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Modern science has found that most traditional practice of using stingless bee honey has great potential as an added value in modern medicine and considered to have a higher medicinal value than other bee species. However, due to the relatively low output of honey compared to other honey so, focus on this honey is limited. Hence, this systematic review provides the updated result on the potential value of stingless bee honey as an antioxidant, anti-inflammatory, cytotoxicity and antimicrobial. The search strategy was developed in four databases (Scopus, Medline and Ovid, EMBASE and PubMed) with the search terms "("honey" and "Kelulut", "honey" and "stingless bee", "honey" and "Trigona", "honey" and "pot honey", and "honey" and "Melipon")". The merged data was assessed using PRISMA guidelines and after the duplicates were removed, 1271 articles were segregated. Afterwards, 1232 articles were eliminated because they do not meet the inclusion criteria and 39 articles were reevaluated again for eligibility. Finally, after the evaluation process, only 26 of the articles were chosen for this review. The data of 26 articles of stingless bee honey were deliberated based on antioxidant properties, anti-inflammatory, cytotoxicity and analysis of antimicrobial activity. Three articles reported on antioxidant properties, one article on anti-inflammatory analysis, two articles on cytotoxicity analysis, and twenty articles on analysis of antimicrobial activity. Based on the feasible affirmation from the literature, stingless bee honey has an antioxidant capacity that able to decrease the ROS. ROS able to lead a variety of health problems thus stingless bee honey can be a dietary supplement to overcome this problem.
Content may be subject to copyright.
*Corresponding author.
Email: razinah@ukm.edu.my eISSN: 2550-2166 / © 2017 The Authors. Published by Rynnye Lyan Resources
Food Research 2 (2) : 124 - 133 (April 2018)
Journal homepage: http://www.myfoodresearch.com
MINI REVIEW
Stingless bee honey and its potential value: a systematic review
1,4Yaacob, M., 2Rajab N.F., 3Shahar, S. and 1*Sharif, R.
1Nutritional Sciences Programme, School of Healthcare Sciences, Faculty of Health Sciences, Universiti
Kebangsaan Malaysia
2 Biomedical Science Programme, Faculty of Health Sciences, Universiti Kebangsaan Malaysia
3 Dietetics Programme, Faculty of Health Sciences, Universiti Kebangsaan Malaysia
4 Faculty of Medicine and Health Sciences, Universiti Sains Islam Malaysia
Article history:
Received: 6 September 2017
Received in revised form: 19
September 2017
Accepted: 22 September 2017
Available Online: 15 October
2017
Keywords:
Kelulut,
Trigona sp.,
Anti-inflammatory,
Antimicrobial,
Antioxidant
DOI:
https://doi.org/10.26656/fr.2017.2(2).212
Abstract
Modern science has found that most traditional practice of using stingless bee honey has
great potential as an added value in modern medicine and considered to have a higher
medicinal value than other bee species. However, due to the relatively low output of honey
compared to other honey so, focus on this honey is limited. Hence, this systematic review
provides the updated result on the potential value of stingless bee honey as an antioxidant,
anti-inflammatory, cytotoxicity and antimicrobial. The search strategy was developed in
four databases (Scopus, Medline and Ovid, EMBASE and PubMed) with the search terms
"("honey" and "Kelulut", "honey" and "stingless bee", "honey" and "Trigona", "honey"
and "pot honey", and "honey" and "Melipon")". The merged data was assessed using
PRISMA guidelines and after the duplicates were removed, 1271 articles were segregated.
Afterwards, 1232 articles were eliminated because they do not meet the inclusion criteria
and 39 articles were reevaluated again for eligibility. Finally, after the evaluation process,
only 26 of the articles were chosen for this review. The data of 26 articles of stingless bee
honey were deliberated based on antioxidant properties, anti-inflammatory, cytotoxicity
and analysis of antimicrobial activity. Three articles reported on antioxidant properties,
one article on anti-inflammatory analysis, two articles on cytotoxicity analysis, and twenty
articles on analysis of antimicrobial activity. Based on the feasible affirmation from the
literature, stingless bee honey has an antioxidant capacity that able to decrease the ROS.
ROS able to lead a variety of health problems thus stingless bee honey can be a dietary
supplement to overcome this problem.
1. Introduction
Honey is a natural food derived from honey bee and
most commonly used as a sweetener. Besides, honey also
is known for its remedial value (Rodríguez et al., 2012).
Even though there has a study on the potential of honey
in treating several health problems but studies mostly are
focusing on Tualang and Manuka honey compared to the
stingless bee honey due to the low production of honey
(Roowi et al., 2012). Therefore, there has no guarantee
of their nutrients to the user since it not yet included in
the Codex Alimentarius for honey (Codex, 2001).
Previous study showed that stingless bee honey
can act as anti-inflammatory (Borsato et al., 2014), anti-
cancer (Kustiawan et al., 2014; Yazan et al., 2016), anti-
microbial (Miorin et al., 2003; Demera et al., 2004;
Garedew et al., 2004; Temaru et al., 2007; Kimoto-Nira
and Amano, 2008; Chanchao et al., 2009; Boorn et al.,
2010; Rodríguez et al., 2012; Ilechie et al., 2012;
Andualem, 2013; Ewnetu et al., 2013; Mercês et al.,
2013; Queiroz et al., 2013; Zainol et al., 2013; Nobre da
Cruz et al., 2014; Massaro et al., 2014; Zamora et al.,
2014; Nishio et al., 2016; Medeiros et al., 2016; De
Sousa et al., 2016; Nishio et al., 2016) and possessed
antioxidant properties (Duarte et al., 2012; Almeida da
Silva et al., 2013; De Sousa et al., 2016). However, the
beneficial of stingless bee honey has been abandoned in
modern medicine due to the paucity of systematic
scientific studies for supporting its medical properties
(Pe´rez et al., 2006).
The composition of stingless bee honey differ from
other species according to some physicochemical
parameters (Özbalci et al., 2013) and other studies prove
that honey from stingless bees are more valuable and it
has been used for a long time to treat various diseases
125 Yaacob and Sharif / Food Research 2 (2) (2018) 124 - 133
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(Souza et al., 2006).
Stingless bees is a small bee from the species of
Trigona or Meliponine and also known as Kelulut bee in
Malaysia is the type of honey that has a high medicinal
beneficial than other bee species which had alleged by
the traditional medical practitioner (Biswa et al., 2017)
They are the main pollinators among the other bees and
can be found mostly in tropical and subtropical regions
(Fowler, 1979) . The color of the honey is usually
clearer, liquid and has a sweet and sour taste (Roowi et
al., 2012). The recent studies showed that the stingless
bee honey has the potential to treat colorectal cancer
(Yazan et al., 2016), anti-inflammatory (Borsato et al.,
2014), antimicrobial (Zainol et al., 2013; Nobre da Cruz
et al., 2014; Massaro et al., 2014; Nishio et al., 2016;
Medeiros et al., 2016; De Sousa et al., 2016; Nishio et
al., 2016) and has an antioxidant property (Almeida Da
Silva et al., 2013; Duarte et al., 2012).
This review aims to prove current scientific evidence
regarding the stingless bee honey and its potential value
on health as anti-inflammatory, cytotoxicity,
antimicrobial and also the antioxidant properties.
2. Materials and methods
2.1 Search strategy
The search for articles from databases namely
Scopus, Medline and Ovid, EMBASE, and PubMed were
performed until October 2016. Search strategies were
adjusted to well-suited with the subject headings and
keywords of each database were carried out. The search
terms encompass “honey” and Kelulut”, “honey” and
“stingless bee”, “honey” and “Trigona”, “honey” and
“pot honey”, and “honey” and Melipon”. The
compatible references were re-evaluated for affirmation
of the search string. In addition, pertinent reviews were
also included as an additional source of literature reports.
All the search databases were exported into an Endnote
library to remove duplicates.
2.2 Inclusion criteria
Stingless bee is also known as Kelulut, Trigona spp,
Melipona spp., Meliponine spp and pot honey bee in
other literature. In this review, in vitro and in vivo studies
that investigated the benefit of honey from stingless bee
were included. From the databases, only stingless bee
honey as anti-inflammatory, cytotoxicity, antimicrobial
and antioxidant properties were included in this study.
Studies published in English and Malay were taken into
deliberation.
2.3 Exclusion criteria
Literature reports on propolis and behavior study of
the honeybee or other species of bee were excluded from
the study. The studies on physicochemical of stingless
bee honey or bioactive chemical component in honey
also were excluded this review.
2.4 Study selection
The prime literature search was executed by authors.
All duplicate articles were first filtered out by a software
and followed by hand search to verify there is no
duplicate articles were included. Potential relevant
papers were chosen by screening the title, abstract, and
retrieval of the full article from the database search.
Afterwards, the resulting irrelevant reports were rejected
according to inclusion and exclusion criteria. After that,
full-text articles were downloaded and then assessed for
eligibility. If the papers were not published in English
and Malay, these studies were excluded at this time
point.
2.5 Data organization and reporting
The information acquired from each study were
arranged particularly according to the data about the
author’s name, year of publication, type of cell or
bacteria used, type of stingless bee species, experimental
method, and outcomes. The inclusion studies were
reported according to PRISMA guidelines (http://
www.prisma-statement.org/statement.htm). PRISMA
also provides a flowchart to illustrate the searching
strategy until the assessment process.
3. Results
3.1 Descriptive of selected studies
Figure 1 is an illustration of the procedure for the
study selection. A total of 1796 articles were found after
searching in four differences databases. 1271 articles
were segregated after removal of duplicates. Afterwards,
1232 articles were rejected because they did not fulfill
the inclusion criteria and 39 articles were reevaluated
again for the qualification. Finally, 13 articles which
were not written in English or Malay language were
removed and only 26 of the reports were deliberated for
this review. All the 26 reports were found and further
analysis regarding the type of honey from difference
stingless bee species and outcomes were summarized in
Tables 1-4.
3.2 Antioxidant properties of stingless bee honey
The clinical finding reported that oxidative stress can
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cause oxidative damage to deoxyribonucleic acid
(DNA), proteins, and fats and antioxidants can stop or
slow down the process of oxidative stress in the cell
(Block et al., 2002). Oxidative stress can lead the
development of neurological diseases (Alzheimer's
disease and Parkinson's disease), atherosclerosis, joint
disorders, cardiovascular diseases, lung and kidney
disorders, eye disorders, cancer, aging and other
degenerative diseases (Rahman et al., 2012). Therefore,
antioxidant properties such as phenolic acid can decrease
the oxidative stress.
Total phenolic content differs among the honey
regarding their type of bee species, region, season and
type of floral sources (Almeida da Silva et al., 2013).
Although Apis spp. is more recognize compared to the
species from a stingless bee, but the total phenolic acid
of stingless bee from species Plebeia spp. was higher
than Apis spp. which is 106.01 ± 9.85 mg GA equivalent/
100g compared to Apis sp. 92.34 ± 13.55 mg GA acid
equivalent/ 100 g (Duarte et al., 2012). Meanwhile for
antioxidant activity of Plebeia spp. is 49.91± 21.36 mg
GA equivalent/ 100 g. Moreover, Almeida da Silva et al.
(2013) reported that honey sample which displayed the
highest total phenolic content have slightly highest
ABTS+ cation radical scavenging capacity. This result
indicates that there is a correlation between phenolic
content and antioxidant activity in the stingless bee’s
honey (Duarte et al., 2012; De Sousa et al., 2016).
3.3 Biology action of antioxidant activity
3.3.1 Anti-inflammatory
Previous literature reported that phenolic compound
had related to anti-inflammatory effects on the animal
(Larrosa et al., 2009). Caffeic and ferulic acids, the
derivatives from phenolic acid can reduce inflammation
in neurovascular and able to inhibit macrophage
inflammatory protein-2 (MIP-2) (Larrosa et al., 2009).
Meanwhile, kaempferol showed an inhibitory effect on
NO synthase (iNOS) and cyclooxygenase- 2 (COX- 2)
(Crespo et al., 2008). The studies conducted by Borsato
et al. (2014) proved that phenolic acid from an extract of
honey from stingless bee had decreased the production of
reactive oxygen species (ROS) in 55 ± 14%. A study
done by Larrosa et al. (2009) is the early report
described the anti-inflammatory activity of honey extract
from stingless bee species (M. marginata) by in vivo
approaches thus, conclude that the stingless bee honey
able to decrease ear edema (Borsato et al., 2014).
3.3.2 Anti-proliferative
There had very few studies anti- proliferative of
stingless bee honey on cancer cell lines. The previous
studies showed the stingless bee honey showed
cytotoxically sensitive to the liver hepatocellular
carcinoma cell lines (HepG2) and lung bronchus
carcinoma cell line (ChaGo- I). In contrast, colon
carcinoma cell lines (SW620), human gastric carcinoma
cell lines (KATO-III) and ductal carcinoma cell lines
(BT474) were insensitive to honey (Kustiawan et al.,
2014). This showed that the honey can gave a different
effect on various cell lines (Porcza et al., 2016). Further
studies on cytotoxicity activity of the known pure
compound of kaempferol, apigenin, caffeic acid
phenethyl ester (CAPE), and narigenin which are derived
from phenolic acid in honey were investigated (Yazan et
al., 2016). The results revealed that these compounds
have cytotoxic effects on the ChaGo-I and KATO-III cell
lines, KATO-III and BT474 respectively (Kustiawan et
al., 2014; Yazan et al., 2016). This suggests that each
compound from phenolic acid can be cytotoxic to the
tested cancer cell. Meanwhile, another studied done on
Sprague Dawley rats which are induced with colorectal
cancer shown that the stingless bee honey able to reduce
the total number of aberrant crypts (AC), crypt
multiplicity and aberrant crypt foci (AFC) thus, indicated
the potential of the honey as chemo-preventive agent
(Yazan et al., 2016).
3.3.3 Antimicrobial
The antimicrobial activities of honey were reported
due to phytochemicals, acidity, high osmolarity, and the
presence of hydrogen peroxide in the honey (Molan,
1992). From the Table 4, honey from stingless bee has a
Figure 1. Flowchart of search strategy and selection process
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Authors and
Year Types Method Outcomes
De Sousa et al.
(2016)
M. subnitida Ducke and
M. scutellaris Latrelle
ABTS cation radical scav-
enging and DPPH scaveng-
ing method
Honey of M. subnitida Ducke showed the
higher antioxidant activity compared to M.
scutellaris Latrelle in both assays.
Almeida da
Silva et al.
(2013)
Melipona (Michmelia)
seminigra merrillae)
ABTS cation radical scav-
enging
The samples showed the highest antioxidant
capacity has a higher total phenolic content.
Duarte et al.
(2012)
Plebeia spp. Ferric reducing antioxidant
power (FRAP) assay and
(DPPH) scavenging assay
Honey from Plebeia spp. has higher content
of total phenolics, flavonoids and antioxi-
dants capacity compared to Apis sp.
Table 1. Antioxidant analysis of stingless bee honey.
Authors
and Year
Study
population Types Method Outcomes
Borsato
et al.
(2014)
Animals.
Male Swiss
mice
Stingless bee from
species Melipona
marginata
Mice induced with 12-O-
tetradecanoylphorbol- 13-
acetate- induced for ear edema model.
The honey extract (1.0 mg/ear)
had the ability to reduce ear edema
with an inhibitory effect of 54 ±
5%.
Table 2. Anti-inflammatory analysis of stingless bee honey.
Authors and
Year
Study
population Types Method Outcomes
Yazan et al.
(2016)
Sprague
Dawley rats
aged 5
weeks (n=
24)
Honey from
Trigona sp.
Rats were injected with azoxymethane
(15mg/kg) and the treatment groups
were given via oral administration of
Kelulut honey (1183mg/kg body
weight) twice per day for 8 weeks.
The total number of aberrant crypt
foci (ACF) and aberrant crypts
(AC) and crypt multiplicity were
significantly reduced. This
suggests that stingless bee honey
has chemopreventive properties.
Kustiawan et
al. (2014)
Human
cancer cell
lines
HepG2
SW620
ChaGo- 1
KATO- III
BT474
Trigona incisa,
Trigona apicalis,
T. fuscobalteata,
T. fuscibisca
Crude extract was screened for in
vitro cytotoxicity against the cell lines
using the 3-(4, 5- dimethylthiazol- 2-
yl) - 2, 5- diphenyltetrazolium
bromide assay.
Crude extract of stingless bee has
cytotoxic effect to HepG2 cell
line.
Table 3. Cytotoxicity studies of stingless bee honey
Figure 2. Schematic diagram on the potential effects of stingless bee’s honey to enhance better life. Abbreviations: ABTS+, 2,
2'-azino-bis (3-ethylbenzothiazoline-6-sulphonic acid); MPO, Myeloperoxidase; MIP-2, macrophage inflammatory protein-2;
COX-2, cyclooxygenase-2; MOA, mode of action
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broad spectrum antibacterial activity because honey can
act against a wide range of bacteria that able to cause
disease (Boorn et al., 2010; Nishio et al., 2016). Most of
the studies of honey were performed on Staphylococcus
aureus (Miorin et al., 2003; Demera et al., 2004; Temaru
et al., 2007; Chanchao et al., 2009; Boorn et al., 2010;
Chan- Rodriguez et al., 2012; Ilechie et al., 2012;
Andualem et al., 2013; Ewnetu et al., 2013; Merces et
al., 2013; Queiroz et al., 2013; Zainol et al., 2013; Nobre
da Cruz et al., 2014; Massaro et al., 2014; Zamora et al.,
2014) showed that it is the most susceptible tested
pathogen to stingless bee honey. As we know,
Staphylococcus aureus is a common pathogen found in
human skin and can cause infection in the presence of a
wound. From the studies, bee honey can reduce the risk
of infection to humans by this pathogen. Meanwhile, De
Sousa et al. (2016) and Chan- Rodriguez et al. (2012)
stated that this honey can control the foodborne disease
by inhibiting the foodborne organism such as
Escherichia coli and Staphylococcus aureus. Stingless
bee honey also can be shortened the infections time for
eye diseases caused by Staphylococcus aureus and
Pseudomonas aeruginosa which were studied on as a
model (Ilechie et al., 2012). Moreover, a study done by
Kimoto-Nira and Amano (2008) proved that stingless
bee honey able to protect against gastrointestinal
infection in humans. Due to the emerging of the
antibiotic resistant bacteria such as Methicillin-resistant
Staphylococcus aureus (MRSA), the potential of the
honey to become an antibacterial agent to against this
problem were proved by studies done by Nishio et al.
(2016) and Medeiros et al. (2016).
4. Discussion
This systematic review identified 26 reports on
antioxidant properties of stingless bee honey and its
potential value on health as anti-inflammatory,
cytotoxicity, and antimicrobial (Figure 2). There are 2
studies on antioxidant properties that revealed the
correlation between the total phenolic content and
antioxidant properties (Duarte et al., 2012; Almeida da
Silva et al., 2013). Generally, phenolic content plays a
role to reduce the disease that associated with oxidative
stress. By the presence of this active compound, it makes
the stingless bee honey valuable for medical purpose.
Meanwhile, another paper focusing on stingless bee
honey from a variety of sample from differences
locations which is best to know either the total phenolic
compound and antioxidant are vary depending on
geographic and type of floral used. The antioxidant
properties also varied depend on soil type although
mainly due to the type of floral sources.
The study conducted by Borsato et al. (2014)
indicates that stingless bee honey extract has a topical
anti-inflammatory activity by reducing the production of
reactive oxygen species, leukocyte migration and as well
as reduced edema. From the study, they are comparing
the correlation between the presence of the phenolic
compound in the stingless bee honey with the anti-
inflammatory effects. This is the good experimental
paper which it determines anti-inflammatory by
measurement ear thickness before and after treatment in
which referring to the inflammation condition and also
histological analysis. Moreover, this is the first report
describing the anti-inflammatory activity of stingless bee
honey extract by using in vivo approaches and this can
lead more studies on the anti-inflammatory effect of the
honey and can make it be a potential therapeutic
opportunity against inflammatory (Borsato et al., 2014).
From the study done by Kuatiawan et al. (2014),
stingless bee honey showed a cytotoxicity effect to most
of the cell lines. Honey has a broad target of mechanism
to become cytotoxic to the cell either act as anti-
proliferative or apoptotic (Porcza et al. 2016).
Meanwhile for the ex-vivo experimental designed by the
Yazan et al. (2016) by using the Sprague Dawley rats
induced with colorectal cancer is the good platform to
show the overall effect of the honey on the living
subject.
Due to a shortage of new development of antibiotic
to combat with the bacteria and multidrug resistance
bacteria, usage of honey as an antimicrobial agent might
be promising. Antimicrobial properties of honey may be
related to the presence of flavonoids (Miorin et al.,
2003). Flavonoids also can combat oxidative stress as
well as inhibit the pathogens (Shashank and Abhay,
2013).
5. Conclusion
From the studies, stingless bee honey showed a
potential for use in medicine as it contains phenolic that
increases antioxidant content as well as it can decrease
oxidative stress-related diseases.
Conflict of Interest
No potential conflict of interest was reported by the
authors.
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Authors
and Year Study population Types Method Outcomes
Nishio et
al.
(2016)
Methicillin-resistant S. aureus
(MRSA) and Methicillin-sensitive
S. aureus (MSSA)
Scaptotrigona
postica (H6)
and
Scaptotrigona
bipunctata
(H7)
Agar diffusion assay,
Minimum inhibitory
concentrations (MIC),
growth curves and viability
curves.
The inhibition zones generated
by the honey samples ranged
from 20mm to 27 mm and
MIC values ranged from 0.62
to 1 2.5%.
Medeiros
et al.
(2016)
MRSA- infected wounds of rats
(n= 24)
Melipona
scutellaris
The uninfected skin
wounds of rats were treated
with honey and inoculated
with MRSA ATTC43300.
Bacterial culture and
wound biopsies was
performed.
Honey of Melipona
scutellaris inhibit the
bacterial growth and
increase the cytokine
expression.
De sousa
et al.
(2016)
Listeria monocytogenes, S.
aureus, E. coli, Salmonella sp.,
and P. aeruginosa.
M. subnitida
Ducke and M.
scutellaris
Latrelle
Minimum inhibitory
concentration (MIC)
Gram-positive bacteria is more
sensitive to the tested honey
compared to Gram-negative
bacteria.
Nishio et
al.
(2016)
E. faecalis, E. faecium, E. coli, K.
pneumoniae, P. aeruginosa, S.
enterica Enteritidis, S. enterica
Thyphimurium, S. aureus, MRSA,
S. epidermidis, S. mutans, and S.
pyogenes.
Scaptotrigona
bipunctata
Lepeletier
(SB)and S.
postica
Latreille (SP)
Agar well diffusion,
minimum inhibitory
concentrations (MIC),
construction of growth and
viability curves and
scanning electron
microscopy (SEM)
The MICs value of honey
ranged from 0.62% to 10%
meanwhile for the inhibition
zones ranged from 8 to 22
mm. SEM images the
disruption of cell wall for both
honeys.
Nobre da
Cruz et
al.
(2014)
Staphylococcus aureus,
Enterococcus faecalis,
Escherichia coli,
Chromobacterium violaceum,
and Candida albicans.
Melipona
compressipes,
Melipona
seminigra
Minimum inhibitory
concentrations (MIC)
All tested honeys at
concentrations able to inhibit
S. aureus, E. faecalis, E. coli,
C. violaceum and C. albicans.
Massaro
et al.
(2014)
Staphylococcus aureus (ATCC
25923) and Klebsiella
pneumoniae (ATCC 13883)
Australian
stingless bee
honey
Agar diffusion and broth
dilution assays
Raw honey were active against
both bacterial strains.
However, the phenolic extracts
inhibited only S. aureus
growth.
Zamora
et al.
(2014)
Staphylococcus aureus (ATCC
25923), Listeria monocytogenes
(ATCC 19116), Escherichia coli
(ATCC 25922), Salmonella
enteritidis (ATCC 13076),
Pseudomonas aeruginosa (ATCC
9027), Staphylococcus
epidermidis (UCR 2902) and
Candida albicans (ATCC
10231).
Meliponini
bees.
Minimum inhibitory
concentration (MIC) assay
The honey inhibits P.
aeruginosa, S. aureus, and C.
albicans.
Ewnetu
et al.
(2013)
Staphylococcus aureus (ATCC
25923), Escherichia coli (ATCC
25922) and Methicillin-resistant
Staphylococcus aureus(MRSA),
Escherichia coli(R) and
Klebsiella pneumoniae (R)
Stingless bees
from northern
and north
western
Ethiopia
Minimum inhibitory
concentration (MIC) and
minimum bactericidal
concentration (MBC)
Honey of the stingless bees
has the highest inhibition zone
(22.27 ± 3.79 mm) compared
to Apis honey. MICs value for
stingless bees honey is 6.25%
(6.25 mg/ml) of the test
organisms.
Table 4. Antimicrobial studies of stingless bee honey
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Authors
and Year Study population Types Method Outcomes
Mercês
et al.
(2013)
Escherichia coli,
Staphylococcus aureus,
Pseudomonas aeruginosa,
Candida albicans
Melipona asilvai,
Melipona
quadrifasciata
anthidioides,
Friseomelita
doederleinei,
Tetragonisca
angustula and
Plebeia sp.
The agar well
diffusion assay
All honey inhibit S. aureus,
meanwhile honey from M.
quadrifasciata anthidioides and
F. doederleinei inhibited E. coli.
Queiroz
Pimentel
et al.
(2013)
Staphylococcus aureus,
Escherichia coli (0157: H7),
Proteus vulgaris, Shigella
sonnei and Klebsiella sp.
M. compressipes
manaosensis.
Agar-well diffusion
and broth
macrodilution
Honey inhibited the growth of S.
aureus, E. coli (0157: H7), P.
vulgaris, S. sonnei and
Klebsiella sp.
Zainol et
al.
(2013)
Staphylococcus aureus,
Bacillus cereus, Escherichia
coli, and Pseudomonas
aeruginosa.
Kelulut honey Minimum Inhibitory
Concentration (MIC)
and Minimum
Bactericidal
Concentration
(MBC)
S. aureus were inhibited by
Kelulut honey with 26.49
equivalent phenol concentrations
(EPC) compared to other
bacteria.
Rodrígu
ez et al.
(2012)
Staphylococcus aureus (ATCC
25923) and (H08M06),
Escherichia coli (ATCC 35922)
and (H12K06) and
Enterococcus faecalis (ATCC
27853) and (H05C06)
Melipona honey Minimum inhibitory
concentrations
Melipona honey inhibited both
Staphylococcus aureus
ATCC25923 and H08M06
strains and both Escherichia coli
ATCC35922 and H12K06
strains.
Ilechie
et al.
(2012)
Bacterial conjunctivitis caused
by Staphylococcus aureus or
Pseudomonas aeruginosa was
induced in Hartley guinea pigs
Meliponula spp. 1 drop (70 μL) of
crude stingless bee
honey were applied
twice daily.
The time of infections of eye
diseases from those bacteria
were shortened.
Boorn et
al.
(2010)
Gram-positive bacteria, Gram-
negative bacteria and Candida
spp.
Trigona carbonaria Agar diffusion, agar
dilution, broth
microdilution and
time-kill viability
assays.
Stingless bee honey has
antibacterial activity against all
the tested bacteria but very
limited to Candida spp.
Chancha
o et al.
(2009)
Staphylococcus aureus (ATCC
25923), Escherichia coli
(ATCC 35218), Candida
albicans (ATCC 10231),
Auriobasidium pullulans
(ATCC 11942) and Aspergillus
niger (ATCC 16404)
Trigona carbonaria Agar Diffusion, Agar
dilution broth
microdilution and
time-kill viability
assays
Stingless bee honey can inhibit
all the tested microorganism but
very limited when tested with
Candida albicans.
Kimoto-
Nira and
Amano,
(2008)
Lactococcus lactis (MAFF
400103), Lactococcus cremoris
(MAFF 40007),
Lactobacillus casei (JCM
1134),
Enterococcus faecalis (IFO
12964), Enterococcus faecium
(IFO 13712) Klebsiella
pneumoniae ssp. (NGRI G-1),
Staphylococcus sp. (K-2).
Melipona,
Scaptotrigona, and
Trigona
Disc assay Ten of the 18 samples of tested
honey inhibit Enterococcus,
Lactococcus, Lactobacillus, and
Staphylococcus strains.
Meanwhile, Lactococcus lactis
MAFF 400103 was sensitive to
the all tested honey samples.
Temaru
et al.
(2007)
Staphylococcus aureus,
Enterococcus faecalis,
Escherichia coli and
Pseudomonas aeruginosa
Meliponinae Agar well diffusion
assay
Inhibited the growth of test
strains
Table 4. Antimicrobial studies of stingless bee honey (cont.)
MINI REVIEW
131 Yaacob and Sharif / Food Research 2 (2) (2018) 124 - 133
eISSN: 2550-2166 © 2017 The Authors. Published by Rynnye Lyan Resources
Acknowledgments
This study was funded by the Ministry of Higher
Education Malaysia under Fundamental Research Grant
Scheme (FRGS), (FRGS/1/2016/SKK05/UKM/02/1)
UKM.
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Honey produced by stingless bees (Tribe: Meliponini) is well‐known for their medicinal and antimicrobial properties from their diverse content of bioactive compounds. However, it has not been possible to fully characterize its active principles. The present systematic review is based on 117 full‐text articles. Our review highlights (1) the need to apply complementary methodologies and consolidate protocols to quantify antimicrobial activity (2) to characterize antimicrobial agents in honeys of Heterotrigona itama, Tetragonisca angustula, and Melipona beecheii, and; (3) to search for compounds against multidrug‐resistant and/or biofilm‐forming pathogens. Moreover, we performed a meta‐analysis of 29 articles with quantitative data using diffusion assays and minimum inhibitory concentration (MIC). Staphylococcus aureus and Escherichia coli were the most evaluated pathogens, evidencing 221 and 149 antimicrobial activity assays against honey samples of 36 and 24 stingless bee species, respectively. The highest pooled mean in diffusion assays against S. aureus showed a difference between methicillin‐resistant S. aureus (MRSA) and non‐MRSA strains {14.43 [95% confidence interval (CI): 12.16–16.71] mm vs. 11.55 (95% CI: 10.22–12.87) mm}, whereas E. coli showed pooled means of 9.09 (95% CI: 7.93–10.25) mm. Regarding MIC expressed as volume/volume percentage (%, v/v), the estimated inhibitory concentrations were 7.89 (95% CI: 3.94–11.83) mL/100 mL for MRSA and 5.60 (95% CI: 2.66–8.55) mL/100 mL considering all S. aureus strains. In contrast, the estimated MICs as weight/volume percentage (%, w/v) showed 15.00 [(95% CI: 12.84–17.16) g/100 mL for S. aureus and 16.17 (95% CI: 5.78–26.55) g/100 mL for E. coli. However, honey remains an unexplored source of antimicrobial molecules.
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Therapeutic use of animal products is an age old and widespread cross-cultural practice. However, there is a general lack of interest about ethnopharmaceutical practices among the busy modern people. Surveys were carried out during 2010 to 2015 for identifying the use of honey of stingless bee, Lepidotrigona arcifera (Cockerell) in the ethnomedicine of Nepali community. Open ended structured questionnaires were used to acquire knowledge about the use of honey for medicinal purposes from medicine men and old resource persons. As much as 18 different ailments have been found to be cured traditionally by the use of Lepidotrigona honey either alone or in combination with other ingredients. Some of the plant parts, cow urine, milk, etc. were also found to be used to prepare concoction with the honey. Diseases treated with the honey singly or in combination with other natural products ranged from simple cold and cough to dreaded disease like cancer. However, clinical trials are further required to confirm the potentiality of honey to treat these diseases. Utilizing the traditional knowledge of use of stingless bee honey will help in harnessing the knowledge of natural resources of medicine all the same domesticating and conserving sub-Himalayan stingless bee diversity. © 2017, National Institute of Science Communication and Information Resources (NISCAIR). All rights reserved.
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Ethnopharmacological Relevance . Colon cancer has been a major problem worldwide. Kelulut honey (KH) is produced by the stingless bees from Trigona species and has strong antioxidant activities that could be one of the potential chemopreventive agents from natural resources. Aim of This Study . This study investigated the chemopreventive properties and toxicity of KH in Sprague Dawley rats induced with azoxymethane (AOM). Material and Method . Twenty-four male Sprague Dawley rats aged 5 weeks were divided into 4 groups: (G1) untreated group not induced with AOM, (G2) untreated group induced with AOM, (G3) treated group induced with AOM, and (G4) treated group not induced with AOM. Injection of AOM (15 mg/kg) was via intraperitoneal route once a week for two subsequent weeks. The treatment groups were given oral administration of KH (1183 mg/kg body weight) twice daily for 8 weeks. Results . Treatment with KH significantly reduced the total number of aberrant crypt foci (ACF) and aberrant crypts (AC) and crypt multiplicity. KH was not toxic to the animals since the level of blood profile parameters, liver enzymes, and kidney functions was in normal range. Conclusions . The current finding shows that KH has chemopreventive properties in rats induced with colorectal cancer and also was found not toxic towards the animals.
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Purpose :: To investigate the antimicrobial, immunological and healing effects of Melipona scutellaris honey on infected wounds of rat skin. Methods:: Twenty four Wistar rats were distributed in four groups (6-each). The uninfected skin wounds of group I rats were treated daily with saline for 7 days. Uninfected wounds (group II) rats were treated with honey. In group III (treated with saline) and group IV (treated with honey) wounds were inoculated with MRSA ATTC43300. The first bacterial culture was performed 24 hours later. In the 7th day new culture was done, and wound biopsies were used for cytokines dosage and histopathology. Results:: In group I and III rats the CFU/g count of S. aureus in wounds was zero. In group II rats the CFU/g counts in the wound tissue were significantly higher than in wounds of group IV rats. The density histopathological parameters and the expression of TNF-α, IL1-β, Il-6 were significantly higher on wounds of group IV then in the other groups. Conclusion:: Honey of Melipona scutellaris was effective in the management of infected wounds, by significant bacterial growth inhibition, enhancement of cytokine expression, and positively influenced the wound repair.
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Several studies have tested antimicrobial activity of combinations of honey and various substances. In this study, we tested a combination of two stingless bee honeys against various bacterial strains. In particular: the antibacterial activity of honeys produced by Scaptotrigona bipunctata (SB) and Scaptotrigona postica (SP) was evaluated against Gram-positive and Gram-negative bacterial strains by agar well diffusion assays, minimum inhibitory concentration (MIC) assessment, construction of growth and viability curves and scanning electron microscopy (SEM). The interaction of the two honeys was also evaluated by the checkerboard assay. Inhibition zones ranged from 8 to 22 mm. The MIC values of the individual honeys ranged from 0.62 to 10% (v v−1) and decreased to 1/4 to 1/32 when the honeys were combined. SEM images showed division inhibition and cell wall disruption for the SB and SP honeys, respectively, and these alterations were observed in same field when the SB and SP honeys were combined. This study demonstrated that the natural honeys possess in vitro antimicrobial activity against Gram-positive and Gram-negative bacteria, including multidrug-resistant strains. Combination of the SB and SP honeys could lead to the development of new broad-spectrum antimicrobials that have the potential to prevent the emergence of resistant bacterial strains.
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Stingless bee honeys from Costa Rica possess etnopharmacological value mainly as a wound dressing. The microbiological study by APHA methods reported that 83 % of the honeys analysed had microbial counts that comply with European Pharmacopoeia's acceptance criteria for microbiological quality of non-sterile substances for pharmaceutical use. All samples reported the absence of Clostridium botuiinum spores by PCR. Over 90 % of Tetragonisca angustula and Melipona beecheii honeys inhibited Pseudomonas aeruginosa and Staphylococcus aureus at minimum inhibitory concentrations lower than MedihoneyTM. Under the conditions tested, MedihoneyTM was not active against Candida albicans, whereas 53 % of T angustula honeys rendered inhibition. The melissopalynological analyses reported a homogeneous (monofloral) botanical composition for the Meliponini honeys, which emphasizes the contribution of nectar constituents to the antimicrobial activity and provides foundation to the standardization of a desired inhibitory effect. The traditional use of Costa Rican stingless bee honey as a dressing for burns and wounds reveals the application of a proficient antiseptic agent with low health associated risks.
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The antibacterial activity of honey produced by the stingless bees Scaptotrigona postica (H6) and Scaptotrigona bipunctata (H7) was evaluated against methicillin-resistant Staphylococcus aureus (MRSA) and methicillin-sensitive S. aureus (MSSA) strains. Fifty-three MRSA strains in the bacterial collection of the hospital of Londrina State University, three standard MRSA strains and two standard MSSA strains were used. Evaluation of the antibacterial activity of honey samples was determined by agar well diffusion assay, calculation of minimum inhibitory concentrations (MICs), and construction of growth and viability curves. The inhibition zones generated by the honey samples ranged from 20 to 27 mm for H6 and 20 to 24 mm for H7, while MIC values ranged from 0.62 to 1.25% for H6 and 1.25 to 2.5% for H7. According to the growth curves, the growth of all MRSA and MSSA strains was completely inhibited. Honey cytotoxicity was evaluated by dimethylthiazol diphenyl tetrazolium bromide (MTT) assay, and the CC50 values were found to be 13% for H6 and 7.3% for H7, which were significantly higher when compared to the MIC values. The honey of both the stingless bees S. bipunctata and S. postica can thus be utilized as antibacterial substances against MSSA and MRSA strains, and this action is probably due to a synergistic action of different components such as hydrogen peroxide, sugars, and other compounds not identified in this study. The application of natural products is important for the control of MRSA infections. Further studies are warranted to demonstrate that the antimicrobial activity of the honey examined here could be used in clinical applications for the prevention of MRSA infections.
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Objective: To determine the key properties of Trigona laeviceps honey from Thailand, including its antimicrobial activity. Methodology: Proline content and the percentage of invert sugar were evaluated as described. Major protein bands were resolved and analyzed by SDS PAGE and MALDI TOF analyses. Antimicrobial activity was assayed by agar well diffusion. Results: The honey was acidic (pH 3.37) but probably undoctored (proline content of 1,723mg/ kg) with a normal sugar content (e.g. invert sugar 15.2% (w/w)) but a higher than expected total protein content (0.28g/100g). From some ten distinct protein bands, six major protein bands were revealed of which the 29 kDa band was likely to be pollen allergen Lol p VA precursor Lolium perenne (Perennial ryegrass). Neat honey is the most effective for use as a contact antimicrobial agent, and Staphylococcus aureus was the most susceptible tested pathogen to honey at all dilutions. Conclusion: The studied honey could perhaps be used as an antimicrobial agent. Since pollen allergen protein was found, it may cause honey intoxication.