Pancreatic Lipase Inhibition Activity in Lipid Absorption Using Traditional Plants: A Systematic Review and Meta-Analysis

Hasim Hasim; Didah Nur Faridah; Eka Nurul Qomaliyah; Frendy Ahmad Afandi

doi:10.22146/ijc.76873

Pancreatic Lipase Inhibition Activity in Lipid Absorption Using Traditional Plants: A Systematic Review and Meta-Analysis

https://doi.org/10.22146/ijc.76873

Hasim Hasim^(1*), Didah Nur Faridah⁽²⁾, Eka Nurul Qomaliyah⁽³⁾, Frendy Ahmad Afandi⁽⁴⁾

(1) Department of Biochemistry, IPB University, Jl. Tanjung, Kampus IPB Dramaga, Bogor 16680, Indonesia
(2) Department of Food Science and Technology, Faculty of Agricultural Technology, IPB University, Jl. Tanjung, Kampus IPB Dramaga, Bogor 16680, Indonesia; Southeast Asian Food and Agricultural Science and Technology (SEAFAST) Center, IPB University, Jl. Tanjung, Kampus IPB Dramaga, Bogor 16680, Indonesia
(3) Department of Pharmacy, Bumigora University, Jl. Ismail Marzuki No.22, Mataram 83127, Indonesia
(4) Deputy Ministry for Food and Agribusiness, Coordinating Ministry for Economic Affairs, Republic of Indonesia, Jakarta 10710, Indonesia
(*) Corresponding Author

Abstract

Obesity is a complex and multifactorial disease resulting from excessive accumulation of fat. With a significant annual increase, it has become a health concern across the globe in the last decades. To tackle this problem, an exploration of traditional medicinal plants (TMP) functioning as anti-obesity drugs using an ethnopharmacology approach has been carried out. Research on the drug development of obesity treatment was directed at how to inhibit pancreatic lipase as the enzyme accounted for lipid absorption. Using a systematic review and meta-analysis, this current study investigated TMP anti-obesity from the articles published in 6 scientific databases, i.e., Scopus, Science Direct, Proquest, Cengage Library, Ebsco, and Emerald, using particular keywords. The review resulted in 19 articles containing 91 eligible data based on inclusive and exclusive criteria. Meta-analysis extracted data as follows: IC₅₀, number of replications, and standard error, regarding the anti-obesity effects of medicinal plants and orlistat as a positive control. The results showed 8 medicinal plants showing anti-obesity via inhibition of pancreatic lipase, including Solenostemma argel, Garcinia vilersiana, Phyllanthus chamaepeuce, Cassia auriculata, Moringa oleifera, Ficus carica, Ocimum gratissimum, and Adiantum capillus-veneris.

Keywords

anti-obesity; ethnopharmacology; medicinal plants; meta-analysis; lipase inhibition

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References

[1] World Health Organization, 2018, Noncomunicable Disease Country Profiles 2018, World Health Organization, Geneva.

[2] Chooi, Y.C., Ding, C., and Magkos, F., 2018, The epidemiology of obesity, Metabolism, 92 (1), 6–10.

[3] Müller, M., and Geisler, C., 2017, Defining obesity as a disease, Eur. J. Clin. Nutr., 71 (11), 1256–1258.

[4] Hu, F.B., 2013, Resolved: There is sufficient scientific evidence that decreasing sugar-sweetened beverage consumption will reduce the prevalence of obesity and obesity-related diseases, Obes. Rev., 14 (8), 606–619.

[5] Williams, E.P., Mesidor, M., Winters, K., Dubbert, P.M., and Wyatt, S.B., 2015, Overweight and obesity: Prevalence, consequences, and causes of a growing public health problem, Curr. Obes. Rep., 4 (3), 363–370.

[6] Ernst, B., Wilms, B., Thurnheer, M., and Schultes, B., 2015, Eating behaviour in treatment-seeking obese subjects – Influence of sex and BMI classes, Appetite, 95, 96–100.

[7] Nicolaidis, S, 2019, Environment and obesity, Metabolism, 100, 153942.

[8] Koliaki, C., Liatis, S., and Kokkinos, A., 2018, Obesity and cardiovascular disease: Revisiting an old relationship, Metabolism, 92, 98–107.

[9] Ginsberg, H.N., and MacCallum, P.R., 2009, The obesity, metabolic syndrome, and type 2 diabetes mellitus pandemic: Part I. Increased cardiovascular disease risk and the importance of atherogenic dyslipidemia in persons with the metabolic syndrome and type 2 diabetes mellitus, J. CardioMetab. Syndr., 4 (2), 113–119.

[10] Csige, I., Ujvárosy, D., Szabó, Z., Lőrincz, I., Paragh, G., Harangi, M., and Somodi, S., 2018, The impact of obesity on the cardiovascular system, J. Diabetes Res., 2018, 3407306.

[11] Hasani-Ranjbar, S., Jouyandeh, Z., and Abdollahi, M., 2013, A systematic review of anti-obesity medicinal plants - An update, J. Diabetes Metab. Disord., 12 (1), 28.

[12] Mahmoud, R.H., and Elnour, W.A., 2013, Comparative evaluation of the efficacy of ginger and orlistat on obesity management, pancreatic lipase and liver peroxisomal catalase enzyme in male albino rats, Eur. Rev. Med. Pharmacol. Sci., 17, 75–83.

[13] Bujjirao, G., and Ratna Kumar, K.P., 2013, Anti-obese therapeutics from medicinal plants-A review, Int. J. Bioassays, 2 (10), 1399–1406.

[14] Yun, J.W., 2018, Possible anti-obesity therapeutics from nature – A review, Phytochemistry, 7 (14-15), 1625–1641.

[15] Rufino, A.T., Costa, V.M., Carvalho, F., and Fernandes, E., 2020, Flavonoids as antiobesity agents: A review, Med. Res. Rev., 41 (1), 556–585.

[16] Hossain, M.K., Dayem, A.A., Han, J., Yin, Y., Kim, K., Saha, S.K., Yang, G.M., Choi, H.Y., and Cho, S.G., 2016, Molecular mechanisms of the anti-obesity and anti-diabetic properties of flavonoids, Int. J. Mol. Sci., 17 (4), 569.

[17] Song, D., Cheng, L., Zhang, X., Wu, Z., and Zheng, X., 2019, The modulatory effect and the mechanism of flavonoids on obesity, J. Food Biochem., 43 (8), e12954.

[18] Nagatomo, A., Nishida, N., Matsuura, Y., and Shibata, N., 2013, Rosehip extract inhibits lipid accumulation in white adipose tissue by suppressing the expression of peroxisome proliferator-activated receptor gamma, Prev. Nutr. Food Sci., 18 (2), 85–91.

[19] Ninomiya, K., Matsuda, H., Kubo, M., Morikawa, T., Nishida, N., and Yoshikawa, M., 2007, Potent anti-obese principle from Rosa canina: Structural requirements and mode of action of trans-tiliroside, Bioorg. Med. Chem. Lett., 17 (11), 3059–3064.

[20] Lesjak, M., Beara, I., Simin, N., Pintać, D., Majkić, T., Bekvalac, K., Orčić, D., and Mimica-Dukić, N., 2018, Antioxidant and anti-inflammatory activities of quercetin and its derivatives, J. Funct. Foods, 40, 68–75.

[21] Batiha, G.E., Beshbishy, A.M., Ikram, M., Mulla, Z.S., Abd El-Hack, M.E., Taha, A.E., Algammal, A.M., and Elewa, Y.H., 2020, The pharmacological activity, biochemical properties, and pharmacokinetics of the major natural polyphenolic flavonoid: Quercetin, Foods, 9 (3), 374.

[22] Bajes, H.R., Almasri, I., and Bustanji, Y., 2020, Plant products and their inhibitory activity against pancreatic lipase, Rev. Bras. Farmacogn., 30 (3), 321–330.

[23] Mohamed, G.A., Ibrahim, S.R.M., Elkhayat, E.S., and El Dine, R.S., 2014, Natural anti-obesity agents, Bull. Fac. Pharm. Cairo Univ., 52 (2), 269–284.

[24] Marrelli, M., Loizzo, M.R., Nicoletti, M., Menichini, F., and Conforti, F., 2013, Inhibition of key enzymes linked to obesity by preparations from Mediterranean dietary plants: Effects on α-amylase and pancreatic lipase activities, Plant Foods Hum. Nutr., 68 (4), 340–346.

[25] de Freitas Junior, L.M., and de Almeida, E.B., 2017, Medicinal plants for the treatment of obesity: Ethnopharmacological approach and chemical and biological studies, Am. J. Transl. Res., 9 (5), 2050–2064.

[26] Liberati, A., Altman, D.G., Tetzlaff, J., Mulrow, C., Gøtzsche, P.C., Ioannidis, J.P.A., Clarke, M., Devereaux, P.J., Kleijnen, J., and Moher, D., 2009, The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: Explanation and elaboration, J. Clin. Epidemiol., 62 (10), e1-e34.

[27] Afandi, F.A, 2020, Meta-analisis faktor-faktor penentu nilai indeks glikemik bahan pangan pati-patian dan verifikasinya dengan menggunakan model pangan, Dissertation, IPB University.

[28] El-Shiekh, R.A., Al-Mahdy, D.A., Mouneir, S.M., Hifnawy, M.S., and Abdel-Sattar, E.A., 2019, Anti-obesity effect of argel (Solenostemma argel) on obese rats fed a high fat diet, J. Ethnopharmacol., 238, 111893.

[29] Dechakhamphu, A., and Wongchum, N., 2015, Screening for anti-pancreatic lipase properties of 28 traditional Thai medicinal herbs, Asian Pac. J. Trop. Biomed., 5 (12), 1042–1045.

[30] Mopuri, R., Ganjayi, M., Meriga, B., Koorbanally, N.A., and Islam, M.S., 2018, The effects of Ficus carica on the activity of enzymes related to metabolic syndrome, J. Food Drug Anal., 26 (1), 201–210.

[31] Inthongkaew, P., Chatsumpun, N., Supasuteekul, C., Kitisripanya, T., Putalun, W., Likhitwitayawuid, K., and Sritularak, B., 2017, α-Glucosidase and pancreatic lipase inhibitory activities and glucose uptake stimulatory effect of phenolic compounds from Dendrobium formosum, Rev. Bras. Farmacogn., 27 (4), 480–487.

[32] Kumar, D., Karmase, A., Jagtap, S., Shekhar, R., and Bhutani, K.K., 2013, Pancreatic lipase inhibitory activity of cassiamin A, a bianthraquinone from Cassia siamea, Nat. Prod. Commun., 8 (2), 195–198.

[33] Adisakwattana, S., Intrawangso, J., Hemrid, A., Chanathong, B., and Mäkynen, K., 2012, Extracts of edible plants inhibit pancreatic lipase, cholesterol esterase and cholesterol micellization, and bind bile acid, Food Technol. Biotechnol., 50 (1), 11–16.

[34] Habtemariam, S., 2012, Identification of the antidiabetic and antihyperlipidemic principles of Cassia auriculata, Planta Med., 78 (11), PD51.

[35] Kaewpiboon, C., Lirdprapamongkol, K., Srisomsap, C., Winayanuwattikun, P., Yongvanich, T., Puwaprisirisan, P., Svasti, J., and Assavalapsakul, W., 2012, Studies of the in vitro cytotoxic, antioxidant, lipase inhibitory and antimicrobial activities of selected Thai medicinal plants, BMC Complementary Altern. Med., 12, 217.

[36] Teixeira, L.S., Lima, A.S., Boleti, A.P.A., Lima, A.A.N., Libório, S.T., de Paula, L., Oliveira, M.I.B., Lima, E.F., Costa, G.M., Reginatto, F.H., and Lima, E.S., 2013, Effects of Passiflora nitida Kunth leaf extract on digestive enzymes and high caloric diet in rats, J. Nat. Med., 68 (2), 316–325.

[37] Buchholz, T., and Melzig, M.F., 2015, Medicinal plants traditionally used for treatment of obesity and diabetes mellitus - Screening for pancreatic lipase and α-amylase inhibition, Phytother. Res., 30 (2), 260–266.

[38] Huang, R., Zhang, Y., Shen, S., Zhi, Z., Cheng, H., Chen, S., and Ye, X., 2020, Antioxidant and pancreatic lipase inhibitory effects of flavonoids from different citrus peel extracts: An in vitro study, Food Chem., 326, 126785.

[39] Bais, S., and Patel, N.J., 2012, In vitro anti diabetic and anti obesity effect of J. communis extract on 3T3L1 mouse adipocytes: A possible role of MAPK/ERK activation, Obes. Med., 18, 100219.

[40] Al-Rimawi, F., Jaradat, N., Qneibi, M., Hawash, M., and Emwas, N., 2020, Free radicals and enzymes inhibitory potentials of the traditional medicinal plant Echium angustifolium, Eur. J. Integr. Med., 38, 101196.

[41] Spínola, V., Llorent-Martínez, E.J., and Castilho, P.C., 2019, Inhibition of α-amylase, α-glucosidase and pancreatic lipase by phenolic compounds of Rumex maderensis (Madeira sorrel). Influence of simulated gastrointestinal digestion on hyperglycaemia-related damage linked with aldose reductase activity and protein glycation, LWT, 118, 108727.

[42] Anyanwu, G.O., Anzaku, D., Donwell, C.C., Usunobun, U., Adegbegi, A.J., Ofoha, P.C., and Rauf, K., 2021, Chemical composition and in vitro antiobesity and in vivo anti-hyperlipidemic effects of Ceratotheca sesamoides, Jatropha tanjorensis, Mucuna flagellipes, Pterocarpus mildbraedii and Piper guineense, Phytomed. Plus, 1 (3), 10042.

[43] Al-Yousef, H.M., Alqahtani, A.S., Hassan, W.H., Alzoubi, A., and Sahar, A.A., 2021, Chemical profile, in vitro antioxidant, pancreatic lipase, and alpha-amylase inhibition assays of the aqueous extract of Elettaria cardamomum L. fruits, J. Chem., 2021, 5583001.

[44] Jaradat, N., Qadi, M., Abualhasan, M.N., Al-lahham, S., Al-Rimawi, F., Hattab, S., Hussein, F., Zakarneh, D., Hamad, I., Sulayman, I., Issa, L., and Mousa, A., 2020, Carbohydrates and lipids metabolic enzymes inhibitory, antioxidant, antimicrobial and cytotoxic potentials of Anchusa ovata Lehm. from Palestine, Eur. J. Integr. Med., 34, 101066.

[45] Kasabri, V., Al-Hallaq, E.K., Bustanji, Y.K., Abdul-Razzak, K.K., Abaza, I.F., and Afifi, F.U., 2017, Antiobesity and antihyperglycaemic effects of Adiantum capillus-veneris extracts: In vitro and in vivo evaluations, Pharm. Biol., 55 (1), 164–172.

[46] Gururaja, G.M., Mundkinajeddu, D., Kumar, S., Allan, J., Dethe, S.M., and Agarwal, A., 2016, Cholesterol lowering potentials of a blend of standardized methanol extracts of Moringa oleifera leaves and fruits in albino wistar rats, Int. J. Pharm. Pharm. Sci., 8 (11), 262–268.

[47] Wang, F., Bao, Y., Shen, X., Zengin, G., Lyu, Y., Xiao, J., and Weng, Z., 2019, Niazirin from Moringa oleifera Lam. attenuates high glucose-induced oxidative stress through PKCζ/Nox4 pathway, Phytomedicine, 86, 153066.

[48] Rajan, L., Palaniswamy, D., and Mohankumar, S.K., 2020, Targeting obesity with plant-derived pancreatic lipase inhibitors: A comprehensive review, Pharmacol. Res., 155, 104681.

[49] Lee, E.M., Lee, S.S., Chung, B.Y., Cho, J.Y., Lee, I.C., Ahn, S.R., Jang, S.J., and Kim, T.H., 2010, Pancreatic lipase inhibition by C-glycosidic flavones isolated from Eremochloa ophiuroides, Molecules, 15 (11), 8251–8259.

[50] Lunagariya, N.A., Patel, N.K., Jagtap, S.C., and Bhutani, K.H., 2014, Inhibitors of pancreatic lipase: State of the art and clinical perspectives, EXLI J., 13, 897–921.

[51] Chemat, F., Rombaut, N., Sicaire, A.G., Meullemiestre, A., Fabiano-Tixier, A.S., and Abert-Vian, M., 2016, Ultrasound assisted extraction of food and natural products. Mechanisms, techniques, combinations, protocols and applications. A review, Ultrason. Sonochem., 34, 540-560.

[52] Azmir, J., Zaidul, I.S.M., Rahman, M.M., Sharif, K.M., Mohamed, A., Sahena, F., Jahurul, M.H.A., Ghafoor, K., Norulaini, N.A.N., and Omar, A.K.M., 2013, Techniques for extraction of bioactive compounds from plant materials: A review, J Food Eng., 117 (4), 426–436.

[53] Altemimi, A., Lakhssassi, N., Baharlouei, A., Watson, D.G., and Lightfoot, D.A., 2017, Phytochemicals: Extraction, isolation, and identification of bioactive compounds from plant extracts, Plants, 6 (4), 42.

[54] Dai, J., and Mumper, R.J., 2010, Plant phenolics: Extraction, analysis and their antioxidant and anticancer properties, Molecules, 15 (10), 7313–7352.

[55] Iswantini, D., Darusman, L.K., and Fitriyani, A., 2010, Uji in vitro ekstrak air dan etanol dari buah asam gelugur, rimpang lengkuas, dan kencur sebagai inhibitor aktivitas lipase pancreas, JSTI, 12 (1), 15–20.

[56] Hassan, H.A., Hamed, A.I., El-Emary, N.A., Springuel, I.V., Mitome, H., and Miyaoka, H., 2001, Pregnene derivatives from Solenostemma argel leaves, Phytochemistry, 57 (4), 507–511.

[57] El-shiekh, R.A., Al-Mahdy, D.A., Hifnawy, M.S., and Abdel-Sattar, E., 2019, In-vitro screening of selected traditional medicinal plants for their anti-obesity and anti-oxidant activities, S. Afr. J. Bot., 123, 43–50.

[58] Angami, T., Wangchu, L., Debnath, P., Sarma, P., Singh, B., Singh, A.K., Singh, S., Singh, M.C., Aochen, C., and Lungmuana, L., 2021, Garcinia L.: A gold mine of future therapeutics, Genet. Resour. Crop Evol., 68 (1), 11–24.

[59] Hoffmann, P., Kathriarachchi, H., and Wurdack, K.J., 2006, A phylogenetic classification of Phyllanthaceae (Malpighiales; Euphorbiaceae sensu lato), Kew Bull., 61 (1), 37–53.

[60] Jantan, I., Haque, M.A., Ilangkovan, M., and Arshad, L., 2019, An insight into the modulatory effects and mechanisms of action of Phyllanthus species and their bioactive metabolites on the immune system, Front. Pharmacol., 10, 878.

[61] Meena, V., Baruah, H., and Parveen, R., 2019, Cassia auriculata: A healing herb for all remedy, J. Pharmacogn. Phytochem., 8 (3), 4093–4097.

[62] Garg, A., and Singh, R., 2015, Antiobesity activity of ethanolic extract of Cassia auriculata in high fat diet induced obese rats, Int. J. Pharm. Pharm. Sci., 7 (4), 237–243.

[63] Singh, M., Singh, S., and Verma, D., 2020, Morphological and pharmacognostical evaluation of Moringa oleifera Lam. (Moringaceae): A plant with high medicinal value in tropical and subtropical parts of the world, Pharmacogn. Rev., 14 (28), 138–145.

[64] WWF and Knorr, 2019, Future 50 Food: A Report, https://www.wwf.org.uk/sites/default/files/2019-02/Knorr_Future_50_Report_FINAL_Online.pdf, accessed on July 30, 2021.

[65] Redha, A.A., Perna, S., Riva, A., Petrangolini, G., Peroni, G., Nichetti, M., Iannello, G., Naso, M., Faliva, M.A., and Rondanelli, M., 2021, Novel insights on anti-obesity potential of the miracle tree, Moringa oleifera: A systematic review, J. Funct. Foods, 84, 104600.

[66] Nahar, S., Faisal, F.M., Iqbal, J., Rahman, M.M., and Yusuf, M.A., 2016, Antiobesity activity of Moringa oleifera leaves against high fat diet-induced obesity in rats, Int. J. Basic Clin. Pharmacol., 5 (4), 1263–1268.

[67] Kim, K.B., and Shin, Y.A. 2020, Males with obesity and overweight, J. Obes. Metab. Syndr., 29 (1), 18–25.

[68] Bao, Y., Xiao, J., Weng, Z., Lu, X., Shen, X., and Wang, F., 2020, A phenolic glycoside from Moringa oleifera Lam. improves the carbohydrate and lipid metabolisms through AMPK in db/db mice, Food Chem., 311, 125948.

[69] Mawa, S., Husain, K., and Jantan, I., 2013, Ficus carica L. (Moraceae): Phytochemistry, traditional uses and biological activities, Evidence-Based Complementary Altern. Med., 2013, 974256.

[70] Arafa, E.S.A., Hassan, W., Murtaza, G., Buabeid, M.A., 2020, Ficus carica and Sizigium cumini regulate glucose and lipid parameters in high-fat diet and streptozocin-induced rats, J Diabetes Res., 2020, 6745873.

[71] Mahajan, N., Rawal, S., Verma, M., Poddar, M., and Alok, S., 2013, A phytopharmacological overview on Ocimum species with special emphasis on Ocimum sanctum, Biomed. Prev. Nutr., 3 (2), 185–192.

[72] Mann, A., 2012, Phytochemical constituents and antimicrobial and grain protectant activities of clove basil (Ocimum gratissimum L.) grown in Nigeria, Int. J. Plant Res., 2 (1), 51–58.

[73] Irondi, E., Agboola, S., Oboh, G., and Boligon, A., 2016, Inhibitory effect of leaves extracts of Ocimum basilicum and Ocimum gratissimum on two key enzymes involved in obesity and hypertension in vitro, J. Intercult. Ethnopharmacol., 5(4), 396–402.

[74] Yumkham, S.D., Elangbam, M., Nongmaithem, R., Naorem, P.D., and Singh, P.K., 2018, Maiden hair ferns (Adiantum L., Pteridaceae–Vittarioideae) of North East India: Diversity, phytochemistry and utilization, Genet. Resour. Crop Evol., 65 (4), 1269–1280.

[75] Jawed, A., Singh, G., Kohli, S., Sumera, A., Haque, S., Prasad, R., and Paul, D., 2018, Therapeutic role of lipases and lipase inhibitors derived from natural resources for remedies against metabolic disorders and lifestyle diseases, S. Afr. J. Bot., 120, 25–32.

[76] Sánchez, J., Priego, T., Palou, M., Tobaruela, A., Palao, A., and Picó, C., 2008, Oral supplementation wit physiological doses of leptin during lactation in rats improves insulin sensitivity and affects food preferences later in life, Endocrinology, 149 (2), 733–740.

[77] Liu, T.T., Liu, X.T., Chen, Q.X., and Shi, Y., 2020, Lipase inhibitors for obesity: A review, Biomed. Pharmacother., 128, 110314.

[78] Olędzka, A., Cichocka, K., Woliński, K., Melzig, M.F., and Czerwińska, M.E., 2022, Potentially bio-accessible metabolites from an extract of Cornus mas fruit after gastrointestinal digestion in vitro and gut microbiota ex vivo treatment, Nutrients, 14 (11), 2287.

DOI: https://doi.org/10.22146/ijc.76873