_6o8u7KKK57edgEtxJo7gsSHLq_ZcPXge3ldFI15tsBV-3X4IcjVM6yv1a1OJFgrkDr4EIbLcig

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