Bioactivities of Honeys from Bees Fed on Different Plants
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摘要:
目的 特种蜂蜜具有较强的抗氧化能力和抗菌活性，并拥有来自于植物的药用特性，其开发利用具有巨大的潜力与价值。本研究旨在对中国境内的多种特种蜂蜜进行比对分析，以期找到具有优异生物活性的样本，为蜂蜜在医学和保健领域的应用提供科学依据。 方法 检测分析33种不同植物来源的特种蜂蜜的理化指标和生物活性，通过自由基清除法和总抗氧化能力检测法对蜂蜜抗氧化活性进行评价，并使用琼脂扩散法和微量肉汤稀释法检测样品的抗菌活性。 结果 所有蜂蜜样品的理化指标均符合国家标准规定；在33种蜂蜜中，米团蜜具有最强的抗氧化活性，板栗蜜、藿香蜜也表现良好。对金黄色葡萄球菌和大肠杆菌抗菌能力最强的分别为茴香蜜和枸杞蜜。此外，蜂蜜的抗氧化能力与总酚含量呈显著正相关，与抗菌能力的相关性不显著。 结论 米团、茴香、藿香蜂蜜等是具有优良生物活性的特种蜂蜜，它们具有进一步开发利用的潜力和价值。本研究结果可为当前蜂蜜消费市场等级评定提供依据。 Abstract:Objective Specialized honeys exhibit strong antioxidant capabilities, antibacterial activities, and medicinal properties derived from plants, presenting significant potential and value for development and utilization. This study aims to conduct a comparative analysis of various specialized honeys within China, with the goal of identifying samples with outstanding biological activities. Ultimately, the research endeavors to provide a scientific basis for the medical and healthcare applications of honey. Method Thirty-three honey samples from different regions in China were collected for physicochemical and biological activity analyses. Antioxidant activity was evaluated using the free radical scavenging and total antioxidant capacity tests, and antibacterial capacity assessed by means of agar diffusion and microdilution in broth. Result All tested honeys met the national standards on physicochemical properties. Of the 33 specimens, the leucosceptrum honey exhibited the strongest antioxidative activity, the chestnut and agastache honeys performed well, while the fennel honey showed the highest antibacterial effect on Staphylococcus aureus and the Goji honey on Escherichia coli. The antioxidative, but not the antibacterial, capacity of the honeys significantly correlated with the total phenolic content in it. Conclusion Not all sweet-tasting honeys are created equal. The nutritional, antioxidant, and antibacterial functions of some samples tested in this study stood out with special marketing and product development potentials. The evaluation protocol presented in this article might be useful in further investigations that might lead to extended utilization of the common food ingredient. -
Key words:
- specialty honey /
- oxidative stress /
- antimicrobial activity /
- antioxidative capacity
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表 1 蜂蜜样品信息
Table 1. Information on honey samples
样品名称
Sample name植物来源
Plant origin地理来源
Geographical origin采样时间
Sampling time板栗蜜 板栗 Castanea mollissima Blume 浙江 2022年 柽柳蜜 柽柳 Tamarix chinensis Lour . 西藏 2020年 鹅掌柴蜜 鹅掌柴 Schefflera octophylla (Linn.) Frodin 湖北 2021年 枸杞蜜 枸杞 Lycium chinense Miller 西藏 2020年 红柳蜜 多枝柽柳 Tamarix ramosissima Ledeb. 新疆 2018年 黄芪蜜 黄芪 Astragalus membranaceus (Fisch.) Bunge 甘肃 2020年 黄芩蜜 黄芩 Scutellaria baicalensis Georgi 甘肃 2020年 茴香蜜 茴香 Foeniculum vulgare Mill. 甘肃 2020年 火炭母蜜 火炭母 Persicaria chinensis (L.) H. Gross 重庆 2021年 藿香蜜 藿香 Agastache rugosa (Fisch. & C. A. Mey.) Kuntze 重庆 2021年 九龙藤蜜 龙须藤 Phanera championii Benth. 广西 2021年 桔梗蜜 桔梗 Platycodon grandiflorus (Jacq.) A. DC. 安徽 2020年 咖啡蜜 咖啡树 Coffea arabica 云南 2021年 柯树蜜 柯树 Lithocarpus glaber (Thunb.) Nakai 浙江 2021年 苦丁茶蜜 大叶冬青 Ilex latifolia Thunb. 浙江 2021年 狼牙刺蜜 白刺花 Sophora davidii Kom. ex Pavol. 西藏 2021年 罗布麻蜜 罗布麻 Apocynum venetum L. 新疆 2020年 米团蜜 米团花 Leucosceptrum canum Sm. 云南 2021年 木通蜜 木通 Akebia quinata (Houtt.) Decne. 重庆 2021年 枇杷蜜 枇杷 Eriobotrya japonica (Thunb.) Lindl. 浙江 2021年 苹果蜜 苹果 Malus pumila Mill. 甘肃 2020年 蒲公英蜜 蒲公英 Taraxacum mongolicum Hand.-Mazz. 新疆 2019年 沙枣蜜 沙枣 Elaeagnus angustifolia L. 新疆 2020年 苕子蜜 苕子Vicia dasycarpa Ten. 云南 2021年 石榴蜜 石榴 Punica granatum L. 安徽 2020年 五倍子蜜 盐肤木 Rhus chinensis Mill. 重庆 2021年 夏枯草蜜 夏枯草 Prunella vulgaris L. 河南 2019年 玄参蜜 玄参 Scrophularia ningpoensis Hemsl. 重庆 2021年 薰衣草蜜 薰衣草 Lavandula angustifolia Mill. 新疆 2020年 野桂花蜜 野桂花 Osmanthus yunnanensis (Franch.) P. S. Green 江西 2021年 野黄柏蜜 川黄檗 Phellodendron chinense Schneid. 重庆 2019年 益母草蜜 益母草 Leonurus japonicus Houtt. 云南 2019年 益智花蜜 益智 Alpinia oxyphylla Miq. 广东 2019年 
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表 2 不同特种蜂蜜样品理化参数
Table 2. Physicochemical parameters of honey
样品
Sample水分
Hydration/%色度值
Chrominance value/
mm果葡比
Fructoglucose
ratio5-羟甲基糠醛
5-hydroxymethylfurfural/
(mg·kg−1)淀粉酶值
Amylase value/
(mL·g−1·h−1)电导率
Conductivity/
(μs·cm−1)板栗蜜 16.97±0.09 150.00±0.77 1.00±0.00 16.86±0.08 4.13±0.68 676.00±9.64 柽柳蜜 20.95±0.18 38.00±0.00 1.15±0.02 0.63±0.03 40.00±2.01 647.30±5.42 鹅掌柴蜜 20.63±0.10 23.00±0.00 1.02±0.00 0.33±0.03 10.00±0.79 207.60±4.17 枸杞蜜 18.41±0.08 22.00±0.00 1.17±0.00 0.38±0.01 30.00±1.47 284.00±2.35 红柳蜜 17.62±0.18 42.00±0.00 1.05±0.00 11.42±0.05 6.67±0.06 1067.00 ±5.50黄芪蜜 18.41±0.18 25.00±0.00 1.10±0.01 0.44±0.05 42.86±1.51 323.20±2.49 黄芩蜜 19.19±0.03 22.00±0.00 1.13±0.00 0.51±0.03 33.33±1.17 278.10±0.77 茴香蜜 19.11±0.08 88.00±0.00 1.57±0.00 0.94±0.03 50.00±2.01 587.30±0.35 火炭母蜜 23.96±0.04 71.00±1.41 1.18±0.00 0.92±0.04 30.00±1.69 587.40±1.37 藿香蜜 20.28±0.11 67.00±1.41 1.44±0.01 4.10±0.16 37.5±0.85 374.00±0.28 九龙藤蜜 21.41±0.06 64.00±1.15 1.68±0.01 13.36±0.03 6.98±0.61 402.00±0.21 桔梗蜜 23.89±0.28 31.00±0.00 1.14±0.04 1.51±0.03 17.65±1.36 336.10±4.11 咖啡蜜 15.98±0.16 28.00±0.00 1.12±0.00 5.42±0.01 11.11±0.08 225.80±1.58 柯树蜜 21.14±0.01 75.00±2.83 1.23±0.00 1.23±0.01 8.57±0.94 940.00±3.82 苦丁茶蜜 19.11±0.08 83.00±1.41 1.58±0.01 8.71±0.03 6.32±0.22 758.80±3.28 狼牙刺蜜 17.23±0.15 4.00±0.00 1.13±0.01 0.60±0.04 33.33±1.87 141.20±1.14 罗布麻蜜 20.75±0.12 38.00±0.00 0.96±0.00 5.23±0.01 20.00±0.50 865.60±5.57 米团蜜 19.15±0.00 150.00±2.08 1.27±0.02 2.68±0.02 16.60±2.16 1722.00 ±6.49木通蜜 19.34±0.31 32.00±0.00 1.00±0.01 0.34±0.03 9.52±1.40 219.00±1.38 枇杷蜜 22.27±0.36 19.00±0.00 1.12±0.01 0.48±0.04 9.38±0.64 237.80±4.42 苹果蜜 18.08±0.22 72.00±0.00 1.08±0.00 0.69±0.01 23.08±0.93 252.90±2.21 蒲公英蜜 16.65±0.17 34.00±1.73 1.17±0.00 1.05±0.01 14.29±0.12 314.40±0.86 沙枣蜜 21.06±0.09 37.00±0.00 1.04±0.00 2.03±0.03 25.00±1.32 320.30±2.71 苕子蜜 19.34±0.28 11.00±0.00 1.10±0.01 2.80±0.05 23.00±2.19 179.40±0.42 石榴蜜 22.04±0.04 20.00±0.00 1.24±0.00 0.40±0.01 30.00±1.34 245.40±3.49 五倍子蜜 23.73±0.03 41.00±0.00 0.92±0.01 0.84±0.03 4.76±0.03 315.60±2.46 夏枯草蜜 23.91±0.04 48.00±0.71 1.58±0.00 1.51±0.03 25.00±1.05 269.80±1.78 玄参蜜 20.67±0.01 79.00±0.00 1.19±0.00 0.70±0.03 9.09±0.45 487.70±0.28 薰衣草蜜 17.62±0.06 9.00±0.00 1.14±0.01 1.68±0.01 23.08±2.01 153.70±0.87 野桂花蜜 21.41±0.18 31.00±0.00 1.13±0.00 0.53±0.03 8.57±0.11 302.80±0.42 野黄柏蜜 19.97±0.07 30.00±0.00 0.99±0.00 2.39±0.02 4.23±0.48 299.40±3.16 益母草蜜 17.55±0.11 75.00±2.65 1.10±0.00 1.26±0.03 60.00±2.31 826.10±4.64 益智花蜜 19.11±0.05 70.00±0.71 1.10±0.01 6.18±0.02 8.57±1.04 503.20±2.21
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表 3 蜂蜜样品的抗氧化活性
Table 3. Antioxidative activities of honeys
样品名称
Sample name总酚含量
Total phenolic content/
(µg·g−1)总抗氧化能力（FRAP法）
Total antioxidant capacity/
(mmol·g−1)DPPH自由基清除能力
DPPH radical scavenging capacity/
(mmol·kg−1)板栗蜜 1050.16 ±213.67ab7.53±1.42a 2.73±0.95b 柽柳蜜 357.84±131.10fghi 1.69±0.66a 0.67±0.05ef 鹅掌柴蜜 323.94±25.32hi 7.65±0.42fg 0.26±0.04ef 枸杞蜜 183.16±8.23fghi 0.94±0.33cdefg 0.27±0.04def 红柳蜜 315.08±47.77fghi 1.65±0.30cdefg 1.61±0.15c 黄芪蜜 287.13±78.18ghi 1.18±0.35efg 0.30±0.02ef 黄芩蜜 275.58±91.77ghi 0.88±0.32fg 0.27±0.02ef 茴香蜜 982.35±231.54bc 3.03±0.68cde 1.08±0.06cd 火炭母蜜 327.85±62.54fghi 1.47±0.26defg 0.53±0.08def 藿香蜜 676.83±170.85cde 3.37±0.91bcd 0.69±0.33def 九龙藤蜜 406.29±18.48efghi 1.98±0.71cdefg 0.69±0.06def 桔梗蜜 353.32±34.21fghi 0.94±0.32fg 0.28±0.02ef 咖啡蜜 722.86±134.11cd 0.83±0.21fg 0.33±0.05ef 柯树蜜 413.71±24.46efghi 2.27±0.72cdefg 0.70±0.04def 苦丁茶蜜 616.91±22.68def 2.35±0.17cdefg 0.86±0.04de 狼牙刺蜜 125.07±11.39i 0.69±0.38fg 0.16±0.03ef 罗布麻蜜 332.50±53.77fghi 2.02±0.41cdefg 1.64±0.19c 米团蜜 1346.09 ±108.60a9.07±1.36a 4.66±0.35a 木通蜜 263.84±21.02ghi 5.06±0.68b 0.23±0.04ef 枇杷蜜 152.58±48.86hi 0.46±0.19g 0.18±0.04ef 苹果蜜 340.77±50.61fghi 1.92±0.16cdefg 0.55±0.06def 蒲公英蜜 242.99±36.30ghi 1.00±0.21fg 0.31±0.05ef 沙枣蜜 256.78±40.65ghi 1.19±0.34efg 0.37±0.09def 苕子蜜 147.26±47.40i 0.63±0.44g 0.19±0.04ef 石榴蜜 234.48±43.94ghi 0.72±0.28fg 0.23±0.03ef 五倍子蜜 164.90±20.37hi 0.82±0.28fg 0.30±0.04ef 夏枯草蜜 519.92±49.41defg 3.55±0.26bc 0.75±0.07def 玄参蜜 294.20±29.87ghi 1.59±0.41cdefg 0.48±0.10def 薰衣草蜜 347.18±82.62fghi 0.58±0.44g 0.12±0.02f 野桂花蜜 252.93±3.70ghi 1.45±0.36defg 0.36±0.06def 野黄柏蜜 255.80±30.11ghi 1.14±0.18efg 0.31±0.03ef 益母草蜜 538.64±45.45defg 2.68±0.44cdef 0.88±0.05de 益智花蜜 457.65±40.73defgh 1.87±0.34cdefg 0.65±0.08def 同列数据后不同小写字母表示在0.01水平差异显著。表5同。
Data with different lowercase letters on same column indicate significant difference at 0.01 level. Same for Table 5.
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表 4 抗氧化指标的相关性分析
Table 4. Correlation between antioxidant indexes
指标
Index总酚含量
Total phenolic contentFRAP总
抗氧化能力
Total antioxidant capacityDPPH自由基
清除能力
DPPH radical scavenging
capacity总酚含量
Total phenolic content1.000 0.695** 0.801** FRAP总抗氧化能力
Total antioxidant capacity0.695** 1.000 0.712** DPPH自由基清除能力
DPPH radical scavenging capacity0.801** 0.712** 1.000 **表示在0.01级别（双尾）相关性显著。表6同。
** indicates significance at 0.01 level (two-tailed). Same for Table 6.
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表 5 蜂蜜样品对微生物的抑菌圈直径（琼脂扩散法）
Table 5. Microbial inhibition zone of honeys (diameters on agar diffusion medium)
样品名称
Sample name抑菌圈直径
Inhibition zone/mm金黄色葡萄球菌
S. aureus大肠杆菌
E. coli阳性对照（10%苯酚） 30.30±1.07a 29.99±0.62a 阴性对照（蒸馏水） — — 柽柳蜜 14.74±0.98fg nd 枸杞蜜 — 11.35±0.43b 黄芪蜜 24.33±1.21bc — 黄芩蜜 20.04±0.59de — 茴香蜜 25.51±1.04b 12.82±0.48b 火炭母蜜 14.47±1.36fg — 藿香蜜 23.74±1.06bcd 12.83±0.97b 九龙藤蜜 12.89±0.44g — 罗布麻蜜 13.66±1.73ef — 苹果蜜 21.06±1.18cde 10.51±0.70b 蒲公英蜜 15.07±1.16fg — 沙枣蜜 14.44±1.27fg — 苕子蜜 19.32±1.13e — 石榴蜜 17.47±2.02ef — 五倍子蜜 14.72±1.11fg — 薰衣草蜜 13.14±1.16g — 野桂花蜜 13.53±0.37fg — 野黄柏蜜 13.44±0.59fg — 益母草蜜 24.69±0.4bc — 益智花蜜 12.82±1.36g — “—”表示未检出＞8 mm的抑菌圈。
"—" indicates absence of inhibition zone larger than 8 mm in diameter.
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表 6 抗菌活性与抗氧化活性之间的相关性
Table 6. Correlation between antibacterial and antioxidative activities of honey
指标
Index对金黄色葡萄球菌
抗菌能力
Antibacterial
activity against
S. aureus对大肠杆菌
抗菌能力
Antibacterial
activity against
E. coli总酚含量
Total phenolic content−0.089 0.213 FRAP总抗氧化能力
Total antioxidant capacity−0.306 0.023 DPPH自由基清除能力
DPPH radical scavenging capacity−0.212 −0.023 对金黄色葡萄球菌的抗菌能力
Antibacterial activity against S. sureus1 0.321 对大肠杆菌的抗菌能力
Antibacterial activity against E. coil0.321 1
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表 7 蜂蜜样品对金黄色葡萄球菌和大肠杆菌的MIC和MBC
Table 7. MIC and MBC ranges of honeys against S. aureus and E. coli
样品名称
Sample
name金黄色葡萄球菌
S. aureus大肠杆菌
E. coli最小抑菌浓度
MIC/%最小杀菌浓度
MBC/%最小抑菌浓度
MIC/%最小杀菌浓度
MBC/%枸杞蜜 — — 6.25～10.00 6.25～10.00 茴香蜜 1.25～2.50 1.25～2.50 6.25～10.00 10.00～12.50 益母草蜜 1.25～2.50 2.50～3.13 — — 藿香蜜 3.13～5.00 2.50～3.13 6.25～10.00 10.00～12.50 苹果蜜 3.13～5.00 3.13～5.00 10.00～12.50 12.50～20.00 黄芪蜜 3.13～5.00 3.13～5.00 柽柳蜜 3.13～5.00 3.13～5.00 — — 苕子蜜 5.00～6.25 5.00～6.25 — — 黄芩蜜 6.25～10.00 6.25～10.00 — — 石榴蜜 6.25～10.00 6.25～10.00 — — 沙枣蜜 6.25～10.00 6.25～10.00 — — 蒲公英蜜 6.25～10.00 10.00～12.50 — 罗布麻蜜 6.25～10.00 12.50～20.00 — — 野桂花蜜 6.25～10.00 12.50～20.00 — — 野黄柏蜜 6.25～10.00 12.50～20.00 — — 五倍子蜜 10.00～12.50 12.50～20.00 — — 薰衣草蜜 12.50～20.00 12.50～20.00 — — 火炭母蜜 12.50～20.00 20.00～25.00 — — 九龙藤蜜 12.50～20.00 25.00～50.00 — — 益智花蜜 12.50～20.00 25.00～50.00 — —
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