Finding alternative uses for Australian rosella (Hibiscus sabdariffa) byproducts: nutritional potential and in vitro digestibility studies
Ryan J. Batley
A # * , Joel B. Johnson A # , Janice S. Mani A , Daniel A. Broszczak B and Mani Naiker A
+ Author Affiliations
- Author Affiliations
A School of Health, Medical & Applied Sciences, CQUniversity, Bruce Highway, North Rockhampton, Qld 4701, Australia.
B School of Biomedical Sciences, Faculty of Health, Queensland University of Technology, Kelvin Grove Campus, Kelvin Grove, Qld 4059, Australia.
* Correspondence to: ryan.batley@cqumail.com
# These authors contributed equally to this paper
Handling Editor: Penny Back
Animal Production Science 62(6) 581-589 https://doi.org/10.1071/AN21475
Submitted: 20 September 2021 Accepted: 15 December 2021 Published: 8 February 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Context: Rosella (Hibiscus sabdariffa L.) is a relatively new crop in Australia, with only a few commercial producers. The calyces are harvested for human consumption, with the seed pods often discarded as a waste byproduct. However, this material may have potential as a livestock feed supplement or as a value-added product in the food processing industry.
Aims: This study aimed to investigate the nutritional potential of rosella pods for use as a feed supplement, including an in vitro assessment of their digestibility in beef cattle.
Methods: Samples of rosella plants were separated into leaves, pods and calyces, then freeze-dried and ground. These products were measured in duplicate for their antioxidant capacity, as well as protein, metal, phenolic and anthocyanin content. Samples of the dried rosella pods (n = 3) underwent in vitro digestibility analysis using rumen/pepsin digestions and were compared with samples of commercial feedstock (n = 3). The resulting simulated gastrointestinal fluids from these digestions were tested for antioxidant capacity and phenolic content.
Key results: The highest antioxidant and phenolic contents of plant parts were observed in the pods (14 300 mg Trolox equivalents and 2960 mg gallic acid equivalents 100 g−1, respectively), highlighting their potential for human or animal nutrition. The pods also contained moderate to high levels of minerals including calcium, potassium, sodium, magnesium, copper, iron, manganese and zinc. Although the in vitro dry matter digestibility was lower (P < 0.001) than that of a conventional grain feedstock, the rosella pod substrate released significantly higher (P = 0.02) levels of antioxidants upon digestion than the commercial feedstock.
Conclusion: Although rosella pod digestibility was lower than that of a conventional grain feedstock, it was comparable to mean values for Australian hays and silages. Given the higher levels of antioxidants released during digestion, rosella waste product has potential to be used in small amounts as a feed supplement, with the added benefit of enhancing free radical quenching ability.
Implications: This study provides evidence for further investigation of the use of rosella waste as an animal feed, which would improve sustainability in agriculture as well as potentially improve animal health.
Keywords: antioxidant, bioaccessibility, cattle, digestibility, in vitro, phenolics, rosella, waste.
References
Abuelo A, Hernández J, Benedito JL, Castillo C (2015) The importance of the oxidative status of dairy cattle in the periparturient period: revisiting antioxidant supplementation. Journal of Animal Physiology and Animal Nutrition 99, 1003–1016.| The importance of the oxidative status of dairy cattle in the periparturient period: revisiting antioxidant supplementation.Crossref | GoogleScholarGoogle Scholar | 25475653PubMed |
Alfian R, Susanti H (2013) Penetapan kadar fenolik total ekstrak metanol kelopak bunga rosella merah (Hibiscus sabdariffa Linn) dengan variasi tempat tumbuh secara spektrofotometri. Pharmaciana 2, 73–81.
| Penetapan kadar fenolik total ekstrak metanol kelopak bunga rosella merah (Hibiscus sabdariffa Linn) dengan variasi tempat tumbuh secara spektrofotometri.Crossref | GoogleScholarGoogle Scholar |
Aminul Islam AKM, Jamini TS, Mominul Islam AKM, Yeasmin S (2016) Roselle: a functional food with high nutritional and medicinal values. Fundamental and Applied Agriculture 1, 44–49. https://www.f2ffoundation.org/faa/index.php/home/article/view/56
Apak R, Gorinstein S, Böhm V, Schaich KM, Özyürek M, Güçlü K (2013) Methods of measurement and evaluation of natural antioxidant capacity/activity (IUPAC Technical Report). Pure and Applied Chemistry 85, 957–998.
| Methods of measurement and evaluation of natural antioxidant capacity/activity (IUPAC Technical Report).Crossref | GoogleScholarGoogle Scholar |
Apul S, Sisilia FY (2018) The utilization of red seed guava and rosella flower as sources of vitamin C. IOP Conference Series: Earth and Environmental Science 205, 012042
| The utilization of red seed guava and rosella flower as sources of vitamin C.Crossref | GoogleScholarGoogle Scholar |
Arpita M, Kabita B, Kumar DA (2017) Review on amaging benefits of roseelle (Hibiscus Sabdarifa L) and their uses. Word Journal of Pharmacy and Pharmaceutical Sciences 6, 217–227.
| Review on amaging benefits of roseelle (Hibiscus Sabdarifa L) and their uses.Crossref | GoogleScholarGoogle Scholar |
Atta S, Sarr B, Diallo AB, Bakasso Y, Lona I, Saadou M (2013) Nutrients composition of calyces and seeds of three Roselle (Hibiscus sabdariffa L.) ecotypes from Niger. African Journal of Biotechnology 12, 4174–4178.
Benzie IF, Strain JJ (1996) The ferric reducing ability of plasma (FRAP) as a measure of ‘antioxidant power’: the FRAP assay. Analytical Biochemistry 239, 70–76.
| The ferric reducing ability of plasma (FRAP) as a measure of ‘antioxidant power’: the FRAP assay.Crossref | GoogleScholarGoogle Scholar | 8660627PubMed |
Bouwstra RJ, Nielen M, Newbold JR, Jansen EHJM, Jelinek HF, van Werven T (2010) Vitamin E supplementation during the dry period in dairy cattle. Part II: Oxidative stress following vitamin E supplementation may increase clinical mastitis incidence postpartum. Journal of Dairy Science 93, 5696–5706.
| Vitamin E supplementation during the dry period in dairy cattle. Part II: Oxidative stress following vitamin E supplementation may increase clinical mastitis incidence postpartum.Crossref | GoogleScholarGoogle Scholar | 21094741PubMed |
Camacho LF, Silva TE, Palma MNN, Assunção AS, Rodrigues JP, Costa e Silva LF, Detmann E (2019) Evaluation of buffer solutions and urea addition for estimating the in vitro digestibility of feeds. Journal of Animal Science 97, 922–931.
| Evaluation of buffer solutions and urea addition for estimating the in vitro digestibility of feeds.Crossref | GoogleScholarGoogle Scholar | 30535309PubMed |
Castillo C, Pereira V, Abuelo Á, Hernández J (2013) Effect of supplementation with antioxidants on the quality of bovine milk and meat production. The Scientific World Journal 2013, 616098
| Effect of supplementation with antioxidants on the quality of bovine milk and meat production.Crossref | GoogleScholarGoogle Scholar | 24348176PubMed |
Chao MD, Domenech-Pérez KI, Voegele HR, Kunze EK, Calkins CR (2018) Effects of dietary antioxidant supplementation of steers finished with 30% wet distillers grains plus solubles on fatty acid profiles and display life of strip loins. Animal Production Science 58, 1949–1957.
| Effects of dietary antioxidant supplementation of steers finished with 30% wet distillers grains plus solubles on fatty acid profiles and display life of strip loins.Crossref | GoogleScholarGoogle Scholar |
Ferreira JFS, Cornacchione MV, Liu X, Suarez DL (2015) Nutrient composition, forage parameters, and antioxidant capacity of alfalfa (Medicago sativa, L.) in response to saline irrigation water. Agriculture 5, 577–597.
| Nutrient composition, forage parameters, and antioxidant capacity of alfalfa (Medicago sativa, L.) in response to saline irrigation water.Crossref | GoogleScholarGoogle Scholar |
Francis FJ, Markakis PC (1989) Food colorants: anthocyanins. Critical Reviews in Food Science and Nutrition 28, 273–314.
| Food colorants: anthocyanins.Crossref | GoogleScholarGoogle Scholar | 2690857PubMed |
Fu L, Xu B-T, Xu X-R, Gan R-Y, Zhang Y, Xia E-Q, Li H-B (2011) Antioxidant capacities and total phenolic contents of 62 fruits. Food Chemistry 129, 345–350.
| Antioxidant capacities and total phenolic contents of 62 fruits.Crossref | GoogleScholarGoogle Scholar | 30634236PubMed |
Hashem NM, Gonzalez-Bulnes A, Simal-Gandara J (2020) Polyphenols in farm animals: source of reproductive gain or waste? Antioxidants 9, 1023
| Polyphenols in farm animals: source of reproductive gain or waste?Crossref | GoogleScholarGoogle Scholar |
Hayes M (2020) Measuring protein content in food: an overview of methods. Foods 9, 1340
| Measuring protein content in food: an overview of methods.Crossref | GoogleScholarGoogle Scholar |
Holden LA (1999) Comparison of methods of in vitro dry matter digestibility for ten feeds. Journal of Dairy Science 82, 1791–1794.
| Comparison of methods of in vitro dry matter digestibility for ten feeds.Crossref | GoogleScholarGoogle Scholar | 10480105PubMed |
Ikhwan Rizki M, Nurkhasanah N, Yuwono T, Hayu Nurani L, Kraisintu K (2017) Antioxidant activity of nanoparticle from rosella (Hibiscus sabdariffa L) calyx extract originated Indonesia and Thailand. Research Journal of Pharmaceutical, Biologycal and Chemical Sciences 8, 149–157.
Johnson J, Collins T, Skylas D, Naiker M (2019) ATR-MIR: a valuable tool for the rapid assessment of biochemically active compounds in grains.. In ‘Proceedings 69th Australasian grain science conference’. 27–29 August 2019, Melbourne, Vic., Australia. Australian Grain Science Association (ASGA), pp. 81–87. Available at https://www.researchgate.net/publication/334644936_ATR-MIR_a_valuable_tool_for_the_rapid_assess
Johnson J, Collins T, Power A, Chandra S, Skylas D, Portman D, Panozzo J, Blanchard C, Naiker M (2020a) Antioxidative properties and macrochemical composition of five commercial mungbean varieties in Australia. Legume Science 2, e27
| Antioxidative properties and macrochemical composition of five commercial mungbean varieties in Australia.Crossref | GoogleScholarGoogle Scholar |
Johnson J, Collins T, Walsh K, Naiker M (2020b) Solvent extractions and spectrophotometric protocols for measuring the total anthocyanin, phenols and antioxidant content in plums. Chemical Papers 74, 4481–4492.
| Solvent extractions and spectrophotometric protocols for measuring the total anthocyanin, phenols and antioxidant content in plums.Crossref | GoogleScholarGoogle Scholar |
Kaiser A, Piltz J (2004) Feed testing assessing silage quality in successful silage. In ‘Successful silage’. (Eds A Kaiser, J Piltz, H Burns, N Griffiths) pp. 312–333. (Dairy Australia and New South Wales Department of Primary Industries: Orange, NSW, Australia)
Khaghani S, Razi F, Yajloo MM, Paknejad M, Shariftabrizi A, Pasalar P (2011) Selective cytotoxicity and apoptogenic activity of Hibiscus sabdariffa aqueous extract against MCF-7 human breast cancer cell line. Journal of Cancer Therapy 2, 394–400.
| Selective cytotoxicity and apoptogenic activity of Hibiscus sabdariffa aqueous extract against MCF-7 human breast cancer cell line.Crossref | GoogleScholarGoogle Scholar |
Kuhnen S, Moacyr JR, Mayer JK, Navarro BB, Trevisan R, Honorato LA, Maraschin M, Pinheiro Machado Filho LC (2014) Phenolic content and ferric reducing–antioxidant power of cow’s milk produced in different pasture-based production systems in southern Brazil. Journal of the Science of Food and Agriculture 94, 3110–3117.
| Phenolic content and ferric reducing–antioxidant power of cow’s milk produced in different pasture-based production systems in southern Brazil.Crossref | GoogleScholarGoogle Scholar | 24633643PubMed |
Lako J, Trenerry VC, Wahlqvist M, Wattanapenpaiboon N, Sotheeswaran S, Premier R (2007) Phytochemical flavonols, carotenoids and the antioxidant properties of a wide selection of Fijian fruit, vegetables and other readily available foods. Food Chemistry 101, 1727–1741.
| Phytochemical flavonols, carotenoids and the antioxidant properties of a wide selection of Fijian fruit, vegetables and other readily available foods.Crossref | GoogleScholarGoogle Scholar |
Lee J, Durst RW, Wrolstad RE (2005) Determination of total monomeric anthocyanin pigment content of fruit juices, beverages, natural colorants, and wines by the pH differential method: collaborative study. Journal of AOAC international 88, 1269–1278.
| Determination of total monomeric anthocyanin pigment content of fruit juices, beverages, natural colorants, and wines by the pH differential method: collaborative study.Crossref | GoogleScholarGoogle Scholar | 16385975PubMed |
Luvonga W (2011) Nutritional characterisation of Roselle (Hibiscus Sabdariffa) calyces, evaluation of its functional properties and sensory quality of its novel products. In ‘Jkuat annual scientific conference proceedings’. Available at http://ir.jkuat.ac.ke/handle/123456789/3125
Luvonga WA, Njoroge M, Makokha A, Ngunjiri P (2010) Chemical characterisation of Hibiscus sabdariffa (Roselle) calyces and evaluation of its functional potential in the food industry. In ‘Jkuat annual scientific conference proceedings’.
Mabjeesh SJ, Cohen M, Arieli A (2000) In vitro methods for measuring the dry matter digestibility of ruminant feedstuffs: comparison of methods and inoculum source. Journal of Dairy Science 83, 2289–2294.
| In vitro methods for measuring the dry matter digestibility of ruminant feedstuffs: comparison of methods and inoculum source.Crossref | GoogleScholarGoogle Scholar | 11049071PubMed |
Mahfudh N, Fajrin A (2018) The effect of subchronic administration of rosella (Hibiscus sabdariffa L.) extract on levels of ureum, creatinine, and renal histopathology. International Journal of Pharmaceutical Sciences and Research 21, 649–654.
Mahfudh N, Ikarini N (2018) In vivo effect of sub-chronic administration of ethanol extract of Rosella (Hibiscus sabdariffa L.) calyx on total blood cholesterol, triglyceride level, and heart histopathologic profile. International Food Research Journal 25, 1253–1257.
Mavangira V, Sordillo LM (2018) Role of lipid mediators in the regulation of oxidative stress and inflammatory responses in dairy cattle. Research in Veterinary Science 116, 4–14.
| Role of lipid mediators in the regulation of oxidative stress and inflammatory responses in dairy cattle.Crossref | GoogleScholarGoogle Scholar | 28807478PubMed |
McDougall EI (1948) Studies on ruminant saliva. 1. The composition and output of sheep’s saliva. Biochemical Journal 43, 99–109.
| Studies on ruminant saliva. 1. The composition and output of sheep’s saliva.Crossref | GoogleScholarGoogle Scholar |
Mellenberger RW, Satter LD, Millett MA, Baker AJ (1970) An in vitro technique for estimating digestibility of treated and untreated wood. Journal of Animal Science 30, 1005–1011.
| An in vitro technique for estimating digestibility of treated and untreated wood.Crossref | GoogleScholarGoogle Scholar |
Nockels CF (1996) Antioxidants improve cattle immunity following stress. Animal Feed Science and Technology 62, 59–68.
| Antioxidants improve cattle immunity following stress.Crossref | GoogleScholarGoogle Scholar |
Peng C-H, Chyau C-C, Chan K-C, Chan T-H, Wang C-J, Huang C-N (2011) Hibiscus sabdariffa polyphenolic extract inhibits hyperglycemia, hyperlipidemia, and glycation-oxidative stress while improving insulin resistance. Journal of Agricultural and Food Chemistry 59, 9901–9909.
| Hibiscus sabdariffa polyphenolic extract inhibits hyperglycemia, hyperlipidemia, and glycation-oxidative stress while improving insulin resistance.Crossref | GoogleScholarGoogle Scholar | 21870884PubMed |
Prommachart R, Cherdthong A, Navanukraw C, Pongdontri P, Taron W, Uriyapongson J, Uriyapongson S (2021) Effect of dietary anthocyanin-extracted residue on meat oxidation and fatty acid profile of male dairy cattle. Animals 11, 322
| Effect of dietary anthocyanin-extracted residue on meat oxidation and fatty acid profile of male dairy cattle.Crossref | GoogleScholarGoogle Scholar | 33525410PubMed |
Shen C-Y, Zhang T-T, Zhang W-L, Jiang J-G (2016) Anti-inflammatory activities of essential oil isolated from the calyx of Hibiscus sabdariffa L. Food & Function 7, 4451–4459.
| Anti-inflammatory activities of essential oil isolated from the calyx of Hibiscus sabdariffa L.Crossref | GoogleScholarGoogle Scholar |
Shruthi VH, Ramachandra CT, Nidoni U, Hiregoudar S, Naik N, Kurubar AR (2016) Roselle (Hibiscus sabdariffa L.) as a source of natural colour: a review. Plant Archives 16, 515–522.
Sindi HA, Marshall LJ, Morgan MRA (2014) Comparative chemical and biochemical analysis of extracts of Hibiscus sabdariffa. Food Chemistry 164, 23–29.
| Comparative chemical and biochemical analysis of extracts of Hibiscus sabdariffa.Crossref | GoogleScholarGoogle Scholar | 24996300PubMed |
Skylas DJ, Blanchard CL, Quail KJ (2017) Variation in nutritional composition of Australian mungbean varieties. Journal of Agricultural Science 9, 45–53.
| Variation in nutritional composition of Australian mungbean varieties.Crossref | GoogleScholarGoogle Scholar |
Terry ME, Bonner BA (1980) An examination of centrifugation as a method of extracting an extracellular solution from peas, and its use for the study of indoleacetic acid-induced growth. Plant Physiology 66, 321–325.
| An examination of centrifugation as a method of extracting an extracellular solution from peas, and its use for the study of indoleacetic acid-induced growth.Crossref | GoogleScholarGoogle Scholar | 16661430PubMed |
Tilley JMA, Terry RA (1963) A two-stage technique for the in vitro digestion of forage crops. Grass and Forage Science 18, 104–111.
| A two-stage technique for the in vitro digestion of forage crops.Crossref | GoogleScholarGoogle Scholar |
University of Nebraska-Lincoln (2013) ‘In vitro dry matter disappearance’. (University of Nebraska-Lincoln Animal Science Ruminant Nutrition Lab: Lincoln, NE, USA). Available at https://animalscience.unl.edu/Research/RumNut/RumNutLab/47-InVitroDryMatterDisappearance.pdf
Vázquez-Añón M, Nocek J, Bowman G, Hampton T, Atwell C, Vázquez P, Jenkins T (2008) Effects of feeding a dietary antioxidant in diets with oxidized fat on lactation performance and antioxidant status of the cow. Journal of Dairy Science 91, 3165–3172.
| Effects of feeding a dietary antioxidant in diets with oxidized fat on lactation performance and antioxidant status of the cow.Crossref | GoogleScholarGoogle Scholar | 18650293PubMed |
Wu H-Y, Yang K-M, Chiang P-Y (2018) Roselle anthocyanins: antioxidant properties and stability to heat and pH. Molecules 23, 1357
| Roselle anthocyanins: antioxidant properties and stability to heat and pH.Crossref | GoogleScholarGoogle Scholar |
Yang Y-S, Huang C-N, Wang C-J, Lee Y-J, Chen M-L, Peng C-H (2013) Polyphenols of Hibiscus sabdariffa improved diabetic nephropathy via regulating the pathogenic markers and kidney functions of type 2 diabetic rats. Journal of Functional Foods 5, 810–819.
| Polyphenols of Hibiscus sabdariffa improved diabetic nephropathy via regulating the pathogenic markers and kidney functions of type 2 diabetic rats.Crossref | GoogleScholarGoogle Scholar |
Zhang B, Mao G, Zheng D, Zhao T, Zou Y, Qu H, Li F, Zhu B, Yang L, Wu X (2014) Separation, identification, antioxidant, and anti-tumor activities of Hibiscus sabdariffa L. extracts. Separation Science and Technology 49, 1379–1388.
| Separation, identification, antioxidant, and anti-tumor activities of Hibiscus sabdariffa L. extracts.Crossref | GoogleScholarGoogle Scholar |
Zhang YY, Panozzo J, Hall MS, Ajlouni S (2018) Bioaccessibility of some essential minerals in three selected australian pulse varieties using an in vitro gastrointestinal digestion model. Journal of Food Science 83, 2873–2881.
| Bioaccessibility of some essential minerals in three selected australian pulse varieties using an in vitro gastrointestinal digestion model.Crossref | GoogleScholarGoogle Scholar | 30370926PubMed |
