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Do bioactive components in non-animal food sources contribute to the beneficial health effect of a Japanese dietary pattern?

Published online by Cambridge University Press:  21 June 2019

Allison M Hodge
Affiliation:
Cancer Epidemiology DivisionCancer Council VictoriaMelbourne, VIC 3004, Australia Email: allison.hodge@cancervic.org.au Centre for Epidemiology and BiostatisticsThe University of MelbourneMelbourne, Victoria, Australia
Mona S Calvo
Affiliation:
RetiredFormerly, Center for Food Safety and Applied NutritionUS Food and Drug AdministrationSilver Spring, MD, USA
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Abstract

Type
Invited Commentary
Copyright
© The Authors 2019 

In their article, ‘Dietary patterns and abnormal glucose tolerance in Japan’ in this issue of Public Health Nutrition, Okada et al.( Reference Okada, Takahashi and Nakamura 1 ) identified three dietary patterns using factor analysis of data from approximately 100 000 participants in the 2012 Japanese National Health and Nutrition Survey (NHNS) to explore associations with diabetes risk based on glycated Hb (HbA1c) cut-off values. Of three patterns identified, only the predominantly plant-based dietary pattern was significantly and inversely associated with diabetes risk, leading us to speculate that both the amount of specific foods consumed and their bioactive components may afford a protective mechanism against abnormal glucose tolerance. Two foods characterising this ‘vegetable pattern’ and which are widely consumed in Japan, namely soya/soya products and mushrooms, differ in both quantity of consumption and their bioactive components compared with the plant foods predominant in Western cultures. The objective of our commentary is to delve deeper into these differences and speculate on possible mechanisms through which these foods may reduce disease risk.

Three dietary patterns were found: (i) ‘high-bread and low-rice’, (ii) ‘high-meat and low-fish’ and (iii) ‘vegetable’. The first pattern, on which bread, milk/dairy products, confectionery, butter/margarine and fruit were positively loaded, and animal meats/poultry and rice were negatively loaded, was weakly inversely associated with elevated HbA1c. The ‘vegetable’ pattern, with positive loadings for vegetables, fruit, mushrooms, soyabeans/soya products, was significantly inversely associated with elevated HbA1c. No association was seen for the second pattern( Reference Okada, Takahashi and Nakamura 1 ).

It is perhaps no surprise that the first pattern did not show a strong association with HbA1c given that foods loading on this factor included some that would be considered beneficial, such as positive loadings for fruit and negative loadings for meat and poultry; but other items like confectionery with a positive loading would be expected to be associated with a greater risk of elevated HbA1c or diabetes( Reference Schwingshackl, Hoffmann and Lampousi 2 ). The strong negative loading for rice and the similar strength positive loading for bread are difficult to interpret without more detail of the main foods consumed within these groups. White rice is low in nutrients, including fibre, and can have a low glycaemic index( Reference Atkinson, Foster-Powell and Brand-Miller 3 ), which might also contribute to diabetes risk( Reference Hodge, English and O’Dea 4 ). However, even within white rice Atkinson et al. report a wide range of glycaemic indices ranging from below 50 for some types to above 100 for others( Reference Atkinson, Foster-Powell and Brand-Miller 3 ). Bread similarly is reported to have a range of glycaemic indices, both within and between different types of grains( Reference Atkinson, Foster-Powell and Brand-Miller 3 ).

The second pattern, with positive loadings for bread, noodles, animal meats/poultry, butter/margarine, vegetable fats/oils and coffee/cocoa, and inverse associations for rice, pickles, raw fish/shellfish and tea, is similar to other ‘unhealthy’ dietary patterns that have been associated with increased diabetes risk( Reference Jannasch, Kroger and Schulze 5 ).

The ‘vegetable’ pattern loads all plant-based foods and mushrooms, and in that respect is similar to other ‘healthy’ patterns that have been inversely associated with diabetes risk( Reference Jannasch, Kroger and Schulze 5 ). Although we recognise that mushrooms are fungi and in fact part of a separate kingdom to plants, we refer to them with plant foods here. Due to differences in the sort of foods consumed in Japan compared with Western countries, the actual components of this ‘vegetable’ pattern may be quite different, in particular the focus on soyabean-derived foods and mushrooms. The positive effects of the ‘vegetable’ dietary pattern in Japan may relate specifically to the component foods that are consumed at significantly higher levels than in Western cultures.

Soya products are more common in Japanese than Western diets. According to the most recently available FAO data, the soya food supply in Japan for 2013 was about 20 g/capita per d which was the third highest consumption after China and Korea. For Australia, the equivalent figure was 0·53 g/capita per d and for the USA, 0·11 g/capita per d( 6 ). A recent systematic review and meta-analysis of soya intake and diabetes risk identified weak evidence for an inverse association, but results were heterogeneous, possibly because of the different soya products evaluated and differences between study populations. Subgroup analysis showed that in women, Asian populations and cross-sectional rather than longitudinal studies, there were consistent inverse associations( Reference Li, Ruan and Peng 7 ). The significantly higher soya intakes in Asian populations may contribute to the finding of beneficial associations.

The 2015 Japanese NHNS report, cited by Shimizu et al.( Reference Shimizu, Mori and Ouchi 8 ), indicated that in Japan the average intake of mushrooms was 15 g/d, including a number of different species rich in a range of nutrients, including B vitamins, vitamin D, fibre and folic acid, and with some reported antidiabetic actions( Reference Shimizu, Mori and Ouchi 8 ). Flammulina velutipes, Hypsizygus marmoreus, Lentinus edodes, Grifola frondosa and Pleurotus eryngii are the top five mushroom varieties grown and consumed in Japan( Reference Shimizu, Mori and Ouchi 8 ). Data presented by Freidman( Reference Friedman 9 ) show the variation in nutrient contents (protein, fat, ash, dietary fibre and sugar) between the last three of these and Agaricus bisporus, which is the common white button, brown crimini or Portobello mushroom consumed in Western cultures. In comparison, statistics from the USA show that between 2009 and 2017 annual mushroom intake per capita increased from 1·6 to 1·8 kg (equivalent to 4·4 to 4·9 g/d), and 61 % were white mushrooms( 10 ). Mean mushroom intake for Australia in the 2011–12 nutrition component of the Australian Health Survey was 10·7 g/d( 11 ). Although there are no readily accessible data on consumption of different mushroom types in Australia, personal observation in shops suggests that most are the common A. bisporus. In a review looking at dietary patterns and diabetes risk, Schwingshackl et al.( Reference Schwingshackl, Hoffmann and Lampousi 2 ) noted that inverse associations between ‘vegetables’ and diabetes risk were observed only in Australian and Asian studies, which may reflect to some extent the different combinations of vegetables consumed.

The Japanese clearly consume more soya and soya products, as well as mushrooms compared with Europeans or North and South Americans. The health benefits of soya and soya products are well established with respect to chronic disease( Reference Li, Ruan and Peng 7 , Reference Gilbert and Liu 12 ), while much less is known about the human health effects of mushroom consumption. In a cross-sectional population study in elderly Japanese, high mushroom consumption was associated with lower prevalence of dementia and impaired cognitive function( Reference Zhang, Tomata and Sugiyama 13 ). An important factor to consider in the Japanese ‘vegetable’ diet pattern is that two of the dominant foods contain high levels of bioactive compounds that have been linked to mechanisms that may protect against chronic diseases such as diabetes and impaired cognitive function leading to dementia.

Both soya and mushrooms are rich in polyphenolic compounds and other bioactive components not found in other non-animal foods, for example ergocalciferol (vitamin D2) in light-exposed mushrooms, which has been shown to be a potent modulator of inflammation in immune-challenged rats( Reference Babu, Balan and Garthoff 14 ). The Japanese have long been recognised for their higher natural intake of vitamin D, with the contribution from mushrooms second only to fish( Reference Calvo, Whiting and Barton 15 ). Vitamin D is a critical nutrient in the prevention of inflammation, as well as having an important role in calcium and phosphorus homeostasis. Both soya and mushrooms are rich sources of antioxidants, but one potent antioxidant in mushrooms, ergothioneine, is not found in significant quantities in other plant or animal sources and is not synthesised by human or other animal species( Reference Kalaras, Calcagnotto and Beelman 16 ). In fact, ergocalciferol and ergothioneine are bioactive components unique to mushrooms( Reference Kalaras, Beelman and Elias 17 ) and their content varies with the type of mushroom, with the varieties consumed in Japan having higher levels of both relative to A. bisporus ( Reference Beelman, Kalaras and Richie 18 ). Retrospective analysis of findings from a 16-week mushroom feeding study in older individuals with metabolic syndrome (pre-diabetes) showed that even A. bisporus consumption at the level of 100 g of fresh mushrooms per day was associated with significant increases from baseline in the anti-inflammatory hormone, adiponectin, and decreases in the oxidative stress-inducing advanced glycation end products, carboxymethylysine and methylglyoxal, which like HbA1c are elevated in diabetes( Reference Calvo, Mehrotra and Beelman 19 ). Ergothioneine is proposed by some researchers to be a potent adaptive antioxidant that functions in the protection of injured tissues( Reference Halliwell, Cheah and Drum 20 ).

Chronic inflammation and oxidative stress are now widely considered to be the underlying mechanisms of most chronic diseases including diabetes( Reference Mendes, Cruz and Gualillo 21 ). Higher consumption of soya and soya products and consumption of a variety of mushrooms with high levels of ergocalciferol and ergothioneine theoretically provide the Japanese with the anti-inflammatory vitamins and potent antioxidants needed to reduce the risk of chronic diseases.

Notwithstanding these potentially interesting findings and their implications, Okada et al.’s study has some important limitations as outlined by the authors; in particular, the dietary data based on a single day and evaluated at the household level is likely to have significant error. The authors adjusted the multivariate models for diet patterns and elevated HbA1c for BMI, but did not show causal diagrams to clarify whether they considered BMI as a confounder or potentially a mechanism linking diet and diabetes. If the latter, it should not have been adjusted for. Given that it is never clear which is the correct causal pathway, it may have been useful to perform the analysis with and without BMI or other body size measure and explain clearly why this had been done.

The new Japanese study supports previous work indicating that healthy, predominantly plant-based dietary patterns may help to reduce diabetes risk and provides insight for hypothesising possible mechanisms of action. This is timely with the recent release of the EAT–Lancet commission report( Reference Willett, Rockstrom and Loken 22 ) calling for a move away from high consumption of meat, for both health and sustainability reasons. More studies specifically examining the possible benefits of soya products and mushrooms, including variety of species, on glucose metabolism should be conducted to confirm these potential associations.

Acknowledgements

Financial support: This research received no specific grant from any funding agency in the public, commercial or not-for-profit sectors. Conflict of interest: There are no conflicts of interest. Authorship: M.S.C. came up with the idea to write a commentary and the focus on mushrooms, A.M.H. wrote the first draft, and the both finalised the manuscript. Ethics of human subject participation: Not applicable.

Author ORCID

Allison M Hodge, 0000-0001-5464-2197.

References

Okada, E, Takahashi, K, Nakamura, K et al. (2019) Dietary patterns and impaired abnormal glucose tolerance among Japanese: findings from the National Health and Nutrition Survey, 2012. Public Health Nutr. Published online: 6 March 2019. doi: 10.1017/S1368980019000120.CrossRefGoogle Scholar
Schwingshackl, L, Hoffmann, G, Lampousi, AM et al. (2017) Food groups and risk of type 2 diabetes mellitus: a systematic review and meta-analysis of prospective studies. Eur J Epidemiol 32, 363375.CrossRefGoogle ScholarPubMed
Atkinson, FS, Foster-Powell, K & Brand-Miller, JC (2008) International tables of glycemic index and glycemic load values: 2008. Diabetes Care 31, 22812283.CrossRefGoogle ScholarPubMed
Hodge, AM, English, DR, O’Dea, K et al. (2004) Glycemic index and dietary fiber and the risk of type 2 diabetes. Diabetes Care 27, 27012706.CrossRefGoogle ScholarPubMed
Jannasch, F, Kroger, J & Schulze, MB (2017) Dietary patterns and type 2 diabetes: a systematic literature review and meta-analysis of prospective studies. J Nutr 147, 11741182.CrossRefGoogle ScholarPubMed
Food and Agriculture Organization of the United Nations (2018) FAOSTAT | Food supply – crops primary equivalent. http://www.fao.org/faostat/en/#data/CC (accessed February 2019).Google Scholar
Li, W, Ruan, W, Peng, Y et al. (2018) Soy and the risk of type 2 diabetes mellitus: a systematic review and meta-analysis of observational studies. Diabetes Res Clin Pract 137, 190199.CrossRefGoogle ScholarPubMed
Shimizu, T, Mori, K, Ouchi, K et al. (2018) Effects of dietary intake of Japanese mushrooms on visceral fat accumulation and gut microbiota in mice. Nutrients 10, E610.CrossRefGoogle ScholarPubMed
Friedman, M (2016) Mushroom polysaccharides: chemistry and antiobesity, antidiabetes, anticancer, and antibiotic properties in cells, rodents, and humans. Foods 5, E80.CrossRefGoogle ScholarPubMed
Statista (2019) Per capita consumption of fresh mushrooms in the United States from 2009 to 2017 (in pounds). https://www.statista.com/statistics/257314/per-capita-consumption-of-fresh-mushrooms-in-the-us/ (accessed February 2019).Google Scholar
Australian Bureau of Statistics (2014) 4364.0.55.007 – Australian Health Survey: Nutrition First Results – Food and Nutrients, 2011–12. Canberra: Commonwealth of Australia.Google Scholar
Gilbert, ER & Liu, D (2013) Anti-diabetic functions of soy isoflavone genistein: mechanisms underlying its effects on pancreatic beta-cell function. Food Funct 4, 200212.CrossRefGoogle ScholarPubMed
Zhang, S, Tomata, Y, Sugiyama, K et al. (2017) Mushroom consumption and incident dementia in elderly Japanese: the Ohsaki cohort 2006 study. J Am Geriatr Soc 65, 14621469.CrossRefGoogle ScholarPubMed
Babu, US, Balan, KV, Garthoff, LH et al. (2014) Vitamin D2 from UVB light exposed mushrooms modulates immune response to LPS in rats. Mol Nutr Food Res 58, 318328.CrossRefGoogle ScholarPubMed
Calvo, MS, Whiting, SJ & Barton, CN (2005) Vitamin D intake: a global perspective of current status. J Nutr 135, 310316.CrossRefGoogle ScholarPubMed
Kalaras, MD RJ, Calcagnotto, A & Beelman, RB (2017) Mushrooms: a rich source of antioxidants ergothioneine and glutathione. Food Chem 233, 429433.CrossRefGoogle ScholarPubMed
Kalaras, MD, Beelman, RB & Elias, RJ (2012) Effects of post-harvest pulsed UV light treatment of white button mushrooms (Agaricus bisporus) on vitamin D2 content and quality attributed. J Agric Food Chem 60, 220225.CrossRefGoogle Scholar
Beelman, R, Kalaras, MD & Richie, JP (2019) Micronutrients and bioactive compounds in mushrooms: a recipe for healthy aging? Nutr Today 54, 1622.CrossRefGoogle Scholar
Calvo, MS, Mehrotra, A, Beelman, RB et al. (2016) A retrospective study in adults with metabolic syndrome: diabetic risk factor response to daily consumption of Agaricus bisporus (white button mushrooms). Plant Foods Hum Nutr 71, 245251.CrossRefGoogle Scholar
Halliwell, B, Cheah, IK & Drum, CL (2016) Ergothioneine, an adaptive antioxidant for the protection of injured tissues? A hypothesis. Biochem Biophys Res Commun 470, 245250.CrossRefGoogle ScholarPubMed
Mendes, AF, Cruz, MT & Gualillo, O (2018) Editorial: the physiology of inflammation – the final common pathway to disease. Front Physiol 9, 1741.CrossRefGoogle ScholarPubMed
Willett, W, Rockstrom, J, Loken, B et al. (2019) Food in the Anthropocene: the EAT–Lancet Commission on healthy diets from sustainable food systems. Lancet 393, 447492.CrossRefGoogle ScholarPubMed