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/lp/springer-journals/encapsulation-of-e-coli-phage-zcec5-in-chitosan-alginate-beads-as-a-ritlRy3bJ3
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- Springer Journals
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- Copyright © 2019 by The Author(s)
- Subject
- Life Sciences; Microbiology; Microbial Genetics and Genomics; Biotechnology
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- 2191-0855
- DOI
- 10.1186/s13568-019-0810-9
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Abstract
Bacteriophages can be used successfully to treat pathogenic bacteria in the food chain including zoonotic patho‑ gens that colonize the intestines of farm animals. However, harsh gastric conditions of low pH and digestive enzyme activities affect phage viability, and accordingly reduce their effectiveness. We report the development of a natural protective barrier suitable for oral administration to farm animals that confers acid stability before functional release of bead‑ encapsulated phages. Escherichia coli bacteriophage ZSEC5 is rendered inactive at pH 2.0 but encapsulation −1 in chitosan–alginate bead with a honey and gelatin matrix limited titer reductions to 1 log PFU mL . The encapsu‑ lated phage titers were stable upon storage in water but achieved near complete release over 4–5 h in a simulated intestinal solution (0.1% bile salt, 0.4% pancreatin, 50 mM KH PO pH 7.5) at 37 °C. Exposure of E. coli O157:H7 to 2 4 the bead‑ encapsulated phage preparations produced a delayed response, reaching a maximal reductions of 4.2 to −1 4.8 log CFU mL after 10 h at 37 °C under simulated intestinal conditions compared to a maximal reduction of −1 5.1 log CFU mL at 3 h for free phage applied at MOI = 1. Bead‑ encapsulation is a promising reliable and cost‑ effec‑ tive method for the functional delivery of bacteriophage targeting intestinal bacteria of farm animals. Keywords: E. coli, Bacteriophage, Biocontrol, Phage encapsulation Introduction Enterohemorrhagic Escherichia coli O157:H7 is a Antibiotic resistance is a serious public health prob- zoonotic pathogen frequently isolated from healthy cat- lem worldwide. Commercially available antibiotics are tle and other farm animals. The organism causes human becoming less effective as resistance rates rise over time gastroenteritis, haemorrhagic colitis, and can lead to the (Akinkunmi and Lamikanra 2015). Accordingly, many development of hemolytic uremic syndrome (Karmali intestinal bacterial infections are showing greater viru- et al. 1983). Isolates often show multi-drug resistant phe- lence and/or persistence (Munot and Kotler 2016). Such notypes with reports indicating resistance to 14 different resistance phenotypes are generally attributed to the antibiotics (Verstraete et al. 2013). E. coli O157:H7 can misuse of antibiotics, which have increased invulnerabil- be acquired from direct contact with infected animals ity to hamper the treatment of infection, and indirectly (Belongia et al. 1991), or through cross-contamination of increase the rate of mortality. Antibiotic use and resist- raw materials in the preparation of foods, or through the ance presents a real dilemma for developed and develop- consumption of contaminated food (Neil et al. 2012). E. ing countries (Fortini et al. 2011; Pavlickova et al. 2015; coli O157:H7 remains a threat to public health. Wellington et al. 2013). Bacteriophages represent an alternative treatment for the control of bacterial contamination in foods as well as the control of bacterial infections in man and ani mals due to their abilities to specifically target bacterial *Correspondence: aelshibiny@zewailcity.edu.eg host cells and self-replicating nature (Jassim and Limo- Center for Microbiology and Phage Therapy, Zewail City of Science ges 2014; Summers 2001; Taha et al. 2018). Research has and Technology, October Gardens, 6th of October City, Giza 12578, Egypt demonstrated the use of bacteriophages to reduce E. coli Full list of author information is available at the end of the article © The Author(s) 2019. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creat iveco mmons .org/licen ses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. Abdelsattar et al. AMB Expr (2019) 9:87 Page 2 of 9 O157:H7 in the gastrointestinal tracts of mice (Tanji et al. coli O157:H7 viable counts under simulated intestinal 2005) and sheep (Bach et al. 2003; Raya et al. 2011), and conditions. on the surface of the meat (El-Shibiny et al. 2017; O’Flynn et al. 2004). Studies also suggest phage application could Materials and methods decrease the mortality rate of poultry on infected farms Bacterial strain and culture conditions (Xie et al. 2005). Studies were conducted using the bacterial host E. coli The oral application of phage in human trials has not O157:H7 NCTC 12900 (the kind gift of Dr. Elizabeth reported any adverse effects (Bruttin and Brussow 2005; Kutter). Bacteriophage were routinely propagated on Sarker et al. 2012; McCallin et al. 2013). However, the E. coli O157:H7 NCTC 12900. Stocks were maintained oral application of phage is not without difficulty due in 20% (v/v) glycerol at − 80 °C. In the following experi- to exposure to gastric juice (GJ) during stomach transit, ments, bacterial strains were grown on tryptic soy agar which may affect the viability of bacteriophages (Tóthová (TSA; Oxoid, England) overnight and infections car- et al. 2012). In light of the above, phage encapsulation ried out in Tryptic Soya Broth (TSB; Oxoid, England) in techniques have provided a protective delivery tech- Erlenmeyer flasks at 37 °C and 120 RPM to reach OD600 nique for phage against the harsh conditions of GJ with approximately 0.3. minimal phage loss (Choińska-Pulit et al. 2015). Previ- ous publications have highlighted the possibility of using Bacteriophage isolation and enumeration food-grade alginate and chitosan as biomaterials for the Bacteriophages were isolated by us from environmen- microencapsulation of bacteriophages (Ma et al. 2008, tal and sewage samples against E. coli O157:H7 NCTC 2012; Tang et al. 2013; Kim et al. 2015; Colom et al. 2017). 12900. Each sample (~ 1 mL) was mixed with TSB con- Alginate is considered a good system for phage encapsu- taining the bacterial host and incubated overnight at lation because of its ability to resist acidity, and to con- 37 °C to amplify any available phage. After incubation, trol and sustain the release of live products to the gut each sample was serially diluted and spotted on to bacte- such as probiotic bacteria and bacteriophages (Gbassi rial lawns of E. coli O157:H7 NCTC 12900 to identify any et al. 2009; Lee and Heo 2000). Alginate polysaccharide bacteriophages by checking the production of plaques in can be obtained naturally from bacteria and algae, which the bacterial lawn by the 2nd day. A single plaque from a crosslinks to form a gel with calcium (Lee and Heo 2000). positive agar plate was purified by repeated single plaque Chitosan is a natural polymer that can be obtained from isolation using sterile micropipette tips (Adams 1959). crustaceans with inherent bacteriostatic and antifungal All isolated bacteriophages were amplified in TSB and properties (Mcknight et al. 1988). Accordingly, it is inap- the lysate was centrifuged at 6400×g for 15 min at 4 °C to propriate for use as a core solution for capsules (Sudar- remove the bacterial cells and debris (Marcó et al. 2012). shan et al. 1992), but can be used as a coating material in The supernatant was then centrifuged at 15,300×g at 4 °C pharmaceutical applications due to its solubility in acid for 1 h to obtain the precipitated pellet of bacteriophages. conditions coupled with excellent biodegradable and bio- Bacteriophage pellets were re-suspended in SM buffer compatible properties (Allan et al. 1984). Retention of (100 mM MgSO ·7H O; 10 mM NaCl; 50 mM Tris- the bead structure and preservation of the phage payload 4 2 HCl pH 7.5) and filtered using 0.22 μm syringe filters requires that the inner matrix have suitable aqueous vis- (Chromtech, Taiwan). The purified bacteriophage stock cosity. To this end formulations with gelatin to improve was then enumerated as plaque-forming unit (PFU) using the functional properties of the beads (Gbassi and Van- double-agar overlay plaque assays (Kropinski et al. 2009), damme 2012), and honey to stabilize the phage (Oliveira and stored in SM buffer at 4 °C prior to use (Lillehaug et al. 2017) were explored. In general, the encapsulation 1997). The phage isolate ZCEC5 used in this study can be process could protect phages against harsh conditions obtained from Biomedical Sciences Program, Zewail City such as acidity and oxidation, control of the release of of Science and Technology, 12578 Giza, Egypt. the active agents, facilitate their diffusion and improve effectiveness (Ghosh et al. 2006; Jyothi et al. 2010; Tang et al. 2013). The objective of this study was to develop Characterization of bacteriophage ZCEC5 a stable chitosan–alginate bead delivery system for the Bacteriophage ZCEC5 was examined using transmission controlled release of bacteriophages. We have examined electron microscopy at the National Research Center the protection afforded by the beads for E. coli O157:H7 (Cairo, Egypt) as previously described (Atterbury et al. bacteriophages under simulated GI conditions and stor- 2003). Briefly, fixed phages on Pioloform grids using glu - age conditions with respect to retention of bacteriophage taraldehyde were negatively stained with 0.5% uranyl ace- titers. We demonstrate that the beads are an effective tate. After drying, the specimens were examined using a delivery agent for phage with advantages in reducing E. JEOL 100CX transmission electron microscope. Abdelsattar et al. AMB Expr (2019) 9:87 Page 3 of 9 Genomic DNA was extracted from a lysate of phage buffer solution (pH 4.2) for 30 min. The beads were 10 −1 ZCEC5 (10 PFU mL ) treated with proteinase K washed with distilled water and stored at 4 °C prior to −1 (100 μg mL in 10 mM EDTA at pH 8) before purifica - use. tion by the Wizard DNA kit (Promega, UK) according to the manufacturer’s instructions. The genome DNA Bacteriophage stability and release under simulated of phage ZCEC5 was sequenced from libraries prepared intestinal conditions using the Illumina tagmentation protocol on the MiSeq The stability of encapsulated phages in simulated intesti - platform. The data was composed of 0.52 million paired- nal conditions was tested by preparing an artificial intes - end sequence reads with read lengths of approximately tinal juice by dissolving 0.1% bile salt and 0.4% pancreatin 250 bp. The data was de novo assembled using CLC (Sigma-Aldrich, MO, USA) in 50 mM KH PO pH 7.5 2 4 Genomics Workbench version 10.0.1 (Qiagen, Aarhus, (Kim et al. 2015). The beads of encapsulated bacterio - 7 −1 Denmark). The open reading frames (ORFs) were pre - phages at 2 × 10 PFU mL were incubated in simulated dicted from PHASTER (Arndt et al. 2016). The genome intestinal juice for 6 h at 37 °C with agitation. The free DNA sequence appears in GenBank under the Accession bacteriophage titer was determined using double-agar Number MK542015. overlay plaque assays as described above. Encapsulation of bacteriophages Acid stability assay Encapsulated bacteriophages were prepared using a chi- The stability of encapsulated bacteriophages (beads) at tosan–alginate coating shell (Fig. 1). Four matrices were the digestive system pH ranges was evaluated in 0.5% prepared to produce the beads for study. The matrices NaCl solution adjusted to different pH values (2, 2.5, 3, 4 for beads 1 and 2 were prepared by suspending bacterio- and 7) by the addition of 1 M HCl solutions. Beads were phages in either 0.3% commercial honey and 0.25% gela- incubated in solutions of various pH for 60 min at 37 °C. tin or 3% honey to 2.5% gelatin, respectively. The matrix After washing with distilled water, beads were incubated for bead 3 was prepared by suspending bacteriophages in at 37 °C for 60 min in a dissolving buffer solution (50 mM 50 mM Tris-HCl pH 7.4, while the matrix for beads 4 was sodium citrate, 0.2 M sodium bicarbonate and 50 mM prepared by suspending bacteriophages in 0.01% gelatin, Tris-HCl at pH 7.3) (Liu et al. 2002), and the titers of the 0.05% honey, 0.15 M NaCl and 10 mM M gSO ·7H O. released bacteriophages determined using the double- 4 2 Each type of matrix was mixed with 1.5% sodium alginate agar overlay plaque assays. and then extruded into a 100 mM CaCl solution using a syringe before it was washed with distilled water after Thermal stability assay 30 min. The prepared Ca-alginate beads were coated with The stability of encapsulated and non-encapsulated bac - chitosan applied in a chitosan (0.4%)-acetate (100 mM) teriophages over a range of temperatures was evaluated by incubating phage suspensions in SM buffer at 25, 40, 60 and 80 °C for 60 min. To detect the protective effect of matrices against thermal conduction, the encapsulated and non-encapsulated bacteriophage were exposed to 80 °C and samples were taken at 0, 30, 180 s intervals to detect the change in phage titer upon sudden tempera- ture alteration. The titers of released bacteriophages were determined using the double-agar overlay plaque assays. Examination of bead morphology Encapsulated bacteriophages samples were investigated using a Trinocular Zoom Stereo microscope (Meiji Techno, EMZ-13TR). Diffusion properties of stored encapsulated bacteriophages Encapsulated bacteriophages were stored in flasks con - taining 200 mL of distilled water at 4 °C. Samples of water Fig. 1 Representation of the bead encapsulation components in cross‑section. The blue color refers to the chitosan, purple the were collected at various time points to determine the Ca‑alginate, green the internal matrix and yellow represents the phage titers released using double-agar overlay plaque bacteriophage assays. Abdelsattar et al. AMB Expr (2019) 9:87 Page 4 of 9 Lytic activity assay Lytic activity of non‑encapsulated and encapsulated Encapsulated and non-encapsulated bacteriophage bacteriophages were tested for their lytic activity against E. coli The lytic activities of non-capsulated and encapsu - O157:H7 NCTC 12900 by incubating each type of lated bacteriophages were determined against E. coli beads with E. coli in intestinal buffer at 37 °C with O157:H7 NCTC 12900 over 3, 6 and 10 h in simu- agitation at 120 rpm. The infection was performed at lated intestinal conditions at MOI = 1 (Fig . 4a). Non- MOI = 1 and samples were collected after 3, 6 and 10 h encapsulated ZCEC5 showed maximal reductions in of incubation for analysis. the viable count of E. coli O157:H7 NCTC 12900 of −1 5.1 log CFU mL after 3 h and declined upon increas- ing the incubation time under the simulated intestinal Statistical analysis conditions. Conversely, bead-encapsulated bacterio- All statistical analyses were carried out in triplicates. phages exhibit a delay in the observed reduction of E. In this study, the Student’s t-test and one-way ANOVA coli O157:H7 NCTC 12900 that is commensurate with were used as statistical analysis test. The significance the cumulative release of bacteriophage ZCEC5 over level was p < 0.05. Data were analyzed using GraphPad time. After 10 h maximal reductions for the bead- PRISM version 5.01 for Windows (GraphPad Software, −1 encapsulated treatments (4.2 to 4.8 log CFU mL ) La Jolla, USA). were comparable to that of free phage at 3 h (Fig. 4a). Host infection in gastrointestinal fluid lead to a 100- Results fold amplification of the bead-encapsulated phages over Bead morphology of the encapsulated bacteriophage −1 the initial titer of 7 log PFU mL at 10 h, compared preparations 10 to tenfold recorded for free ZCEC5 phage infection The morphological characteristics of the ZCEC5 (Fig. 4b). phage-encapsulated beads were determined by inverted microscopy. Beads 1, 2 and 3 appeared spherical shape with mean diameters of 2.38 ± 0.14, 2.8 ± 0.11 and Acid and thermal acid stability of bead‑encapsulated 2.33 ± 0.12 mm, respectively (Fig. 2a–c). Bead prepa- phage ration 4 (0.01% gelatin, 0.05% honey, 0.15 M NaCl The stability of the bead-encapsulated bacteriophages in and 10 mM MgSO ·7H O) appeared non-uniform and 4 2 comparison to non-encapsulated bacteriophages were irregular in shape (Fig. 3d), and was withdrawn from evaluated at acidic pH values, pH 2, 2.5, 3 and 4 over further experiments. 1 h at 37 °C (Fig. 5b). The viability of non-encapsulated bacteriophages at pH 2 was measured after 30 s, 5 min Assessing leakage of encapsulated bacteriophages and 10 min, where their titers were observed to decrease upon storage −1 by 2 log PFU mL after 30 s before falling below the To determine the retention and stability of the encap- −1 detection limit (3 log PFU mL ) after 10 min. The via - sulated bacteriophages, beads were stored in distilled bility of the bead-encapsulated phages were tested after water at 4 °C and samples collected every day for 8 days 1 h incubation at the pH indicated at 37 °C for 60 min in a and after 8 weeks of storage. Over the course of the dissolving buffer solution to release the encapsulated bac - experiment, no phage release was observed under the teriophages. Bead-encapsulation of bacteriophages has a storage conditions. protective effect against acid stress with approximately a 1 log PFU reduction observed at pH 2 compared to Release rate of encapsulated bacteriophages complete inactivation of the free phage. The matrix for - under stimulated intestinal conditions mulation of bead preparation 3 containing higher con- The bacteriophage release properties of the beads were centrations of glycerol and honey provided the greatest measured after incubation in simulated gastrointestinal protection against low pH with no significant difference fluid (Fig. 3). The beads performed similarly produc - −1 in the titer recovered post treatment at pH 3. ing titers in the range of 5.3 to 5.8 log PFU mL after −1 The role of each matrix component in conferring 1 h incubation and achieving 7.4 to 7.5 log PFU mL thermal protection was investigated by determining after 5 h of incubation that approximates to full release the phage titers released from the beads after 0.5, 1 and of the matrix titer. 3 min of heat treatment at 80 °C (Fig. 5a). Phage encapsu- lated in the matrix formulations of beads 1 and 2 contain- ing honey and glycerol were more resistant to the heat −1 treatment (titer reductions of 0.8 to 1 log PFU mL ) than free phage (titer reduction 2.2 ± 0.22 log PFU) or 10 Abdelsattar et al. AMB Expr (2019) 9:87 Page 5 of 9 Fig. 2 Optical micrographs of beads 1 (0.3% honey, 0.25% gelatin) in fresh form (a), beads 1 after 1‑h incubation (a1), beads 2 (3% honey, 2.5% gelatin) in fresh form (b), beads 2 after 1‑h incubation (b1), beads 3 (50 mM Tris‑HCl pH 7.4) in fresh form (c), beads 3 after 1‑h incubation (c1) and beads 4 (0.01% gelatin, 0.05% honey, 0.15 M NaCl and 10 mM MgSO ·7H O) in fresh form (d), each bead was loaded with bacteriophage ZCEC5 in 4 2 simulated intestinal juice Abdelsattar et al. AMB Expr (2019) 9:87 Page 6 of 9 −1 Fig. 3 In vitro L og PFU mL release of phages from chitosan– alginate capsules during incubation in gastrointestinal fluid for 6 h the Tris-buffer based matrix of bead preparation 3 (titer reduction 2.3 ± 0.14 log PFU). Discussion Ensuring the stability of bacteriophages is a key con- cern in the design of any phage therapy delivery method. Phage encapsulation is a promising technique that employs feed compatible materials that have no detrimental effect on phage activity. We demonstrate that bead-encapsulation can control the delivery of bacteriophage ZCEC5 in simulated gastrointesti- nal fluid and protect the phage from harsh conditions encountered in the stomach and intestinal tract to enable therapeutic delivery to farm animals. The sim - ple protocol produced an efficiency of encapsulation that approached 100% and conferred increased acid and thermal stability comparable to previous reports of phage encapsulation (Ma et al. 2008; Dini et al. 2012; Fig. 4 a Log reductions of E. coli O157:H7 incubated with encapsulated and non‑ encapsulated bacteriophages in Tang et al. 2013; Colom et al. 2017). Bead-encapsu- gastrointestinal fluid at 37 °C for 6 h and 10 h. Nt stands for the lated bacteriophages showed excellent stability with number of E. coli O157:H7 after treatment with encapsulated and no loss in phage titer when stored at 4 °C for 8 weeks. non‑ encapsulated bacteriophages at MOI = 1 and Nc represents the We have reduced the concentration of alginate to 1.5% number of E. coli O157:H7 at the control state. All phage treatments compared to previous reports of 2–2.2% without leak- produced significant falls in the viable count of E. coli O157:H7 (p value < 0.01). b Bacteriophage titers (Log PFU) of non‑ capsulated age of phage from the matrix (Kim et al. 2015; Ma et al. and encapsulated phages after infecting E. coli O157:H7 at MOI = 1 in 2008). Bacteriophage administered to farm animals gastrointestinal fluid for 6 h and 10 h must tolerate the acidic environment of the stomach. Under simulated intestinal conditions, chitosan–algi- nate encapsulated phages showed greater stability than the non-encapsulated phages (p < 0.01), with phage titer Abdelsattar et al. AMB Expr (2019) 9:87 Page 7 of 9 bacteriophage payload; a strategy based on reducing the rate of proton diffusion by increasing the viscosity of the bead matrix (Tyrrell 1981; Ma et al. 2012). The controlled time-dependent release of bacterio - phage ZCEC5 was achieved using the chitosan–alginate multilayer bead, which forms a cross-linked matrix that is preferable to fixing phages in gel networks (Anal and Stevens 2005; Colom et al. 2017). The pore size of the car - bohydrate polymer shell is less than 200 nm (Andresen et al. 1977), which is smaller than the ZCEC5 phage size (223 nm) and ensures the encapsulated phages are retained. Controlled release alters the dynamics of phage infection to delay the delivery of the active phage and extend the period in which the host bacteria are lysed. The prolonged activity of the bead-encapsulated phage is in contrast to the action of free phage that exhibit a reduction in the ability to kill the host and increase phage titers with time. The extended time of delivery and lysis activity, have the potential to reduce the development of phage resistance. In conclusion, this study demonstrates the efficient protective effect of core matrix materials in chitosan– alginate bead-encapsulated phage against inactivation by low pH, and to sustain bacteriophage release and lysis activity over time. Bead-encapsulation represents a sim- ple inexpensive phage oral drug delivery system suitable for on farm applications directed to control the intesti- nal colonization of zoonotic and pathogenic bacteria. Further studies have the potential to combine nutritional and therapeutic components with phages to aid recovery. Acknowledgements The authors like to thank all the members of Microbiology and Phage Therapy lab. This work is supported by Zewail City of Science and Technology. Author contributions Fig. 5 a The stability of non‑ encapsulated and encapsulated AE‑S and AA: primary responsibility for design of the work. AA, FA, AD and bacteriophages against high temperature (80 °C) for 3 min. b Low pH AE‑S: substantial contributions to the design of the work and analysis. AE‑S stability of the non‑ encapsulated and encapsulated bacteriophages and IC contributed to the interpretation of the data. AA, IC, and AE‑S: drafting 3 −1 1 h at 37 °C. Limit of detection is < 10 PFU mL the work and revising it critically for important intellectual content. All authors read and approved the final manuscript. Funding −1 This research was supported by Zewail City of Science and Technology and losses of 0.95–1.3 log PFU mL after 1 h of incuba- the Science and Technology Development Fund (STDF), Grant Number 25543. tion at 37 °C at pH 2 compared to non-encapsulated This work was supported by the Biotechnology and Biological Sciences phage that were extremely sensitive to acidic conditions Research Council [Grant Number BB/GCRF‑IAA/15]. at pH 2. Although limited, the phage titer reductions Availability of data and materials observed suggest that the chitosan–alginate capsule All data are available. does not prevent acid diffusion to the core of the cap - Ethics approval and consent to participate sule, a process that will contribute to exposure time Not applicable. dependent phage release in simulated intestinal solu- tions. These observations are consistent with those Consent for publication Not applicable. reported previously using phage preparations against Vibrio vulnificus (Koo et al. 2000). The incorporation Competing interests of honey and gelatin in the matrices of bead prepara- The authors declare that they have no competing interests. tions 1 and 2 increased their ability to protect the Abdelsattar et al. AMB Expr (2019) 9:87 Page 8 of 9 Author details Gbassi GK, Vandamme T, Ennahar S, Marchioni E (2009) Microencapsulation Center for Microbiology and Phage Therapy, Zewail City of Science and Tech‑ of Lactobacillus plantarum spp in an alginate matrix coated with whey nology, October Gardens, 6th of October City, Giza 12578, Egypt. Center proteins. Int J Food Microbiol 129:103–105. https ://doi.org/10.1016/j.ijfoo for X‑Ray and Determination of Structure of Matter, Zewail City of Science dmicr o.2008.11.012 and Technology, October Gardens, 6th of October, Giza 12578, Egypt. 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Published: Jun 17, 2019