How Much Bean Hemagglutinin Is Safe for Human ... - ACS Publications

Jun 26, 2018 - Department of Food Science, College of Agriculture and Life Sciences, Cornell University , Ithaca , New York 14853 , United States. J. ...
1 downloads 0 Views 737KB Size
Viewpoint Cite This: J. Agric. Food Chem. XXXX, XXX, XXX−XXX

pubs.acs.org/JAFC

How Much Bean Hemagglutinin Is Safe for Human Consumption? Zhong Zhang and Alireza Abbaspourrad* Department of Food Science, College of Agriculture and Life Sciences, Cornell University, Ithaca, New York 14853, United States

Downloaded via UNIV OF CALIFORNIA SANTA BARBARA on June 28, 2018 at 15:41:21 (UTC). See https://pubs.acs.org/sharingguidelines for options on how to legitimately share published articles.

S Supporting Information *

time and hemagglutinin testing). The sufficiency of such quality control measures is unknown because currently there are no clear regulations for the food industry to follow. Because the demand for plant-based protein has surged in recent years, bean proteins have been made commercially available as food ingredients and dietary supplements for human consumption, such as mung bean (e.g., Hampton Creek mung bean protein isolate), fava bean (e.g., Ingredion fava bean concentrate), kidney beans (e.g., Federal Ingredients red kidney protein powder), etc. During the protein production process, bean hemagglutinins will be unavoidably co-extracted.6,8,9,18 Do ingredient manufacturers have to implement a process to denature hemagglutinins in bean proteins? What is the safe concentration of hemagglutinins for humans to consume? To answer the questions, we investigated the hemagglutinin levels in canned beans commercially available in the U.S. markets. Such canned beans are widely distributed and regularly consumed across the country; it is reasonable to speculate that the level of hemagglutinins in these canned beans are generally recognized as safe for human consumption.



INTRODUCTION Hemagglutinins, also known as lectins, are a storage protein found in leguminous seeds, such as beans.1−5 The first pure hemagglutinin was isolated from jack beans (Canavalia ensiformis) in 1919.5 It was later determined that hemagglutinins in beans can agglutinate cells, such as erythrocytes, and also precipitate glycogen from solution through their carbohydrate recognition and binding sites.6−9 Hemagglutinins can also bind with the intestinal epithelium and disrupt the intestinal brush border, leading to abdominal discomfort and an irritated gastrointestinal tract.10,11 Ingestion of raw and improperly handled beans can lead to lectin poisoning, associated with vomiting and diarrhea within 1−7 h of ingestion. Many incidents of hemagglutinin poisoning have been reported for white and red kidney beans.12 Hemagglutinins in beans are resistant to digestive enzymes in the gastrointestinal tract and can sustain medium heat treatment.13,14 High heat treatment, such as pressure cooking and boiling, can destroy hemagglutinins in legumes in a short time. However, the lower temperatures used in slow cookers might not be efficient for denaturing hemagglutinins.15 It was reported that the hemagglutinin activity in kidney beans cooked at 80 °C for 45 min increased about 5-fold compared to raw beans.16 The U.S. Food and Drug Administration (FDA) has suggested that the beans should be boiled for at least 30 min to ensure that the product reaches a sufficient temperature for a sufficient amount of time to completely destroy hemagglutinin.17 However, the FDA has not recommended the maximum allowed level of hemagglutinins in bean products. The bean product companies usually have their own quality control measures (i.e., heating temperature/ © XXXX American Chemical Society



REVELATION FROM COMMERCIALLY AVAILABLE CANNED BEANS AND SAFETY CONSIDERATIONS FOR PROTEINS EXTRACTED FROM BEANS Table 1 shows the hemagglutination units (hau) of five species of canned beans, including black bean, red kidney bean, dark red kidney bean, white kidney bean, and great northern bean from four different brands (Goya, Bush’s, Market Pantry, and Simply Balanced). These beans were selected for the study because they are known for their high levels of hemagglutinins in raw beans. We also tested two lots for each sample to minimize the variations between lots. A total of 22 canned beans were used for our investigation. The results showed that canned black beans contained anywhere from 9728 to 22 719 hau/g of solid, which were among the highest levels among all of the canned beans investigated. No significant difference was observed between two lots from the same manufacturer. There was also no significant difference in the hemagglutinin levels for canned black beans from Market Pantry and Bush’s. The hemagglutinin units were estimated to be between 1 028 169 and 2 068 162 hau for each can of black beans. The hemagglutinin units in canned red kidney beans, white kidney beans, and great northern beans were in the range of 2747−6596 hau/g, with mostly around 3000 hau/g. No significant difference was observed between two lots of beans Received: May 30, 2018

A

DOI: 10.1021/acs.jafc.8b02842 J. Agric. Food Chem. XXXX, XXX, XXX−XXX

Viewpoint

Journal of Agricultural and Food Chemistry Table 1. Hemagglutinin Units (hau) of Canned Beans from Different Manufacturersa number

beans used

solid (1.5×) (%)

HAU/g of solid

HAU/can

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22

Goya black bean lot A Goya black bean lot B Market Pantry black bean lot A Market Pantry black bean lot B Bush’s black beans lot A Bush’s black beans lot B Market Pantry black bean low sodium lot A Market Pantry black bean low sodium lot B Goya red kidney bean lot A Goya red kidney bean lot B Market Pantry dark red kidney bean lot A Market Pantry dark red kidney bean lot B Simply Balanced organic red kidney bean lot A Simply Balanced organic red kidney bean lot B Bush’s red kidney bean lot A Bush’s red kidney bean lot B Bush’s white kidney bean lot A Bush’s white kidney bean lot B Bush’s great northern bean lot A Bush’s great northern bean lot B Market Pantry great northern bean lot A Market Pantry great northern bean lot B average

16.4 16.4 15.1 14.1 15.8 15.7 14.1 13.0 14.6 14.0 13.3 14.4 12.5 12.1 14.0 12.8 13.2 13.8 12.1 12.8 10.6 11.7 13.8

9728 9749 21232 22719 20294 20323 11387 12262 2747 2861 3003 2770 3206 6596 2849 3119 3022 2890 3303 3129 3775 3414 7926

1029028 1031249 2067891 2066179 2068162 2058009 1035591 1028169 258685 258348 257612 257278 258484 514785 257265 257505 257293 257239 257783 258330 258097 257638 738665

a

The canned beans were diluted by a factor of 1.5 with water. Two lots from each product were tested.

from the same manufacturer, except the Simply Balanced organic beans. It is reasonable some variations of hemagglutinin exist between lots. The variations are relatively small compared to the amount of hemagglutinins of raw beans, which can be as high as 2 700 000 hau/g for red kidney beans.19 For all of the red kidney bean investigated, the canning process denatured more than 99% of hemagglutinins. The total amount of hemagglutinins in each can were estimated between 257 265 and 514 785 hau, which is a very low value compared to that of raw red kidney beans. The hemagglutinin level in one can of red kidney beans were about 19.0% of that in 1 g of raw beans. The average hemagglutinin level in all beans investigated herein was 7926 hau/g. The average total hemagglutinin in each can of beans was 738 665 hau. The canned beans are widely distributed across the country and constantly purchased by consumers; it should be thus rational to speculate that the levels of hemagglutinins in the canned beans are safe for human consumption. Given the fact that the beans in this study contained the highest concentrations of hemagglutinins compared to other species, it would also be reasonable to suggest a safe level of hemagglutinin intake for human consumption based on the results of this investigation. To establish a preliminary guidance, the protein/other ingredients isolated from beans containing less than 738 665 hau per serving should be considered safe for direct human consumption. It is recommended for the processor to incorporate a hau measurement or a hemagglutinin reduction process to ensure the safety of ingredients, such as protein supplement, that are directly consumed by the customers. On the other hand, if the bean protein is used as a fortification ingredient to produce foods that require further heat treatment (e.g., baking or cooking), a value higher than 738 665 hau might be used. In either case, it would be beneficial to add the

hau measurement as part of the quality control program for the bean protein/ingredient manufacturers.



ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jafc.8b02842. Materials and methods (PDF)



AUTHOR INFORMATION

Corresponding Author

*Telephone: 607-255-2923. E-mail: [email protected]. ORCID

Zhong Zhang: 0000-0001-6891-7825 Alireza Abbaspourrad: 0000-0001-5617-9220 Notes

The authors declare no competing financial interest.



REFERENCES

(1) Roy, F.; Boye, J.; Simpson, B. Bioactive proteins and peptides in pulse crops: Pea, chickpea and lentil. Food Res. Int. 2010, 43, 432− 442. (2) Dan, X.; Ng, T. B.; Wong, J. H.; Chan, Y. S.; Cheung, R. C. F.; Chan, W. Y. A hemagglutinin isolated from Northeast China black beans induced mitochondrial dysfunction and apoptosis in colorectal cancer cells. Biochim. Biophys. Acta, Mol. Cell Res. 2016, 1863, 2201− 2211. (3) Boyd, W. C. The lectins: Their present status. Vox Sang. 2017, 8, 1−32. (4) Nasi, A.; Picariello, G.; Ferranti, P. Proteomic approaches to study structure, functions and toxicity of legume seeds lectins. Perspectives for the assessment of food quality and safety. J. Proteomics 2009, 72, 527−538. (5) Sharon, N.; Lis, H. History of lectins: From hemagglutinins to biological recognition molecules. Glycobiology 2004, 14, 53R−62R. B

DOI: 10.1021/acs.jafc.8b02842 J. Agric. Food Chem. XXXX, XXX, XXX−XXX

Viewpoint

Journal of Agricultural and Food Chemistry (6) Ganesan, K.; Xu, B. Polyphenol-Rich Dry Common Beans (Phaseolus vulgaris L.) and Their Health Benefits. Int. J. Mol. Sci. 2017, 18, 2331. (7) Goldstein, I. J.; Poretz, R. D. Isolation, Physicochemical Characterization, and Carbohydrate-Binding Specificity of Lectins. The Lectins: Properties, Functions, and Applications in Biology and Medicine; Academic Press: Orlando, FL, 1986; pp 33−247, DOI: 10.1016/B978-0-12-449945-4.50007-5. (8) Dan, X.; Wong, J. H.; Fang, E. F.; Wai Chan, F. C.; Ng, T. B. Purification and characterization of a novel hemagglutinin with inhibitory activity toward osteocarcinoma cells from northeast China black beans. J. Agric. Food Chem. 2015, 63, 3903−3914. (9) Yin, C.; Wong, J. H.; Ng, T. B. Isolation of a hemagglutinin with potent antiproliferative activity and a large antifungal defensin from Phaseolus vulgaris cv. Hokkaido Large Pinto Beans. J. Agric. Food Chem. 2015, 63, 5439−5448. (10) Nakata, S.; Kimura, T. Effect of ingested toxic bean lectins on the gastrointestinal tract in the rat. J. Nutr. 1985, 115, 1621−1629. (11) Nciri, N.; Cho, N.; Bergaoui, N.; Mhamdi, F. E.; Ammar, A. B.; Trabelsi, N.; Zekri, S.; Guémira, F.; Mansour, A. B.; Sassi, F. H.; Aissa-Fennira, F. B. Effect of white kidney beans (Phaseolus vulgaris L. var. Beldia) on small intestine morphology and function in Wistar rats. J. Med. Food 2015, 18, 1387−1399. (12) Noah, N. D.; Bender, A.; Reaidi, G. B.; Gilbert, R. J. Food poisoning from raw red kidney beans. Br. Med. J. 1980, 281, 236−237. (13) Lajolo, F. M.; Genovese, M. I. Nutritional significance of lectins and enzyme inhibitors from legumes. J. Agric. Food Chem. 2002, 50, 6592−6598. (14) Lagarda-Diaz, I.; Guzman-Partida, A. M.; Vazquez-Moreno, L. Legume lectins: Proteins with diverse applications. Int. J. Mol. Sci. 2017, 18, 1242. (15) Khalil, A.; Mansour, E. The effect of cooking, autoclaving and germination on the nutritional quality of faba beans. Food Chem. 1995, 54, 177−182. (16) Bender, A.; Reaidi, G. Toxicity of kidney beans (Phaseolus vulgaris) with particular reference to lectins. J. Plant Foods 1982, 4, 15−22. (17) U.S. Food and Drug Administration (FDA). Bad Bug Book: Handbook of Foodborne Pathogenic Microorganisms and Natural Toxins; FDA: Silver Spring, MD, 2005. (18) Ng, T. B.; Chan, Y. S.; Ng, C. C. W.; Wong, J. H. Purification and characterization of a lectin from green split peas (Pisum sativum). Appl. Biochem. Biotechnol. 2015, 177, 1374−1385. (19) Thompson, L. U.; Rea, R. L.; Jenkins, D. J. Effect of heat processing on hemagglutinin activity in red kidney beans. J. Food Sci. 1983, 48, 235−236.

C

DOI: 10.1021/acs.jafc.8b02842 J. Agric. Food Chem. XXXX, XXX, XXX−XXX