Caryologia. International Journal of Cytology, Cytosystematics and Cytogenetics 75(2): 89-99, 2022

Firenze University Press 
www.fupress.com/caryologia

ISSN 0008-7114 (print) | ISSN 2165-5391 (online) | DOI: 10.36253/caryologia-1571

Caryologia
International Journal of Cytology,  

Cytosystematics and Cytogenetics

Citation: Made Pharmawati, Ni 
Nyoman Wirasiti, Luh Putu Wrasiati (2022) 
Genotoxic and antigenotoxic potential 
of encapsulated Enhalus acoroides (L. 
f.) Royle leaves extract against nickel 
nitrate. Caryologia 75(2): 89-99. doi: 
10.36253/caryologia-1571

Received: February 08, 2022

Accepted: March 24, 2022

Published: September 21, 2022

Copyright: © 2022 Made Pharmawati, Ni 
Nyoman Wirasiti, Luh Putu Wrasiati. 
This is an open access, peer-reviewed 
article published by Firenze University 
Press (http://www.fupress.com/caryo-
logia) and distributed under the terms 
of the Creative Commons Attribution 
License, which permits unrestricted 
use, distribution, and reproduction 
in any medium, provided the original 
author and source are credited.

Data Availability Statement: All rel-
evant data are within the paper and its 
Supporting Information files.

Competing Interests: The Author(s) 
declare(s) no conflict of interest.

ORCID
MP: 0000-0002-3064-4582 

Genotoxic and antigenotoxic potential of 
encapsulated Enhalus acoroides (L. f.) Royle 
leaves extract against nickel nitrate

Made Pharmawati1,*, Ni Nyoman Wirasiti1, Luh Putu Wrasiati2

1 Biology Study Program, Faculty of Mathematics and Natural Sciences, Universitas 
Udayana, Jalan Raya Kampus Unud, Jimbaran, Kecamatan Kuta Selatan, Kabupaten 
Badung, Bali 80361, Indonesia
2 Agroindustrial Technology Study Program, Faculty of Agricultural Technology, Universi-
tas Udayana, Jalan Raya Kampus Unud, Jimbaran, Kecamatan Kuta Selatan, Kabupaten 
Badung, Bali 80361, Indonesia
*Corresponding author. E-mail: made_pharmawati@unud.ac.id

Abstract. Several environmental pollutants can cause damage to chromosomes, one 
of which is the heavy metal NiNO3. Some plant extracts have antigenotoxic proper-
ties that result in a decrease in chromosomal damage. Member of flowering plants 
that need to be tested is seagrass. One seagrass species is Enhalus acoroides which was 
found to contain phytochemical compounds. This study aimed to analyse the geno-
toxic effect and the potential of encapsulated E. acoroides leaf extract as antigenotoxic 
against nickel nitrate NiNO3. The extraction was conducted using a mixture of chloro-
form and ethanol, and crude extract encapsulated using maltodextrin and tween 80. 
Chromosomal aberrations were evaluated using the squash technique of Allium cepa 
var. aggregatum root tips. Triphenyltetrazolium chloride and Evans Blue staining were 
used to observe mitochondrial and apoptotic activities. The results showed that at 
higher concentrations (250 ppm and 500 ppm), the encapsulated E. acoroides extract 
decreased mitotic indices; however, no chromosome aberration observed. NiNO3 itself 
induced a genotoxic effect as observed by low mitotic index and a high percentage of 
chromosome aberration. The modulation of NiNO3 effect by adding the encapsulated 
E. acoroides extract at low concentration (100 ppm) increased mitotic index compared 
to treatment with Ni alone, but did not reduce chromosome aberration. Simultaneous 
encapsulated E. acoroides extract and Ni treatment, significantly reduced nuclear frag-
mentation and nuclear lesion. The encapsulated E. acoroides extract can repair several 
types of nuclear damage but cannot minimise chromosomal damage.

Keywords: chromosome aberration, Enhalus acoroides, heavy metal, nuclear abnor-
mality, seagrass.

INTRODUCTION

Heavy metals are hazardous inorganic environmental pollutants due to 
their toxicity. However, when present in low amounts, several heavy metals 
such as Cu, Fe, Mn, Co, Zn, and Ni are required for plants and animals as 



90 Made Pharmawati, Ni Nyoman Wirasiti, Luh Putu Wrasiati

micronutrients (Singh et al. 2020). Recently, due to high 
industrial activities and the extensive use of fertilizer 
and pesticides, heavy metals are present in enormous 
amounts in the environment, posing a serious global 
environmental threat. 

One of the most common heavy metal contaminants 
found in the environment is nickel (Ni), along with 
Arsenic (As), Cadmium (Cd), Chromium (Cr), Copper 
(Cu), Mercury (Hg), Lead (Pb), and Zinc (Zn) (Huang 
et al. 2020). Nickel is widely distributed in the environ-
ment including air, water, soil, and biological materials. 
It is mainly derived from natural sources such as wind-
blown dust, resulting from the weathering of rocks and 
soils, forest fires, and volcanic activity. Nickel is also 
present in the environment due to the combustion of 
coal, diesel oil, and fuel oil, as well as the incineration 
of trash and sewage (Cempel and Nikel 2006). In plants, 
high nickel concentrations can inhibit growth by caus-
ing oxidative damage and disrupting nutrient uptake 
and translocation (Amjad et al. 2020). Nickel has also 
been reported to have cytotoxic and mutagenic effects in 
plants (Gantayat et al. 2018). 

Natural ingredients with bioactive compounds that 
can fight mutagenic and carcinogenic effects are now 
getting more and more attention. Compounds capable 
of reducing the mutagenicity of physical and chemi-
cal mutagens are referred to as antimutagens. However, 
considering that all mutagens are genotoxic, then com-
pounds that reduce DNA damage caused by genotoxic 
agents are also called antigenotoxic agents (López-Rome-
ro et al. 2018). For example, aqueous extracts of medici-
nal plants, Spondias mombin, Nymphea lotus and Luffa 
cylindrica reduced chromosomal and nuclear aberration 
induced by PbNO3 in A. cepa root tip cells (Oyeyemi and 
Bakare 2013). Butanol and ethyl acetate fractions of Par-
kinsonia aculeata L. leaf extract demonstrated the most 
significant reduction in chromosomal abnormalities 
in A. cepa cells treated with maleic hydrazide, indicat-
ing that they had chemo-preventive efficacy (Sharma et 
al. 2018). Previously, Sharma et al. (2012) reported that 
using the A. cepa root chromosomal aberration assay, 
the chloroform extract of Brasicca juncea seeds possesses 
antigenotoxic potential against mercury-induced geno-
toxicity. 

Exploration of antitoxic properties from natural 
products has also been done at marine organisms such 
as Ulva fasciata (Rodeiro et al. 2015), Sargassum sp. (Kil-
awati and Islamy 2019). However, limited studies were 
conducted in seagrass. Seagrass are flowering plants that 
grow in a marine environment. One of the seagrass spe-
cies is Enhalus acoroides (L.f.) Royle. Enhalus acoroides 
is tropical seagrass, a member of the Family of Hydro-

charitaceae, found throughout the Indo-Pacific region, 
including southern Japan, Southeast Asia, northern 
Australia, southern India, and Sri Lanka (Short and 
Waycott 2010). In Indonesia, this species is distributed 
widely in Papua, North Maluku, Ambon, Sulawesi, Bali, 
Java, Borneo, and Sumatra in Indonesia (Kiswara and 
Hutomo 1985). Extract of E. acoroides leaves contains 
phytochemical compounds such as phenols, flavonoids, 
and tannins as well as several pigments including chlo-
rophyll, lutein, pheophytin, and b-carotene (Pharmawati 
and Wrasiati 2020). It has been known that flavonoids, 
phenolic compounds and pigments have antioxidant 
activity. To extend self-life and protect oxidative stabil-
ity of plant extract, microencapsulation is often applied 
(Yusop et al. 2017) using colloidal particles such as 
maltodextrin, Arabic gum, or chitosan (Özkan and Bilek 
2014, Šturm et al, 2019).

The aim of this study was to analysed the genotoxic 
effect of encapsulated E. acoroides leaves extracts and 
its antigenotoxic potential against heavy metal nickel 
nitrate Ni(NO3)2.6H2O using Allium cepa var. aggrega-
tum root tips assay. 

MATERIALS AND METHODS

Sample Collection, Extraction and Encapsulation

Leaves of E . acoroides were col lected f rom 
Semawang Beach, Denpasar, Bali, Indonesia. The meth-
ods of den Hartog and Kuo (2006) and McKenzie and 
Yoshida (2009) were used to identify E. acoroides based 
on morphological traits. The voucher specimen was 
deposited in the Herbarium Biology Udayana (HBU-
MP10), Biology Study Program, Universitas Udayana. 
Leaves were washed in running water, cut into 10 cm 
long, and air-dried for three days. The leaves were then 
further dried for one day using an oven at 50°C. Using 
a blender, the dried leaves were mashed and sieved 
through a 60-mesh sieve. Using 200 mL of chloroform: 
ethanol at a 9:1 (v/v) ratio, up to 20 g of dried leaves 
powder was extracted. The extraction was done using a 
Soxhlet extractor. The solvent was filtered using What-
man filter paper, and the filtrate was vacuum evaporated 
using an IKA® RV10 rotary evaporator at 40°C and 100 
mbar (Pharmawati and Wrasiati 2020) 

The encapsulation of crude extract was conducted 
using a 20% maltodextrin solution. As much as 10% 
extract of E. acoroides and 2% tween 80 were mixed with 
the encapsulated solution and homogenized at 6000 rpm 
for 30 minutes. After that, the mixture was dried up to 
8% moisture content, mashed with a blender and then 
sieved through a 60 mesh sieve (Sulistyadewi et al. 2014).



91Genotoxic and antigenotoxic potential of encapsulated Enhalus acoroides (L. f.) Royle leaves extract against nickel nitrate

Treatment of Allium cepa var. aggregatum root

The base of A. cepa var. aggregatum bulbs were 
soaked in water to induce roots. When the length of the 
root was approximately 1 cm, bulbs were transferred to a 
glass jar containing treatment solutions. The treatments 
were 30 ppm Ni in the form of Ni(NO3)2.6H2O, encap-
sulated E. acoroides extract at 100 ppm, 250 ppm, and 
500 ppm, and combined 30 ppm Ni with each of 100 
ppm, 250 ppm and 500 ppm of encapsulated E. acoroides 
extract. The treatments were given for 72 hrs. As con-
trols, bulbs were soaked in H2O. Three bulbs were used 
in each treatment. 

Chromosome preparation

Modified procedures were used to prepare mitotic 
squash (Sharma and Sharma 1994). Following treat-
ments, roots were rinsed in distilled water and cut in 
the morning. Roots were then soaked in Farmer’s fixa-
tive containing of ethanol and acetic acid (3:1) for 24 hrs 
in the refrigerator. For hydrolysis, root tips were cut 2 
mm long and treated with 1N HCl for 15 minutes. The 
root tips were cleaned in distilled water before being col-
oured with 2% acetoorcein for 20 min. Excess stain was 
absorbed using filter paper. Stained root tips were cov-
ered with cover glass and then squashed. Slides were 
inspected for mitotic chromosomes and aberration using 
microscope binocular XSZ 107BN (Nanjing BW Optics 
and Instrument Co.) with 400x total magnification. The 
photographs were taken using the top mount camera 
Optilab Advance (Miconos). The data was collected from 
a total of six roots of three bulbs for each treatment and 
six fields chosen at random from each root. 

Metabolic Activity

Following the treatment and control procedures, 5 
root tips were removed and soaked in 0.5% 2,3,5-triphenyl 
tetrazolium chloride (TTC) for 15 minutes in the dark at 
35°C. The root tips were then analysed qualitatively after 
being rinsed with distilled water. Furthermore, the roots 
were soaked in 95% ethanol to extract the colourful triph-
enyl formazan complex. The absorbance was measured at 
490 nm (Vazhangat and Thoppil 2017). Three replications 
were conducted in this experiment.

Apoptotic Activity

The Evans Blue staining method was used to investi-
gate the loss of cell viability. After treatments, five roots 

with identical lengths were cut and dyed with a 0.25% 
(w/v) aqueous Evans Blue solution for 15 minutes before 
being rinsed with distilled water for 30 minutes. The 
experiment was conducted with three replications. The 
roots were then macro-imaged to determine cell death 
qualitatively. Roots then were soaked in 3 mL of N,N-
dimethylformamide for 1 hour at room temperature for 
a quantitative estimation by measuring the absorbance 
of Evans Blue at 600 nm (Vazhangat and Thoppil 2017).

Data Analyses

The mitotic index (%) was computed as the number 
of dividing cells divided by the total number of cells ´ 
100. The chromosomal aberrations were calculated by 
dividing the number of abnormal cells by the total num-
ber of cells counted × 100 (Sarac et al. 2019). Phase index 
(%) was determined by calculating the number of divid-
ing cells in phases by the total number of dividing cells ´ 
100 (Kumar and Thonger 2016).

The antigenotoxicity of encapsulated E. acoroides 
extract was determined by calculating the inhibitory 
activity of chromosomal aberration induced by Ni. The 
formula used was following Prajitha and Thoppil (2016). 
Inhibitory activity (%)= A−B: A−C × 100, where A: 
Number of aberrant cells induced by Ni, B: Number of 
aberrant cells induced by the mixture of Ni and encap-
sulated E. acoroides extract, C: Number of aberrant cells 
induced in the control 

Statistical analyses were performed using Minitab 
20, with randomised experimental design. The differ-
ences between treatments were analysed using the Tukey 
test with a 95% confidence level. The data were presented 
as mean ± standard deviation, except for the data of the 
types of aberration.

RESULTS 

Mitotic Index

Using Allium cepa var. aggregatum root tips, the 
antigenotoxic potential of encapsulated extract of E. 
acoroides leaves was investigated. One of the metrics 
used to assess antigenotoxicity was mitotic activity as 
measured by the mitotic index. The mitotic indices were 
significantly affected by the treatments (p<0.01). Treat-
ment of A. cepa root with Ni reduced mitotic index sig-
nificantly. There are no differences between the mitotic 
index of control and treatment with 100 ppm encapsu-
lated extract of E. acoroides leaves. The concentration of 
250 ppm and 500 ppm encapsulated extract had a sig-



92 Made Pharmawati, Ni Nyoman Wirasiti, Luh Putu Wrasiati

nificantly lower mitotic index than control, but signifi-
cantly higher than nickel (Table 1). 

Treatment with nickel resulted in the lowest mitotic 
index indicating genotoxic activity of nickel. When nick-
el and encapsulated extract of E. acoroides leaves were 
given simultaneously, the mitotic indices were higher 
than the mitotic index of Ni alone; however, statistical 
analysis showed that only the addition of 100 ppm encap-
sulated extract had a significant increase of the mitotic 
index. Table 1 shows the mitotic indices of control, treat-
ment with Ni, encapsulated E. acoroides extract, and 
combined treatment of Ni and encapsulated extract. 

Phase index

The distribution of mitotic phases was shown in 
Table 2. The treatments significantly affected prophase, 
metaphase and telophase indices (p<0.05), while ana-
phase index was not affected by treatments. The major-
ity of chromosomes in all treatments and control were in 
metaphase. Treatment of Nickel resulted in the highest 
percentage of metaphase chromosomes, and Ni inhibited 
telophase as indicated by the significantly lowest index 
of telophase in Ni treatment. The addition of encapsulat-
ed E. acoroides extract to the Ni treatment increased the 
percentage of telophase.

Chromosomal Aberration and Nuclear Abnormality

Statistical analysis shows that the treatments affect-
ed chromosomal aberration (p<0.01) and nuclear abnor-
mality (p<0.01). Mitotic chromosomal aberrations were 
detected in all treatments including control (Table 1) 
and control has a very low percentage of aberration. 
Treatment with Ni resulted in 1,677% of aberrant chro-
mosomes. The percentage of the aberrant chromo-
some at root tips treated with encapsulated E. acoroides 
extract at the concentration of 100 ppm, 250 ppm and 
500 ppm had no significant difference to control, sug-
gesting that the encapsulated extract had no or very 
low genotoxic effect. Simultaneous treatments of Ni 
and encapsulated E. acoroides extract at concentrations 
100 ppm, 250 ppm, and 500 ppm showed a similar per-
centage of chromosomal aberration to treatment with 
Ni alone. Modulation of Ni-induced genotoxicity with 
encapsulated E. acoroides extract showed no significant 
reduction of chromosomal aberration. The inhibitory 
activities of encapsulated extract to the genotoxic activ-
ity of Ni were only 4.9%, 6.5%, and 14.4% with simul-
taneous addition of 500 ppm, 250 ppm, and 100 ppm 
encapsulated extract.

The types of chromosomal aberration at mitotic 
phases included prolonged prophase, stickiness, frag-
ment, chromosoma l brea k /fragmentation at meta-
phase, diagonal metaphase, diagonal telophase, chro-
mosome bridge, star anaphase, fragment at anaphase, 
and vagrant telophase. Figure 1 shows normal mitotic 
phases, while Figure 2 shows types of aberrant chro-
mosomes. Table 3 shows the percentage of each type of 
chromosomal aberration.

Nuclear abnormalities were observed in a different 
set of fields of view than that of chromosomal aberra-
tion. The nuclear abnormalities observed were micro-
nuclei, nuclear fragments, and nuclear lesions (Figure 

Table 1. The Mitotic index and percentage of chromosomal aber-
ration of A. cepa root tip cells induced by Ni, encapsulated E. 
acoroides leaves extract and mixture of Ni and encapsulated extract.

Treatment (ppm) Mitotic index 
Chromosome 
aberration (%)

Control 5.036± 0.497a 0.091±0.1b

30Ni 2.248±0.497c 1.677±0.487a

100Ea 5.048±0.864a 0.553±0.462b

250Ea 3.612±0.444b 0.542±0.227b

500Ea 3.383±0.418b 0.551±0.2097b

30Ni+100Ea 3.262±0.29b 1.453±0.343a

30Ni+250Ea 2.905±0.2176bc 1.575±0.1974a

30Ni+500Ea 2.779±0.489bc 1.601±0.289a

Ni=nickel in the form of Ni(NO3)2.6H2O; Ea=encapsulated E. 
acoroides leaves extract.
Means with same letters at the same column are not significantly 
different.

Table 2. Phase index of mitosis of A. cepa root tip cells after treat-
ment with Ni, encapsulated E. acoroides leaves extract and mixture 
of Ni and encapsulated extract.

Treatment 
(ppm)

Prophase 
Index

Metaphase 
Index

Anaphase 
Index

Telophase 
Index

Control 21.68±8.02a 27.8±5.38b 27.08±7.57a 23.44±5.08a

30 Ni 19.22±8.82a 59.17±18.87a 19.14±13.58a 2.74±3.83b

100 Ea 26.6±8.27a 32.96±4.89b 20.13±7.21a 18.31±7.08a

250 Ea 22.98±6.02a 37.88±5.54b 16.61±4.96a 24.22±3.21a

500 Ea 24.11±9.85a 37.72±13.86b 14.91±4.54a 21.57±3.49a

30 Ni+100 Ea 35.1±12.19a 29.42±11.86b 19.3±6.22a 16.17±5.75a

30 Ni+250 Ea 33.86±7.03a 36.21±4.82b 14.77±10.07a 15.16±5.46a

30 Ni+500 Ea 22.69±8.88a 43.34±15.44ab 17.97±2.83a 16±9.7a

Ni=nickel in the form of Ni(NO3)2.6H2O; Ea=encapsulated E. 
acoroides leaves extract.
Means with same letters at the same column are not significantly 
different.



93Genotoxic and antigenotoxic potential of encapsulated Enhalus acoroides (L. f.) Royle leaves extract against nickel nitrate

3, Table 4). Micronuclei were not detected in control 
and in treatment using 100 ppm, 250 ppm of encapsu-
lated E. acoroides extract, while it was detected at 500 
ppm encapsulated E. acoroides extract but not signifi-
cantly different than control. Treatments with Ni alone 
and combined Ni and encapsulated E. acoroides extract 
resulted in the formation of micronuclei and statisti-
cally, they were not significantly different, although the 
percentage of combined treatments was much lower 
than Ni alone.

Fragmented nuclei were not observed in control and 
in treatment with 100 ppm, 250 ppm, and 500 ppm of 
encapsulated E. acoroides extract. The highest percentage 
of nuclear fragmentation was induced by Ni treatment 
only. The encapsulated E. acoroides extract also induced 
nuclear fragmentation in a significantly lower percentage 
than Ni treatment. The encapsulated E. acoroides extract 

given simultaneously with Ni, significantly reduced the 
percentage of fragmented nuclear (Table 4).

Another nuclear abnormality observed was nuclear 
lesion and Ni treatment showed the highest percentage. 
The addition of encapsulated extract to Ni treatments 
significantly reduced the percentages of nuclear lesions 
compared to Ni treatment (Table 4). 

Metabolic activity

The triphenyl tetrazolium chloride (TTC) stain-
ing was used to examine the influence of Ni and encap-
sulated E. acoroides extract on mitochondrial func-
tion. Treatment of roots with Ni revealed a substantial 
decrease in mitochondrial activity. Visually, the encap-
sulated E. acoroides extract as well as combined encap-
sulated extract and Ni shows an increase in mitochon-
drial activity (Figure 4).

Based on the absorbance value of 490 nm, the 
encapsulated extract at concentrations of 100 ppm and 
250 ppm has no effect, while 500 ppm extract reduced 
mitochondrial activity; however, the reduction was sig-
nificantly less than treatment with Ni (Table 5). Simulta-
neous treatment of encapsulated extract at 100 ppm and 
Ni showed improvement of mitochondrial activity com-
pared to Ni alone. In comparison, the addition of 250 
ppm and 500 ppm encapsulated extract to Ni treatment 
did not show improvement of mitochondrial activity. 

Apoptotic activity

Evans blue stain was used to analyse in situ cell 
death by assessing the cell membrane’s integrity. Living 
cells keep the dye out due to the semipermeable nature 
of cell membranes. On the other hand, damaged cells 
are unable to remove the dye and are thus stained blue 
(Roy et al. 2019). Figure 5 shows the visualization of cell 
death using Evan’s blue staining. 

Evan’s Blue staining method for in situ cell death 
revealed that the encapsulated E. acoroides extract at con-
centrations 100 ppm, 250 ppm, and 500 ppm showed less 
colour than treatment with Ni only. Simultaneous treat-
ment of Ni and encapsulated E. acoroides extract also 
showed a reduction of blue colour indicating a reduc-
tion of cell death (Figure 5). Quantitative analysis using a 
spectrophotometer is shown in Table 5. Statistical analy-
sis revealed that 100 ppm and 250 ppm of encapsulated 
extract had similar effect as control. The 500ppm extract 
showed higher absorbance than control, but significantly 
lower than Ni alone. The data of in situ cell death is simi-
lar to that of mitochondrial activity. The 100 ppm encap-

Figure 1. Normal mitosis of A. cepa root tip cells. a. Prophase; b. 
Metaphase; c. Anaphase; d. Telophase. Scale bar=10μm.

Figure 2. Types of chromosomal aberrations of A. cepa root tip 
cells after treatment with Ni, encapsulated E. acoroides leaves 
extract and combined Ni and encapsulated extract. a=prophase 
abnormality with fragments; b= sticky metaphase; c= fragment 
at metaphase; d=chain metaphase; e=vagrant telophase (circle); 
f=diagonal anaphase; g=chromosome bridge; h=diagonal meta-
phase; i=fragment at anaphase; j=star anaphase; k=sticky anaphase. 
Scale bar=10μm. Arrows indicate abnormalities.



94 Made Pharmawati, Ni Nyoman Wirasiti, Luh Putu Wrasiati

sulated extract when given simultaneously with Ni demon-
strated significantly less cell death than treatment with Ni. 

DISCUSSION

As a result of increased urbanization and industrial-
isation, toxic metal poisoning has become a global issue. 
Moreover, accumulated heavy metal in plants has been 
known to induced chromosome abnormalities as shown 
by Sabeen et al. (2020). 

This present study confirmed that nickel has a geno-
toxic effect by significantly decreasing mitotic index and 

inducing chromosomal aberration. At the concentration 
of 30 ppm Ni(NO3)2.6H2O the reduction of the mitotic 
index was 44.53% in comparison to control. The decline 
of the mitotic index below 50% has sub-lethal effects and 
is known as the limit value of cytotoxicity (Madike et 
al. 2019). The genotoxic effect of nickel has been studied 
using nickel chloride (NiCl2) (Ganesan and Panneersel-
vam 2013), nickel sulfate (NiSO4.6H2O) (Pavlova 2017) 
and nickel nitrate Ni(NO3)2 (Sarac et al. 2019). The con-
centration of 30 ppm Ni was used in this study, to evalu-
ate a lower concentration than that used by Sarac et al. 
(2019) which was 50 ppm. 

Nickel at 30 ppm induced chromosomal aberration 
where chromosome stickiness and chromosome break 

Table 3. The percentage of each type of chromosomal aberration of A. cepa root tip cells after treatment with Ni, encapsulated E. acoroides 
leaves extract and combined Ni and encapsulated extract.

Treatment (ppm)
Frag.pro 

(%)
Sty.meta

(%)
Frag.meta

(%)
Ch.meta

(%)
Diag.meta

(%)
Diag.ana

(%)
Star.ana

(%)
Sty.ana

(%)
Frag.ana

(%)
Bridge

(%)
Vr.telo

(%)

Control 0c 0.091b 0c 0a 0a 0a 0b 0a 0a 0a 0a

30Ni 0.256ab 0.509a 0.656ab 0.062a 0.062a 0.042a 0.1ab 0a 0.081a 0.023a 0a

100Ea 0.069b 0.180ab 0.071c 0.071a 0.032a 0a 0.039ab 0.026a 0.027a 0.039a 0a

250Ea 0.034bc 0.156ab 0.226c 0.026a 0.033a 0a 0b 0.033a 0.034a 0a 0a

500Ea 0.029bc 0.151ab 0.233c 0.032a 0a 0.037a 0.034ab 0a 0.036a 0a 0a

30Ni+100Ea 0.394ab 0.221ab 0.357bc 0.034a 0.069a 0.029a 0.225a 0.059a 0.064a 0a 0a

30Ni+250Ea 0.224ab 0.292ab 0.73ab 0.027a 0a 0a 0.086ab 0.1a 0.027a 0.027a 0.065a

30Ni+500Ea 0.229ab 0.181ab 0.758a 0.034a 0.029a 0.029a 0.13ab 0.068a 0.073a 0.073a 0a

Ni=nickel in the form of Ni(NO3)2.6H2O; Ea=encapsulated E. acoroides leaves extract.
Frag.pro=prophase abnormality with fragments; Sty.meta= sticky metaphase; Frag.meta=fragment at metaphase; Ch.meta=chain metaphase; 
Diag.meta=diagonal metaphase; Diag.ana=diagonal anaphase; Star.ana=star anaphase; Sty.ana=sticky anaphase, Frag.ana=fragment at ana-
phase; Bridge=chromosome bridge; Vr.telo=vagrant telophase.
Means with same letters at the same column are not significantly different.

Table 4. The percentages of nuclear abnormalities of A. cepa root 
tip cells after treatment with Ni, encapsulated E. acoroides leaves 
extract and combined Ni and encapsulated extract.

Treatment 
(ppm)

Micronuclei (%)
Nuclear lesion 

(%)

Nuclear 
fragmentation 

(%)

Control 0±0b 4.57±5.75d 0±0b

30 Ni 0.222±0.192a 90.67±3.58a 0.73±0.609a

100 Ea 0±0b 20,11±2.84c 0±0b

250 Ea 0±0b 20.03±3.78c 0±0b

500 Ea 0.020±0.063b 21.76±3.84c 0±0b

30 Ni+100 Ea 0.083±0.092ab 60.43±8.2b 0.083±0.091b

30 Ni+250 Ea 0.082±0.092ab 62.73±6.29b 0.079±0.087b

30 Ni+500 Ea 0.091±0.1ab 67.48±6.14b 0.076±0.084b

Ni=nickel in the form of Ni(NO3)2.6H2O; Ea=encapsulated E. 
acoroides leaves extract.
Means with same letters at the same column are not significantly 
different.

Table 5. Metabolic and apoptotic activities of A. cepa root tips after 
treatment with Ni, encapsulated E. acoroides leaves extract and 
combined Ni and encapsulated extract.

Treatment (ppm) Metabolic activity Apoptotic activity

Control 0.482±0.034a 0.166±0.03c

30 Ni 0.157±0.006d 0.448±0.053a

100 Ea 0.486±0.05a 0.268±0.07bc

250 Ea 0.479±0.024a 0.286±0.071bc

500 Ea 0.334±0.026b 0.301±0.035b

30 Ni+100 Ea 0.277±0.022bc 0.304±0.015b

30 Ni+250 Ea 0.242±0.057bcd 0.320±0.011ab

30 Ni+500 Ea 0.222±0.024cd 0.344±0.053ab

Ni=nickel in the form of Ni(NO3)2.6H2O; Ea=encapsulated E. 
acoroides leaves extract.
Means with same letters at the same column are not significantly 
different.



95Genotoxic and antigenotoxic potential of encapsulated Enhalus acoroides (L. f.) Royle leaves extract against nickel nitrate

were at a high percentage. This agrees with Sarac et al. 
(2019) and Kaur et al. (2019) who observed that chromo-
some break and chromosome stickiness were the major 
types of chromosomal aberration found due to heavy 
metal treatments. Nickel promotes the generation of a 
large quantity of reactive oxygen species (ROS) which is 
a factor of nickel toxicity. Reactive oxygen species harm 
all cellular components in plants, including cell mem-
branes, lipids, pigments, enzymes, chloroplasts, and 
nucleic acids (Gopal and Nautiyal 2012). Excessive ROS 
promotes DNA break which can be observed through 
the chromosomal break (Ganesan and Panneerselvam 
2013). Chromosome stickiness is caused by chromo-

some loss of physical identity due to physical attachment 
of chromatin material or inter-chromosomal connec-
tions (Asita et al. 2017). Heavy metal complexes are very 
reactive, and their complexes interact directly or indi-
rectly with DNA, histone, or non-histone proteins, caus-
ing chromosomal surface properties to change, making 
them sticky (Kumar and Srivastava 2015). 

The cytotoxicity of encapsulated E. acoroides extract 
was tested by calculating the mitotic index. The mitotic 
index of encapsulated E. acoroides extract at a concen-
tration of 100 ppm was similar to control. Higher con-
centrations of encapsulated extract decreased mitotic 
index but were still higher than the mitotic index of Ni 
treatment. This suggests that at 250 ppm and 500 ppm, 
the encapsulated E. acoroides extract was less toxic than 
Ni. The reduction in the mitotic index shows that the 
encapsulated E. acoroides extract inhibits mitotic activity 
in A. cepa. The reduction in mitotic index is attributable 
to compounds in the aqueous extracts that have cytotox-
ic effects, as the mitotic index is a quantitative measure 
of mitotic activity in an organism or a particular organ 
(Sreeranjini and Siril 2011). 

When Ni and encapsulated extract were given 
simultaneously, only 100 ppm encapsulated extract 
resulted in a significant increase of the mitotic index. 
This indicates that the encapsulated E. acoroides extract 
had the potential in modulated Ni-inhibited mitotic 
activity by increasing the proliferative activity of cells. 
The antigenotoxic activity of low concentrations of plant 
extract was also reported by Prajitha and Thoppil (2016). 
The lower concentration (5 ppm) of Amaranthus spino-
sus employed in the antigenotoxicity experiment was 
beneficial in reversing the genotoxicity. 

Treatment with higher concentrations of encap-
sulated E. acoroides extract combined with Ni did not 
significantly increase mitotic index. A study using Che-
nopodium album extract found that at low concentra-
tion, the extract reduced the genotoxic effect induced 
by EMS (ethylmethane sulfonate). At higher concentra-
tions, C. album extract showed synergistic action with 
EMS, resulting in an increased genotoxic effect (Asita et 
al. 2015). In the present study, encapsulated E. acoroides 
extract did not have a synergetic effect with Ni since the 
addition of encapsulated extract together with Ni, had 
no significantly different with Ni alone on the chromo-
somal aberration. 

Based on analysis of phase index, Ni treatment had 
a significantly higher metaphase index, while the ana-
phase indices were not significantly different between 
treatments. This means that in Ni treatment the ana-
phase index was low. The telophase index of Ni treat-
ment was significantly lower than other treatments. 

Figure 5. Analysis of apoptotic activity using Evans Blue stain-
ing of root of A. cepa. a=control, b=30 ppm Ni, c=100 ppm Ea, 
d=100 ppm Ea, d= 250 ppm Ea, e=500 ppm Ea, f=30ppmNi+100 
ppm Ea, g=30 ppm Ni+250 ppm Ea, h=30 ppm Ni+500 ppm Ea. 
Ea=encapsulated E. acoroides leaves extract.

Figure 4. Analysis of metabolic activity using TTC staining of root 
of A. cepa. a=control, b=30 ppm Ni, c=100 ppm Ea, d=100 ppm 
Ea, d= 250 ppm Ea, e=500 ppm Ea, f=30ppmNi+100 ppm Ea, g=30 
ppm Ni+250 ppm Ea, h=30 ppm Ni+500 ppm Ea. Ea=encapsulated 
E. acoroides leaves extract.

Figure 3. Types of nuclear abnormalities of A. cepa root tip cells 
after treatment with Ni, encapsulated E. acoroides leaves extract and 
combined Ni and encapsulated extract. a. nuclear fragmentation; b. 
micronucleus; c. nuclear lesion. Scale bar=10μm.



96 Made Pharmawati, Ni Nyoman Wirasiti, Luh Putu Wrasiati

According to Asita et al. (2017), a decrease in the pro-
portion of dividing cells in A + T indicates that the 
chromosome spindles were poisoned, resulting in 
metaphase arrest. Low anaphase and telophase indices 
can cause daughter cells to be damaged, limiting plant 
growth. The simultaneous addition of Ni and encapsu-
lated E. acoroides extracts at all concentrations signifi-
cantly increased the telophase indices. 

The percentage of chromosome abnormality between 
control and treatment with all concentrations of encap-
sulated E. acoroides extract were not significantly differ-
ent, indicating the possibility of the non-toxic effect of 
encapsulated E. acoroides extract. This result is impor-
tant since the encapsulated E. acoroides extract had an 
antiproliferative effect by reducing the mitotic index. 
Therefore, it can be further explored in anticancer 
research.

Chromosome aberrations were detected in the com-
bined treatment of Ni and encapsulated E. acoroides 
extract at all concentrations tested. Although there were 
decreases in percentages of chromosome aberration in 
combined Ni and encapsulated extract treatments, the 
percentages were not significantly different from that of 
Ni treatment alone. This result indicates that the concen-
trations of encapsulated E. acoroides extract used unable 
to effectively suppress chromosome aberration induced 
by Ni. However, it is worth noting that there was 14.4% 
inhibitory activity of Ni when 100 ppm encapsulates E. 
acoroides extract was given simultaneously with 30 ppm 
Ni. This suggests that the mixtures were less genotoxic 
than Ni alone. 

Nickel induced the formation of micronuclei and 
nuclear fragmentation at low levels but formed nuclear 
lesions in extremely high percentages. Nuclear lesions 
provide cytological evidence of DNA biosynthesis inhi-
bition (Sajitha and Thoppil 2018). At all concentrations 
tested, the encapsulated E. acoroides extract did not 
induce micronuclei and chromosome fragmentation. 
However, it induced nuclear lesions at low percentag-
es, significantly lower than induced by Ni. The control 
group had a low level of nuclear lesion, which could be 
due to unintentional DNA changes. According to Nefic 
et al. (2013), root tip cells show a very low frequency of 
spontaneous abnormalities. 

In TTC analysis, the roots treated with Ni were 
unable to convert TTC to red coloured TF, indicating 
a significantly lower activity of the mitochondrial res-
piratory chain compared to control. The roots treated 
with encapsulated E. acoroides extract at 250 ppm and 
500 ppm demonstrated no effect on mitochondrial 
activity. The addition of lower concentration of encap-
sulated E. acoroides extract (100 ppm) to 30 ppm Ni 

increased mitochondrial activity compared to treat-
ment with Ni alone.

Apoptotic activity was highly induced in Ni treated 
root, while encapsulated E. acoroides extract showed 
lower apoptotic activity than Ni, but higher activity than 
control. This suggests that encapsulated E. acoroides 
extract was less toxic than Ni. Supplementation of 
encapsulated E. acoroides extracts to Ni, visually result-
ed in lower apoptotic activity than Ni alone as observed 
as less blue colour. However, when measured using a 
spectrophotometer, there were no differences between 
the apoptotic activities at Ni treatment and Ni sup-
plemented with 250 ppm and 500 ppm encapsulated E. 
acoroides extract. Lower concentration of encapsulated 
E. acoroides extract (100 ppm) when given together with 
30 ppm Ni, induced reduction of apoptotic activity. 

The effects of simultaneous addition of Ni and 
encapsulated E. acoroides extract at a lower concentra-
tion to metabolic activity and apoptotic activity agreed 
with their effect on the mitotic index. According to Pra-
jitha and Thoppil (2016), a higher concentration of an 
extract can have mutagenic effect and a lower concen-
tration can have an antimutagenic effect or vice versa. 
In mice, lower levels of b-carotene increased the anti-
clastogenic activity of cyclophosphamide-induced clas-
togenicity, but there was no protective impact at higher 
concentrations. This finding implies distinct processes of 
b-carotene modulation and a probable shift in the bal-
ance of the promutagen activation/detoxification mecha-
nism (Salvadori et al. 1992). Similar reasoning may apply 
to the effect of simultaneous addition of Ni and low con-
centration encapsulated E. acoroides extract on increas-
ing mitotic index and metabolic activity and reducing 
apoptotic activity.

Enhalus acoroides leaves extract contained phyto-
chemical compounds, including phenols, tannins, and 
flavonoids. The FTIR analysis confirmed the presence of 
flavonoid and polyphenols as a high C-H out-of-plane 
bending (oop bend) vibration for the substituted ben-
zene ring was identified in the extract (Pharmawati and 
Wrasiati 2020). These phytochemical components in the 
plant extracts may be responsible for the reduced mitotic 
index in A. cepa root meristematic cells when roots were 
treated with encapsulated E. acoroides leaves extract. 
On the other hand, these phytochemical compounds 
may contribute to the increasing mitotic index, lowering 
nuclear abnormalities when the encapsulated extract is 
present together in the Ni treatment. This kind of result 
where plant extract showed the opposite effect was also 
observed by Prajitha and Thoppil (2016) in Amaranthus 
spinosus extract. The encapsulated E. acoroides leaves 
extract also contained pigments such as chlorophyll b, 



97Genotoxic and antigenotoxic potential of encapsulated Enhalus acoroides (L. f.) Royle leaves extract against nickel nitrate

ethyl-chlorophyllide a, Mg-free chlorophyll b, lutein, Mg 
free chlorophyll a, pheophytin, and β-carotene (Phar-
mawati and Wrasiati 2020). It is well known that phe-
nolic compounds, tannins, flavonoids, chlorophyll, and 
carotenoids have antioxidant properties (Aryal et al. 
2019). Antioxidants containing phenolics can prevent 
the generation of free radicals and/or stop the spread 
of autoxidation. At the same plant pigments can chelate 
metals and transfer hydrogen to oxygen radicals, delay-
ing oxidation (Brewer 2011).

In the present investigation, the encapsulated E. 
acoroides extract was found to have preventive activity, 
as evidenced by the reduction and reversion of nuclear 
damages (nuclear lesions and nuclear fragmentations) 
caused by Ni. However, the encapsulated extract can-
not reduce chromosomal aberration. Preincubation with 
the encapsulation extract before Ni treatment needs to 
be evaluated to test the ability of encapsulated extract to 
suppress chromosomal abnormalities. Further study is 
also needed to test the protective activity of the encapsu-
lated extract on animal cells.

ACKNOWLEDGMENT

The authors thank Universitas Udayana for sup-
porting this study through the Study Program Flagship 
Research Scheme No. B/773/UN14.2.8.II/PT.01.03/2021

FUNDING

Universitas Udayana through the Study Program 
Flagship Research Scheme No. B/773/UN14.2.8.II/
PT.01.03/2021

REFERENCES

Amjad M, Raza H, Murtaza B, Abbas G, Imran M, Sha-
hid M, Naeem MA, Zakir A, Iqbal MM. 2020. Nick-
el toxicity induced changes in nutrient dynamics 
and antioxidant profiling in two maize (Zea mays 
L.) Hybrids. Plants. 9(1):5. https://doi.org/10.3390/
plants9010005

Aryal S, Baniya MK, Danekhu K, Kunwar P, Gurung R, 
Koirala N. 2019. Total phenolic content, flavonoid 
content and antioxidant potential of wild vegetables 
from Western Nepal. Plants. 8(4):96. doi:10.3390/
plants8040096

Asita AO, Heisi DH, Tjale T. 2015. Modulation of muta-
gen-induced genotoxicity by two Lesotho medicinal 

plants in Allium cepa L. Environ Nat Resour Res. 
5(3):37-55

Asita OA, Moramang S, Rants’o T, Magama S. 2017. Mod-
ulation of mutagen-induced genotoxicity by vitamin 
C and medicinal plants in Allium cepa L. Caryologia. 
70: 51-165. doi: 10.1080/00087114.2017.1311166 

Brewer MS. 2011. Natural antioxidants: sources, com-
pounds, mechanisms of action, and potential appli-
cations. Compr Rev Food Sci Food Saf. 10:221-247. 
doi: 10.1111/j.1541-4337.2011.00156.x

Cempel M, Nikel G. 2006. Nickel: A Review of Its Sourc-
es and Environmental Toxicology. Polish J Environ 
Stud. 15(3):375-382

den Hartog C, Kuo J. 2006. Taxonomy and biography of 
seagrasses. In: Larkum T, Orth RJ, Duarte CM, edi-
tors. Seagrasses: Biology, ecology and conservation. 
The Netherlands: Springer: p. 1-23. 

Ganesan A, Panneerselvam N. 2013. Analysis of Ni 
induced genotoxicity in root meristem of Allium 
cepa. Inter. J. Biological Technol. 4:19-22 

Gantayat S, Mania S, Pradhan C, Das AB. 2018. Ionic 
stress induced cytotoxic effect of cadmium and nickel 
ions on roots of Allium cepa L. Cytologia 83(2):143–
148

Gopal R, Nautiyal N. 2012. Growth, antioxidant enzymes 
activities, and proline accumulation in mustard due 
to nickel. Int. J. Veg. Sci . 18:223–234. 

Huang L, Rad S, Xu L, Gui L, Song X, Li Y, Wu Z, Chen 
Z. 2020. Heavy metals distribution, sources, and eco-
logical risk assessment in Huixian Wetland, South 
China. Water.12(2):431. https://doi.org/10.3390/
w12020431

Kaur M, Sharma A, Soodan RK, Chahal V, Kumar V, Kat-
noria JK, Nagpal AK. 2019. Allium cepa root chro-
mosomal aberration assay: A tool to assess genotox-
icity of environmental contaminants. Environ Con-
tam Nat Prod. 2019:65-93

Kilawati Y, Islamy RA. 2019. The antigenotoxic activity of 
brown seaweed (Sargassum sp.) Extract Against Total 
Erythrocyte and Micronuclei of Tilapia (Oreochromis 
niloticus) Exposed by Methomyl-Base Pesticide. J Exp 
Life Sci. 9:205-210

Kiswara W, Hutomo M. 1985. Habitat Dan Sebaran Geo-
grafik Lamun. Oseana. XII(1): 21-30.

Kumar G, Srivastava A. 2015. Comparative genotoxicity 
of herbicide ingredients glyphosate and atrazine on 
root meristem of buckwheat (Fagopyrum esculentum 
Moench). Jordan J Biol Sci. 8(3):221-226 

Kumar S, Thonger T. 2016. Study on 24 Hour Root Tip 
Cell Division Mitotic and Mitotic Phase Index of 
Allium chinense. American-Eurasian J. Agric. Envi-
ron. Sci. 16(1):172-183



98 Made Pharmawati, Ni Nyoman Wirasiti, Luh Putu Wrasiati

López-Romero D, Izquierdo-Vega JA, Morales-González 
JA, Madrigal-Bujaidar E, Chamorro-Cevallos G, 
Sánchez-Gutiérrez M, Betanzos-Cabrera G, Alvarez-
Gonzalez I, Morales-González Á, Madrigal-Santillán 
E. 2018. Evidence of some natural products with 
antigenotoxic effects. Part 2: Plants, Vegetables, and 
Natural Resin. Nutrients, 10(12):1954. https://doi.
org/10.3390/nu10121954

Madike LN, Takaidza S, Ssemakalu C, Pillay M. 2019. 
Genotoxicity of aqueous extracts of Tulbaghia 
violacea as determined through an Allium cepa 
assay. S Afr J Sci. 115(1/2), Art. #4391, https://doi. 
org/10.17159/sajs.2019/4391

McKenzie LJ, Yoshida RL. 2009. Seagrass-watch. Proceed-
ing of a workshop for monitoring seagrass habitats in 
Indonesia. The Nature Conservancy, Coral Triangle 
Center, Sanur, Bali: pp. 29-32

Nefic H, Musanovic J, Metovic A, Kurteshi K. 2013. 
Chromosomal and nuclear alterations in root tip cells 
of Allium cepa L. induced by alprazolam. Med Arch. 
(Sarajevo, Bosnia and Herzegovina) 67(6):388–392. 
doi.org/10.5455/medarh.2013.67.388-392

Oyeyemi IT, Bakare AA. 2013. Genotoxic and antigeno-
toxic effect of aqueous extracts of Spondias mombin 
L., Nymphea lotus L. and Luffa cylindrica L. on Alli-
um cepa root tip cells. Caryologia. 66(4): 360-367. 
https://doi.org/10.1080/00087114.2013.857829

Özkan G, Bilek SE. 2014. Microencapsulation of natural 
food colourants. Intl J Nutr Food Sci. 3(3):145–56. 
doi:10.11648/j.ijnfs.20140303.13

Pavlova D. 2017. Nickel effect on root-meristem cell divi-
sion in Plantago lanceolata (Plantaginaceae) seed-
lings. Aust J Bot. 65:446-452. https://doi.org/10.1071/
BT17054

Pharmawati M, Wrasiati LP. 2020. Phytochemical screening 
and FTIR spectroscopy on crude extract from Enhalus 
acoroides leaves. Malays J Anal Sci. 24(1):70-77

Prajitha V, Thoppil JE. 2016. Genotoxic and antigenotoxic 
potential of the aqueous leaf extracts of Amaranthus 
spinosus Linn. using Allium cepa assay. S Afr J Bot. 
102:18-25 https://doi.org/10.1016/j.sajb.2015.06.018.

Rodeiro I, Olguín S, Santes R, Herrera JA, Pérez CL, 
Mangas R., Hernández Y, Fernández G, Hernández I, 
Hernández-Ojeda S, Camacho-Carranza R, Valencia-
Olvera A, Espinosa-Aguirre JJ. 2015. Gas chroma-
tography-mass spectrometry analysis of Ulva fasciata 
(green seaweed) extract and evaluation of its cytopro-
tective and antigenotoxic effects. Evid Base Comple-
mentary Altern Med. 2015. Article ID 520598. http://
dx.doi.org/10.1155/2015/520598

Roy B, Krishnan SP, Chandrasekaran N, Mukherjee A. 
2019. Toxic effects of engineered nanoparticles (met-

al/metal oxides) on plants using Allium cepa as a 
model system. In: Verma SK, Das AK, (editors). Com-
prehensive Analytical Chemistry, Elsevier: p. 125-143

Sabeen M, Mahmood Q, Ahmad Bhatti, Z., Faridullah, 
Irshad M, Bilal M, Hayat MT, Irshad U, Ali Akbar T, 
Arslan M, Shahid N. 2020. Allium cepa assay based 
comparative study of selected vegetables and the 
chromosomal aberrations due to heavy metal accu-
mulation. Saudi J Biol Sci. 27(5):1368–1374. https://
doi.org/10.1016/j.sjbs.2019.12.011

Sajitha MK, Thoppil JE. 2018. Screening of cytotoxicity, 
metabolic inhibition and possible apoptotic cell death 
induced by Gomphostemma heyneanum Wall. ex 
Benth. var. heyneanum using Allium cepa root tips. 
Int J Pharm Biol Sci. 8(2):56-64

Salvadori DMF, Ribeiro LR, Oliveira MDM, Pereira CAB, 
Beçak W. 1992. The protective effect of β-carotene on 
genotoxicity induced by cyclophosphamide. Mutat 
Res. 265(2):237–244

Sarac I, Bonciu E, Butnariu M, Petrescu I, Madosa E. 
2019. Evaluation of the cytotoxic and genotoxic 
potential of some heavy metals by use of Allium test. 
Caryologia. 72:37-43.

Sharma AK, Sharma A. 1994. Chromosome Technique 
A Manual. CRC Press, Taylor & Francis Group, Boca 
Raton, Florida, USA. p. 1-32

Sharma S, Nagpal A, Vig AP. 2012. Genoprotective 
potential of Brassica juncea (L.) Czern. Against mer-
cury-induced genotoxicity in Allium cepa L. Turk J 
Biol. 36:622-629 doi:10.3906/biy-1110-18

Sharma S, Sharma S, Vig AP. 2018. Antigenotoxic potential 
of plant leaf extracts of Parkinsonia aculeata L. using 
Allium cepa assay. Plant Physiol Biochem. 130:314-323. 
https://doi.org/10.1016/j.plaphy.2018.07.017

Short, F.T. & Waycott, M. 2010. Enhalus acoroides. 
The IUCN Red List of Threatened Species 2010: 
e.T173331A6992567. https://dx.doi.org/10.2305/IUCN.
UK.2010-3.RLTS.T173331A6992567.en. Accessed on 
31 January 2022.

Singh SB, Singh K, Butola SS, Rawat S, Arunachalam K. 
2020. Determination of macronutrients, micronutri-
ents and heavy metals present in Spilanthes acmella 
Hutch and Dalz: possible health effects. Nat Prod Sci. 
26(1):50-58. 10.20307/nps.2020.26.1.50.

Sreeranjini S, Siril EA. 2011. Evaluation of anti-genotox-
icity of the leaf extracts of Morinda citrifolia Linn. 
Plant Soil Environ. 57:222–227

Šturm L, Črnivec IGO, Istenič K, Ota A, Megušar P, Slu-
kan A, Humar M, Levic S, Nedović V, Kopinč R, 
Deželak M, Gonzales AP, Ulrih NP. 2019. Encapsula-
tion of non-dewaxed propolis by freeze-drying and 
spray-drying using gum Arabic, maltodextrin and 



99Genotoxic and antigenotoxic potential of encapsulated Enhalus acoroides (L. f.) Royle leaves extract against nickel nitrate

inulin as coating materials. Food Bioprod Process. 
116:196-211,

Sulistyadewi ENP, Wrasiati LP, Wartini NM. 2014. Peru-
bahan kadar MDA, SOD, dan kapasitas antioksidan 
hati tikus 13prague dawley pada pemberian ekstrak 
bubuk daun cemcem (Spondias Pinnata (L.f ) Kurz). 
Media Ilmiah Teknol Pangan. 1(1):71-80.

Vazhangat P, Thoppil JE. 2016. Apoptotic induction via 
membrane/DNA damage and metabolic inactivation 
by synthetic food colorants in Allium cepa root mer-
istem. Turk J Biol. 40: 922-933

Yusop FHM, Manaf SFA, Hamzah F. 2017. Preserva-
tion of bioactive compound via microencapsulation. 
Chem Eng Res Bull. 19:50-56


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