2 3 Potential effluent oil mills and antibacterial activity polyphenols against some pathogenic...

1 23

Research on Chemical Intermediates ISSN 0922-6168 Res Chem IntermedDOI 10.1007/s11164-013-1267-0

Potential effluent oil mills and antibacterialactivity polyphenols against somepathogenic strains

Majdouline Larif, Mohammed Ouhssine,Abdelmajid Soulaymani & AzzedineElmidaoui

1 23

Your article is protected by copyright and all

rights are held exclusively by Springer Science

+Business Media Dordrecht. This e-offprint

is for personal use only and shall not be self-

archived in electronic repositories. If you wish

to self-archive your article, please use the

accepted manuscript version for posting on

your own website. You may further deposit

the accepted manuscript version in any

repository, provided it is only made publicly

available 12 months after official publication

or later and provided acknowledgement is

given to the original source of publication

and a link is inserted to the published article

on Springer's website. The link must be

accompanied by the following text: "The final

publication is available at link.springer.com”.

Potential effluent oil mills and antibacterial activitypolyphenols against some pathogenic strains

Majdouline Larif • Mohammed Ouhssine •

Abdelmajid Soulaymani • Azzedine Elmidaoui

Received: 1 February 2013 / Accepted: 7 May 2013

� Springer Science+Business Media Dordrecht 2013

Abstract The recovery of polyphenols from olive mill wastewaters (OMWs)

provides the double opportunity to obtain high-added value biomolecules and to

reduce the phytotoxicity of the effluent. The purpose of this study is to gain

information about the hygienic quality of the raw material by performing a

microbiological analysis of olive mill wastewater, from an extraction system of

three phases. The determination of total coliforms,fecal coliforms,aecal strepto-cocci, and another group of microorganisms have been explored, namely yeasts,

molds and total aerobic mesophilic flora. We examined the results of the confron-

tation of olive mill wastewater polyphenols with certain strains known for their

pathogenicity, and the minimum concentrations inhibiting bacteria and the minimal

bactericidal concentration (MBC) were determined by the dilution method. Poly-

phenols are particularly the delipidated fraction of OMW extracts according to

liquid–liquid phase. The overall yield is 1.367 ± 0.108 %. The quantitative esti-

mation of total polyphenols was assessed by the colorimetric reagent Folin–Cio-

calteu, gallic acid and tyrosol, tannic acid and total flavonoids catechin (the method

using aluminum trichloride). The results of microbiological analysis confirmed that

there is no fecal contamination. For the in vitro bioassay, polyphenols showed a

variable antimicrobial activity against six bacteria: Escherichia coli, Proteus sp.,

Pseudomonas aeruginosa, Enterroccus feculis, Staphylococcus aureus, and

M. Larif (&) � A. Elmidaoui

Separation Processes Laboratory, Department of Chemistry, Faculty of Science, University Ibn

Tofail, Kenitra, Morocco

e-mail: [email protected]

M. Ouhssine

Microbial Biotechnology Laboratory, Improvement and Microbial and Plant Transformation,

Department of Biology, Faculty of Science, University Ibn Tofail, Kenitra, Morocco

A. Soulaymani

Genetics and Biometry Laboratory, Department of Biology, University Ibn Tofail, Kenitra, Morocco

123

Res Chem Intermed

DOI 10.1007/s11164-013-1267-0

Author's personal copy

Klebsiella pneumoniae. This variability depends essentially on the microorganism

tested and the nature of the product tested. Indeed, we found complete inhibition of

the growth of Proteus sp. and E. fecalis by the sinks method. Some microorganisms

were sensitive to phenols with MBC values between 1/50 and 1/25.

Keywords Olive mill wastewater � Polyphenols � Hygienic quality � Antimicrobial

agents

Introduction

Pseudomonas aeruginosa and Klebsiella pneumoniae are common nosocomial

pathogens [1, 2]. Because these bacterial pathogens are multiply resistant to many

antibiotics, such as ceftazidime and gentamicin, the infections caused by them not

only require expensive antibiotic treatment but also increase the morbidity and

mortality in hospitalized patients [3, 4]. In order to control these infections, there is

a need for the development of agents with marked antibacterial activity, greater

sensitivity, and less toxicity [5].

Faced with this, the technologies dedicated to the recovery and purification of

bioactive compounds from natural effluents and biowastes are under implementa-

tion [6, 7]. The recovery of polyphenols from olive mill wastewaters (OMWs) has

been mostly undertaken by membrane processes [8–10] and liquid–liquid extraction

[11, 12].

Polyphenols of OMW extracts have shown their effectiveness in several areas,

with excellent biological properties as biopesticides against several species of fungi

and weeds [13] and against the pests, Aphis citricola and Euphylura olivina [11, 14].

In previous work, we also tested the effect of polyphenols extracted from olive

vegetation water as a corrosion inhibitor for carbon steel in 1 M HCl, using different

methods: weight loss, potentiodynamic polarization, and spectroscopy and electro-

chemical impedance measurements [15].

Thus, the selective recovery of phenolic compounds from OMWs can accomplish

both the reduction of the intrinsic wastewater environmental toxicity and the

obtainment of high added-value molecules [16]. Given that phenolic compounds are

known for their antibacterial activity [17, 18], we proposed to confirm this activity

using extracts of vegetable polyphenols. In addition, phenolic extracts could be

more beneficial than isolated constituents because the bioactivity of a single

component can change its properties in the presence of other compounds [19, 20].

The purpose of this study is to evaluate the sanitary quality of OMW proceeding

by microbiological analysis on the one hand, and to test the antimicrobial activity of

polyphenols by the methods of diffusion disks and agar dilution on the other hand.

Escherichia coli, Proteus, P. aeruginosa, Enteroccus feculis, Staphylococcusaureus, and Klebsiella pneumoniae were chosen for this study because they are the

source of many infections (urinary, intestinal, respiratory, etc.). The valorisation of

polyphenols as of bactericidal vegetable nature contributes firstly to serving as an

inexhaustible source and for their potential health benefits, and secondly, to avoid

M. Larif et al.

123


the use of antibiotics phytochemical synthesis of waste material and the time taken

for the synthesis of a molecule that may or may not be active [21].

Materials and methods

Origin of olive mill wastewater (OMW)

The olives were from Moroccan Picholine, Meknes-Tafilalt, Morocco. The OMW

were collected from a three-phase crushing unit (producing olive residue oil and

OMW) equipped with two centrifugations. The first separates the oil from the olive

cake and OMW, while the second separates the oil and OMW. The samples of

OMW collected were fresh from the second centrifugation of the industrial

apparatus and were placed in sterile plastic containers and brought back to the

laboratory for microbiological analysis. One sample was kept in the dark at 4 �C

until further use by the standards of Rodier [22].

Extraction of polyphenols

The amount of 100 g of vegetable filtered through a Whatman filter paper No.1

were delipidated by 29 100 mL of hexane. The delipidated OMW was then

extracted with 29 100 mL of ethyl acetate. The organic phase was dried over 3 g of

anhydrous sodium sulfate and then concentrated using a rotary evaporator set at

60 �C and a speed of 140 rpm [23].

Estimation of quantitative total polyphenols, total flavonoids and total tannins

The assay methods of total polyphenols equivalent/gallic acid and tannins/

equivalents/tannic acid were by the colorimetric reagent Folin–Ciocalteu [24].

The method of aluminum trichloride (AlCl3) was used to quantify flavonoids

equivalents/catechin [25].

Microbiological analysis of OMW

The analysis of microorganisms associated with OMW was performed by the

method of inoculation in liquid medium according to Ref. [26].

As the OMW are loaded in organic matter and are dark in color, we proceeded to

a series of dilutions from 10-1 to 10-7 to facilitate the counting of bacteria with the

naked eye. Thus, 1 mL of OMW crude was collected and poured into 9 mL of

sterile distilled water. A series of dilutions to 10-7 was then performed. The

appropriate dilution is set at 0.1 mL on the surface of the culture medium, with

Tergitol agar specific, total coliforms (TC), and fecal coliforms (FC). These bacteria

are recognizable by a yellow domed appearance. These seeds are incubated at 37 �C

for 24 h for TC and 44 �C for 48 h for FC. Fecal streptococci (FS) have a brick red

appearance after incubation at 37 �C in a culture medium (Slanetz yellow). To

determine the presence of total aerobic mesophilic flora (TAMF), 1 mL of the

Potential effluent oil mills and antibacterial activity polyphenols

123


dilution was further placed in the culture medium, plate count agar (PCA).

Incubation was performed at 37 �C for 24 h. For molds and yeasts, we incubated

them by spreading 0.1 mL of the appropriate dilution on Sabouraud medium. The

boxes were then incubated at 30 �C for 2 days for yeasts and 3 days for molds.

Preparation of biological material

The biological material was isolated from the pathological products in the

bacteriology laboratory. Different bacterial species were subcultured by the

streaking method, and then incubated at 37 �C to obtain isolated colonies that

were used to prepare the inoculum.The six bacterial strains: E. coli, Proteus sp., P.aeruginosa, E. feculis, S. aureus and Klebsiella selected during this study are the

origins of several infections (urinary, intestinal, respiratory, etc.). These bacterial

strains were obtained from the American Type Culture Collection (ATCC). They

were maintained by subculture on nutrient agar supports growth for 24 h in the dark

at 37 �C.

Disk diffusion method

The qualitative antibacterial study was carried out by the disk diffusion method. It

was performed using a culture growth at 37 �C for 18 h and adjusted to *5 colony-

forming units per milliliter (CFU/mL). The culture medium used for the bacteria

was Mueller–Hinton Agar (MHA) [27, 28]. Five hundred microliters (lL) of the

inoculums were spread over plates containing MHA, and a Whatman paper disc

(6 mm) impregnated with 5 lL of the polyphenols was placed on the surface of the

media. Other discs impregnated with sterile distilled water served as a negative

control. The plates were left for 30 min at room temperature to allow the diffusion

of the polyphenols. They were then incubated for 24 h at 37 �C [29, 30]. After the

incubation period, the inhibition zone obtained around the disc was measured. The

experiments were run in triplicate, and the developing inhibition zones were

compared with those of reference discs.

Dilution method

Preparation and cell concentration of inocula

Preparations of inocula were made according to traditional methods. Bacterial

inoculum concentrations were evaluated by turbidity and expressed by measuring

the optical density (OD at 600 nm) on a spectrophotometer; OD of 0.08–0.1

corresponds to 108 CFU/mL.

Minimum inhibitory concentrations (MIC) of polyphenols were determined

according to the methods reported by Remmal et al. [31] and Satrani et al. [32].

Dilutions at 1/10, 1/25, 1/50, 1/100 1/200, 1/300, and 1/500 of polyphenols in

distilled water were prepared. Test tubes, each containing 13.5 mL of solid medium

Tryptic Soy Agar (TSA) for bacteria, were autoclaved for 20 min at 121 �C and

cooled to 45 �C and final concentrations at 1/100, 1/250, 1/500, 1/1,000, 1/2,000,

M. Larif et al.

123


1/3,000, and 1/5,000 (v/v) were added aseptically. The tubes were stirred to

thoroughly disperse the extract in the culture medium before pouring into Petri

dishes. Controls, containing the culture medium and agar solution at 0.2 % alone,

were also prepared. The inoculation was done by streaking using a calibrated

platinum loop in order to collect the same volume of inoculum. The latter was in the

form of a broth cultured for 24 h. Each test was repeated three times.

Data analysis

Conventional statistical methods were used to calculate averages and standard

deviations. All measurements were replicated three times, and the data are presented

as mean ± standard deviation.

Results and discussion

Yield and quantitative estimation of total polyphenols, total flavonoids and total

tannins

The overall yield was 1.367 ± 0.108 of dry extract of polyphenols per 100 g of

(OMW) according to five repetitions. The value found belongs to the domain found

by Amaral et al. [33] which is 1–1.5. By membrane processes, the potential of

polyphenols reached a beach of 0.5–19.3 g/L polyphenols [10], which is compa-

rable to a liquid–liquid extraction, which is 13.67 g/L. This difference in

performance can be attributed to several factors, essentially the origin, species,

period of harvesting, drying time, and extraction technique [34, 35].

The quantitative estimations of total polyphenols, total flavonoids, and tannins

were carried out on a dry weight basis as the equivalent of gallic acid, equivalent

catechin, and tannic acid equivalent, respectively, and shown in Table 1.

The content in total polyphenols in gallic acid equivalent was lower than that

found by Nefzaoui [36], which was 0.86 g/L. The value obtained was higher in

flavonoids than found by Debo et al. [16], which was 6.67 g/L. The value tyrosol

was higher than the one found by Jail et al. [37], which was 0.2 g/L. Total tannin

value was found by Leulmi et al. [38], which was still below 0.45 %. The difference

in results can be explained by several factors that have an influence on the content

was phenolic compounds: Extrinsic factors (such as geographic and climatic) and

Table 1 Results of the

determination of total

polyphenols, flavonoids of

condensed tannins and total

tannin in fresh OMW

Parameters Mean Standard

deviation (CV)

Total phenols/Ac. Gallic (g/L) 11.600 0.160

Flavonoids (catechin) (g/L) 7.335 0.930

Total tannins/tannic acid (g/L) 1.832 0.462

Tyrosol (g/L) 0.393 0.051


123


genetic factors, but also the degree of maturation of the olives and the duration of

storage, have an effect on the polyphenol content [39, 40].

Bacteriological analysis

The results for the microbiological analysis are shown in Table 2.

Yeasts and molds are the most common flora which seem to adapt better to the

acidity of the OMW; they are, respectively, of about 4.6 9 105 and 7.33 9 106

CFU/100 mL, and these values are comparable to those obtained by Jouraiphy [41].

For total aerobic mesophilic flora (TAMF), it is around 6–7 9 105 compared with

domestic wastewater where the load is of the order of 6 9 106 [42], and can be

considered as revivable spoilage flora whose abundant presence indicates a process

of ongoing degradation and presents no health risk [43]. It was noted that there was

a complete absence of total coliforms and fecal coliforms in OMW, which

confirmed that there is no fecal contamination.

The antimicrobial capacity of effluent from olive oil mills is essentially linked to

the action of monomeric phenols and brown pigments or dark-colored catechol [44].

These effluents are acting on bacteria by denaturing proteins and by altering the

cellular membranes [45].

Antimicrobial activity of polyphenols

Method of wells

The diffusion method with disks allowed us to highlight the antibacterial

polyphenols, with a negative control with distilled water, against pathogenic

bacteria (E. coli, Proteus sp., P. aeruginosa, E. fecalis, S. aureus and K.pneumoniae). Results of the antibacterial activity of polyphenols in its fractions are

shown in Table 3.

The results show that the antibacterial activity is not the same, with the same

concentration of the product applied to the six bacteria giving diameters of

inhibition zones between 11 and 21 mm.

Table 2 Evaluation of the

hygienic quality of OMWMicrobial flora UFC

(mL)

UFC

(mL)

UFC

(mL)

Total coliforms in 37 �C/

100 mL

0 0 0

Fecal streptococci in 37 �C/

100 mL

0 0 0

Fecal coliforms in 44 �C/

100 mL

0 0 0

Yeast 4 9 105 5 9 105 5 9 105

Molds 8 9 106 7 9 106 7 9 106

Total aerobic mesophilic flora

in 30 �C

7 9 105 6 9 105 6 9 105

M. Larif et al.

123


We note that the polyphenols have an inhibitory effect which is greater in the

presence of Proteus sp. (Gram-negative) and E. fecalis (Gram-positive) as for these

strains the diameters are the highest compared to other bacteria and in contrast to the

control which does not have an antibacterial effect (Fig. 1).

Minimum inhibitory concentration of polyphenols (MIC)

The MIC is the lowest concentration inhibiting bacterial growth visible to the eye

after 18 or 24 h of contact at 37 �C. The results of the antibacterial activity of

polyphenols and its fractions are presented in Table 4.

Polyphenols present in vitro, a good inhibitory activity against the tested germs.

However, the microorganisms studied did not exhibit the same sensitivity by

polyphenols. For bacteria, Proteus sp., S. aureus and P. aeruginosa showed a

greater sensitivity to an inhibitory concentration of 1/25 compared with E. coli, K.pseudomonas, and E. fecalis, the growth of which was inhibited at 1/50 (Fig. 2).

Table 3 Antibacterial activity by the disk method

Germs Minimum Maximum Mean Standard deviation

(CV)

Gram (-) Pseudomonas aeroginosa 11.000 14.000 13.000 1.732

Proteus sp. 16.000 18.000 17.000 1.000

Echerichiacoli 13.000 16.000 14.667 1.528

Klebsilla pneumoniae 15.000 16.000 15.333 0.577

Gram (?) Enteroccus fecalis 12.000 21.000 17.000 4.583

Staphylococcus aureus 12.000 20.000 15.667 4.041

Fig. 1 Disk diffusion inhibitor activity of polyphenols is most important on Proteus sp. and E. fecalis


123


Concentration minimal bactericidal of the polyphenols (MBC)

The minimal bactericidal concentration (MBC) is the lowest concentration of

polyphenols leaving only 0.01 % or less of the initial inoculum surviving after 18 h

of culture at 37 �C according to Table 5. This value characterizes the bactericidal

Table 4 Antibacterial activity of polyphenols on different germs

Germs 1/10 1/25 1/50 1/100 1/200 1/300 1/500 C.

Gram (-) Echerichia coli - - - ? ? ? ? ?

Proteus sp. - - ? ? ? ? ? ?

Klebsilla pseudonomas - - - ? ? ? ? ?

Pseudomonas aeroginosa - - ? ? ? ? ? ?

Gram (?) Enteroccus fecalis - - - ? ? ? ? ?

Staphyloccocus aureus - - ? ? ? ? ? ?

C control, - clear, ? trouble

Fig. 2 Agar dilution minimum inhibitory concentration (MIC) of polyphenols on a E. fecalis, b K.pseudomonas and c E. coli the growth of which was inhibited at 1/50

M. Larif et al.

123


effect of polyphenols, which is 1/25 for E. coli (Gram-negative) which is the most

resistant strain and 1/50 for E. fecalis Gram (?) and Klebsilla pseudomonas (Gram-

positive) (Fig. 3).

Discussion

Following these results, polyphenols have shown very interesting antibacterial

characteristics on the microorganisms tested. Several authors who have shown that

polyphenols inhibit mycelial development of strains and their antimicrobial power

[46–48].

Phenolic compounds are also characterized by very strong protein cross-linking

and protein-denaturizing activity, and other studies have reported that different

bacterial species (Gram-positive and Gram-negative) exhibit different sensitivities

towards phenolic compounds and phenolic acids in which our extract is rich [49,

50].

Due to their acidic side chain, phenolic acids are much less polar. This property

might facilitate the transport of these molecules across the cell membrane, which

might be related in turn to the stronger inhibitory effect of phenolic acids. On the

other hand, they are known to interact with membrane lipids by a neutralization of

the membrane’s electric potential following penetration of the molecule. A similar

effect could occur in the bacterial cell membrane affecting their energy metabolism.

Indeed, the antibacterial activity of polyphenols can be explained by the

mechanism of toxicity of flavonoids against microorganisms, by, for example, non-

specific interactions such as hydrogen bonding setting with proteins or cell wall

enzymes, chelation of metal ions, inhibition of bacterial metabolism, or sequestra-

tion of substances necessary for the growth of bacteria [51].

Their activity is probably due to their ability to complex with extracellular and

soluble proteins and to complex with bacterial cell walls, as is the case for quinones.

More lipophilic flavonoids may also disrupt microbial membranes [52, 53].

Flavonoid compounds also exhibit inhibitory effects against multiple viruses.

Numerous studies have documented the effectiveness of flavonoids such as

swertifrancheside, glycyrrhizin, and chrysin against human immunodeficiency virus

(HIV) [54]. According to several studies, the synergistic interactions between

Table 5 Bactericidal activity (MBC)

Germs 1/10 1/25 1/50 Control

Gram (-) Echerichia.coli - - ? ?

Proteus sp. - - ?

Klebsilla pseudonomas - - – ?

Pseudomonas aeroginosa - - ?

Gram (?) Enteroccus fecalis - - - ?

Staphyloccocus aureus - - ?

- inhibits (MBC), ? persists


123


different compounds may be the origin of the much more pronounced activity than

that expected for the major compounds [55, 56].

Phenolic compounds (phenolic acids, tannins, and flavonoids) form a group of

the most important phytochemical polyphenols [53, 57]. The majority of the

pharmacological effects of polyphenols are mainly due to their phenolic group. In

fact, the location and number of hydroxyl groups on the phenolic compounds

increases the toxicity against microorganisms [20]. The bactericidal activity arises

from the synergistic effect of constituents such as the total polyphenols, flavonoids,

and tannins. Consequently, we note that the inhibition of bacterial growth depends

on two factors: the bacteria used, and the nature of the product tested [54, 58].

Comparing the disk diffusion method and agar dilution, the disk diffusion

method is simple and inexpensive to test sensitivities, and any zone of inhibition

should be obtained to determine the MIC category sensitivity. Therefore, it is

recommended that the agar dilution method is used for MIC determination for

isolates with a zone diameter of 20 mm or more than 26 mm [59].

Conclusion

The extraction of polyphenols from OMW provided an important yield of 1.367 %.

With the wealth of vegetable phenolics, the biological effectiveness of polyphenols

against pathogenic strains is related to their chemical composition, by the functional

groups of the major compounds, and possible synergistic effects between

components. These preliminary results can be supplemented by other more detailed

studies (toxicological tests, mode of delivery, cost, etc.). To exploit the antibacterial

properties, the nature of the chemical structures and their proportions play a role.

This efficiency often reduces the activity of the major compounds, or those likely to

be active.

Fig. 3 Agar dilution minimum bactericidal concentration (MBC) of polyphenols against the mostsensitive strains

M. Larif et al.

123


References

1. C.H. Lu, W.N. Chang, Y.C. Chuang, H.W. Chang, The prognostic factors of adult gram-negative

bacillary meningitis. J. Hosp. Infect. 40, 27–33 (1998)

2. S.C. Chang, W.C. Hsieh, C. Liu, High prevalence of antibiotic resistance of common pathogenic

bacteria in Taiwan. The Antibiotics Resistance Study Group of the Infectious Disease Society of the

Republic of China. Diagn. Microbiol. Infect. Dis. 36, 107–112 (2000)

3. M. Ho, L.C. McDonald, T.L. Lauderdale, L.L. Yeh, P.C. Chen, Y.R. Shiau, Surveillance of antibiotic

resistance in Taiwan, 1998. J. Microbiol. Immunol. Infect. 32, 239–249 (1999)

4. J. Carlet, P. Collignon, D. Goldmann, H. Goossens, I.C. Gyssens, S. Harbarth et al., Society’s failure

to protect a precious resource: antibiotics. Lancet 378, 369–371 (2011)

5. J. Carlet, J.L. Mainardi, Antibacterial agents: back to the future? Can we live with only colistine,

cotrimoxazole, and fosfomycin? Clin. Microbiol. Infect. 18, 1–3 (2012)

6. A. De Leonardis, A. Aretini, G. Alfano, V. Macciola, G. Ranalli, Isolation of a hydroxytyrosol-rich

extract from olive leaves (Olea europaea L.) and evaluation of its antioxidant properties and bio-

activity. Eur. Food Res. Technol. 226, 653–659 (2008)

7. I.S. Arvanitoyannis, A. Kassaveti, Fish industry waste: treatments, environmental impacts, current

and potential use. Int. J. Food Sci. Technol. 43, 726–745 (2008)

8. A. El-Abbassi, A. Hafidi, M.C. Garcia-Payo, M. Khayet, Concentration of olive mill wastewater by

membrane distillation for polyphenols recovery. Desalination 245, 670–674 (2009)

9. E. Garcia-Castello, A. Cassano, A. Criscuoli, C. Conidi, E. Drioli, Recovery and concentration of

polyphenols from olive mill wastewaters by integrated membrane system. Water Res. 44, 3883–3892

(2010)

10. O.A. Mudimu, M. Peters, F. Brauner, G. Braun, Overview of membrane processes for the recovery of

polyphenols from olive mill wastewater. Am. J. Environ. Sci. 8(3), 195–201 (2012)

11. M. Larif, A. Zarrouk, A. Soulaymani, A. Elmidaoui, New innovation in order to recover the poly-

phenols of olive mill wastewater extracts for use as a biopesticide against the Euphyllura olivina and

Aphis citricola. Res. Chem. Intermed. (2012). doi:10.1007/s11164-012-0947-5

12. C.M. Galanakis, E. Tornberg, V. Gekas, Clarificationofhigh-added value products from olive mill

wastewater. J. Food Eng. 99, 190–197 (2010)

13. M.L. Cayuela, P.D. Millner, S.L.F. Meyer, A. Roig, Potential of olive mill waste and compost as

biobased pesticides against weeds, fungi, and nematodes. Sci. Total Environ. 399, 11–18 (2008)

14. M. Larif, A. Soulaymani, M. Hnach, A. Elmidaoui, Olive wastewater’s impact on Oued Boufekrane

in Meknes-Tafilalet. Am. J. Environ. Sci. 8, 236 (2012)

15. M. Larif, A. Elmidaoui, A. Zarrouk, H. Zarrok, R. Salghi, B. Hammouti, H. Oudda, F. Bentiss, An

investigation of carbon steel corrosion inhibition in hydrochloric acid medium by an environmentally

friendly green inhibitor. Res. Chem. Intermed. (2012). doi:10.1007/s11164-012-0788-2

16. A. Debo, T. Yangui, A. Dhouib, M. Ksantini, S. Sayadi, Efficacy of a hydroxytyrosol-rich prepa-

ration from olive mill wastewater for control of olive psyllid, Euphyllura olivina, infestations. Crop

Prot. 30, 1529–1534 (2011)

17. V.L. Singleton, J.A. Rosi, Colorimetry of total phenolics with phosphomolybdic–phosphotungstic

acid reagents. Am. J. Oenol. Vitic. 16, 144–158 (1965)

18. T. Hanato, H. Kagawa, T. Yasuhara, T. Okuda, Two new flavonoids and other constituents in licorice

root: their relative relative astringency and radical scavenging effects. Chem. Pharm. Bull. 36,

2090–2097 (1988)

19. P.D. Duh, G.C. Yen, Antioxidant activity of water extract of Harng Jyur (Chrysanthemum morifoliumRamat.) varieties in soybean oil emulsion. Food Chem. 66, 471–476 (1999)

20. H. Falleh, R. Ksouri, K. Chaieb, N. Karray-Bouraoui, N. Trabelsi, M. Boulaaba, C. Abdelly, Phenolic

composition of Cynara cardunculus L. organs, and their biological activities. C. R. Biol. 331,

372–379 (2008)

21. M. Larif, A. Adad, R. Hmammouchi, A. Idrissi Taghki, A. Soulaymani, A. Elmidaoui, M. Bou-

achrine, T. Lakhlifi, Biological activities of triazine derivatives. Combining DFT and QSAR results.

Arab. J. Chem. (2013). doi:10.1016/j.arabjc.2012.12.033

22. Agence Francaise de Normalisation (Afnor), Recueil de normes Francaises: Eau, methodes d’essai,2nd edn. (Paris, France, 1983), p. 621

23. J.J. Macheix, A. Fleuriet, J.A. Billot, Fruit phenolics (CRC Press Inc., Boca Raton, 1990)


123


http://dx.doi.org/10.1007/s11164-012-0947-5

http://dx.doi.org/10.1007/s11164-012-0788-2

http://dx.doi.org/10.1016/j.arabjc.2012.12.033

24. H.B. Li, K.W. Cheng, C.C. Wong, K.W. Fan, F. Chen, Y. Tian, Evaluation of antioxidant capacity

and total phenolic content of different fraction of selected microalgae. Food Chem. 102, 771–776

(2007)

25. T. Bahorun, B. Grinier, F. Trotin, G. Brunet, T. Pin, M. Luncky, J. Vasseur, M. Cazin, C. Cazin, M.

Pinkas, Oxygen species scavenging activity of phenolic extracts from hawthorn fresh plant organs

and pharmaceutical preparations. Arzneimittelforschung 46(11), 1086–1089 (1996)

26. J. Rodier, L. Bernard, M. Nicole, coll. L’analyse de l’eau, eaux naturelles, eaux residuaires, eaux demer, 9eme edn. (Dunod, Paris, 2009). ISBN 987-2-10-054179-9

27. L. Gachkar, D. Yadegari, M.B. Rezaei, M. Taghizadeh, S.A. Astaneh, I. Rasooli, Chemical and

biological characteristics of Cuminum cyminum and Rosmarinus officinalis essential oils. Food

Chem. 102, 898–904 (2007)

28. G. Leyral, J.N. Joffin, Microbiologie technique: 2eme Edition., Collection Biologie technique. Ped-

agogique d’Aquitaine 2, 290 (2001)

29. C. Bekhech, F. Atik-Bekkara, E. Abdelouahid, F. Tomi, J. Casanova, Composition and antibacterial

activity of the essential oil of Thymus fontanesii Boiss. Et Rent. from Algeria. J. Essent. Oil Res. 19,

594–596 (2007)

30. M. Bourkhiss, M. Hnach, B. Bourkhiss, M. Ouhssine, A. Chaouch, Composition chimique et pro-

prietes antimicrobiennes de l’huile essentielle extraite des feuilles de Tetraclinis articulata (Vahl) du

Maroc. Afrique Science 03(2), 232–242 (2007)

31. A. Remmal et al., Improved method of determination of antimicrobial activity of essential oils in agar

medium. J. Essent. Oil Res. 5(2), 179–184 (1993)

32. B. Satrani et al., Composition chimique et activite antimicrobienne des huiles essentielles de Satureja

calamintha et Satureja alpina du Maroc. Ann. Falsif. Expert. Chim. Toxicol. 94(956), 241–250 (2001)

33. C. Amaral, M.S. Lucas, J. Coutinho, L.A. Crespi, M.D.R. Anjos, C. Pais, Microbiological and

physiochemical characterization of olive mill in Northeastern Portugal. Bioresour. Technol. 99,

7215–7223 (2008)

34. K. Loziene, P.R. Venskutonis, Influence of environmental and genetic factors on the stability of

essential oil composition of Thymus pulegioides. Biochem. Syst. Ecol. 33, 517–525 (2006)

35. M.A. Curado et al., Environmental factors influence on chemical polymorphism of the essential oils

of Lychnophora ericoides. Phytotherapy 67, 2363–2369 (2006)

36. A. Nefzaoui, Contribution a la rentabilite de l’oleiculture par une valorisation optimale des sous

produits. Option mediterraneennes 16, 101–108 (1991)

37. A. Jail, E. Boukhoubza, A. Nejmeddine, S. Sayadi, L. Hassani, Co-treatment of olive-mill and urban

wastewaters by experimental stabilization ponds. J. Hazard. Mater. 176, 893–900 (2010)

38. N. Leulmi, Etude de la valorisation nutritionnelle des margines et de leur impact sur la reduction dela methanogenese ruminale chez l’ovin (Magister en Microbiologie appliquee, Nature du diplome,

2011)

39. A.A. Aganga, K.W. Mosase, Tannins content, nutritivantee value and dry matter digestibility of

Lonchocarous capussa, Ziziphus mucropata, Sclerocarya birrea, Kirkia acuminata and Rhus lanceaseeds. Animal Feed Sci. Technol. 91, 107–113 (2001)

40. K. Pedneault, S. Leonhart, L. Angenol, A. Gosselin, A. Ramputh et J. T. Arnason. Influence de la

culture hydroponique de quelques plantes medicinales sur la croissance et la concentration en

composes secondaires des organes vegetaux. Texte de conference, 5eme colloque sur les produits

naturels d’origine vegetale, Universite Laval, Quebec City, 1–5 (2001)

41. A. Yaacoubi, A. Chahlaoui, M. El yachioui, A. Chaouch, Traitement des margines a pH neutre et en

conditions d’aerobie par la microflore du sol avant epandage. Bull. Soc. Pharm. Bordeaux. 149,

43–56 (2010)

42. A. Jouraiphy, S.M. El Gharous, J.C. Revel, M. Hafidi, Chemical and spectroscopic analysis of

organic matter transformation during composting of sewage sludge and green plant waste. Int.

Biodeterior. Biodegrad. 56, 101–108 (2005)

43. G. Leray, E. Vierling, Microbiologie et toxicologie des aliments: Hygiene et securite alimentaire, 4th

edn. (CRDI d’Aquitaine, Malmaison Doin Bordeaux, 2007), p. 290

44. M. Hamdi, R. Ellouz, Treatment of detoxified olive mill wastewater by anaerobic filter and aerobic

fluidized bed process. Environ. Technol. 19, 183–188 (1993)

45. A. Ranalli. L’effluent des huileries d’olive proposition en vue de son epuration, References aux

normes italiennes en la matiere, premiere partie Olivia 37, 30–39 (1991)

46. A. Tantaoui-Elaraki, N. Lattaoui, A. Errifi, Composition and antimicrobial activity of the essential oil

of Thymus broussonetii, T. Zygis and T. Satureoıde. J. Essent. Oil Res. 5, 45–53 (1993)

M. Larif et al.

123


47. S. Takac, A. Karakaya, Recovery of phenolic antioxidants from olive mill wastewater. Recent Pat.

Chem. Eng. 2, 230–237 (2009)

48. A.P.A.D. Gurgel et al., Antibacterial effects of P. amboinicus (Lour.) Spreng (Lamiaceae) in

methicillin resistant S. aureus (MRSA). Biol. Res. 3(3–4), 117–122 (2009)

49. G. Ciafardini, B.A. Zullo, Antibacterial activity of oil mill water polyphenols on the phytopathogenXanthomonas campestris spp. Ann. Microbiol. 53, 283–290 (2003)

50. A. Sousa, I.C.F.R. Ferriara, R. Calhella, P.B. Andrade, P. Valentao, R. Seabra et al., Phenolics and

antimicrobial activity of traditional stoned table olives alcaparra. Bioorg. Med. Chem. 14, 8533–8538

(2006)

51. D. Karou, M. H. Dicko, J. Simpore, S. Yameogo, S. Sanon et A. S. Traore. Activites antioxydantes et

antibacteriennes des polyphenols extraits de plantes medicinales de la pharmacopee traditionnelle du

Burkina Faso. Maitrise des procedes en vue d’ameliorer la qualite des aliments, utilisation des OGM,

analyse des risques en agroalimentaire. 8–11 novembre. Ouagadougou (2005)

52. A. Firas, F. Hassan, Antibacterial and antifungal activities of different parts of Tribulus terrestris L.growing in Iraq. J. Zhejiang Univ. Sci. 9(2), 154–159 (2008)

53. A. Dhiman, A. Nanda, A. Sayeed, A quest for staunch effects of flavonoids: Utopian protection

against hepatic ailments. Arab. J. Chem. (2012). doi:10.1016/j.arabjc.2012.05.001

54. M.M. Cowan, Plant products as antimicrobial agents. Clin. Microbiol. Rev. 12, 564–582 (1999)

55. A. Zhiri, D. Baudoux, Huiles essentielles chemotypees et leurs synergies: aromatherapie scientifique(Edition Inspir Development, Luxembourg, 2005)

56. M. Viuda-Martos, Y. Ruiz-Navajas, J. Fernandez-Lopez, J. Perez-Alvarez, Antibacterial activity of

lemon (Citrus lemon), mandarin (Citrus reticulata), grapefruit (Citrus paradisi) and orange (Citrussinensis) essential oils. J. Food Saf. 28(4), 567–576 (2008)

57. T. Beta, S. Nam, J.E. Dexter, H.D. Sapirstein, Phenolic content and antioxidant activity of pearled

wheat and Roller-Milled fractions. Cereal Chem. 82, 390–393 (2005)

58. S. Omar Said Hassane, B. Satrani, M. Ghanmi, N. Mansouri, H. Mohamed, A. Chaouch, Activite

antimicrobienne et composition chimique de l’huile essentielle de Plectranthus aromaticus Roxb. de

l’Ile de la Grande Comore. Biotechnol. Agron. Soc. Environ. 15(2), 251–258 (2011)

59. C.Y. Gaudreau, H. Jilbert, I. Josee Gagnon, S. Bekal, Comparison of disk diffusion and agar dilution

methods for erythromycin, ciprofloxacin, and tetracycline susceptibility testing of Campylobactercoli and for tetracycline susceptibility testing of Campylobacter jejuni subsp. Jejuni Antimicrob

Agents Chemother 52(12), 4475–4477 (2008)


123


http://dx.doi.org/10.1016/j.arabjc.2012.05.001

2 3 Potential effluent oil mills and antibacterial activity polyphenols against some pathogenic...

Documents

Transcript of 2 3 Potential effluent oil mills and antibacterial activity polyphenols against some pathogenic...