0% found this document useful (0 votes)
25 views8 pages

100 1688327937

This study examined the phytochemical compounds, antioxidant capacity, and antibacterial effects of okra fruit extracts at different maturity stages. Okra fruits were collected at three maturity stages: early, mid, and late stage. The extracts were tested for total phenolic content, total flavonoid content, and antioxidant and antibacterial activities. The results showed that the mid-stage maturity okra fruits had the highest levels of total phenolics and flavonoids as well as the strongest antioxidant and antibacterial effects against Vibrio anguillarum, indicating they are an excellent source of bioactive compounds. The phytochemical compounds and bioactivities decreased in the late stage fruits.

Uploaded by

G
Copyright
© © All Rights Reserved
We take content rights seriously. If you suspect this is your content, claim it here.
Available Formats
Download as PDF, TXT or read online on Scribd
0% found this document useful (0 votes)
25 views8 pages

100 1688327937

This study examined the phytochemical compounds, antioxidant capacity, and antibacterial effects of okra fruit extracts at different maturity stages. Okra fruits were collected at three maturity stages: early, mid, and late stage. The extracts were tested for total phenolic content, total flavonoid content, and antioxidant and antibacterial activities. The results showed that the mid-stage maturity okra fruits had the highest levels of total phenolics and flavonoids as well as the strongest antioxidant and antibacterial effects against Vibrio anguillarum, indicating they are an excellent source of bioactive compounds. The phytochemical compounds and bioactivities decreased in the late stage fruits.

Uploaded by

G
Copyright
© © All Rights Reserved
We take content rights seriously. If you suspect this is your content, claim it here.
Available Formats
Download as PDF, TXT or read online on Scribd
You are on page 1/ 8

Open Veterinary Journal, (2023), Vol.

13(12): 1562–1569
ISSN: 2226-4485 (Print) Original Research
ISSN: 2218-6050 (Online) DOI: 10.5455/OVJ.2023.v13.i12.6

Submitted: 09/07/2023 Accepted: 20/11/2023 Published: 31/12/2023

Phytochemical compounds, antiradical capacity, and in vitro inhibitory effect


against fish pathogenic bacteria of okra fruits (Abelmoschus esculentus L.) at
different maturity stages
Salma Guebebia1* , Abdalla A. Mohamed2 , Cristóbal Espinosa-Ruiz3 , Maria Ángeles Esteban3 ,
Lazhar Zourgui4 and Mehrez Romdhane1
1
Laboratory of Energy, Water, Environment and Process (LR18ES35), National School of Engineers of Gabes
(ENIG), University of Gabes, Gabes, Tunisia
2
Biomedical Research Team, Department of Medical Nutrition, Faculty of Medical Technology, University of Zawia,
Zawia, Libya
3
Immunobiology for Aquaculture Group, Department of Cell Biology and Histology, Faculty of Biology, Campus
Regional de Excelencia Internacional “Campus Mare Nostrum,” University of Murcia, Murcia, Spain
4
Research Unit of Active Biomolecules Valorisation, Department of Biological Engineering, Higher Institute of
Applied Biology of Medenine (ISBAM), University of Gabes, Gabes, Tunisia

Abstract
Background: Abelmoschus esculentus L., okra, has been known as a healthy plant and classically employed in food
and folk medicine for several human and animal diseases.
Aim: The in vitro antioxidant and antibacterial capacities, in addition to the phytochemical compounds of the okra fruit
extracts gathered at three maturity stages, were the objectives of this study.
Methods: This study examined the modifications in total phenolic content (TPC), total flavonoid content (TFC), and
antioxidant and antibacterial capacities of three okra fruit hydroalcoholic extracts during three comestible maturity
stages. The different maturity stages of okra pods were demonstrated as early-stage, mid-stage, and late-stage
maturation.
Results: The mid-stage of okra fruit maturity had the highest TPC (43.27 ± 2.029 mg GAE g−1), TFC (29.96 ± 0.19
mg RE g−1), and antioxidant capacity (75.64% ± 0.79%). Moreover, at mid-stage maturity, okra fruit extracts exhibited
a major antibacterial effect against Vibrio anguillarum. The phenolic content was significantly increased at the mid-
stage maturity, while the flavonoid level and the antioxidant activity were greatly decreased at the end of fruit maturity.
Conclusion: The results confirmed that A. esculentus L. fruits at mid-stage maturity are an excellent source of
biomolecules with high antiradical and bactericidal activities, which could be used as functional foods and as an option
for chemical compounds for fish farming to prevent and treat numerous marine animal diseases.
Keywords: Okra fruits, Phenolic compounds, Antioxidant capacity, Antibacterial activity, Maturity stage.

Introduction received more and more attention and has been studied,
Since immemorial times vegetables have played a due to their low toxicity than synthetic antioxidants
vital role in traditional diets. In addition, vegetables which explains the increased attention to plants with
are functional foods used as nutrition and herbal therapeutic potential in recent years (Umme et al.,
medicines, thanks to their abundant bioactive medicinal 2023). Besides, many studies have confirmed that plant
molecules and chemical properties (Poobalan et al., species are traditionally used as medicinal plants due
2019). A noticeable amount of work has been carried to their antibacterial and antifungal agents (Erfan and
out on the richness of vegetable extracts in phenol Marouf, 2019).
and flavonoid contents with a growing interest in the Abelmoschus esculentus L. also called okra, lady’s
food industry and the medical field (Mohammed et finger, and gumbo included in the Malvaceae family
al., 2016). Then, natural antioxidants are ubiquitous (Dhruve et al., 2015). The plant is an essential
in fruits and vegetables known as medicinal plants. vegetable culture widely progressed in Africa, Asia,
Currently, the demand for biological antioxidants has Southern Europe, and America, mostly in tropical, sub-

*Corresponding Author: Salma Guebebia. Laboratory of Energy, Water, Environment and Process (LR18ES35), National
School of Engineers of Gabes (ENIG), University of Gabes, Gabes, Tunisia. Email: salmaguebebia1992@gmail.com
Articles published in Open Veterinary Journal are licensed under a Creative Commons Attribution-NonCommercial 4.0 International License

1562
http://www.openveterinaryjournal.com
S. Guebebia et al. Open Veterinary Journal, (2023), Vol. 13(12): 1562–1569

tropical, and warm temperate regions (Xia et al., 2015). plant material samples were stored at 4°C in the dark
Okra is a multifunctional plant thanks to its different until their analysis. Besides, ethanol (70%) (PanReac
uses of pods, leaves, flowers, and seeds (Habtamu et AppliChem) was used for the preparation of extracts
al., 2014). Furthermore, medicinally several diseases as a safe solvent for both food and natural medicinal
are treated using this plant. Abelmoschus esculentus purposes. Then, ethanol/water has been used to extract
L. and its constituents have many bioactivities such as strongly phenolic and antioxidant compounds from
cardioprotective, renal, neuroprotective, anti-fatigue, natural substances (Sultana et al., 2009).
anti-cancer, antimicrobial, and hypoglycemic activities Extracts were prepared by microwave extraction.
(Solomon et al., 2016). Briefly, 1 g of each dried powdered okra fruit, was
Furthermore, okra fruit is a green-colored capsule mixed with 25 ml of ethanol (70%) solution. Samples
containing numerous seeds. Abelmoschus esculentus L. of microwave-assisted extractions were carried at 100
fruit is slightly curved measuring up to about 5–10 W for 2 minutes. After that, all mixed samples were
cm long and 1.5–3 cm in diameter (Lengsfeld et al., filtered using a 100 µm pore size nylon net filter before
2004). Moreover, thanks to their wealth in secondary their centrifugation at 8,000 g for 10 minutes. Then, the
metabolites, okra fruit extract has multiple bioactivities. supernatants are collected, filtered, and stored at 4°C
Thus, A. esculentus L. fruit extract contains mostly until utilized. In conformity with Elik et al. (2017) with
phenolic compounds, flavonoids, and tannins (Saha some modifications, the solid–liquid extraction was
et al., 2011). Various studies have confirmed that provided.
okra fruit phenolic compounds deliberated the Determination of okra fruit weight, length, and diameter
principal responsible for its biological effects, such as The harvested fruit was transported in a closed plastic
antioxidant, anti-diabetic, and antibacterial properties sack to the laboratory. After that, the length and
(Jiang et al., 2017; Zhang et al., 2018). Besides, diameter (size) of the fruit were measured. In addition,
cultivars, growing conditions, and fruit sizes can swing fruit weight was resolved using an electronic balance.
okra fruit phenolic content and their bioactivities. Determination of phenolic contents
Particularly, the quality of the harvested okra fruit is As a principal quantitative analysis, the total phenolic
linked to their size proportional to time (Petropoulos content (TPC) of okra fruit extracts was determined
et al., 2018). However, huge variation in level and using the Folin–Ciocalteu’s approach following the
chemical composition has been noted between the procedure described previously by Singleton and
harvest stage of okra pods (Piloo and Kabir, 2011). Lamuela-Raventos (2012) with modifications.
Besides, once okra fruit reaches a length of 3–5 cm, Briefly, 0.4 ml of fruit extract was reacted with 2 ml
it is collected in the Mediterranean countries contrary of Folin–Ciocalteu reagent (LOBA Chemie). Then,
to other markets of the world where the harvested okra 1.6 ml of Na2CO3 (Chemi-Pharma) solution (7%) was
fruit size is longer (7–12 cm or larger) (Petropoulos et added to each sample with simple agitation. Following
al., 2018). that, the absorbance was measured using a UV-visible
Whereas, A. esculentus L. fruit is the most consumed spectrophotometer (T60 UV-visible spectrophotometer)
part of the plant. Hence, for the reason of studying the after 45 minutes in the dark conditions at room
phenolic compounds in okra fruits, this work aims to temperature. All measurements were performed at
evaluate A. esculentus L. fruits at three marketable sizes a wavelength = 765 nm. The data were expressed in
to reveal ripe-stage extract with high levels of phenolic milligrams of gallic acid per gram (mg GAE g−1) of dry
and flavonoid compounds as well as to compare their sample.
antiradical and antibacterial activities from okra fruit Determination of flavonoid contents
produced in Gabes, Tunisia. The total flavonoid content (TFC) was measured as per
the colorimetric method of Bahroun et al. (1996) with
Materials and Methods minor modifications. Besides, 1 ml of each okra fruit
Plant material and sample preparation aliquot was mixed with 1 ml of an aluminum solution
Abelmoschus esculentus L. fresh fruits were harvested (AlCl3 10%) (LOBA Chemie). After an incubation of 30
separately at three maturity stages based on the fruits’ minutes, the measurement of absorbance at 430 nm was
morphology (size) from July to September 2020 from a determined. The results were expressed as milligrams
local farm (Gabes, Tunisia). The three maturity stages of rutin equivalent per gram of dry extract (mg RE g−1).
were consumables. The samples were established as Determination of total antioxidant activity using the
early-stage maturity, mid-stage maturity, and late-stage DPPH method
maturity. The total antioxidant activity was determined using the
Afterward, to get rid of the foreign materials, samples DPPH method. The ability to scavenge DPPH radicals
were washed extensively with distilled water. After was performed using the method illustrated previously
that, they were sliced into portions of 5 mm. As by Velazquez et al. (2003). Briefly, each extract (0.75
well, until their masses stabilized, they were parched ml) was combined with 1.5 ml of DPPH solution
at 40°C for 6 days. Then, they were powdered and in methanol 90% (20 mg l−1). After that, the mixture
sieved before being sifted to a smooth powder. Finally, was incubated for 15 minutes at room temperature

1563
http://www.openveterinaryjournal.com
S. Guebebia et al. Open Veterinary Journal, (2023), Vol. 13(12): 1562–1569

and the absorbance was measured at 517 nm using a the dissolved formazan was then measured at 570 nm.
spectrophotometer. In this analysis, we have zeroed The bacterial capacity was expressed as a percentage
the spectrophotometer with methanol. On the other of viable bacteria, measured by the difference between
hand, we have considered DPPH radical absorbance the absorbance of the existing bacteria in test samples
without extract as a control. All tests were performed and the absorbance of bacteria from positive controls
in triplicate. (100%).
The antioxidant activity was expressed as a percentage Statistical analysis
inhibition using the following formula: All analyses were realized in triplicates and the
Inhibition (%) = [(AB − AS) / AB] × 100 experimental data were reported as means ± SEM.
where AS is the sample (tested extract solution) One-factor analysis of variance analyses using Xlstat
absorbance and AB is the blank absorbance. software were used to evaluate the statistical differences
Evaluation of bactericidal activity among the treatments. The significance level was 95%
Pathogens and growth conditions in all cases (p < 0.05) and was assessed using the Tukey
To evaluate the bactericidal effect of A. esculentus test.
L. fruit extract at three ripening stages, pathogenic Ethical approval
bacteria for fish (Vibrio anguillarum) were adopted. Not needed for this study.
The sterilized tryptic soy agar (Difco Laboratories) was
used to cultivate the bacteria. Thus, single colonies were Results
first inoculated in tryptic soy broth 30 g l−1 (TSB, Difco Weight, length, and diameter of okra fruits at different
Laboratories). Then, they were enhanced with NaCl maturation stages
until reaching a final concentration of 1% (w/v), for 24 The changes in physical properties [fruit weight (g),
hours at 25°C with continuous agitation. Considerably length (cm), and diameter (cm)] of A. esculentus L.
proliferating bacteria were washed and resuspended in fruits at different maturity stages are indicated in
sterile PBS at 108 cfu ml−1. Table 1. Furthermore, during maturation, the weight,
The in vitro bactericidal activity of the okra extracts length, and diameter of fresh okra fruits increased
was estimated using the method described by Stevens considerably. In addition, the maximum level was
et al. (1991) with minor modifications. achieved at the end of maturation.
Antibacterial assay Extracts phenolic compound contents
In this bactericidal assay, aliquots of 20 µl the The main phenolic compounds present in ethanolic A.
bacterial suspensions were conducted in each well of esculentus L. fruit extracts are represented in Figure
a flat-bottomed plate (96-well plate). Then, they were 1. In the current research, the phenolic contents were
incubated (5 hours, 25°C) with 20 µl of each tested present in important quantities in all maturation stages
extract (0.5 mg ml−1). After that, instead of the extracts, of okra extracts.
PBS solution was inserted into some wells as a positive Although, the mid-maturation stage of okra fruit extract
control. While, to evaluate the growth of bacteria showed significantly higher phenolic levels (43.27 ±
without treatment (0% activity), the control sample 2.029 mg GAE g−1) than the fruits harvested early and
was prepared only with the bacterial solution and TSB the late harvested ones (37.38 ± 4.22 mg GAE g−1),
medium and to ensure the sterility of the analysis, the respectively.
blank contains only 200 µl of culture medium. After Extracts flavonoids contents
the incubation time, 25 µl of MTT (1 mg ml−1), giving In this study, the results showed that the flavonoid
a purple color, was added to each well. After that, contents were present in important quantities in the
the plates were re-intubated (10 minutes, 25°C) to different maturation stages of A. esculentus L. fruit
promote the formation of formazan. Finally, they were extracts (Fig. 2). As regards, Figure 2 revealed the
centrifuged (2,000 × g, 10 minutes). variations of TFC in okra fruit extracts belonging to
After the removal of the supernatant, each precipitate their stage of maturity. Briefly, the TFC of okra fruits
was dissolved in 200 µl of DMSO. The absorbance of increased significantly from 25.08 ± 0.93 g RE g−1

Table 1. Weight, length, and diameter of okra fruits at different stages of maturity of A. esculentus L. fruits.
Different maturation
Weight (g) Length (cm) Diameter (cm)
stages
Early-stage 1.76 ± 0.90 2.04 ± 0.40 1.83 ± 0.58
Mid-stage 1.95 ± 0.95 3.07 ± 0.43* 2.55 ± 0.43
Late-stage 4.05 ± 0.64* 5.64 ± 0.55* 2.95 ± 0.56*
The results are expressed as mean ± SEM (n = 5).
*Note significant differences between treatment groups (p < 0.05).

1564
http://www.openveterinaryjournal.com
S. Guebebia et al. Open Veterinary Journal, (2023), Vol. 13(12): 1562–1569

Fig. 1. Effect of different maturity stages on TPC of ethanolic Fig. 3. Effect of different ripening stages on radical scavenging
okra fruit extracts. The results are representative of at least activity of okra fruit. The results are representative of at least
three independent experiments and are expressed as mean ± three independent experiments and are expressed as mean ±
SEM (n = 5). (*): Significant differences between treatment SEM (n = 5). (*): Significant differences between treatment
groups (p < 0.05). groups (p < 0.05).

Fig. 2. Effect of different maturity stages on TFC of ethanolic Fig. 4. Bactericidal activity (expressed as a percentage)
okra fruit extracts. The results are representative of at least of okra fruit extract against V. anguillarum depending on
three independent experiments and are expressed as mean ± different maturity stages. The results are representative of
SEM (n = 5). (*): Significant differences between treatment at least three independent experiments and are expressed as
groups (p < 0.05). mean ± SEM (n = 5). (*): Significant differences between
treatment groups (p < 0.05).

(mid-stage maturity) to 29.96 ± 0.19 g RE g−1 (late-


stage maturity). red okra fruits has an important percent inhibition via
In fact, the TPCs and TFCs of okra fruits were the DPPH test.
significantly influenced by their ripening process. All the antioxidant-tested activities of okra fruits varied
While the mid-ripe ethanolic extract of A. esculentus depending on their maturity stages. While, the extract
L. fruits contained the highest phenolic and flavonoid showed the highest antioxidant effect at a medium
contents. maturity, followed by fruits harvested at the beginning
DPPH radical-scavenging activity of maturity. While the DPPH radical scavenging activity
In the present research, the antioxidant activity of okra of okra fruit was significantly lower at the late ripe stage
was determined using the DPPH method. The results (70.61% ± 0.15%). This result can be connected to the
are highlighted in Figure 3. As regards, the percent TPC that could be the origin of the antiradical capacity.
inhibition of fruit extracts was determined. As shown in These data are in correlation with previous results that
Figure 3, all ripening stages of okra fruits have a major indicate that several vegetal phenolic compounds are
anti-radical effect. In addition, the extract capacity was important sources of natural antioxidants (Khomsug et
dependent on the maturation stage. Furthermore, the al., 2010).
antioxidant capacities of okra fruits contribute partially Bactericidal activity
to the health amelioration (Xia et al., 2015). The The in vitro evaluation of A. esculentus L. fruits
antioxidant capacities of okra fruit extracts were ranged extracts bactericidal effect belonging to three maturity
from 60.7% ± 0.26% to 75.64% ± 0.79%. Wahyuningsih stages was assigned against V. anguillarum, fish
et al. (2021) suggested also that the ethanolic extract of pathogenic bacteria (Fig. 4). However, the results

1565
http://www.openveterinaryjournal.com
S. Guebebia et al. Open Veterinary Journal, (2023), Vol. 13(12): 1562–1569

demonstrated that the viability of V. anguillarum was (2019) noted that okra fruits flavonoid contents were
influenced by the fruit extract at all the tested stages. 10 times lower than ours (2.95 ± 0.06 mg RE g−1).
Then, as shown in Figure 4, the bactericidal capacity Generally, fluctuations in the reported flavonoid values
quantitatively varied depending on the maturity stages. can arise from several factors like nonrepresentative
Vibrio anguillarum showed a remarkable sensitivity to sampling, different cultivars, and different growing and,
all okra fruit extracts. Then, the ethanolic extracts at analytical conditions (Harnly et al., 2006). Besides,
the mid-maturity stage recorded the major inhibitory such variations in flavonoid contents might be due to a
effect of the bacteria viability. Furthermore, at the three number of causes as well as genotype, maturity stages,
maturity stages the okra fruit extracts have noticeably environmental and post-harvest conditions techniques
affected the bacteria growth compared to the control. (Koh et al., 2009). In addition, previous research
suggested, similarly, that small fruit (3–5 cm) had a
Discussion higher nutritional value (Petropoulos et al., 2018).
The length of fresh fruit is considered a major indicator The antioxidant activity of A. esculentus L. fruits
for okra fruit harvest. Generally, the two sizes of okra is correlated with the ripening stage. In that sense,
fruits (small and big) are collected and consumed our results showed variation in DPPH value among
(Petropoulos et al., 2018). The increase in size and maturity process from 60.7% ± 0.26% to 75.64% ±
weight indicates an improvement in the quality of okra 0.79%. Our findings are in accordance with Siddique
fruit during maturity (Uchoi et al., 2018). et al. (2022), which highlighted that Pakistan fruit
Besides, phenolic elements are considered crucial extract has a scavenging percentage of DPPH radicals
biomolecules in okra fruits (Hussain et al., 2012). In around 13.487% lower than the Tunisian one. This
the same context, Shen et al. (2019) have shown that fluctuation is caused by the existence of biomolecules
the main bioactive component in okra fruits is phenolic such as quercetin and catechin which are more soluble
compounds. Whereas the fruit ripening stage had a in methanol as a solvent (Wahyuningsih et al., 2020).
marked influence on the secondary metabolite contents Numerous further studies have highlighted a directly
extracts. proportional relationship between phenolic, and
During the ripening of okra, various changes in phenolic flavonoid contents and antioxidant effects of vegetable
level have been established ranging from 37.38 ± 4.22 extracts (Abdel-Hameed, 2009; Shen et al., 2019).
mg GAE g−1 (late harvested fruits) to 43.27 ± 2.029 mg In addition, the high antioxidant capacity of okra
GAE g−1 (mid-stage maturation of fruits). fruit extract could be explained by its high content of
Similar to our findings, previous research presented a phenolic compounds which function as singlet oxygen
similar level of TPC varied from 33.33 ± 0.02 to 37.38 quenchers, reduction agents, and hydrogen donors
± 4.22 mg GAE g−1 (Mohammed et al., 2016). While, (Reine et al., 2018).
previous studies have reported a similar phenolic level Otherwise, as already reported by Uchoi et al. (2018)
in okra fruits (49.72 ± 2.24 mg GAE g−1) (Rohman et al., antioxidant activity can increase depending on the
2010). Otherwise, another study indicated a lower level maturation stage of fruits (between the beginning of
of okra fruit phenolic content was indicated (13.456 mg okra maturity to the mid-ripe stage) contradictory to a
GAE g−1) (Zainuddin et al., 2022). The difference in previous study by Rekha et al. (2012) that revealed the
phenols concentration can also relied on the extraction reduction in phenolic contents and then in antioxidant
technique and the polarity of the solvent used (Jing capacity as shown between mid-ripe stage and the late
et al., 2015). In addition, these variations are often one of okra fruits.
connected with the difference in geographical origin, Concerning the antibacterial activity, the inhibitory
the extraction technique used and the experimental effect of A. esculentus L. fruits extracts against Gram-
protocol adopted (Benchikh et al., 2014). negative fish pathogenic bacteria (V. anguillarum) was
In the current study, the effect of ripening stages on illustrated. Because of its causes of fish diseases and
flavonoids level was investigated. The medium stage important economic losses in the aquaculture industry,
of maturity reported the most important extractive yield V. anguillarum was selected. Overall, at three maturity
of flavonoids (25.08 ± 0.93 g RE g−1). Our findings are stages, A. esculentus L. fruit extracts were significantly
in correlation with Shen et al. (2019) who highlighted active against V. anguillarum viability. This result was
the TFC variation of okra fruits during fruit maturity. previously reported by Shaeroun et al. (2021), who
Literature has explained these results by the dilution detected the bactericidal effect of ethanolic extract
effect slowing the biosynthesis of new phenolic of okra fruit against two Gram-negative bacterial
compounds which increase the size during ripening pathogens (Klebsiella and Escherichia coli). The
for fruits (Anand and Aradhya, 2005). Accordingly, antibacterial capacity of okra fruit could be derived
with our results, Mohammed et al. (2016) indicated from the bioactive molecules present in okra fruits
okra fruit flavonoid contents about 29.979 ± 0.036 mg which show antibacterial capacity (Septianingrum et
RE g−1. In addition, similar flavonoid contents of okra al., 2018). Furthermore, the major inhibitory effect
fruits have been earlier expressed (31.21 ± 8.64 mg was estimated at the middle maturity stage of fruits.
RE g−1) (Rohman et al., 2010). Whereas, Shen et al. Recently, this illustration was confirmed by the study

1566
http://www.openveterinaryjournal.com
S. Guebebia et al. Open Veterinary Journal, (2023), Vol. 13(12): 1562–1569

of Aldhanhani et al. (2022) which detected that at all Anand, P.K. and Aradhya, S.M. 2015. Chemical
maturity stages the jujube fruit extracts showed growth changes and antioxidant activity in pomegranate
inhibition against several bacteria at different degrees. arils during fruit development. Food Chem. 93(2),
However, these mentioned data were in accordance 319–324.
with those found by Ghazghazi et al. (2021) showing Bahroun, T., Gressier, B., Trotim, F., Brunet, C., Dime,
the antimicrobial potential of Eucalyptus marginata’s T., Luyvkx, M., Vasseur, J., Cazin, M., Cazin, J.C.
fruits was associated with the fruit ripening stage and Pinkas, M. 1996. Oxygen species scavenging
against four species of pathogenic bacteria. activity of phenolic extracts from hawthom fresh
The current investigation estimated that mid-stage plant organs and pharmaceutical preparations.
maturity fruits had the highest antibacterial capacity, Arzneimittelforschung 46, 1086–1089.
followed by late-stage and early-stage maturity fruits Benchikh, Y., Louaileche, H., George, B. and Merlin,
respectively. This may be explained by the important A. 2014. Changes in bioactive phytochemical
phenolic compound content detected in mid-stage and content and in vitro antioxidant activity of carob
late-stage fruits than that in early-stage maturity of okra (Ceratoniasiliqua L.) as influenced by fruit
fruits. ripening. Ind. Crop. Prod. 60, 298–303.
Dhruve, J.J., Shukla, Y.M., Shah, R., Patel, J. and Talati,
Conclusion J.G. 2015. Contribution of okra (Abelmoschus
To conclude, in the present research, noticeable esculentus L.) seeds towards the nutritional
fluctuations in A. esculentus L. fruits’ phenolic, characterization. World J. Pharm. Sci. 4, 1009–
flavonoid contents, and antioxidant activities were 1023.
observed at three ripening stages. The results Elik, A., Kocak, D. and Gogus, F. 2017. Optimization
highlighted the okra fruit as an excellent source of of microwave-assisted extraction of phenolics
phenolic compounds with a large amount of flavonoids from organic strawberry using response surface
and optimal antioxidant and antibacterial capacities in methodology. Harran Tarım Gıda Bilimleri Derg.
its mid-stage maturity. Therefore, okra fruits could be 21(2), 143–154.
Erfan, A.M. and Marouf, S. 2019. Cinnamon oil
used as functional foods for industrial exploitation or
downregulates virulence genes of poultry
for the production of dietary supplements.
respiratory bacterial agents and revealed significant
Acknowledgments bacterial inhibition: an in vitro perspective. Vet.
World 12(11), 1707–1715.
Salma Guebebia thankfully acknowledges the
Ghazghazi, H., Essghaier, B., Jawadi, I., Riahi, L.,
scholarship assistance from Gabes University (Gabes,
Ben Salem, R. and Rigane, G. 2021. Effects
Tunisia).
of fruit maturity stages on GC-FID fatty acid
Authors contribution
profiles, phenolic contents, and biological
SG drafted the manuscript. LZ and AAM revise and edit activities of Eucalyptus marginata L. J. Food Qual.
the manuscripts. SG and MR took part in preparing and 2021, 5546969.
critically checking this manuscript. MAE, CER,` and Habtamu, F., Ratta, N., Haki, G.D., Woldegiorgis,
SG performed the methodology. All authors have read A.Z. and Beyene, F. 2014. Nutritional quality and
and agreed to the published version of the manuscript. health benefits of okra (Abelmoschus esculentus): a
Conflict of interest review. J. Food Sci. Qual. Manag. 33, 87–96.
The authors declare that there is no conflict of interest. Harnly, J.M., Doherty, R.F., Beecher, G.R., Holden,
Funding J.M., Haytowitz, D.B., Bhagwat, S. and Gebhart, S.
This research received no external funding. 2006. Flavonoid content of U.S. fruits, vegetables,
Data availability and nuts. J. Agric. Food Chem. 54, 9966−9977.
Data is available upon request from the corresponding Hussain, M.S., Fareed, S., Saba Ansari, M., Rahman,
author. A., Ahmad, I.Z. and Saeed, M. 2012. Current
approaches toward production of secondary plant
References
metabolites. J. Pharm. Bioallied. Sci. 4, 10–20.
Abdel-Hameed, E.S.S. 2009. Total phenolic contents Jiang, N., Liu, C., Li, D., Zhang, Z., Liu, C., Wang, D.,
and free radical scavenging of certain Egyptian Niu, L. and Zhang, M. 2017. Evaluation of freeze
Ficus species leaf samples. Food Chem. 114, 1271– drying combined with microwave vacuum drying
1277. for functional okra snacks: antioxidant properties,
Aldhanhani, A.R.H., Ahmed, Z.F.R., Tzortzakis, N. and sensory quality, and energy consumption. LWT
Singh, Z. 2022. Maturity stage at harvest influences Food Sci. Technol. 82, 216–226.
antioxidant phytochemicals and antibacterial Jing, L., Ma, H., Fan, P., Gao, R. and Jia, Z. 2015.
activity of jujube fruit (Ziziphus mauritiana Lamk. Antioxidant potential, total phenolic and
and Ziziphus spina-christi L.). Ann. Agric. Sci. total flavonoid contents of Rhododendron
67(2), 196–203. anthopogonoides and its protective effect on

1567
http://www.openveterinaryjournal.com
S. Guebebia et al. Open Veterinary Journal, (2023), Vol. 13(12): 1562–1569

hypoxia-induced injury in PC12 cells. BMC Aktivitas Antibiotik Terhadap Bakteri Escherichia
Complem. Altern. Med. 15, 1–12. coli. J. Insan. Farm. Indones. 1(2), 170–177.
Khomsug, P., Thongjaroenbuangam, W., Pakdeenarong, Shaeroun, E., Alshebani, A.M.A., Rashed, A. and
N., Suttajit, M. and Chantiratikul, P. 2010. Oshkondali, S.T.M. 2021. Phytochemical screening
Antioxidative activities and phenolic content of and antibacterial activity of okra extract. S. Asian
extracts from okra (Abelmoschus esculentus L.). Res. J. Biol. Appl. Biosci. 3(4), 51–56.
Res. J. Biol. Sci. 5, 310–313. Shen, D.D., Li, X., Qin, Y.L., Li, M.T., Han, Q.H.,
Koh, E., Wimalasiri, K.M.S., Chassy, A.W. and Mitchell, Zhou, J. and Wu, D.T. 2019. Physicochemical
A.E. 2009. Content of ascorbic acid, quercetin, properties, phenolic profiles, antioxidant capacities,
kaempferol and total phenolics in commercial and inhibitory effects on digestive enzymes of
broccoli. J. Food Comp. Anal. 22, 637–643. okra (Abelmoschus esculentus) fruit at different
Lengsfeld, C., Titgemeyer, F., Faller, G. and Hensel, A. maturation stages. J. Food Sci. Technol. 56(3),
2004. Glycosylated compounds from okra inhibit 1275–1286.
adhesion of Helicobacter pylori to human gastric Siddique, M.H., Ashraf, A., Hayat, S., Aslam, B.,
mucosa. J. Agric. Food Chem. 52, 1495–1503. Fakhar-e-Alam, M., Muzammil, S., Atif, M., Shahid,
Mohammed, M.I., Bayero, A.S. and Shettima, U.I. M., Sulman Shafeeq, S. Afzal, M. and Ahmad, S.
2016. Levels of total phenolic and flavonoids in 2022. Antidiabetic and antioxidant potentials of
Abelmoschus esculentus L. from some irrigation Abelmoschus esculentus: in vitro combined with
areas of kano state-Nigeria. Bayero J. Pure Appl. molecular docking approach. J. Saudi Chem. Soc.
Sci. 9(2), 121–124. 26, 101418.
Petropoulos, S., Fernandes, A., Barros, L. and Ferreira, Singleton, V.I. and Lamuela-Raventos, R.M. 2012.
I.C.F.R. 2018. Chemical composition, nutritional Analysis of total phenols and other oxidation
value and antioxidant properties of Mediterranean substrates and antioxidants by means of Folin-
okra genotypes in relation to harvest stage. Food Ciocalteu reagent. Method Enzymol. 15, 152–178.
Chem. 242, 466–474. Solomon, S., Muruganatham, N. and Senthamiselvi,
Piloo, N. and Kabir, J. 2011. Effect of age of harvest on M. 2016. Anticancer activity of Abelmoschus
fruit quality of okra (Abelmoschus esculentus L.). J. esculentus (flower) against human liver cancer. Int.
Environ. Res. Develop. 5(3), 615–622. J. Pharmacol. Biol. Sci. 6, 145–157.
Poobalan, V., Praneetha, S., Arumugam, T., Stevens, M.G., Kehrli, M.E. and Canning, P.C. 1991.
Kumaravadivel, N. and Jeyakumar, P. 2019. A colorimetric assay for quantitating bovine
Medicinal properties of vegetable crops. Int. J. neutrophil bactericidal activity. Vet. Immunol.
Chem. Stud. 7(5), 1538–1542. Immunopathol. 28, 45–56.
Reine, B.G.S., Houndekon, B.A.P., Marcelline, G., Sultana, B., Anwar, F. and Ashraf, M. 2009. Effect of
Pascal, A.D.C., Worou, C.N., Hounankpon, Y. and extraction solvent/technique on the antioxidant
Félicien, A. 2018. Phytochemical composition and activity of selected medicinal plant extracts.
antioxydant capacity of Abelmoschus esculentus L. Molecules. 14, 2167–2180.
fresh immature fruits. Am. J. Food Sci. Technol. Uchoi, J., Singh, R.S., Bhargava, R., Krishna, H.,
6(5), 223–227. Venkatesan, K. and Kumar, A. 2018. Effect of
Rekha, C., Poornima, G., Manasa, M., Abhipsa, V., harvesting of fruits at different stage of maturity on
Pavithra Devi, J., Vijay Kumar, H.T. and Prashith nutritional quality of Kinnow under Hot Arid Zone
Kekuda, T.R. 2012. Ascorbic acid, total phenol of North western India. Green Farming Int. J. 9(2),
content and antioxidant activity of fresh juices of 379–382.
four ripe and unripe citrus fruits. Chem. Sci. Trans. Umme, A., Ksenia, M., Giovanna, F. and Matteo,
1(2), 303–310. S. 2023. Apples and apple by-products:
Rohman, A., Riyanto, S., Yuniarti, N., Saputra, W.R., antioxidant properties and food applications.
Utami, R. and Mulatsih, W. 2010. Antioxidant Antioxidants 12(7), 1456.
activity, total phenolic, and total flavonoid of Velazquez, E., Tournier, H.A., Mordujovich de
extracts and fractions of red fruit (Pandanus Buschiazzo, P., Saavedra, G. and Schinella, G.R.
conoideus Lam). Int. Food Res. J. 17, 97–106. 2003. Antioxydant activity of Paraguayan plant
Saha, D., Jain, B. and Jain, V.K. 2011. Phytochemical extracts. Fitoterapia 74, 91–97.
evaluation and characterization of hypoglycemic Wahyuningsih, S.P.A., Winarni, D., Pramudya, M.,
activity of various extracts of Abelmoschus Setianingsih, N., Mwendolwa, A.A. and Nindyasari,
esculentus Lin. fruit. Int. J. Pharm. Pharm. Sci. F. 2021. Antioxidant potential of red okra pods
3(2), 183–185. (Abelmoschus esculentus Moench). EPiC Series
Septianingrum, N.M., Hapsari, W. and Syariffudin, A. Biol. Sci. 1, 158–163.
2018. Identifikasi Kandungan Fitokimia Ekstrak Wahyuningsih, S.P.A., Savira, N.I.I., Anggraini,
Okra Merah (Abelmoschus esculentus) dan Uji D.W., Winarni, D., Suhargo, L., Kusuma, B.W.A.,

1568
http://www.openveterinaryjournal.com
S. Guebebia et al. Open Veterinary Journal, (2023), Vol. 13(12): 1562–1569

Nindtasari, F., Setianingsih, N. and Mwendolwa, compounds, total phenolic content, and
A.A. 2020. Antioxidant and nephroprotective antioxidant activity test of ethanol extract of okra
effects of okra pods extract (Abelmoschus (Abelmoschus esculentus L.) from the traditional
esculentus L.) against lead acetate-induced toxicity market of Kendari. J. Hunan Univ. (Nat. Sci.)
in mice. Scientifica 2020, 4237205. 49(7), 89–95.
Xia, F., Zhong, Y., Li, M., Chang, Q., Liao, Y., Liu, Zhang, T., Xiang, J., Zheng, G., Yan, R. and Min,
X. and Pan, R. 2015. Antioxidant and anti-fatigue X. 2018. Preliminary characterization and anti-
constituents of okra. Nutrients 7(10), 8846–8858. hyperglycemic activity of a pectic polysaccharide
Zainuddin, A., Sabilu, Y., Majid, R., Pratiwi, A. and from okra (Abelmoschus esculentus (L.) Moench).
Jafriati, D. 2022. Analysis of phytochemical J. Funct. Food 41, 19–24.

1569

You might also like