A meta-analysis of the effects of gamma irradiation on biochemical and physical characteristics of honey

Gamma irradiation can be used to sterilize honey products. Many previous reports related to biochemical, physical characteristics and antibacterial activity on irradiated honey have not been combined into one quantitative report. Therefore, this study was conducted to determine the effects of gamma irradiation on biochemical and physical characteristics of honey. The source of data in meta-analysis study was conducted on search engines (Scopus®, PubMed®, and Google scholar®), searched with “irradiation”, “gamma”, and “honey” as keywords. Data on gamma irradiation dosage and characteristics of honey were extracted from 12 articles and 44 studies (control vs. irradiated honey). The meta-analysis results showed that gamma irradiation reduced moisture content (p < 0.01). However, gamma irradiation had no effect on viscosity, sugars, total soluble solids, and ash content. It is interesting to note that gamma irradiation significantly increased flavonoid and phenolic compounds (p < 0.01). Gamma irradiation also reduced the level of microorganism in honey (p < 0.01), as reported in total aerobic plate count variable. In summary, except for moisture and vitamin C, gamma irradiation did not influence biochemical characteristics of honey. Gamma irradiation also had no effect on viscosity as physical parameters.


Introduction
Since ancient times, honey has been used as a traditional medicine to treat bacterial infections, colds, coughs, and many infectious conditions [1].Honey has evolved from its origins as a traditional curative cure to a contemporary medicinal treatment worthy of consideration [2].In addition to the source of nectar, climate, and storage period, the conditions of preservation are one of the most important variables influencing the quality of honey [1].Sensory and physicochemical qualities are crucial factors in determining honey's quality and acceptability [3].
During the harvesting and packaging processes, honey is regularly contaminated with many pathogenic bacteria.However, some microorganisms, such as yeast and mold, as well as bacterial spores, have been found in honey [4].To maintain the quality of honey, selecting the appropriate sterilization method is essential.Gamma irradiation, as a sterilization technique, is strongly advised for 1230 (2023) 012053 IOP Publishing doi:10.1088/1755-1315/1230/1/012053 2 the use of honey in medical research.It has been demonstrated that gamma radiation of honey destroys vegetative microbial cells as well as microbial spores without reducing honey's overall antibacterial efficacy [5,6].Previous studies have reported the effects of gamma irradiation on biochemical [7,8], physical [9,10], and antibacterial [5,11] characteristics of honey.However, based on our knowledge, there is no quantitative study that summarizes the results of previous research.Therefore, a metaanalysis study was carried out to assessed the effects of gamma irradiation on biochemical and physical characteristics of honey.
The parameters criteria were (1) biochemical characteristics (pH, moisture, total soluble solids, ash, acidity, sugars, sucrose, vitamin C, phenolic content, and flavonoid content); (2) physical characteristics (viscosity at 25 o C and 35 o C); (3) microorganism activity (total aerobic plate and spore count); and (4) sensory parameters (appearance, aroma, and taste).If any data utilized a different measuring unit, they were translated into the same measurement unit.

Data analysis
A mixed model methodology was used to conduct statistical studies on the data [12,13].Various experiments were treated as random effects, whereas the dosages of gamma irradiation treatment were treated as fixed effects.P-value, root mean square error (RMSE) and the coefficient of determination (R 2 ) were the model statistics used.The statistical analysis was performed using R software version 4.1.2developed by R Core Team 12 [14] and a 'lme4' package version 1.1-28.Statistical significance was declared if p < 0.05.If the p-value ranged between 0.05 -0.10, there was a tendency to be significant.

Results and discussion
The main purpose of gamma irradiation in livestock products is to reduce the contamination of pathogenic microorganisms.However, in several previous studies, irradiation treatment also affected the physical and biochemical properties of honey.Although, some reports stated that only some of the honey's characteristics are affected.Therefore, this meta-analysis study was conducted to present a summary of the quantitative data.Table 2. shows the influence of gamma irradiation on biochemical and physical characteristics of honey.Gamma irradiation did not influence the main of biochemical and physical characteristics of honey (total soluble solids, ash, acidity, sugars, and viscosity).Furthermore, gamma irradiation significantly decreased moisture content (p < 0.01).Gamma treatment also tend to reduced pH value (p = 0.07) and sucrose content (p = 0.051).Since moisture, pH, and total acidity are critical for the freshness and stability of honey against microbial spoilage, especially during storage, these parameters were examined to evaluate the irradiation effect [6].Gamma rays preserve the quality of honey by decreasing the moisture content and, consequently, the fermentation rate [10].This is due to the fact that any yeast cells existing in honey will be able to ferment the sugar due to the high-water content [9].Honey is resistant to fermentation unless the moisture is managed below 17% [20].
The increase of vitamin C after irradiation treatment was observed during present meta-analysis study.Our finding is in agreement with previous studies by Hussein et al. [9] and Khatun et al. [6].With regard to vitamin C content, many researchers found that irradiation is very sensitive to water soluble vitamin in honey [6].However, its sensitivity to a number of variables is similarly considerable (exposure to oxygen, temperature elevation, pH modifications) [21].It is interesting to note that gamma irradiation enhanced phenolic and flavonoid contents (p < 0.01).The release of phenolic components from glycosidic constituents and the breakdown of larger phenolic compounds by gamma rays into smaller phenolic compounds are causing an increase in phenols concentration [10].Radiolysis of phenolics in an aqueous solution resulted in effective hydroxylation degradation [16].Apparently, irradiation treatment could be enhanced honey antioxidant activity.There are strong relationships between polyphenols and honey antioxidant capacity [3].
Apparently, gamma irradiation is an efficient technique for reducing the level of microorganisms, which is represented by the parameters of total aerobic plate count and spore count (p < 0.01).A reduction of microorganism activity due to irradiation treatment is expected since irradiation has the main function of sterilization.From the present study, it seems that, a reduction of total aerobic count was caused by: 1) damage to the bacterial nucleic acid after irradiation; and 2) decrease in moisture content which has a negative impact on the environment of pathogenic bacteria.According to our metaanalysis, the best doses for reducing total aerobic count are 10 and 15 kGy.Similarly, Saxena et al. [8] reported that, at 15 kGy dosage, total microbiological decontamination was performed in all tested honey.Honey treated with gamma radiation has been demonstrated to eradicate both vegetative and spore-forming microorganisms [5].In addition to sterilizing honey, gamma irradiation enhanced its antibacterial properties [11].In our findings, except for moisture and vitamin C, gamma irradiation did not affect biochemical and physical characteristics of honey.Although there is a little effect on pH value and sucrose content, apparently, gamma irradiation did not affect total soluble solids, ash, acidity, and sugar contents.In agreement with our findings, a study from Bera et al. [7] reported that gamma irradiation at a level of 10 kGy did not result in substantial physicochemical changes.However, the lack of changes in biochemical and physical characteristics actually had a positive impact on sensory parameters.This was confirmed by the appearance, aroma and taste values which tended to be similar between control vs irradiated honey.

Conclusion
Gamma irradiation is apparently an effective method to reduce the microorganism activity in honey without affecting physical and some biochemical characteristics.However, gamma irradiation can reduce moisture content.Apart from these properties, gamma irradiation may potentially provide benefits to improving antioxidant activity of honey through increasing phenolic and flavonoid content.

Figure 1 .
Figure 1.Diagram of literature search

Table 1 .
Study included in the meta-analysis of gamma irradiation effects on biochemical and physical characteristics of honey

Table 2 .
Effect of gamma irradiation on biochemical and physical characteristics of honey