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Background/Objective: Nanotechnology is a recent technology, but its application to meat preservation is limited. Materials and Methods: The silver bio-nanoparticle was sythensized from the extract of pawpaw and 1 mM solution of silver nitrate using standard method. Meat samples were treated with solutions containing 10%–20% silver bio-nanoparticle suspension and were kept for 2, 4 and 6 h. Protein, crude fat, ash, weight loss, water loss, solid gain, absorbed silver ion, bacterial count and sensory characteristics were determined using standard methods. Results: The protein, crude fat, ash, weight loss, water loss, solid gain, absorbed silver ion and total plate count varied from 21.63%–30.89%, 3.71%–4.21%, 1.55%–3.98%, 0.04 to 0.25 g, 0.42–0.84, 5 11 0.38–0.62, 18.00–48.42 µg/mL and 2.74 × 10 –1.39 × 10 cfu/g respectively. The results showed that qualities of meat were positively affected by silver bionanoparticle treatment. Conclusion: Meat treated with10% of silver bio-nanoparticle concentration for 4 h had the best quality. Key words: bio-nanoparticle; technological properties; chemical properties; sensory properties. Nanotechnology is an inter-disciplinary science that connects Introduction knowledge of biology, chemistry, physics, engineering, and material Meat is a good source of protein, fat, and minerals, and it also con- science (Islam and Miyazaki, 2009) and deals with the design, pro- tains high percentage of moisture which has a significant impact on its duction, and application of nanoparticles with a size below 100 nm physico-chemical, sensory, and technological properties (Barat et al., (Nowack, 2010). Silver nanoparticles (Ag-NPs or nanosilver) have 2009). Several meat preservation methods have been reported by many attracted increasing interest due to their unique physical, chemical, researchers. Kozempel et al. (2003) reported on preservation of meat and biological properties compared with their macro-scaled counter- using steaming method and concluded that it reduced the meat nutrient parts (Sharma et al., 2009). Ag-NPs exhibit broad-spectrum bacteri- quality, most especially the vitamin B complex which soluble in water. cidal and fungicidal activities (Ahamed et al., 2010), which makes it During low temperature preservation of meat, the freezing and thaw- extremely popular in a diverse range of consumer products, including ing cycles have deleterious effect on meat quality (Kondratowicz et al., plastics, soaps, pastes, food, and textiles (Garc´ıa-Barrasa et al., 2011). 2008). However, the use of chemical preservatives for meat preserva- Ag-NPs can be synthesized using different methods. The physical tion is limited by reduction in its sensory quality (Schirmer et al., 2010). and chemical methods used to synthesize Ag-NPs are expensive and Therefore, there is a need to develop sound science or technologically often raise questions of environmental risk because it involves the use of based preservation methods with the possibility retaining meat quality. toxic and hazardous chemicals (Tripathy et al., 2010). The prospect of © The Author(s) 2018. Published by Oxford University Press on behalf of Zhejiang University Press. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/ by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact email@example.com Downloaded from https://academic.oup.com/fqs/article-abstract/2/3/159/5069533 by Ed 'DeepDyve' Gillespie user on 28 August 2018 160 S. W. Oluwatofarati et al., 2018, Vol. 2, No. 3 exploiting natural resources for metal nanoparticle synthesis has become an environmentally benign approach (Bhattacharya et al., 2005). The synthesis of Ag-NPs, by reducing the silver ions present in the solution of silver nitrate in aqueous extract of papaya fruit, was reported by Maqdoom et al., (2013) and discovered that the biologically synthesized nanoparticles were found to be highly toxic against different multi-drug- resistant human pathogens. This suggests that biologically synthesized nanoparticles can also be used for food preservation. Therefore, applying bio-nanoparticles synthesized from an antimicrobial silver nitrate and a meat tenderizer papain extract for meat treatment might have a positive effect on the quality of treated meat. The aim of this research is to inves- tigate the preservative potential of silver bio-nanoparticles from papaya fruit extract and silver nitrate solution. Materials and Methods Materials Raw materials and sample preparation Figure 1 Flow chart for the production of bio-nanoparticle-treated meat. The cow meat was purchased at Bodija Market in Ibadan, Nigeria. The meat was cut into dimensions of 3 × 3 × 2 cm using a sharp stainless steel knife. The preparation of extract and synthesis of silver Determination of technological properties bio-nanoparticles were done according to the method of Maqdoom Percentage weight reduction et al. (2013) described below. Five grams of each sample was weighed and immersed in a bio-nan- oparticles solution. The weight observed was recorded before and Preparation of extract after treatment. The weight reduction (WR) was determined accord- Unripe papaya fruits of 25 g in weight were thoroughly washed ing to the following equation (AOAC, 2005): in distilled water, drained, and cut into pieces, and the pieces were ground into slurry using a blender. The slurry was then poured into ww − 100 100 ml sterile distilled water and filtered through Whatman No. %, WR = x w 1 1 filter paper (pore size 11 μm). The filtrate was further filtered through 6 μm-sized filters, and the free biomass residue that was not the capping ligand of the nanoparticles was removed from the solu- where w is the initial sample weight (g) and w is the sample weight tion obtained and centrifuged at 5000 rpm for 10 min. The result- after osmotic dehydration (g). ing suspension was dispersed into 10 ml sterile distilled water. The centrifugation and dispersion processes were repeated three times Percentage solid gained (Maqdoom et al., 2013). Five grams of fresh and bio-nanoparticle-treated samples were placed in an oven already set at 100°C to dry to constant weight Synthesis of silver bio-nanoparticles for 8 h. The change in weight observed was recorded. The One millimolar (1 mM) of aqueous solution of silver nitrate (AgNO ) solid gained (SG) was determined from the following equation was prepared and used for the synthesis of Ag-NPs. Papaya fruit (AOAC, 2005): extract (10 ml) was added into 90 ml of aqueous solution of 1 mM silver nitrate for reduction into Ag ions and the mixture was kept at uu − room temperature for 24 h (Maqdoom et al., 2013). %, SG = x w 1 Methods where u is the initial solid content in the fresh sample (g) and u is the The pure silver bio-nanoparticle suspension produced was measured solid content in the sample after osmotic dehydration (g). into 10, 15, and 20 ml and made up to 100 ml by adding sterile distilled water in order to achieve 10, 15, and 20 per cent concentra- tions, respectively. The meat sample was immersed into each solu- Determination of absorbed silver ion in bio- tion and left without agitation for a period of 2, 4, and 6 h for each nanoparticle-treated meat: wet oxidation of the sample (Figure 1). sample Five grams (5 g) of the samples were weighed into digestion Determination of UV-vis spectra of the prepared flask, and 10 ml of 2:1 by volume of nitric/perchloric acid silver bio-nanoparticles solution was added to the sample and digested until dense white fumes appeared. The digest was allowed to cool and some quantity The reduction of pure Ag+ ions was monitored by measuring the of distilled water was added to the digest. The solution was UV-vis spectrum of the reaction medium. UV-vis spectral analysis then filtered into 50 ml volumetric flask and diluted to volume was done using a double-beam UV-vis spectrophotometer (AOAC, (Hossner, 1996). 2005). Downloaded from https://academic.oup.com/fqs/article-abstract/2/3/159/5069533 by Ed 'DeepDyve' Gillespie user on 28 August 2018 Silver bio-nanoparticle treatment effects, 2018, Vol. 2, No. 3 161 Ag analysis using the atomic absorption spectrophotometer Nanosilver was analysed using model 210VGP of the Buck Scientific Atomic Absorption Spectrometer series with air-acetylene gas mix- ture as oxidant. Extract from the digestion were aspirated and the equipment calibrated for silver (Ag). The results were recorded as mg −1 −1 l of solution and calculated as mg kg of sample (Hossner, 1996). Calculation −1 mgkg =− digest concxdilution factor, digest −= conc analytereading on ASS, volo . fdigestx aliquot dilution factor = . weight of thesamplee Determination of wet preservation effect of silver bio-nanoparticle-treated meat The wet preservative effect of silver bio-nanoparticles was determined using the method of Hossner (1996). Each treated sample was wrapped in polythene nylon and stored without refrigeration for 7 days. The microbial quality was determined for day one, three, and seven by con- ducting an aerobic mesophilic plate count test on the samples. Total plate count Figure 2 UV-vis absorption spectrum of silver nanoparticles synthesized. The total plate count for microbial enumeration was determined using standard procedure established by Prescott (2005). reaction media had absorbance peak at 430 nm, and broadening of Determination of chemical composition peak indicated that the particles were polydispersed. The protein, ash, and crude fat contents of the meat samples were The size of Ag-NPs is very important because it is connected with evaluated using the standard AOAC (2005) procedure. their antimicrobial properties as reported by Fernandez et al. (2009). However, when their size increases, the activity of silver nanaoparti- cles decreases (Nabikhan et al., 2010). The particle sizes were below Sensory evaluation 100 nm and their optimum wavelength under UV spectrophotom- Cooking was carried out on the samples at 80°C for 50 min in a water eter was at 430 nm (Figure 2). The particle sizes obtained fell within bath. Each sample was properly wrapped and labelled before cooking. the range reported by Fernandez et al. (2009). After the cooking process, the samples were provided to the judges. Twenty trained panelists were selected from the staff and students of the Technological properties of silver bio-nanoparticle- University of Ibadan, Ibadan, Nigeria. The panelists evaluated the char- treated meat acteristics of bio-nanoparticle-treated meat for aroma, texture, taste, juiciness, and overall acceptability, using a 9-point Hedonic scale where The effects of the bio-nanoparticles solution on technological prop- 1 and 9 represent dislike extremely and like extremely, respectively. erties (water reduction, solid gained, and water loss) of the samples were presented in Tables 1–3, respectively. All parameters measured showed significant difference (P < 0.05) except for solid gained with Statistical analysis concentration contact period of 4 h. The highest weight reduction Data obtained were analysed using SPSS (Version 17.0, 2002) statis- was 0.25 g at a contact period of 6 h in 20 per cent concentration, tical package. Data analysed with SPSS were subjected to analysis of whereas the lowest was 0.04 g at a contact period of 2 h in 10 per variance (ANOVA) and their means were separated with Duncan’s cent concentration. The highest solid gained was 0.62 g at a contact Multiple Range Test (DMRT) according to Larmond (1977) with a period of 6 h in 20 per cent concentration, whereas the lowest was statistical significance number of P < 0.05. 0.38 g at a contact period of 2 h in 10 per cent concentration. The highest water loss was 0.84 g at a contact period 6 h in 20 per cent concentration, whereas the lowest was 0.42 g at a contact period Results and Discussion of 2 h in 10 per cent concentration. The effect could be related to UV-vis spectra analysis of silver bio-nanoparticles pH and the salt concentration. The pH value of 5 could result in solution weight loss, which was probably due to swelling that occurs in the Figure 2 shows the UV-vis spectra recorded from the reaction myofibrillar proteins and connective tissue (Barat et al., 2009). The medium after 24 h. Absorption spectra of Ag-NPs formed in the technological properties increased with increase in concentration Downloaded from https://academic.oup.com/fqs/article-abstract/2/3/159/5069533 by Ed 'DeepDyve' Gillespie user on 28 August 2018 162 S. W. Oluwatofarati et al., 2018, Vol. 2, No. 3 Table 1. Weight reduction (wr) Table 4. Silver ion (Ag) concentration in samples of bio-nanoparti- cle-treated meat (μg/ml) Time (h) Concentration Time (h) Concentration 10 15 20 10% 15% 20% wr (g) wr (g) wr (g) e d d 2 18.00 ± 1.15 21.06 ± 0.58 21.89 ± 0.58 g f e b b b 2 0.04 ± 0.00 0.07 ± 0.00 0.10 ± 0.01 4 36.84 ± 0.58 36.78 ± 0.58 39.41 ± 1.15 d b b c b a 4 0.16 ± 0.01 0.21 ± 0.00 0.22 ± 0.00 6 25.94 ± 0.58 39.86 ± 1.15 48.42 ± 1.73 d c a 6 0.15 ± 0.01 0.19 ± 0.01 0.25 ± 0.00 Mean values having different superscripts are significantly different Mean values having different superscripts are significantly different (P < 0.05). (P < 0.05). Table 2. Solid gained (g) Table 5. Wet preservation effect for 10 per cent concentration (cfu/g) Time (h) Concentration No. of days 0 3 7 10% 15% 20% Immersion time (h) Microbial count c b b 2 0.38 ± 0.02 0.51 ± 0.02 0.55 ± 0.02 5 9 11 b b b 0 3.77 × 10 9.54 × 10 1.39 × 10 4 0.51 ± 0.01 0.50 ± 0.01 0.50 ± 0.01 5 8 9 c b a 2 3.55 × 10 2.70 × 10 7.44 × 10 6 0.42 ± 0.02 0.52 ± 0.01 0.62 ± 0.02 5 7 8 4 2.86 × 10 1.72 × 10 4.54 × 10 5 7 9 6 3.02 × 10 9.89 × 10 1.12 × 10 Mean values having different superscripts are significantly different (P < 0.05). Table 3. Water loss (g) Table 6. Wet preservation effect for 15 per cent concentration (cfu/g) Time (h) Concentration No. of days 0 3 7 10% 15% 20% Immersion time (h) Microbial count e d c 2 0.42 ± 0.01 0.58 ± 0.02 0.65 ± 0.02 5 9 11 0 3.77 × 10 9.54 × 10 1.39 × 10 bc ab b 4 0.67 ± 0.01 0.72 ± 0.02 0.75 ± 0.02 5 8 9 2 3.42 × 10 2.56 × 10 6.52 × 10 d ab a 6 0.58 ± 0.02 0.71 ± 0.01 0.84 ± 0.02 5 7 8 4 2.91 × 10 1.68 × 10 4.25 × 10 5 7 8 6 2.74 × 10 1.43 × 10 3.19 × 10 Mean values having different superscripts are significantly different (P < 0.05). and residence time. This could be related to the effect of mass trans- of bio-nanoparticles wet preservation of meat increased with fer which is affected by pH of sample and behaviour of salt during increase in concentration. The total plate count value of 7 × 10 −1 the osmotic process. According to Koprivca et al. (2010), mass trans- cfu·g was considered as an upper microbiological limit for fer is caused by a difference in osmotic pressure, water outflow from good fresh meat quality, as defined by Dainty et al. (1992). product to solution, solute transfer from solution into the product, Therefore, all meat samples stored beyond a day without treat- and leaching out of the products own solutes. ment were found unsafe for consumption due to heavy micro- bial load. However, samples with a contact period of 6 h in 15 and 20 per cent concentrations had the least microbial popula- Silver ion concentration of bio-nanoparticle- tions, and extension of the retention time at a contact period of treated meat 6 h beyond 6 days resulted in an increase in microbial popula- The result of concentration of silver ion absorbed is shown in tion. This might be due to reduction in the efficacy of the bio- Table 4. The concentration measured showed significant difference nanoparticles over time. This implies that microbial growth (P < 0.05) for every sample except for sample with a contact period inhibition in the samples was dependent on concentration and of 4 h. The result obtained was within the range of most reported retention time. Similar findings were observed by Shrivastava toxicology and microbial inhibition concentration of 1–100 µg/ml et al. (2007) who discovered that Ag-NPs antimicrobial activi- (Morones et al., 2005). However, the size used in this study is small ties were influenced by the dosage applied. compared with most in the literature and is expected to be of high- dose range. In Table 4, the maximum value recorded was 48.42 µg/ ml for a contact period of 6 h in 20 per cent concentration, whereas Chemical composition of silver bio-nanoparticle- the lowest value recorded was 18.00 µg/ml for a contact period of treated meat 2 h immersion at 10 per cent concentration. The effects of the bio-nanoparticles solution on chemical compo- sitions (protein, fat, and ash) of the samples were studied and the Effect of treatment on microorganisms results are presented in Table 8. The concentration of the silver bio- The results are shown in Table 5–7 for 10, 15, and 20 per nanoparticles significantly influenced the protein, fat, and ash con- cent concentrations. The result showed that the effectiveness tents of the meat samples (P < 0.05). Downloaded from https://academic.oup.com/fqs/article-abstract/2/3/159/5069533 by Ed 'DeepDyve' Gillespie user on 28 August 2018 Silver bio-nanoparticle treatment effects, 2018, Vol. 2, No. 3 163 The protein, fat, and ash contents of the samples ranged from (TVB), trimethyl amine (TMA) hydrogen sulphide, and ammonia. 21.63 to 37.19 per cent, 3.71 to 5.00 per cent, and 1.55 to 3.98 Also, it might be due to a decrease in salt-soluble and water-soluble per cent, respectively. The protein and fat content decreased as the proteins (Chomnawang et al., 2007) or to autolytic deterioration concentration of the silver bio-nanoparticles increased. Limited associated with the actions of endogenous enzymes and bacteria reduction in protein and fat contents (30.88% and 4.21%, respect- (Hultman and Rustard, 2004). Fats play protective roles in the body ively) was observed from the sample treated with 10 ml concentra- system (Olusanya, 2008) and some important fatty acids such as tion of silver bio-nanoparticles for 2 h. Protein denaturation can be omega-3-fatty acid, etc., that are derived from fats played significant explained as the changes in the protein structures due to the disrup- roles in the proper functioning of body system (Obidoa et al., 2010). tion of chemical bonds and by secondary interactions with other The reduction in fat content indicates an increase in lipid oxida- constituents (Alizadeh, 2009). The reduction in crude protein of the tion. The reduction in the fat contents of the silver bio-nanoparticle- meat samples during treatment with solutions containing silver bio- treated samples could be due to the release of oxidative enzymes and nanoparticles could be attributed to the gradual degradation of the prooxidants from various rupture cellular organelles (Boonsumrej initial crude protein to more volatile products as total volatile bases et al., 2007). Ash content is an index of mineral contents in biota (Akubugwo et al., 2007). The ash contents of the samples increased as the Table 7. Wet preservation effect for 20 per cent concentration (cfu/g) concentration of the silver bio-nanoparticles increased (Table 8). Reductions in other chemical components (protein and fat) might No. of days 0 3 7 result into corresponding increase in ash contents due to the concen- Immersion time (h) Microbial count tration of soluble solids with relatively chemically stable products. 5 9 11 0 3.77 × 10 9.54 × 10 1.39 × 10 5 8 9 2 3.42 × 10 2.54 × 10 6.48 × 10 5 7 8 Sensory evaluation 4 2.77 × 10 1.55 × 10 4.32 × 10 5 7 8 6 2.58 × 10 1.36 × 10 3.02 × 10 The result of the sensory evaluation as displayed in Table 9 indicated the concentration of solutions (10%, 15%, and 20%) and time of immersion (2, 4, and 6 h) of meat samples. All parameters meas- ured showed significant differences (P < 0.05). The highest value for Table 8. Chemical composition of silver bio-nanoparticle-treated aroma (8.10) was recorded for samples treated with 20 per cent con- meat (%) centration for a period of 6 h, whereas the lowest value (5.90) was Time (h) Concentration recorded for samples treated with 20 per cent concentration for a period of 2 h. Considering the texture of the treated meat samples, 10% 15% 20% samples treated with 15 per cent concentration for a period of 2 h had the highest value of 8.15, whereas samples treated with 15 per Protein content a ab ab 2 30.89 ± 1.73 29.88 ± 1.15 29.25 ± 1.73 cent concentration for a period of 6 h had the lowest value of 3.95. bc cd bc 4 26.85 ± 0.58 25.63 ± 1.15 26.44 ± 1.15 For taste, samples treated with 10 and 15 per cent concentrations for ab de e 6 28.44 ± 1.15 22.25 ± 1.15 21.63 ± 0.58 2 h had the highest value of 8.25, whereas samples treated with 15 Fat content per cent for 6 h had the lowest value of 5.95. For juiciness, samples a ab b 2 4.21 ± 0.035 4.13 ± 0.023 4.11 ± 0.035 treated with 10 per cent concentration for a period of 2 h had the d d de 4 3.88 ± 0.046 3.88 ± 0.023 3.86 ± 0.023 highest value of 8.15, whereas samples treated with 15 per cent for c ef f 6 4.02 ± 0.029 3.78 ± 0.012 3.71 ± 0.029 6 h had the lowest value of 3.95, respectively. The value for colour Ash content showed that samples treated with 15 per cent concentration for 6 h d cd c 2 1.55 ± 0.06 1.76 ± 0.12 1.87 ± 0.17 b b b had the highest value of 8.10, whereas samples treated with 15 per 4 3.19 ± 0.11 3.22 ± 0.06 3.26 ± 0.03 c a a cent concentration for 2 h had the lowest value of 3.90, respectively. 6 1.90 ± 0.06 3.90 ± 0.06 3.98 ± 0.05 However, samples in 10 per cent concentration and with 4 h immer- sion time had all their sensory attribute scores above 5, giving this Mean values having different superscripts are significantly different (P < 0.05). time as the optimum immersion time. Table 9. Sensory evaluation of bio-nanoparticle osmotic–treated meat Parameters Aroma Texture Taste Juiciness Colour Overall acceptability d b a a d a s102 6.10 ± 0.06 7.9 ± 0.06 8.25 ± 0.06 8.13 ± 0.07 4.25 ± 0.06 7.16 ± 0.10 d a b b e a s152 6.06 ± 0.14 8.15 ± 0.06 7.96 ± 0.06 7.95 ± 0.06 3.90 ± 0.06 7.10 ± 0.06 d ab b de ef a s202 5.92 ± 0.07 7.97 ± 0.07 7.93 ± 0.06 6.92 ± 0.07 3.97 ± 0.07 7.37 ± 0.23 b d c c b a s104 7.20 ± 0.06 6.95 ± 0.06 7.11 ± 0.11 7.10 ± 0.06 6.10 ± 0.06 6.94 ± 0.07 b d c e b a s154 7.15 ± 0.06 6.9 ± 0.06 7.15 ± 0.06 6.90 ± 0.06 6.11 ± 0.06 6.90 ± 0.06 c c c de c a s204 6.79 ± 0.13 7.26 ± 0.08 6.94 ± 0.11 6.98 ± 0.60 5.75 ± 0.22 6.91 ± 0.06 a e d f a b s106 7.90 ± 0.06 4.25 ± 0.06 6.00 ± 0.06 4.10 ± 0.06 7.97 ± 0.06 5.49 ± 0.61 a f d f a b s156 7.96 ± 0.06 3.96 ± 0.06 5.95 ± 0.61 3.95 ± 0.06 8.10 ± 0.06 5.91 ± 0.06 a ef d f a b s206 8.10 ± 0.06 4.06 ± 0.11 6.05 ± 0.06 3.95 ± 0.06 7.97 ± 0.06 5.94 ± 0.06 Mean values having different superscripts within a column are significantly different (P < 0.05). Downloaded from https://academic.oup.com/fqs/article-abstract/2/3/159/5069533 by Ed 'DeepDyve' Gillespie user on 28 August 2018 164 S. W. Oluwatofarati et al., 2018, Vol. 2, No. 3 Fernandez, A., et al. (2009). Preservation of aseptic conditions in absorbent pads Conclusions by using silver nanotechnology. Food Research International, 42: 1105–1112. The result of the study showed that qualities of meat were posi- Garcı´a-Barrasa, J., Lo´pez-de-Luzuriaga, J. M., Monge, M. (2011). Silver nano- tively affected by silver bio-nanoparticle treatment. The silver particles: synthesis through chemical methods in solution and biomedical concentration of 10 per cent, 4 h immersion having absorption of applications. Central European Journal of Chemistry, 9: 7–19. 36.84 µg/ml could be said to be the optimum condition for the Hossner, L. R. (1996). ‘Dissolution for total elemental analysis’, In: D. L. Sparks et al. (eds.) Methods of Soil Analysis, Part 3, Chemical Methods, bio-nanoparticle treatment in terms of quality parameters consid- SSSA Book Series No. 5, ASA and SSSA, Madison, WI, USA. pp. 49–64. ered. The sensory evaluation was within the highest range (7) of Hultman, L., Rustard, T. (2004). Iced storage of Atlantic salmon (Salmo salar) the overall acceptability in the degree of preference which indi- effects on endogenous enzymes and their impact on muscle proteins and cated ‘like moderately’. The microbial count was within the lowest texture. Food Chemistry, 87: 31–34. colony obtained (10 ) after 7 days. The chemical composition (pro- Islam, N., K. Miyazaki (2009). Nanotechnnology innovation system: under- tein 29%, fat 3.88%, and ash 3.19%) and technological proper- standing hidden dynamics of nanoscience fusion trajectories. 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Food Quality and Safety – Oxford University Press
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