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\def\RunningAuthor{Preeti Bajpai et al.}
\firstPage{1575}
\articleType{Original Article}
\receivedDate{16.03.2019}
\acceptedDate{08.06.2019}
\revisedDate{05.06.2019}
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\title{An investigation of bioactive and free radical scavenging potential of \textit{moringa Oliefera} leaf extracts}
\author{Uzma~Sayyed\textsuperscript{1},  
            Pratibha~Pandey\textsuperscript{2},  
            Rohit~K.~Tiwari\textsuperscript{1},  
            Rafia~Shekh\textsuperscript{1}, 
            Preeti~Bajpai\textsuperscript{*}\textsuperscript{1}~\\[5pt]{\textsuperscript{1}Department of Bioscience, Integral University, Lucknow, Uttar Pradesh, India}~\\{\textsuperscript{2}Department of Bioengineering, Integral University, Lucknow, Uttar Pradesh, India}}

\begin{abstract}
\textit{Moringa oleifera} Lam, commonly known as Sehjan belongs to the \mbox{}\protect\newline Moringaceae family. It is widely used for the treatment of infectious and inflammatory diseases. This study was an attempt to evaluate the morphological characteristics, percent yield, the bioactive and antioxidant potential of \textit{M. oleifera} leaves that would help in elucidating a promising therapeutic and curative agent for the treatment of different ailments. The maximum percentage yield was obtained in methanolic extract (29.55\%) of \textit{M. oliefera} leaves. Qualitative analysis also revealed the maximum presence of all the metabolites in methanolic extract. Quantitative analysis revealed an appreciable presence of phenol (53.1 mg/g) flavonoids (47.7mg/g) and carotenoids (16.46 mg/g) in \textit{M. oleifera} leaves. The methanolic extract had shown the maximum antioxidant potency in a dose-dependent manner during the evaluation of enzymatic (SOD and CAT) and nonenzymatic (DPPH and FRAP) antioxidants with minimum IC\ensuremath{_{50}} value. Thus, it could be concluded from the present study that methanolic leaf extract of \textit{M. oliefera} could be amongst the principle extract for the antioxidant activity of \textit{M. oliefera}, which could be used for the treatment of several ailments. 
\end{abstract}\def\keywordstitle{Keywords}

\begin{keywords}Moringa oliefera,\newline Leaves,\newline Phytochemical,\newline Antioxidant
\end{keywords}
\twocolumn[ \maketitle {\printKwdAbsBox}]
\makeatletter{\raggedright\textsuperscript{*}Corresponding Author\par Name:\ Preeti~Bajpai~\\ Phone:\ +91-9918040777~\\  Email:\ pbajpai@iul.ac.in
        \par}\vspace*{-11pt}\hrulefill\par{\fontsize{12}{14}\selectfont ISSN: 0975-7538}\par% 
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\section{Introduction}
 Medicinal plants have always been vital for mankind all over the globe since the beginning of life to combat various diseases. Antioxidants contribute towards a plethora of significance in preventing stress by stabilizing or deactivating free radicals caused by several degenerative disease \unskip~\citep{1578661:26369685,1578661:26369688}. Antioxidants present in food are important in lowering oxidative damage to proteins, lipids and nucleic acids induced by free radicals \unskip~\citep{1578661:26369697}. This effect may be due to the presence of phytochemicals and antioxidants present in them including flavonoids and anthocyanins. The Moringaceae family is a monogeneric family with 14 well-known species. Moringa oleifera, commonly known as horseradish tree or drumstick tree and Sahjan in Hindi has widely used species of  moringaceae family ranges in 5 to 10 m height \unskip~\citep{1578661:26369690,1578661:26369686}. It is native to sub-Himalayan areas of northwest India, Africa, Arabia, Southeast Asia, and the Pacific and Caribbean Islands \unskip~\citep{1578661:26369690}. The species is drought resistant and tolerate a wide range of soil and rainfall conditions. For centuries, \textit{M. oleifera} is used as a nutritional supplement with a wide variety of medicinal properties. Various studies have reported that \textit{M. oleifera} leaves are a potent source of protein, vitamins, fatty acids,  \mbox{}\protect\newline 


\begin{table*}[!htbp]
\caption{\boldmath {Qualitative phytochemical analysis of\textit{ M.oleifera} leaves} }
\label{tw-bf7db3ad0632}
\def\arraystretch{1.1}
\ignorespaces 
\centering 
\begin{tabulary}{\linewidth}{p{\dimexpr.0882\linewidth-2\tabcolsep}p{\dimexpr.252\linewidth-2\tabcolsep}p{\dimexpr.4783\linewidth-2\tabcolsep}p{\dimexpr.18150000000000002\linewidth-2\tabcolsep}}
\tbltoprule \rowcolor{kwdboxcolor}S. No. & Phytochemicals  & Name of Test  & References \\
\tblmidrule 
1  &
  Alkaloids &
  Mayer's Test &
  \unskip~\cite{1578661:26369687}\\
2  &
  Saponins &
  Froath foaming Test &
  \unskip~\cite{1578661:26369694}\\
3  &
  Phenolics &
  Ferric Chloride Test &
  \unskip~\cite{1578661:26369702}\\
4  &
  Flavonoids &
  Dilute Ammonia and Conc H2SO4 &
  \\
5  &
  Tannins &
  0.1\% ferric chloride solution &
  \\
6  &
  Terpenoids &
  Salkovaski's Test &
  \\
7  &
  Sterols &
  Chloroform and Conc H2SO4 &
  \\
8  &
  Volatile Oils &
  NaOH and dilute HCl &
  \\
9  &
  Glycosides &
  Glacial acetic acid, ferric chloride and sulphuric acid &
  \\
\tblbottomrule 
\end{tabulary}\par 
\end{table*}
phenolics, flavonoids, carotenoids, moringine, and natural antioxidants such as kaempferol and ascorbic acid \unskip~\citep{1578661:26369683}. Leaves of this plant have been reported to contain different flavonoid such as kaempferol, kaempferitrin, rhamnetin, quercetin and isoquercitrin \unskip~\citep{1578661:26369699}. This plant family is also rich in a fairly unique group of compounds containing the simple sugar rhamnose, glucosinolates and isothiocyanates \unskip~\citep{1578661:26369696}. In India and the Philippines, villager used the leaves of M. oleifera for preparing fatty foods to increase the shelf life of the foods and the presence of a good source of natural antioxidants in it \unskip~\citep{1578661:26369698}. Anwar and Bhange also studied \textit{M. oleifera} as a non-conventional source of oil with significant oxidative stability \unskip~\citep{1578661:26369700}. The efficacy of this plant relies on identifying therapeutically and an industrially valuable compound having medicinal significance.  Therefore, the present investigation is an attempt for the exploration of phytocompounds of \textit{M. oliefera} leaf extracts, evaluation of their bioactive and antioxidant potential that may lead to the development of the promising therapeutic agent for the treatment of various ailments. 
    
\section{Materials and Methods}
\textbf{Chemicals}

All solvents used were of analytical grade. 2, 2Diphenyl1picrylhydrazyl (DPPH), L ascorbic acid, 3(4,5dimethylthiazol2yl) 2,5diphenyltetrazolium bromide, NBT (Nitro- Blue Tetrazolium) dye, were obtained from HiMedia, India. 

\textbf{Collection and Authentication of Plant Materials} \mbox{}\protect\newline The leaves of Moringa oleifera Lam. plant were obtained from the Integral University and authenticated (Authentication No is LS-106) by National \mbox{}\protect\newline Botanical Research Institute (NBRI), Lucknow, India. 

\textbf{Preparation of plant extract}

The crude extracts of leaves were prepared in different polar and nonpolar solvents which included n-hexane, methanol ethanol and aqueous using soxhlet extraction method.

\textbf{Preparation of Extract for Phytochemical Screening} \mbox{}\protect\newline The leaves were taken in separate containers, and 50 ml of solvent (water, methanol, ethanol and hexane) was added followed by rotary shaker for \mbox{}\protect\newline 24 hours. The extracts were centrifuged and stored in 4\text{\textordmasculine} C until use. \mbox{}\protect\newline \textbf{Total phenolic contents (TPC)} \mbox{}\protect\newline Total phenolic content was determined using UV Visible dual beam spectrophotometer (2202, Systronics, India) and optical density was measured at 750 nm \unskip~\citep{1578661:26369693}. \mbox{}\protect\newline \textbf{Total flavonoid content (TFC)} \mbox{}\protect\newline TFC was estimated by the modified method of Park et al., 2008. The optical density was recorded at 506 nm wavelength against the reagent blank \mbox{}\protect\newline \unskip~\citep{1578661:26369692}. \mbox{}\protect\newline \textbf{Total Carotenoids content} \mbox{}\protect\newline Total carotenoids content was determined by the modified method of \unskip~\citep{1578661:26369684}. The absorbance was taken at 480nm against 80\% acetone as blank \unskip~\citep{1578661:26369684}. \mbox{}\protect\newline Carotenoids content was calculated as: \mbox{}\protect\newline Carotenoids (mg/g fresh wt.) = A480 + (0.114 \ensuremath{\times} A663) {\textendash} (0.638 \ensuremath{\times} A645) \mbox{}\protect\newline Where: A = Absorbance at respective wavelengths.


\begin{table}[!htbp]
\caption{\boldmath {Observation of Organoleptic Characteristics of \textit{M.oleifera} Leaves} }
\label{tw-f7c5365a0bda}
\def\arraystretch{1.1}
\ignorespaces 
\centering 
\begin{tabulary}{\linewidth}{LLL}
\tbltoprule \rowcolor{kwdboxcolor}S.No.  & Parameters & Characteristics \\
\tblmidrule 
1. &
  Colour &
  Green\\
2. &
  Odour &
  Pleasant\\
3. &
  Taste &
  Like green beans\\
4. &
  Size &
  1- 5 cm\\
5. &
  Shape &
  Tripinnate\\
6. &
  Touch &
  Smooth\\
7. &
  Season &
  Evergreen\\
\tblbottomrule 
\end{tabulary}\par 
\end{table}

\begin{table}[!htbp]
\caption{\boldmath {Percentage yield of \textit{M.oleifera }Leaves extract in different solvents} }
\label{tw-3cb9d7b5bad2}
\def\arraystretch{1.1}
\ignorespaces 
\centering 
\begin{tabulary}{\linewidth}{LLL}
\tbltoprule \rowcolor{kwdboxcolor}S. No  & Extract  & Percent Yield \\
\tblmidrule 
1  &
  Methanol &
  29.55\\
2  &
  Ethanol &
  27.68\\
3  &
  Aqueous &
  11.05\\
4  &
  Hexane &
  6.8\\
\tblbottomrule 
\end{tabulary}\par 
\end{table}
\textbf{Thin Layer Chromatography} \mbox{}\protect\newline In TLC, the solvent system having better resolution was selected by using a polarity based selection of solvent. The different solvent systems used were  Chloroform: Methanol: H2O (7:3:1), Chloroform: Methanol: H2O (5:4:2), Hexane: Acetone (60:40) etc. The developed TLC plates were observed under ultraviolet light (UV) at both 254 nm and 366 nm. The retention factor (Rf) was used to express the movement of the analyte. Non-Enzymatic Antioxidant Assays DPPH radical scavenging activity \mbox{}\protect\newline The free radical scavenging activity of M. oliefera extracts was determined by 1, 1- diphenyl-2-picrylhydrazyl (DPPH) \unskip~\citep{1578661:26369691}. Ascorbic \mbox{}\protect\newline acid was taken as a standard. DPPH radical scavenging activity was calculated by using the following equation- \mbox{}\protect\newline DPPH Scavenging activity (\%) = (A0-A1/A0) \ensuremath{\times}100. \mbox{}\protect\newline Where A1 is the absorbance of the sample and A0 is the absorbance of the control. All extracts were analyzed in triplicates.

\textbf{Ferric Reducing Antioxidant Power (FRAP) Assay} \mbox{}\protect\newline The ferric reducing activity (FRAP) of the M.oliefera extract was determined by the modified method of Benzie and Strain. The absorbance of the colored product (ferrous tripyridyltriazine complex) was taken at 593 nm. Results were compared with FeSO4 (Ferrous Sulfate), \unskip~\cite{1578661:26369688}.

\textbf{Preparation of plant extract for Antioxidant Assay} \mbox{}\protect\newline The leaves samples (1g) were homogenized in 10 ml of 0.2 mM phosphate buffer (pH 7.8), and the homogenates were centrifuged at 5000 rpm for 10 minutes. The supernatants were collected and used for the different enzymatic assay.


\begin{table*}[!htbp]
\caption{\boldmath {Screening of phytocompounds in different extracts of \textit{M.oliefera}} }
\label{tw-c42afc2c2f44}
\centering 
\begin{threeparttable}

\def\arraystretch{1.1}
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\begin{tabulary}{\linewidth}{p{\dimexpr.2382\linewidth-2\tabcolsep}p{\dimexpr.195\linewidth-2\tabcolsep}p{\dimexpr.1917\linewidth-2\tabcolsep}p{\dimexpr.17509999999999998\linewidth-2\tabcolsep}p{\dimexpr.20\linewidth-2\tabcolsep}}
\tbltoprule \rowcolor{kwdboxcolor} &  & \multicolumn{2}{p{\dimexpr(.3668\linewidth-2\tabcolsep)}}{\cAlignHack Plant Extracts  } & \\
\rowcolor{kwdboxcolor}Phytocompounds  & Methanol & Ethanol  & Aqueous  & Hexane \\
\tblmidrule 
Sterols &
  +++ &
  ++ &
  ++ &
  - \\
Alkaloids &
  +++ &
  +++ &
  ++ &
  ++\\
Tannins &
  +++ &
  ++ &
  -  &
  ++\\
Saponins &
  ++ &
  ++ &
  +++ &
  +++\\
Phenol &
  +++ &
  ++ &
  +  &
  - \\
Flavonoids &
  +++ &
  +++ &
  ++ &
  ++\\
Terpenoids &
  +++ &
  ++ &
  ++ &
  + \\
Glycosides &
  ++ &
  ++ &
  -  &
  ++\\
Volatile oils &
  +  &
  -  &
  ++ &
  - \\
\tblbottomrule 
\end{tabulary}\par 
\begin{tablenotes}\footnotesize 
    
\item{*Values are mean \ensuremath{\pm} SD of triplicates. * `-' symbolizes the absence of phytocompound; *`+' symbolizes the presence of phytocompound; *`++' symbolizes the moderate presence ofphytocompound; *+++ symbolizes the good presence of phytocompound}
\end{tablenotes}
\end{threeparttable}

\end{table*}

\begin{table*}[!htbp]
\caption{\boldmath {Quantitative estimation of phytocompounds in \textit{M.oliefera} Leaves} }
\label{tw-8b77e3c0f32e}
\centering 
\begin{threeparttable}

\def\arraystretch{1.1}
\ignorespaces 
\centering 
\begin{tabulary}{\linewidth}{p{\dimexpr.3662\linewidth-2\tabcolsep}p{\dimexpr.22089999999999996\linewidth-2\tabcolsep}p{\dimexpr.2106\linewidth-2\tabcolsep}p{\dimexpr.2023\linewidth-2\tabcolsep}}
\tbltoprule \rowcolor{kwdboxcolor}Extracts  & Flavonoids & Phenols & Carotenoids \\
\tblmidrule 
Fresh leaves extracted in acetone &
  47.7\ensuremath{\pm}1.12 &
  53.1\ensuremath{\pm}1.07 &
  16.46\ensuremath{\pm}0.19\\
Extracted in Methanol &
  20.1\ensuremath{\pm}0.96 &
  3.85\ensuremath{\pm}0.46 &
  2.21\ensuremath{\pm}0.30\\
Extracted in Ethanol &
  22.4\ensuremath{\pm}1.01 &
  1.90\ensuremath{\pm}0.31 &
  1.70\ensuremath{\pm}0.12\\
Extracted in Hexane &
  32.5\ensuremath{\pm}0.75 &
  1.74\ensuremath{\pm}0.24 &
  1.11\ensuremath{\pm}0.23\\
\tblbottomrule 
\end{tabulary}\par 
\begin{tablenotes}\footnotesize 
    
\item{*Results expressed in mg/gm of fresh leaves. Values are mean \ensuremath{\pm} SD of triplicates.  Phenolics expressed as mg gallic acid equivalents (GAE)/g plant material. Flavonoids  expressed as mg equivalents of quercetin/g plant material. Carotenoids  expressed as mg equivalents of \ensuremath{\beta } carotene/g plant material}
\end{tablenotes}
\end{threeparttable}

\end{table*}
\textbf{Catalase Assay}

Catalase assay measured the rate of decomposition of H\ensuremath{_{2}}O\ensuremath{_{2}} spectrophotometrically at 240 nm for 1 min and was expressed as units/g. \unskip~\citep{1578661:26369701}.

\textbf{Superoxide dismutase (SOD) Assay}

Superoxide dismutase (SOD) activity was assayed by the reduction of nitro blue tetrazolium formazone at 560 nm and was expressed as units/g. \unskip~\citep{1578661:26369689}.

\textbf{Statistical analysis}

All the data were recorded in triplicate (n=3), and results have been expressed as a mean \ensuremath{\pm} standard deviation. The significance of the test was determined using one-way ANOVA by Tukey's test from Graph Pad Prism 5. Statistical significance was set at P {\textgreater}0.001.
    
\section{Results }
\textbf{Antioxidant Studies}


\bgroup
\fixFloatSize{images/144c535a-bc87-464f-a236-5ca37df1c39b-upicture1.png}
\begin{figure}[!htbp]
\centering \makeatletter\IfFileExists{images/144c535a-bc87-464f-a236-5ca37df1c39b-upicture1.png}{\includegraphics{images/144c535a-bc87-464f-a236-5ca37df1c39b-upicture1.png}}{}
\makeatother 
\caption{\boldmath {Antioxidant Activity of different extracts of \textit{M.Oleifera }Leaves by DPPH Assay}}
\label{f-6aa56e68f9b2}
\end{figure}
\egroup

\bgroup
\fixFloatSize{images/494ce5dd-e518-4c02-a486-b6a2a4c21277-upicture2.png}
\begin{figure}[!htbp]
\centering \makeatletter\IfFileExists{images/494ce5dd-e518-4c02-a486-b6a2a4c21277-upicture2.png}{\includegraphics{images/494ce5dd-e518-4c02-a486-b6a2a4c21277-upicture2.png}}{}
\makeatother 
\caption{\boldmath {Antioxidant Activity of different extracts of \textit{M.Oleifera} Leaves by FRAP Assay}}
\label{f-5b4d35d83794}
\end{figure}
\egroup

\bgroup
\fixFloatSize{images/ae9742ee-e310-483d-8027-cf19fbdcc156-upicture3.png}
\begin{figure}[!htbp]
\centering \makeatletter\IfFileExists{images/ae9742ee-e310-483d-8027-cf19fbdcc156-upicture3.png}{\includegraphics{images/ae9742ee-e310-483d-8027-cf19fbdcc156-upicture3.png}}{}
\makeatother 
\caption{\boldmath {Antioxidant Activity of different extracts of \textit{M.} \textit{Oleifera} Leaves by SOD Assay}}
\label{f-d5a3caf2a573}
\end{figure}
\egroup

\bgroup
\fixFloatSize{images/749437df-443f-4c84-87cb-216c319f6219-upicture4.png}
\begin{figure}[!htbp]
\centering \makeatletter\IfFileExists{images/749437df-443f-4c84-87cb-216c319f6219-upicture4.png}{\includegraphics{images/749437df-443f-4c84-87cb-216c319f6219-upicture4.png}}{}
\makeatother 
\caption{\boldmath {Antioxidant Activity of different extracts of \textit{M.} \textit{Oleifera} Leaves by Catalase Assay }}
\label{f-fa93b6f10c66}
\end{figure}
\egroup
The scavenging effect of different extracts of \textit{M. oliefera }leaves on the DPPH and FRAP is illustrated in Figures~\ref{f-6aa56e68f9b2} and~\ref{f-5b4d35d83794}. All the extracts of \textit{M. oleifera } leaf significantly reduced DPPH radicals IC\ensuremath{_{50}} (242.29 \ensuremath{\mu}g/ml) and ferric ion (IC\ensuremath{_{50}} value 250.48 \ensuremath{\mu}g/ml) in a dose-dependent manner. However, the methanolic extract exhibited maximum inhibition with a minimum IC\ensuremath{_{50\ }}value in both assays as depicted in the figure. Similarly, enzymatic antioxidants SOD and catalase significantly neutralized the free radical (312 units/g) and (8246.51 units/g) as observed as depicted in Figures~\ref{f-d5a3caf2a573} and~\ref{f-fa93b6f10c66}. Since ancient times, people have used medicinal plants as a part of their diet as the secondary compounds derived from these plants act as an imperative source of anti-inflammatory agents \unskip~\citep{1578661:26369703}. \textit{M. oleifera } is one of such medicinal plants highly rich in secondary metabolites like phenols, sterols, glycosides, flavonoids and terpenoids. Many of these phytocompounds have been reported to possess potential antioxidants activity \unskip~\citep{1578661:26369695}. Both the qualitative and quantitative estimation in our study also revealed the presence of a high quantity of flavonoids, phenols and carotenoids in the leaf extracts of \textit{M oleifera. } Considering this the extracts were evaluated for their antioxidant potential by non-enzymatic DPPH radical and FRAP assay as well as enzymatic SOD and Catalase assay. The methanolic leaf extract was found to exhibit significant antioxidant activity among all the other extracts as revealed by DPPH and FRAP assay. The results obtained by the enzymatic assay also determined the presence of high free radical scavenging activity in a dose-dependent manner. Similar results have also been reported by \unskip~\cite{1578661:26369685} stating the potential antioxidant activity by the mature \textit{Moringa oleifera } leaves \unskip~\citep{1578661:26369685}. The potential scavenging abilities present in the different extracts of \textit{M. oliefera } may be due to the appreciable presence of polyphenols and flavonoids which prevents oxidative damage and retains the internal uniformity in the plants. The pronounced presence of these phytocompounds instigated us to focus on the purification and characterization of a potential compound from the leaves of \textit{M. oleifera}.

\textbf{Acknowledgements}

We would also like to extend our thanks to Integral University communication cell, Lucknow, U.P., India for quick and crisp review of the manuscript (MCN No-IU/R\&D/2017-MCN000142) and providing needful suggestions and UGC-MANF, Delhi, India for financial assistance.

\textbf{Conflict of interest}

The authors declare no conflict of interest. 
    

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