Chemical characterization, antibacterial, antibiofilm, and antioxidant activities of the methanolic extract of Paratapes undulatus clams (Born, 1778)

Mosad A. Ghareeb; Salwa A.H. Hamdi; Mona Fathi Fol; Amina M. Ibrahim

doi:10.7324/JAPS.2022.120521

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Abstract

Mollusks represent the second-largest animal phylum in the marine realm. They have direct and indirect commercial and medical importance worldwide. Paratapes undulatus is a species of saltwater clam, a marine bivalve mollusk in the family Veneridae. The current study aimed to examine the chemical profile of the methanolic extract of P. undulatus soft parts using Gas chromatography mass spectroscopy (GC-MS) analysis and then assessing its antibacterial, antibiofilm, and antioxidant activities. GC-MS investigations led to the identification of major components including 7-hexadecenoic acid, methyl ester, (Z) (32.01%), hexadecanoic acid, methyl ester (14.03%), 9-octadecenoic acid, methyl ester (8.43%), palmitoleic acid (5.75%), 5,8,11,14,17-eicosapentaenoic acid, methyl ester (5.25%), tridecanoic acid, 4,8,12-trimethyl-, methyl ester (3.44%), tetradecanoic acid, methyl ester (3.34%), and cis-9-hexadecenoic acid (3.23%). Moreover, the results revealed that the extract showed remarkable antibacterial, antibiofilm, and antioxidant activities. In conclusion, the present results might be helpful for pharmaceutical companies to develop natural supplements from these clams.

Keyword: Paratapes undulatus clams antibacterial antibiofilm antioxidant GC-MS

Citation:

Ghareeb MA, Hamdi SAH, Fol MF, Ibrahim AM Chemical characterization, antibacterial, antibiofilm, and antioxidant activities of the methanolic extract of Paratapes undulatus clams (Born, 1778). J Appl Pharm Sci, 2022; 12(05):219–228.

Copyright: © The Author(s). This is an open-access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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INTRODUCTION

Mollusks represent the second-largest invertebrate animal phylum after Arthropoda (Baldwin, 2003; Rusmore-Villaume, 2008). They are also considered one of the most important elements in food chains as a balanced source of protein (Haszprunar and Wanninger, 2012) and represent the most prominent members of marine faunal ecosystems. Some species have direct and indirect commercial importance and even medical benefits to humans (Rusmore-Villaume, 2008) and are utilized as prospective resources of bioactive products in numerous cultures worldwide (Khan et al., 2009).

Recently, the molluscan natural products (high content of proteins, vitamins, and trace elements) have become very valuable foodstuffs, and their synthetically formulated structural analogs have been recognized in clinical trials as promising therapeutic agents for many diseases (Alves and Diederich, 2021; Tabakaeva et al., 2018). Marine bivalves are considered a rich source of antimicrobial peptides that possess various biological activities such as antibacterial, antioxidant, anticoagulant, anti-inflammatory, and anticarcinogenic (Galdiero et al., 2015). The main cause of their bioactivities is the presence of biologically active peptides (Alves and Diederich, 2021). Bivalves occurring in Egypt represent a neglected animal group, and little is known about them or their diversity and importance (Temraz, 2016). Therefore, more light should be shed on their chemical and biological aspects.

In particular, Paratapes undulatus, common name undulate Venus, is a species of saltwater clams. These clams are a popular food in Egypt, inhabiting the inshore shallow sandy seabed in Timsah Lake, located near Ismailia City at the midpoint of the Suez Canal and about 80?km south of Port Said, Egypt (Loftus et al., 2015). Lately, a broad spectrum of naturally occurring bioactive molecules separated from the mollusks was utilized in the manufacture of several medications (Alves and Diederich, 2021). The strong impact of antimicrobial resistance on healthcare and the economy has led to a crucial demand to secure unique molecules with novel modes of action to reduce the harmful effects of infectious diseases (Ghareeb et al., 2015). Several antimicrobial compounds have been isolated from peptides subunits of marine bivalves due to their thorough capability to resist infection with different types of viruses (Khan et al., 2009). They also exhibit a wide range of antibacterial activities against Gram-positive and Gram-negative bacteria, as well as yeast (Burge et al., 2014; Schmitt et al., 2012). The rapid and increasing development of antimicrobial resistance is one of the current global health challenges. Pathogenic microorganisms have the capability to hinder the effect of antimicrobial agents, which leads to raising the accompanying hazards of infections via pathogenic microorganisms like bacteria, fungi, viruses, and parasites. Furthermore, the appearance of novel pathogens like SARS, H1N1, and various types of influenza has become a vital communal health risk. To overcome this phenomenon, scientists have worked to discover novel antimicrobial and antiviral pharmaceuticals from natural resources like plants, marine organisms, mollusks, and fungal extracts (Abdel-Aziz et al., 2018, 2021; Elkhouly et al., 2021a; Ghareeb et al., 2014a, 2019; Hamed et al., 2020).

On the other hand, overproduction of reactive species led to the initiation of oxidative stress that in turn initiates several dangerous disorders such as “cancer, cardiovascular, and inflammation.” Moreover, the accompanying destructive side effects can be reduced using naturally occurring antiradical ingredients that act as strong free radical scavengers (Ghareeb et al., 2018; Sobeh et al., 2018).

In the current study, we aimed to investigate for the first time the chemical and biological profiles of the soft parts of the marine clams P. undulatus and the scientific evidence regarding their chemical composition and associated antibacterial, antibiofilm, and antioxidant activities.

MATERIALS AND METHODS

Chemicals, reagents, and instruments

All solvents, standards, and reagents are of high analytical grade. Methanol and sulfuric acid were obtained from El-Nasr Pharmaceutical Chemicals Company (Cairo, Egypt). Nutrient agar and Nutrient Broth media were purchased from HiMedia Laboratories Pvt. Ltd. (Mumbai, India). 2,2-Diphenyl-1-picrylhydrazyl (DPPH) radical, ascorbic acid, gallic acid, Folin–Ciocalteu’s reagent, sodium carbonate, sodium phosphate, and ammonium molybdate were purchased from Sigma-Aldrich (Steinheim, Germany). For antioxidant assays, the absorbance was measured using a spectrophotometer (UV-VS spectrophotometer, Milton Roy 601, CO). The obtained extract was concentrated under vacuum using a rotary evaporator, Buchi R-300 (Flawil, Switzerland).

Collection of P. undulatus

Venus clams (P. undulatus) were collected from Timsah Lake which is located close to Ismailia City at the midpoint of the Suez Canal and about 80?km south of Port Said, Egypt (Fig. 1) (El-Serehy et al., 2018). The collected samples were cleaned with distilled water to eliminate any sands or contaminations and then kept in a refrigerator at −18°C till being used.

**Preparation of the methanolic extract of P. undulatus clams (Born, 1778)**

Paratapes undulatus clams are a popular food in Egypt, so after being washed with distilled water, their shells were opened with stainless steel knives and their soft bodies were separated from these shells by forceps. The collected soft bodies (250 g) were homogenized and then were extracted four times with methanol (2 l) at room temperature (25°C ± 2°C). The combined extracts were concentrated to afford 19.0 g methanol extract.

Antibacterial activity assay

The antibacterial activity of the tested extract was evaluated against some pathogenic microbial strains including four Gram-negative bacteria (Escherichia coli ATCC 25955, Pseudomonas aeruginosa ATCC 10145, Proteus vulgaris, and Klebsiella pneumoniae), one Gram-positive bacterium (Staphylococcus aureus NRRL B-767), and one yeast (Candida albicans ATCC 10231) according to the reported procedures (Elkhouly et al., 2021b). Ciprofloxacin and nystatin were utilized as a control.

Antibiofilm activity assay

The biofilm inhibitory potential was determined against four pathogenic microbial strains, including S. aureus and Bacillus subtilis as Gram-positive bacteria as well as P. aeruginosa and E. coli as Gram-negative bacteria, according to the reported procedures (El-Shazly et al., 2021; Hamed et al., 2020).

Total phenolic content (TPC) using Folin–Ciocalteu’s assay

The TPC was evaluated using Folin–Ciocalteu’s reagent according to the reported procedures (El-Neekety et al., 2016; Hathout et al., 2016). Briefly, 100 μl of the tested sample (500 μg/ml) was mixed with 500 μl of Folin–Ciocalteu’s reagent and 1.5 ml of sodium carbonate (20%). The reaction mixture was shaken and completed to 10 ml using distilled water. The mixture was allowed to stand for 120 minutes. Afterward, the absorbance was recorded at 765 nm. All measurements were performed in triplicate. The TPC was presented as mg gallic acid equivalent (GAE) per g extract.

Antioxidant activity evaluation

Free radical scavenging activity using DPPH

Free radical scavenging activity was evaluated using the DPPH assay according to the reported procedures (Ghareeb et al., 2016; Shirwaikar et al., 2006). Briefly, various serial concentrations from the tested sample (1.5 ml) were added to a (1.5 ml) solution of 0.1 mmol/l DPPH. Equivalent volumes of methanol and DPPH acted as the control. After incubation for 20 minutes at 37°C in the absence of light, the absorbance was recorded at 517 nm. The test was carried out in triplicate. The free radical scavenging activity was expressed in IC₅₀ value (concentration from tested sample required to scavenge 50% of the radical).

Figure 1. A map of Timsah Lake with the inset showing the position of the lake on the Suez Canal.

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Total antioxidant capacity (TAC) using phosphomolybdenum assay

The TAC was evaluated using the phosphomolybdenum assay based on the reported procedures (Prieto et al., 1999). Basically, this assay is based on the reduction of molybdenum (VI) to molybdenum (V) by the tested sample and consequent development of a green color [phosphate = molybdenum (V)] complex at low pH with maximum absorption at 695 nm. Briefly, 0.5 ml of the tested sample (500 µg /ml) in methanol was mixed with 5 ml from the test reagent [0.6 M H₂SO₄, 28 mM NaH₂PO₄, and 4 mM (NH₄)6Mo₇O₂₄]. The tubes containing the tested samples and reagents were capped and incubated in a water bath at 95°C for 1.5 hours. After cooling, the absorbance was recorded at 695 nm against a blank. The blank comprised all reagents and solvents without the tested sample. All experiments were carried out in triplicate. The TAC was presented as the number of ascorbic acid equivalent (AAE) (Elkhouly et al., 2021; Prieto et al., 1999).

Chemical characterization using GC-MS analysis

GC-MS examination was conducted according to the reported procedures (Khalaf et al., 2020), using a Thermo Scientific, Trace GC Ultra/ISQ Single Quadrupole MS, TG-5MS fused silica capillary column (30 m, 0.251 mm, and 0.1 mm film thickness). An electron ionization system with ionization energy of 70 eV was utilized for GC/MS recognition. Helium gas was utilized as the carrier gas at a regular flow rate of 1 ml/minute. The injector and MS transfer line temperature was set at 280°C. The oven temperature was instructed to an initial temperature of 50°C (hold 2 minutes) to 150°C at an increasing rate of 7°C/minute, then to 270°C at an increasing rate of 5°C/minute (hold 2 minutes), and subsequently to 310°C as the definitive temperature at a growing level of 3.5°C/minute (hold 10 minutes). The quantitative determination of all the identified compounds was examined using a percent relative peak area. A tentative recognition of the components was accomplished based on the comparison of the irrelative retention time and mass spectra with those of the National Institute of Standards and Technology (NIST), Wiley library data of the GC-MS technique.

Statistical analysis

All investigations were carried out thrice, and the obtained results are recorded as the average and standard deviation (SD). Significant variations were explored using the one-way analysis of variance. Variances at p < 0.05 were considered significant.

RESULTS AND DISCUSSION

Marine bivalves represent a basic source of highly nutritional, low-calorie, and easily digestible food with high protein contents (Panayotova et al., 2020; Nair et al., 2015). Recently, their consumption has highly increased as they contain many bioactive molecules with biomedical importance (Eghianruwa et al., 2019). The extracts of the marine mollusks showed numerous biological activities like anti-infectious disease, antimicrobial, anticancer, antioxidant, and cardiovascular protection activities (Odeleye et al., 2019). Clams are edible bivalve mollusks that represent the most important seafood resources in the coastal regions. Previous reports revealed that the extract of these clams, either ethanolic or methanolic, showed anti-inflammatory, antioxidant, antihypertensive, and antidiabetic activities (Joy et al., 2016). Bivalves could be utilized as naturally occurring antioxidant supplements to relieve oxidative stress-induced diseases, as the clams’ tissues are not damaged after exposure to high water salinity or any toxic chemical compounds (González et al., 2015).

GC-MS investigation of the methanolic extract of P. undulatus

GC-MS examination of the crude methanol extract of P. undulatus (Born, 1778) led to the identification of 38 compounds (Fig. 2). The recognized ingredients comprise 88.54% of the total extract composition; the characterized compounds are listed in Table 1. The major detected ingredients are 7-hexadecenoic acid, methyl ester, (Z) (32.01%), hexadecanoic acid, methyl ester (14.03%), 9-octadecenoic acid, methyl ester (8.43%), palmitoleic acid (5.75%), 5,8,11,14,17-eicosapentaenoic acid, methyl ester (5.25%), tridecanoic acid, 4,8,12-trimethyl-, methyl ester (3.44%), tetradecanoic acid, methyl ester (3.34%), and cis-9-hexadecenoic acid (3.23%) (Fig. 3). The present investigations highlight for the first time the chemical constituents of the marine clam P. undulatus and study the possible activities of its methanolic extract. The characterization was achieved using “computer search user-generated reference libraries” and integrating mass/mass spectra (Abdel-Wareth et al., 2019; Khalaf et al., 2020; Madkour et al., 2017; Shawky et al., 2019).

Concomitantly, Ibrahim et al. (2020) stated that GC-MS analysis of the methanol extract from Holothuria atra (sea cucumber) revealed the presence of 15 major bioactive constituents including methanesulfonylacetic acid (34.70%), 2,3-dihydro-6-hydroxy-3-oxo-2-(piperidinomethyl) pyridazine (39.23%), acetic acid butyl-methyl-phosphinoyl methyl ester (14.13%), S-methyl methanethiosulfonate (85.34%), 1,2,4-trithiolane (62.85%), 2-[4-methyl-6-(2,6,6-trimethylcyclohex-1-enyl)hexa-1,3,5-trienyl]cyclohex-1-en-1carboxaldehyde (5.83%), 4,25-secoobscurinervan-4-one, O-acetyl-22-ethyl-15,16-dimethoxy-,(22à) (29.54%), N,N’-bis(carbobenzyloxy)-lysine methyl(ester) (23.68%), 2-propen-1-ol, 2-methyl-3-(2,6,6-trimethyl-2-cyclohexen-1-yl)-,(E) (8.49%), 2-amino-3-(4-hydroxyphenyl)-propanoic acid (7.64%), cyclohexasiloxane, dodecamethyl (91.46%), Z,Z,Z-4,6,9-nonadecatriene (6.81%), cycloheptasiloxane, tetradecamethyl (72.91%), cyclooctasiloxane, hexadecamethyl (43.78%), and ergosta-5,22-dien-3-ol, acetate, (3á,22E) (6.81%). These compounds were categorized as organic and fatty acids as well as their derivatives, in addition to organic alcohols, steroids, terpenoids, amino acids, esters, and benzene derivatives. However, most of these constituents act as antibacterial and antifungal agents (Hussein et al., 2016; Ibrahim, 2012; Ibrahim et al., 2018).

Recently, Ibrahim et al. (2018) detected the principal components in the sponge Ciocalypta penicillus extracts by GC-MS analysis including fatty acids and their esters (hexadecanoic acid and octadecanoic acid), as well as steroids and terpenoids, which have antimicrobial effects. Fatty acids are able to act as anionic surfactants; they also possess antifungal and antibacterial characteristics at low pH (Donia and Hamann, 2003; Ibrahim and Abd-Elnaby, 2010). More specifically, diterpene isonitriles isolated from the tropical marine sponge Cymbastela hooperi and the sesquiterpene axisonitrile-3 isolated from the tropical marine sponge Acanthella kletra were evaluated as antifouling, antialgal, antiphotosynthetic, antibacterial, antifungal, and antitubercular agents (Wright et al., 2011).

Figure 2. GC-MS chromatogram of the methanolic extract of P. undulatus clams.

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Table 1. Chemical compositions of the methanolic extract of P. undulatus clams.

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Antibacterial and antibiofilm activities

The in vitro antibacterial ability of the methanolic extract of P. undulatus clams was estimated against numerous pathogenic microbes including four Gram-negative and one Gram-positive bacteria and one yeast. Our findings revealed that the tested extract exhibited variable antibacterial activity against tested microbial strains in the (blank/tested extract) manner: (0.449/0.196), (0.503/0.319), (1.048/0.174), (1.077/0.221), (1.067/0.102), and (0.792/0.285), respectively, for E. coli, P. aeruginosa, P. vulgaris, K. pneumoniae, S. aureus, and C. albicans (Table 2, Fig. 4). On the other side, the antibiofilm activity was evaluated using the Media Transfer Protocol (MTP) assay at concentration (100 μg/ml). In this assay, the tested extract was evaluated for its biofilm inhibition activity versus some investigated pathogenic microbial strains as well as their malice factor from the direction of biofilm development. The obtained results revealed that the tested extract exhibited a potent inhibition percentage of 91.98% against S. aureus, followed by 53.01% against B. subtilis, 31.90% against P. aeruginosa, and 24.20% against E. coli (Table 3). Conclusively, the crude methanol extract of P. undulatus clams is likely to be a good candidate against biofilm colonization and cell adherence. It is worth mentioning that bacterial infection leads to a high risk in both human and animal populations (Kandhasamy and Arunachalam, 2008). Antibiotics usage has highly increased during the last decades, and this has led to the development of strong resistance from pathogenic bacteria against drugs (Lavanya and Veerappan, 2011). Due to the high cost of these drugs (Idsoe et al., 1968), there is an urgent need to discover alternative antimicrobials from natural sources (Abubakar et al., 2012; Smith et al., 1994). The marine environment is a huge source of bioactive substances that are widely used in biomedical applications (Omar, 2012). The marine mollusks collected from the Kanyakumari coast comprised numerous biologically active ingredients that could be used as promising antibacterial agents (Giftson and Patterson, 2016). Also, Ibrahim et al. (2020) stated that many of the marine mollusks create their antibacterial factors as a first line of defense versus pathogenic microbial infection. They concluded that the crude extracts of the marine sea cucumber and sponges caused inhibition of different human pathogens such as S. aureus, Enterococcus faecalis, P. aeruginosa, and E. coli and could be represented as a promising source of new bioactive substances that are applied in the clinical field. Additionally, Youssef et al. (2013) confirmed the presence of three types of alkaloids from the Red Sea sponges which have antioxidant, antimicrobial, and anticancer activities.

TPC and antioxidant activity

The methanolic extract was evaluated for its TPC, free radical scavenging activity (DPPH), and TAC. The extract exhibited a TPC value of 177.23 mg GAE/g dry extract. Also, it had the capability to scavenge DPPH free radical with an IC₅₀ value of 14.59 µg/ml in comparison with ascorbic acid as a reference compound with an IC₅₀ value of 7.52 µg/ml. Moreover, it showed a TAC value of 371.66 mg AAE/g dry extract, reflecting its reduction capability to convert molybdenum (VI) to molybdenum (V) (Table 4). Joy et al. (2016) confirmed the antioxidant, antidiabetic, anti-inflammatory, and antihypertensive potential of ethyl acetate-methanol extract of bivalve clams. They stated that the EtOAc-MeOH extract of Paphia malabarica showed total phenolics significantly greater (88.6 mg GAE/g) than those in Villorita cyprinoides (73.9 mg GAE/g). The polyphenolic ingredients exhibited free radical scavenging activities and were ensured to shield the delicate bodied mollusks from photooxidation (Karawita et al., 2005; Rockenbach et al., 2011). Polyphenolics showed high redox potential and act as strong electron donors due to their unique heavy hydroxylation pattern (Ghareeb et al., 2014b). The crude methanol and ethyl acetate extracts of Perna viridis exhibited notable free radical scavenging activity against DPPH free radical, which reinforces our current findings (Sreejamole and Radhakrishnan, 2013). Also, P. undulatus extracts have bioactive molecules called hydrolysates that have shown potential hepatoprotective roles through their antioxidant activities (Nair et al., 2015).

Figure 3. Chemical structures of the major identified compounds.

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Table 2. In vitro antibacterial activity of the methanolic extract of P. undulatus clams against some pathogenic microbial strains.

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Figure 4. In vitro antibacterial activity of the methanolic extract of P. undulatus clams against some pathogenic microbial strains.

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Table 3. Antibiofilm activity of the methanolic extract of P. undulatus clams against some pathogenic microbial strains.

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Table 4. TPC, free radical scavenging activity (DPPH), and TAC of the methanolic extract of P. undulatus clams.

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CONCLUSION

The obtained results disclosed that the methanolic extract of the marine clam P. undulates consists of many bioactive molecules like hexadecenoic acid, methyl ester, hexadecanoic acid, 9-octadecenoic acid, and palmitoleic acid. Additionally, the results showed that the extract has remarkable antibacterial, antibiofilm, and antioxidant activities. The present results might be helpful for pharmaceutical companies to develop natural supplements from these clams. Subjecting the extract to further chromatographic isolation and identification is recommended to identify its main ingredients using developed chromatographic and spectroscopic tools.

AUTHOR CONTRIBUTIONS

All authors made substantial contributions to conception and design, acquisition of data, or analysis and interpretation of data; took part in drafting the article or revising it critically for important intellectual content; agreed to submit to the current journal; gave final approval of the version to be published; and agree to be accountable for all aspects of the work. All the authors are eligible to be an author as per the international committee of medical journal editors (ICMJE) requirements/guidelines.

FUNDING

There is no funding to report.

CONFLICTS OF INTEREST

The authors report no financial or any other conflicts of interest in this work.

ETHICAL APPROVALS

This study does not involve experiments on animals or human subjects.

PUBLISHER’S NOTE

This journal remains neutral with regard to jurisdictional claims in published institutional affiliation.

DATA AVAILABILITY

All the data obtained during the study are presented in this manuscript. Any further inquiries for additional information are available upon request from the corresponding author.

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Khan MK, Sajid MS, Khan MN, Iqbal Z, Iqbal MU. Bovine fasciolosis: prevalence, effects of treatment on productivity and cost benefit analysis in five districts of Punjab, Pakistan. Res Vet Sci, 2009; 87:70–5. CrossRef

Lavanya R, Veerappan N. Antibacterial potential of six seaweeds collected from Gulf of Mannar of southeast coast of India. Adv Biol Res, 2011; 5:38–44.

Loftus E, Rogers K, Lee-Thorp J. A simple method to establish calcite: aragonite ratios in archaeological mollusc shells. J Quat Sci, 2015; 30:731–5. CrossRef

Madkour HMF, Ghareeb MA, Abdel-Aziz MS, Khalaf OM, Saad AM, El-Ziaty AK, and Abdel-Mogib M. Gas chromatography-mass spectrometry analysis, antimicrobial, anticancer and antioxidant activities of n-hexane and methylene chloride extracts from Senna italica. J Appl Pharm Sci, 2017; 7:023–32.

Nair DG, Weiskirchen R, Al-Musharafi SK. The use of marine-derived bioactive compounds as potential hepatoprotective agents. Acta Pharmacol Sin, 2015; 36:158–70. CrossRef

Odeleye T, White WL, Lu J. Extraction techniques and potential health benefits of bioactive compounds from marine molluscs: a review. Food Funct, 2019; 10:2278–89. CrossRef

Omar HH. Antibacterial activity of extracts of marine algae from the Red Sea of Jeddah, Saudi Arabia. African J Biotechnol, 2012; 11:13576–85. CrossRef

Panayotova V, Merdzhanova A, Dobreva DA, Bratoeva K, Makedonski L. Nutritional composition, bioactive compounds and health-beneficial properties of black sea Shellfish. J IMAB-Annu Proc (Sci Pap), 2020; 26(3):3293–7. CrossRef

Prieto P, Pineda M, Aguilar M. Spectrophotometric quantitation of antioxidant capacity through the formation of a phosphomolybdenum complex: specific application to the determination of vitamin E. Anal Biochem, 1999; 269(2):337–41. CrossRef

Rockenbach II, Rodrigues E, Gonzaga LV, Caliari V, Genovese MI, Gonalves AEDSS, Fett R. Phenolic compounds content and antioxidant activity in pomace from selected red grapes (Vitis vinifera L. and Vitis labrusca L.) widely produced in Brazil. Food Chem, 2011; 127:174–9. CrossRef

Rusmore-Villaume ML. Seashells of the Egyptian Red Sea - The Illustrated Handbook, 2008. The American University in Cairo Press, Cairo, Egypt.

Schmitt P, Rosa RD, Duperthuy M, de Lorgeril J, Bachère E, Destoumieux-Garzón D. The antimicrobial defense of the Pacific oyster, Crassostrea gigas. How diversity may compensate for scarcity in the regulation of resident/pathogenic microflora. Front Microbiol, 2012; 3:160. CrossRef

Shawky BT, Nagah M, Ghareeb MA, El-Sherbiny GM, Moghannem SAM, and Abdel-Aziz MS. Evaluation of antioxidants, total phenolics and antimicrobial activities of ethyl acetate extracts from fungi grown on rice straw. J Renew Mater, 2019; 7(7):667–82. CrossRef

Shirwaikar A, Shirwaikar A, Rajendran K, Punitha ISR. In vitro antioxidant studies on the benzyl tetra isoquinoline alkaloid berberine. Biol Pharm Bull, 2006; 29:1906–10. CrossRef

Smith P, Hiney MP, Samuelsen OB. Bacterial resistance to antimicrobial agents used in fish farming: a critical evaluation of method and meaning. Annu Rev Fish Dis, 1994; 4:273–313. CrossRef

Sobeh M, Mahmoud MF, Hasan RA, Abdelfattah MAO, Sabry OM, Ghareeb MA, El-Shazly AM, Wink M. Tannin-rich extracts from Lannea stuhlmannii and Lannea humilis (Anacardiaceae) exhibit hepatoprotective activities in vivo via enhancement of the anti-apoptotic protein Bcl-2. Sci Rep, 2018; 8:9343. CrossRef

Sreejamole KL, Radhakrishnan CK. Antioxidant and cytotoxic activities of ethyl acetate extract of the Indian green mussel Perna viridis. Asian J Pharm Clin Res, 2013; 6:197–201.

Tabakaeva OV, Tabakaev AV, Piekoszewski W. Nutritional composition and total collagen content of two commercially important edible bivalve molluscs from the Sea of Japan coast. J Food Sci Technol, 2018; 55:4877–86. CrossRef

Temraz TA. Egyptian biodiversity strategy and action plan (2015-2030). FAO, 2016. Available via https://www.fao.org/faolex/results/details/en/c/LEX-FAOC156958/

Wright AD, McCluskey A, Robertson MJ, MacGregor KA, Gordon CP, Guenther J. Anti-malarial, anti-algal, anti-tubercular, anti-bacterial, anti-photosynthetic, and anti-fouling activity of diterpene and diterpene isonitriles from the tropical marine sponge Cymbastela hooperi. Org Biomol Chem, 2011; 9:400–7. CrossRef

Youssef DTA, Shaala LA, Asfour HZ. Bioactive compounds from the Red Sea marine sponge Hyrtios species. Mar Drugs, 2013; 11:1061–70. CrossRef

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Khalaf OM, Abdel-Aziz MS, El-Hagrassi AM, Osman AF, Ghareeb MA. Biochemical aspect, antimicrobial and antioxidant activities of Melaleuca and Syzygium species (Myrtaceae) grown in Egypt. J Phys Conf Ser, 2021; 1879:022062. https://doi.org/10.1088/1742-6596/1879/2/022062
Khan MK, Sajid MS, Khan MN, Iqbal Z, Iqbal MU. Bovine fasciolosis: prevalence, effects of treatment on productivity and cost benefit analysis in five districts of Punjab, Pakistan. Res Vet Sci, 2009; 87:70-5. https://doi.org/10.1016/j.rvsc.2008.12.013
Lavanya R, Veerappan N. Antibacterial potential of six seaweeds collected from Gulf of Mannar of southeast coast of India. Adv Biol Res, 2011; 5:38-44.
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Madkour HMF, Ghareeb MA, Abdel-Aziz MS, Khalaf OM, Saad AM, El-Ziaty AK, and Abdel-Mogib M. Gas chromatography-mass spectrometry analysis, antimicrobial, anticancer and antioxidant activities of n-hexane and methylene chloride extracts from Senna italica. J Appl Pharm Sci, 2017; 7:023-32.
Nair DG, Weiskirchen R, Al-Musharafi SK. The use of marinederived bioactive compounds as potential hepatoprotective agents. Acta Pharmacol Sin, 2015; 36:158-70. https://doi.org/10.1038/aps.2014.114
Odeleye T, White WL, Lu J. Extraction techniques and potential health benefits of bioactive compounds from marine molluscs: a review. Food Funct, 2019; 10:2278-89. https://doi.org/10.1039/C9FO00172G
Omar HH. Antibacterial activity of extracts of marine algae from the Red Sea of Jeddah, Saudi Arabia. African J Biotechnol, 2012; 11:13576-85. https://doi.org/10.5897/AJB12.780
Panayotova V, Merdzhanova A, Dobreva DA, Bratoeva K, Makedonski L. Nutritional composition, bioactive compounds and healthbeneficial properties of black sea Shellfish. J IMAB-Annu Proc (Sci Pap), 2020; 26(3):3293-7. https://doi.org/10.5272/jimab.2020263.3293
Prieto P, Pineda M, Aguilar M. Spectrophotometric quantitation of antioxidant capacity through the formation of a phosphomolybdenum complex: specific application to the determination of vitamin E. Anal Biochem, 1999; 269(2):337-41. https://doi.org/10.1006/abio.1999.4019
Rockenbach II, Rodrigues E, Gonzaga LV, Caliari V, Genovese MI, Gonalves AEDSS, Fett R. Phenolic compounds content and antioxidant activity in pomace from selected red grapes (Vitis vinifera L. and Vitis labrusca L.) widely produced in Brazil. Food Chem, 2011; 127:174-9. https://doi.org/10.1016/j.foodchem.2010.12.137
Rusmore-Villaume ML. Seashells of the Egyptian Red Sea - The Illustrated Handbook, 2008. The American University in Cairo Press, Cairo, Egypt. Schmitt P, Rosa RD, Duperthuy M, de Lorgeril J, Bachère E, Destoumieux-Garzón D. The antimicrobial defense of the Pacific oyster, Crassostrea gigas. How diversity may compensate for scarcity in the regulation of resident/pathogenic microflora. Front Microbiol, 2012; 3:160. https://doi.org/10.3389/fmicb.2012.00160
Shawky BT, Nagah M, Ghareeb MA, El-Sherbiny GM, Moghannem SAM, and Abdel-Aziz MS. Evaluation of antioxidants, total phenolics and antimicrobial activities of ethyl acetate extracts from fungi grown on rice straw. J Renew Mater, 2019; 7(7):667-82. https://doi.org/10.32604/jrm.2019.04524
Shirwaikar A, Shirwaikar A, Rajendran K, Punitha ISR. In vitro antioxidant studies on the benzyl tetra isoquinoline alkaloid berberine. Biol Pharm Bull, 2006; 29:1906-10. https://doi.org/10.1248/bpb.29.1906
Smith P, Hiney MP, Samuelsen OB. Bacterial resistance to antimicrobial agents used in fish farming: a critical evaluation of method and meaning. Annu Rev Fish Dis, 1994; 4:273-313. https://doi.org/10.1016/0959-8030(94)90032-9
Sobeh M, Mahmoud MF, Hasan RA, Abdelfattah MAO, Sabry OM, Ghareeb MA, El-Shazly AM, Wink M. Tannin-rich extracts from Lannea stuhlmannii and Lannea humilis (Anacardiaceae) exhibit hepatoprotective activities in vivo via enhancement of the anti-apoptotic protein Bcl-2. Sci Rep, 2018; 8:9343. https://doi.org/10.1038/s41598-018-27452-8
Sreejamole KL, Radhakrishnan CK. Antioxidant and cytotoxic activities of ethyl acetate extract of the Indian green mussel Perna viridis. Asian J Pharm Clin Res, 2013; 6:197-201.
Tabakaeva OV, Tabakaev AV, Piekoszewski W. Nutritional composition and total collagen content of two commercially important edible bivalve molluscs from the Sea of Japan coast. J Food Sci Technol, 2018; 55:4877-86. https://doi.org/10.1007/s13197-018-3422-5
Temraz TA. Egyptian biodiversity strategy and action plan (2015-2030). FAO, 2016. Available via https://www.fao.org/faolex/results/ details/en/c/LEX-FAOC156958/
Wright AD, McCluskey A, Robertson MJ, MacGregor KA, Gordon CP, Guenther J. Anti-malarial, anti-algal, anti-tubercular, antibacterial, anti-photosynthetic, and anti-fouling activity of diterpene and diterpene isonitriles from the tropical marine sponge Cymbastela hooperi. Org Biomol Chem, 2011; 9:400-7. https://doi.org/10.1039/C0OB00326C
Youssef DTA, Shaala LA, Asfour HZ. Bioactive compounds from the Red Sea marine sponge Hyrtios species. Mar Drugs, 2013; 11:1061-70. https://doi.org/10.3390/md11041061

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