The synergistic effects of Moringa Peregrina and Murraya koenigii leaf extracts on antimicrobial activity (against Candida albicans and Helicobacter pylori), antioxidant, and lipase inhibitory properties

Document Type : Original research

Authors

1 Department of Food Sciences & Technology, TeMS.C., Islamic Azad University, Tehran, Iran

2 Department of Food Science and Technology, ShQ. C., Islamic Azad University, Shahr-e Qods, Iran

3 Department of Science, Payame Noor University, Tehran, Iran

4 Department of Agriculture, Payame Noor University, Tehran, Iran

Abstract

This research aimed to evaluate the antimicrobial, antioxidant, and lipase inhibitory properties of leaf extracts from
Moringa peregrina (M. peregrina) and Murraya koenigii (M. koenigii). Antioxidant capacity was assessed using the
ABTS method, while total phenol content was measured via the Folin-Ciocalteu method. The antifungal activity
against Candida albicans was determined through zone inhibition assays, and the ability to inhibit Helicobacter
pylori was evaluated by measuring urease enzyme activity. Lipase activity inhibition was assessed using ELISA at
405 nm. Analysis of variance revealed that increasing concentrations of both extracts significantly enhanced
antioxidant activity and total phenol content (p<0.05). M. peregrina and M. koenigii exhibited the highest
antioxidant activity at 4000 mg/L, while M. koenigii showed the lowest activity at 31.25 mg/L. The highest total
phenol content occurred at 4000 mg/L for M. koenigii. Synergistic effects of both extracts were noted at 1000 mg/L.
At 1500 mg/L, M. peregrina displayed the largest inhibition zone against Candida albicans; conversely, M. koenigii
showed the strongest inhibition of Helicobacter pylori at 2000 mg/L. The greatest lipase inhibitory activity was
found at 4000 mg/L for M. peregrina, while M. koenigii had the least at 2000 mg/L, and there were no synergistic
effects. These findings suggest that M. peregrina and M. koenigii leaf extracts have potential applications in
developing anti-diabetic food products. 

Keywords

Main Subjects

Abdulkarim, S., Long, K., Lai, O., Muhammad, S. & Ghazali, H. (2005).
Some physico-chemical properties of Moringa oleifera seed oil
extracted using solvent and aqueous enzymatic methods. Food
Chemistry, 93, 253-263.
https://doi.org/10.1016/j.foodchem.2004.09.023.
Al Harbi, H., Irfan Uma, M., & Ali, S. (2016). The antibacterial effect of
curry leaves (murraya koenigii). European journal of
pharmaceutical and medical research, 3(10), 387-382.
AL Juhaimi, F., Ghafoor., K., Babiker, E. E., Matthaus, B, & Ozcan, M. M.
(2017). The Biochemical composition of the leaves and seeds
meals of Moringa species as non-conventional sources of
nutrients. Journal of Food Biochemistry, 41(1), 1-7.
https://doi.org/10.1111/jfbc.12322.
Baltas, N., Alpay Karaoglu, S., Tarakci, C., & Kolayli, S. (2016). Effect of
propolis in gastric disorders: inhibition studies on the growth of
and Helicobacter pylori production of its urease. Journal of
Enzyme Inhibition and Medicinal Chemistry, 31(S2), 46-50.
https://doi.org/10.1080/14756366.2016.1186023.
Bamishaiye, E. I., Olayemi, F.F., Awagu, E. F., & Bamshaiye, O. M. (2011).
Proximate and phytochemical composition of Moringa oleifera
leaves at three stages of maturation. Advance Journal of Food
Science and Technology, 3, 233-237.
https://doi.org/10.9734/afsj/2021/v20i1030363.
Bhushan, P. R., Sandip, C. P., & Mahendra, D. (2020). Synergistic
antibacterial activity of Murraya koenigii and Cynodon dactylon
against pathogenic strains. World Journal of Advanced Research
and Reviews, 5 (3), 124–128.
https://doi.org/10.30574/wjarr.2020.5.3.0063.
Burt, S. (2004). Essential oils: their antibacterial properties and potential
applications in foods-a review. Journal of Food Microbiology, 94,
223–253. https://doi.org/10.1016/j.ijfoodmicro.2004.03.022.
Carloni, P., Tiano, L., Padella, L., Bacchetti, T., Customu, C., Kay, A., &
Damiani E. (2013). Antioxidant activity of white, green and black
tea obtained from the same tea cultivar. Food Research
International. 53 (2), 900-908.
https://doi.org/10.1016/j.foodres.2012.07.057.
Chater, P. I., Wilcox, M., Cherry, P., Herford, A., Mustar, S., Wheater, H.,
Brownlee, I., Seal, C., & Pearson J. (2016). Inhibitory activity of
extracts of Hebridean brown seaweeds on lipase activity. Journal
of Applied Phycology, 28, 1303–1313.
https://doi.org/10.1007/s10811-015-0619-0.
Chelliah R., Ramakrishnan S, Antony, U. (2017). Nutritional quality of
Moringa Oleifera for its bioactivity and antibacterial properties.
International Food Research Journal. 24, 825-833.
https://doi.org/10.47262/bl/9.1.20230115.
Chowdhury, B. K., Jha, S., Bhattacharyya, P., Z., & Mukherjee, J. 2001. Two
new carbazole alkaloids from Murraya koenigii. Indian Journal
of Chemistry. 40, 494-490. https://doi.org/10.1002/chin.2001
40212.
Ching, L. S., & S, Mohamed. (2001). Alpha-Tocopherol Content in 62 Edible
Tropical Plants. Journal of Agricultural and Food Chemistry.
49(6), 3101-5. https://doi.org/10.1021/jf000891u.
Das, A., Rajkumar, V., & Dwivedi, D. (2011). Antioxidant effect of curry
leaf (Murraya koenigii) powder on quality of ground and cooked
goat meat. International Food Research Journal, 18, 559-565.
Dhongade, H., Sawarkar, H., Muley, B., Deshmukh, V., & Pande, A. (2013).
Therapeutic potentials of Murraya koenigii Spreng (Rutaceae).
Indo American Journal of Pharmaceutical Research, 3, 7399-
7412.
Erkan, N., Tao, Z., Rupasinghe, H. V., Uysal, B., & Oksal, B. S. (2012).
Antibacterial activities of essential oils extracted from leaves of
Murraya koenigii by solvent-free microwave extraction and
hydro-distillation. Natural Product Communications, 7(1).
https://doi.org/10.1177/1934578X1200700139.
El–Mohamedy, R, S., & Abdalla, A.M )2014). Evaluation of antifungal
activity of Moringa oleifera extracts as natural fungicide against
some plant pathogenic fungi In-vitro. Journal of Agricultural
Technology, 10(4), 963-982.
Faizi, S., Siddiqui, B., Saleem, R., Aftab, K., Shaheen, F., & Gilani, A.
(1998). Hypotensive constituents from the pods of Moringa
oleifera. Planta Med. 64, 225-228.
Farooq, F., Rai, M., Tiwari, A., Khan, A.A., & Farooq, S. (2012). Medicinal
properties of Moringa Oleifera: An overview of Promising
Healer. J. Med. Plants. Res. BMC Complementary and Alternative
Medicine, 6(27): 4368-74. https://doi.org/10.5897/JMPR12.279.
Fatma, A., Kumar, S., & Khan, S. A. (2013). Estimation of total phenolic
content, in-vitro antioxidant and anti-inflammatory activity of
flowers of Moringa Oleifera. Asian Pacific. Journal of
Biomedical Physics and Engineering, 3(8), 623-627.
https://doi.org/10.5897/JMPR12.279.
Ghasemzadeh, A., Jaafar H. Z., Rahmat,,A., & Devarajan T. (2014).
Evaluation of bioactive compounds, pharmaceutical quality, and
anticancer activity of Curry Leaf (Murraya koenigii L.). Hindawi
Publishing Corporation Evidence-Based Complementary and
Alternative Medicine, 873803.
https://doi.org/10.1155/2014/873803.
Gutierrez, D., Weinstock, A., Antharam, V., Gu, H., Jasbi, P., Shi, X. &
Thangamani, S. )2020). Antibiotic-induced gut metabolome and
microbiome alterations increase the susceptibility to Candida
albicans colonization in the gastrointestinal tract. FEMS
Microbiology Ecology, 96(1), 1-15.
https://doi.org/10.1093/femsec/fiz187.
Igara, C. E., D. Omoboyowa, A., Ahuchaogu, A. A., Orji, N. U., & Ndukwe,
M. K. (2016). Phytochemical and nutritional profile of Murraya
Koenigii (Linn) Spreng leaf. Journal of Pharmacognosy and
Phytochemistry, 5(5), 7-9.
https://doi.org/10.1007/springerreference68981.
Iqbal, S., & Bhanger, M. I. (2006). Effect of season and production location
Dashtlali et al. JFBE 7(2): 84-92,2024
91
on antioxidant activity of Moringa oleifera leaves grown in
Pakistan. Journal of Food Composition and Analysis. 19, 551-
554. https://doi.org/10.1016/j.jfca.2005.05.001.
Kaewpiboon, C., Lirdprapamongkol, K., Srisomsap, C., Winayanuwattikun,
P., Yongvanich, T., Puwaprisirisan, P., Svasti, J., &
Assavalapsakul, W. (2012). Studies of the in vitro cytotoxic,
antioxidant, lipase inhibitory and antimicrobial activities of
selected Thai medicinal plants. BMC Complementary and
Alternative Medicine. 12, 217.
https://doi.org/10.1186/1472688212-217.
Kesari, A. N., Gupta, R. K., & Watal, G. (2005). Hypoglycemic effects of
Murraya koenigii on normal and alloxan diabetic rabbits. Journal
of Ethnophamarcology, 97, 247–251.
https://doi.org/10.1016/j.jep.2004.11.006.
Kumar, E., Harsha, K., Shaik, S., Rao, N. N., & Babu, N. G. (2013). In vitro
antioxidant activity and in vivo hepatoprotective activity of
Moringa Oleifera seeds extract against ethanol induced liver
damage in wistar rats. IOSR Journal of Pharmacy, 3(1)10-15.
https://doi.org/10.9790/3013-31401015.
Lalas, S., Athanasiadis, V., Karageorgou, I., Batra, G., Nanos, G. D., &
Makris, D. P. (2017). Nutritional characterization of leaves and
herbal tea of Moringa Oleifera cultivated in Greece. J. Herbs,
Spices & Med. Plants 23(4), 320–333.
https://doi.org/10.1080/10496475.2017.1334163.
Lamou, B., Taiwe, G. S., Hamadou, A., Abene, Houlray, J., Atour, M. M., &
Tan, P. V. (2016). Antioxidant and antifatigue properties of the
aqueous extract of Moringa oleifera in rats subjected to forced
swimming Endurance test. Oxidative Medicine and Cellular
Longevity. 3517824. https://doi.org/10.1155/2016/3517824
Lin, M., Zhang, J., & Chen, X. (2018). Bioactive flavonoids in Moringa
oleifera and their health promoting properties. Journal of
Functional Foods. 47:469-479.
https://doi.org/10.1016/j.jff.2018.06.011.
Liu, T., Liu, X., Chen, Q., & Shi, Y. (2020). Lipase Inhibitors for Obesity:
A Review. Biomedicine & Pharmacotherapy, 128, 110314.
https://doi.org/10.1016/j.biopha.2020.110314.
Mahdavi, D. L., Deshpande, S. S. & Salunkhe, D. K. (1996). Food
Antioxidant. 1 edn. New York: Marcel Dekker, Inc, U.S.A. 512p.
https://doi.org/10.1201/9781482273175.
Mahfuza Shaplaa, U., Raihana, J., Islamb, A., Alamb, F., Solayman, N., &
Hua Ganb, S. )2018). Propolis: The future therapy against
Helicobacter pylori-mediated gastrointestinal diseases. Journal of
Applied Biomedicine, 16(2), 81-99.
https://doi.org/10.1016/j.jab.2017.10.007.
Mayer, F., Wilson, D., & Hube, B., (2013). Candida albicans pathogenicity
mechanisms. Virulence, 4(2), 119-128.
https://doi.org/10.4161/viru.22913.
McDougall, G., N. Kulkarni, N., & Stewart, D. )2009). Berry polyphenols
inhibit pancreatic lipase activity in vitro. Food Chemistry, 115:
193–199. https://doi.org/10.1016/j.foodchem.2008.11.093.
Mensah, J. K., Ikhajiagbe, B., Edema, N. E., Emokhor, J. (2012).
Phytochemical, nutritional and antibacterial properties of dried
leaf powder of Moringa oleifera (Lam.) from Edo Central
Province, Nigeria. J. Nat. Prod. Plant Resour, 2(1),107-112.
Mothana, R. A., Lindequist, U., Gruenert, R., & Bednarski, P. J. (2009).
Studies of the in vitro anticancer, antimicrobial and antioxidant
potentials of selected Yemeni medicinal plants from the island
Soqotra. BMC complementary and alternative medicine, 9(1), 7.
https://doi. org/10.1186/1472-6882-9-7.
Nabati, F., Mojab, F., Habibi-Rezaei, M., Bagherzadeh, K., Amanlou, M., &
Yousefi, B. (2012). Large scale Screening of commonly used
Iranian traditional medicinal plants against urease activity.
Journal of Pharmaceutical Siences, 14 (72), 943–947.
https://doi.org/10.1186/2008-2231-20-72.
Ningappa, M. B., Dinesha, R., Srinivas, L. (2008). Antioxidant and free
radical scavenging activities of polyphenol-enriched curry leaf
(Murraya koenigii L.) extracts. Food Chemistry, 106, 720-728.
https://doi.org/10.1016/j.foodchem.2007.06.057.
Noui Mehidi, I., Ait Ouazzou, A., Tachoua, W., & Hosni, K. (2024).
Investigating the Antimicrobial Properties of Essential Oil
Constituents and Their Mode of Action. Molecules, 29(17), 4119.
https://doi.org/10.3390/molecules29174119.
Omankutty, A. M, Rajaraman, K., Sankarakutty, B., Sumathikutty, M. A.,
Padmakumari, K. P., Narayanan, C. S. (1984). Processing of curry
leaves. Indian Food Packer, 32-36.
Oyedepo TA, Babarinde SO, Ajayeoba TA. (2013). Evaluation of the
antihyperlipidemic effect of aqueous leaves extract of Moringa
oleifera in alloxan induced diabetic rats. International Journal of
Biochemistry Research, 3, 162-170.
https://doi.org/10.9734/ijbcrr/2013/3639.
Pal, S. K., Mukherjee, P. K., & Saha, B. P. (1995). Studies on the antiulcer
activity of Moringa oleifera leaf extract on gastric ulcer models in
rats. Phytother Res, 9, 463–465.
https://doi.org/10.1002/ptr.2650090618.
Pari, L., & Ashok Kumar, N. (2002). Hepatoprotective activity of Moringa
Oleifera on antitubercular drug-induced liver damage in rats.
Journal of Medicinal Food, 5(3), 171-177.
https://doi.org/10.1089/10966 200260398206.
Patel, P., Patel, N., Patel, D., Desai, S., & Meshram, D., (2014(.
Phytochemical analysis and antifungal activity of moringa
oleifera. International Journal of Pharmacy and Pharmaceutical
Sciences, 6(5), 144-147.
Patil, R., Dhawale, K., Gound, H., &Gadakh, R. )2012(. Protective effect of
leaves of Murraya koenigii on reserpine-induced orofacial
dyskinesia. Iranian Journal of Pharmaceutical Research, 11(2),
635-641.
Khanna, S., Raj., N & aparna, K. C. (2015). Moringaoleifera and obesity: a
review. International Journal of Advanced Research in
Engineering and Applied Sciences, 4, 1-23.
https://doi.org/10.63665/ijareas.
Kim, Y. S., Leea, Y. M., Kim, H., Kim, J., Janga, D. S, Kimb J. H, Kim, J. S.
)2010). Anti-obesity effect of Morus bombycis root extract: Antilipase activity and lipolytic effect. Journal of
Ethnopharmacology, 130, 621–624.
https://doi.org/10.1016/j.jep.2010.05.053.
Rajendran, M. P., Pallaiyan B. B., & Selvaraj N. )2014). Chemical
composition, antibacterial and antioxidant profile of essential oil
from Murraya koenigii (L.) leaves. Avicenna journal of
phytomedicine, 4(3), 200–214.
https://doi.org/10.22038/ajp.2014.2564.
Rao, K. S., & Mishra, S. H. (1998). Anti-inflammatory and antihepatoxic
activities of the roots of Moringa pterygosperma Gaertn. Indian
Journal of Pharmaceutical Sciences, 60, 12–16.
Koneni V, Sashidhara., Jammikuntla N, Rosaiah., E, Tyagi., R, Shukla., R,
Raghubir., & Siron M, Rajendran. (2009). Rare dipeptide and urea
derivatives from roots of Moringa oleifera as potential antiinflammatory and antinociceptive agents. European Journal of
Medicinal Chemistry, 44(1), 432-436.
https://doi.org/10.1016/j.ejmech .2007.12.018.
Siddhuraju, P., & Becker, K. (2003). Antioxidant properties of various
solvent extracts of total phenolic constituents from three different
agroclimatic origins of drumstick tree (Moringa oleifera Lam.)
leaves. J. Agric. Food Chemistry. 51, 2144-2155.
https://doi.org/10.1021/jf020444.
Sivasankari, B., Anandharaj, M., & Gunasekaran, P. (2014). An
ethnobotanical study of indigenous knowledge on medicinal
plants used by the village peoples of Thoppampatti, Dindigul
district, Tamilnadu, India. Journal of Ethnopharmacology, 153,
408-423. https://doi.org/10.1016/j.jep.2014.02.040.
Tee, ES., & Lim, C. L. (1991). Carotenoid composition and content of
Malaysian vegetables and fruits by the AOAC and HPLC
methods. Food Chemistry, 41, 309-339.
https://doi.org/10.1016/0308-8146(91)90057-u.
Tripathi, Y. C., Nishat Anjum., & Ashish Rana. (2018). Chemical
composition and in vitro antifungal and antioxidant activities of
essential oil from Murraya koenigii (L.) Spreng leaves. Asian
Journal of Biomedical and Pharmaceutical Sciences, 8, 65.
https://doi.org/10.4066/2249-622x.65.18-729.
Monica A, Valdez-Solana., Veronica Y, Mejía-García., Alfredo TellezValencia., Guadalupe Garcia-Arenas., Jose Salas-Pacheco., Jose
Dashtlali et al. JFBE 7(2): 84-92,2024
92
J. Alba-Romero., & Erick Sierra-Campos (2015). Nutritional
content and elemental and phytochemical analyses of Moringa
Oleifera grown in Mexico. Journal of Chemistry. 1, 860381.
https://doi.org/10.1155/2015/860381 .
Vergara-Jimenez, M., Manal Mused Almatrafi., & Maria Luz Fernandez.
(2017). Bioactive components in Moringa Oleifera leaves protect
against chronic disease. Antioxidants, 6(4), 91.
https://doi.org/10.3390/antiox6040091.
Walter, A., Samuel, W., Peter, A., & Joseph, O. (2011). Antibacterial activity
of Moringa oleifera and Moringa stenopetala methanol and Nhexane seed extracts on bacteria implicated in water borne
diseases. African Journal of Microbiology Research, 5, 153-157.
https://doi.org/ 10.5897/AJMR10.457.
Zida, A., Bamba, S., Yacouba, A., Ouedraogo-Traore R., & Guiguemde R.
T. (2017). Anti-Candida albicans natural products, sources of new
antifungal drugs: A review. Journal de Mycologie Medicale, 27
(1), 1-19. https://doi.org/10.1016/j.mycmed.2016.10.002 .