Effects of trehalose gel on full-thickness skin defect wounds in rats and scar hyperplasia in rabbit ears
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摘要:
目的 探讨海藻糖凝胶对大鼠全层皮肤缺损创面及兔耳瘢痕增生的影响。 方法 该研究为实验研究。制备海藻糖凝胶和卡波姆凝胶,辐照灭菌后观察其外观并检测其粘度、成模率、阻菌率、重金属含量、保湿率、水蒸气透过率、无菌性等理化特性和细胞毒性、皮内刺激、致敏性等生物相容性。取30只8~10周龄雄性SD大鼠,按照随机数字表法分为实验组、阳性对照组、阴性对照组,每组10只。在阴性对照组、阳性对照组、实验组大鼠背部制备全层皮肤缺损创面模型,分别进行常规换药、卡波姆凝胶换药、海藻糖凝胶换药处理。统计伤后6、12 d创面愈合率并记录创面愈合时间。伤后6 d,采用透射电镜观测大鼠创面组织中自噬体和自噬溶酶体数量,采用酶联免疫吸附测定法检测大鼠创面组织中微管相关蛋白轻链3Ⅰ（LC3Ⅰ）和LC3Ⅱ含量并计算其比值,采用天狼星红-苦味酸染色法检测大鼠创面组织中Ⅰ型胶原蛋白、Ⅲ型胶原蛋白占比及其比值和总胶原蛋白占比。前述实验样本数均为5。取3只3~4个月龄雄性新西兰白化模型兔,在每侧兔耳各制备3个深达软骨膜的创面,同前进行分组和处理,每组6个创面。创面愈合后30 d,大体观察并使用温哥华瘢痕量表评估兔耳瘢痕情况,采用苏木精-伊红染色检测兔耳瘢痕组织中表皮和真皮的厚度,采用天狼星红-苦味酸染色检测兔耳瘢痕组织中Ⅰ型胶原蛋白、Ⅲ型胶原蛋白占比及其比值和总胶原蛋白占比及其排布情况。样本数为6。 结果 辐照后的海藻糖凝胶和卡波姆凝胶均呈淡黄色透明状,无异味和杂质。海藻糖凝胶粘度、成膜率、阻菌率、保湿率均显著优于卡波姆凝胶（t值分别为4.13、3.50、4.03、5.80,P<0.05）,但水蒸气透过率显著低于卡波姆凝胶（t=-4.14,P<0.05）。2种凝胶均未检出重金属和细菌。2种凝胶均无细胞毒性,皮内刺激和致敏性均为阴性。伤后6、12 d,阳性对照组大鼠创面愈合率均明显高于阴性对照组（t值分别为-6.82和-4.58,P<0.05）,实验组大鼠创面愈合率均明显高于阳性对照组（t值分别为-8.90和-4.25,P<0.05）和阴性对照组（t值分别为-8.78和-4.25,P<0.05）。阳性对照组和实验组大鼠创面愈合时间分别为（20.4±2.5）、（23.4±2.5）d,均明显短于阴性对照组的（27.0±2.1）d（t值分别为2.45、-4.49,P<0.05）。伤后6 d,实验组大鼠创面组织中自噬体和自噬溶酶体数量均显著多于阳性对照组（t值分别为7.37和9.33,P<0.05）和阴性对照组（t值分别为-7.06和-8.54,P<0.05）。伤后6 d,阳性对照组大鼠创面组织中LC3Ⅱ含量及LC3Ⅱ/LC3Ⅰ均显著高于阴性对照组（t值分别为-4.48和-2.47,P<0.05）；实验组大鼠创面组织中LC3Ⅱ含量及LC3Ⅱ/LC3Ⅰ均显著高于阴性对照组（t值分别为11.98和6.04,P<0.05）和阳性对照组（t值分别为-6.64和-4.17,P<0.05）,LC3Ⅰ含量明显低于阴性对照组（t=2.33,P<0.05）。伤后6 d,3组大鼠创面组织中总胶原蛋白和Ⅰ型胶原蛋白占比均相近,P>0.05。伤后6 d,阳性对照组大鼠创面组织中Ⅲ型胶原蛋白占比显著高于阴性对照组（t=-3.19,P<0.05）,且Ⅰ型胶原蛋白/Ⅲ型胶原蛋白显著低于阴性对照组（t=2.18,P<0.05）；实验组大鼠创面组织中Ⅲ型胶原蛋白占比显著高于阴性对照组和阳性对照组（t值分别为-2.38和5.91,P<0.05）,且Ⅰ型胶原蛋白/Ⅲ型胶原蛋白显著低于阴性对照组和阳性对照组（t值分别为3.08和-4.35,P<0.05）。创面愈合后30 d,可观察到阳性对照组兔耳瘢痕增生情况与阴性对照组相近,而实验组兔耳瘢痕增生情况明显减轻。创面愈合后30 d,实验组兔耳瘢痕色泽、血管、厚度、硬度评分及总分均明显低于阳性对照组（t值分别为3.80、3.80、2.39、2.71、4.84,P<0.05）和阴性对照组（t值分别为-3.81、-4.78、0.04、-2.71、-5.14,P<0.05）。创面愈合后30 d,实验组、阴性对照组和阳性对照组兔耳瘢痕组织中表皮厚度相近（P>0.05）；阳性对照组兔耳瘢痕组织真皮厚度明显小于阴性对照组（t=5.42,P<0.05）,实验组兔耳瘢痕组织真皮厚度明显小于阴性对照组和阳性对照组（t值分别为11.91和8.49,P<0.05）。创面愈合后30 d,3组兔耳瘢痕组织中胶原蛋白排列均紊乱,总胶原蛋白占比相近（P>0.05）；实验组兔耳瘢痕组织中Ⅰ型胶原蛋白占比明显低于阳性对照组（t值分别为3.00,P<0.05）,Ⅲ型胶原蛋白占比明显高于阴性对照组和阳性对照组（t值分别为-4.46和4.05,P值均<0.05）,Ⅰ型胶原蛋白/Ⅲ型胶原蛋白明显低于阴性对照组和阳性对照组（t值分别为8.50和-5.25,P值均<0.05）。 结论 海藻糖凝胶相较于卡波姆凝胶具有更适于创面愈合的理化特性,且生物相容性良好；能基于自噬激活作用促进大鼠全层皮肤缺损创面愈合,减轻兔耳瘢痕增生。 Abstract:Objective To investigate the effects of trehalose gel on full-thickness skin defect wounds in rats and scar hyperplasia in rabbit ears. Methods The study was an experimental study. The trehalose gel and carbomer gel were prepared, their appearance after irradiation sterilization, and their physicochemical characterization such as viscosity, film forming rate, bacteria resistance rate, heavy metal content, moisture retention rate, water vapor permeability, sterility, and biocompatibility such as cytotoxicity, intradermal irritation, and sensitization were observed. Thirty male Sprague-Dawley rats aged 8-10 weeks were divided into experimental group, positive control group, and negative control group using a random number table method, with 10 rats in each group. The full-thickness skin defect wound models were prepared on the back of rats in negative control group, positive control group, and experimental group, and were treated with routine dressing change, carbomer gel dressing change, and trehalose gel dressing change, respectively. The wound healing rates on 6 and 12 days after injury and the wound healing time were recorded. On 6 days after injury, the number of autophagosomes and autophagolysosomes in rat wound tissue was detected using transmission electron microscopy. The content of microtubule associated protein light chain 3Ⅰ (LC3Ⅰ) and LC3Ⅱ in rat wound tissue was detected using enzyme-linked immunosorbent assay method and their ratio was calculated. The proportion of type Ⅰ and Ⅲ collagens and their ratio, as well as the total collagen proportion in rat wound tissue were detected using sirius red picric acid staining method. The number of samples in the aforementioned experiments was all 5. Three male New Zealand albino model rabbits aged 3-4 months were taken, and 3 wounds deep to the perichondrium were created on each of the rabbit ears, with six wounds in each group and being grouped and treated as mentioned above. On 30 days after wound healing, the scar tissue of the rabbit ear was observed and evaluated using the Vancouver scar scale. The thickness of the epidermis and dermis in the scar tissue of the rabbit ear was measured using hematoxylin eosin staining, and the proportion of type Ⅰ and Ⅲ collagens and their ratio, as well as the total collagen proportion and arrangement in the scar tissue of the rabbit ear were measured using sirius red picric acid staining method. The number of samples was 6. Results The irradiated trehalose gel and carbomer gel were light yellow and transparent, without odor and impurities. The viscosity, film forming rate, bacteria resistance rate, and moisture retention rate of trehalose gel were significantly better than that of carbomer gel (with t values of 4.13, 3.50, 4.03, and 5.80, respectively, P<0.05), but the water vapor permeability was significantly lower than that of carbomer gel (t=-4.14, P<0.05). No heavy metals or bacteria were detected in any gel. Both of the two gel had no cytotoxicity, and the intradermal irritation and sensitization were negative. On 6 and 12 days after injury, the wound healing rates of rats in positive control group were significantly higher than that in negative control group (with t values of -6.82 and -4.58, respectively, P<0.05); the wound healing rate of rats in experimental group was significantly higher than those in positive control group (with t values of -8.90 and -4.25, respectively, P<0.05) and negative control group (with t values of -8.78 and -4.25, respectively, P<0.05). The wound healing time ((20.4±2.5), (23.4±2.5) d) of rats in positive control group and experimental group was significantly shorter than (27.0±2.1) d in negative control group (with t values of 2.45 and -4.49, respectively, P<0.05). On 6 days after injury, the number of autophagosomes and autophagolysosomes in wound tissue in experimental group of rats were significantly higher than those in positive control group (with t values of 7.37 and 9.33, respectively, P<0.05) and negative control group (with t values of -7.06 and -8.54, respectively, P<0.05). On 6 days after injury, the content of LC3 Ⅱ and LC3 Ⅱ/LC3 Ⅰ in wound tissue in positive control group of rats were significantly higher than that in negative control group (with t values of -4.48 and -2.47, respectively, P<0.05); the content of LC3Ⅰ and LC3 Ⅱ/LC3 Ⅰ in wound tissue in experimental group of rats were significantly higher than those in negative control group (with t values of 11.98 and 6.04, respectively, P<0.05) and positive control group (with t values of -6.64 and -4.17, respectively, P<0.05), the content of LC3Ⅰ was significantly lower than that in negative control group (t=2.33, P<0.05). On 6 days after injury, the proportions of total collagen and type Ⅰ collagen in wound tissue of rats in the three groups were similar, P>0.05. On 6 days after injury, the proportion of type Ⅲ collagen in wound tissue of rats in positive control group was significantly higher than that in negative control group (t=-3.19, P<0.05), and the type Ⅰ collagen/type Ⅲ collagen was significantly lower than that in negative control group (t=2.18, P<0.05); the proportion of type Ⅲ collagen in the wound tissue of rats in experimental group was significantly higher than those in negative control group and positive control group (with t values of -2.38 and 5.91, respectively, P<0.05), and type Ⅰ collagen/type Ⅲ collagen was significantly lower than those in negative control group and positive control group (with t values of 3.08 and -4.35, respectively, P<0.05). On 30 days after wound healing, it was observed that the rabbit ear scar proliferation in positive control group was similar to that in negative control group, while the rabbit ear scar proliferation in experimental group was significantly reduced. On 30 days after wound healing, the color, blood vessels, thickness, hardness score, and total score of rabbit ear scars in experimental group were significantly lower than those in positive control group (with t values of 3.80, 3.80, 2.39, 2.71, and 4.84, respectively, P<0.05) and negative control group (with t values of -3.81, -4.78, 0.04, -2.71, and -5.14, respectively, P<0.05). On 30 days after wound healing, there was no significant difference in the epidermal thickness of rabbit ear scar tissue among experimental group, negative control group, and positive control group (P>0.05); the dermal thickness of rabbit ear scar tissue in positive control group was significantly smaller than that in negative control group (t=5.42, P<0.05), while the dermal thickness of rabbit ear scar tissue in experimental group was significantly smaller than those in negative control group and positive control group (with t values of 11.91 and 8.49, respectively, P<0.05). On 30 days after wound healing, the collagen protein arrangement of scar tissue of rabbits in the three groups was disordered, and the total collagen proportion was similar (P>0.05). The proportion of type Ⅰ collagen of scar tissue in experimental group was significantly lower than that in positive control group (t=3.00, P<0.05), the content of type Ⅲ collagen was significantly higher than those in negative control group and positive control group (with t values of -4.46 and 4.05, respectively, P<0.05), and the type Ⅰcollagen/type Ⅲ collagen was significantly lower than those in negative control group and positive control group (with t values of 8.50 and -5.25, respectively, P<0.05). Conclusions Compared with carbomer gel, trehalose gel has a more suitable physicochemical characterization for wound healing, and has good biocompatibility. It can promote the wound healing of full-thickness defects in rats and reduce scar hyperplasia in rabbit ears based on autophagy activation. -
Key words:
- Biocompatible materials /
- Trehalose /
- Cicatrix /
- Autophagy /
- Wound repair
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金剑：酝酿和设计实验、实施研究、采集数据、整理数据、统计分析、撰写论文、修改论文；储云高：研究指导、数据整理、论文修改、经费支持所有作者均声明不存在利益冲突
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参考文献
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图 1 海藻糖凝胶生物相容性检测。1A、1B.分别为24、48 h新西兰白化模型兔背部皮内刺激检测结果,均未观察到显著的红斑和水肿；1C.培养24 h后,L929细胞生长状态良好 光学显微镜×10；1D、1E、1F.分别为24、48、72 h豚鼠背部皮肤致敏性检测结果,均未观察到显著的红斑和水肿
图 2 3组大鼠伤后不同时间点全层皮肤缺损创面愈合情况。2A、2B、2C.分别为阴性对照组伤后0(即刻)、6、12 d创面情况；2D、2E、2F.分别为阳性对照组伤后0、6、12 d创面情况,图2E、2F中创面面积分别较图2B、2C缩小；2G、2H、2I.分别为实验组伤后0(即刻)、6、12 d创面情况,图2H、2I中创面面积分别较图2E、2F缩小
注：阴性对照组采用常规换药,阳性对照组采用卡波姆凝胶换药,实验组采用海藻糖凝胶换药
图 3 3组大鼠伤后6 d全层皮肤缺损创面中自噬情况 透射电镜。3A与3B、3C与3D、3E与3F.分别为阴性对照组、阳性对照组、实验组,图3B、3D、3F（放大倍数为400）分别为图3A、3C、3E（放大倍数为4 000）红色线框中图形的放大图,可见图3F中有大量自噬体和自噬溶酶体（红色箭头所示）
注：阴性对照组采用常规换药,阳性对照组采用卡波姆凝胶换药,实验组采用海藻糖凝胶换药
图 4 3组大鼠伤后6 d全层皮肤缺损创面组织中胶原情况 天狼星红-苦味酸×400。4A、4B、4C.分别为阴性对照组、阳性对照组、实验组大鼠创面情况,图4C中的Ⅲ型胶原蛋白面积（绿色荧光标示部分）占比较图4A与4B大
注：阴性对照组采用常规换药,阳性对照组采用卡波姆凝胶换药,实验组采用海藻糖凝胶换药；Ⅰ型胶原蛋白阳性染色为黄色,Ⅲ型胶原蛋白阳性染色为绿色
图 5 3组新西兰白化模型兔耳创面愈合后30 d的瘢痕情况,最右侧瘢痕增生情况较左侧2个瘢痕明显减轻
注：阴性对照组采用常规换药,阳性对照组采用卡波姆凝胶换药,实验组采用海藻糖凝胶换药；从左到右分别为阴性对照组、阳性对照组、实验组瘢痕
图 6 3组新西兰白化模型兔耳创面愈合后30 d的瘢痕评分比较（样本数6,
注：阴性对照组采用常规换药,阳性对照组采用卡波姆凝胶换药,实验组采用海藻糖凝胶换药；与阴性对照组相比,aP<0.05；与阳性对照组相比,bP<0.05
图 7 3组新西兰白化模型兔耳创面愈合后30 d瘢痕组织真皮厚度及胶原情况。7A、7B、7C.分别为阴性对照组、阳性对照组、实验组瘢痕组织真皮厚度情况,图7C中的真皮厚度明显小于图7A、7B 苏木精-伊红×400；7D、7E、7F.分别为阴性对照组、阳性对照组、实验组瘢痕组织胶原情况,图7F中的Ⅲ型胶原蛋白含量（绿色荧光标示部分）占比明显大于图7D、7E 天狼星红-苦味酸×400
注：阴性对照组采用常规换药,阳性对照组采用卡波姆凝胶换药,实验组采用海藻糖凝胶换药
Table 1. 海藻糖凝胶和卡波姆凝胶理化特性比较（
凝胶种类 样本数 粘度（Pa·s） 成膜率（%） 阻菌率（%） 保湿率（%） 水蒸气透过率（g/m2） 卡波姆凝胶 5 12.4±1.1 72.2±2.8 45.0±2.6 13.2±1.3 660±15 海藻糖凝胶 5 15.7±1.5 79.2±3.5 52.8±3.4 17.9±1.2 616±19 t值 4.13 3.50 4.03 5.80 -4.14 P值 0.003 0.008 0.004 0.003 <0.001 
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Table 2. 3组大鼠伤后不同时间点全层皮肤缺损创面愈合情况比较（
组别 样本数 伤后6 d创面愈合率（%） 伤后12 d创面愈合率（%） 创面愈合时间（d） 阴性对照组 5 45.5±2.8 65.1±3.2 27.0±2.1 阳性对照组 5 52.9±2.0a 73.7±2.6a 23.4±2.5a 实验组 5 62.1±2.6ab 79.2±1.9ab 20.4±2.5a F值 112.15 39.03 9.58 P值 <0.001 <0.001 0.003 注：阴性对照组采用常规换药,阳性对照组采用卡波姆凝胶换药,实验组采用海藻糖凝胶换药；创面愈合率处理因素主效应,F=127.26,P<0.001；时间因素主效应,F=585.46,P<0.001；两者交互作用,F=1.24,P=0.301；与阴性对照组比较,aP<0.05；与阳性对照组比较,bP<0.05
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Table 3. 3组大鼠伤后6 d全层皮肤缺损创面中自噬情况比较（
组别 样本数 自噬体数量（个） 自噬溶酶体数量（个） LC3Ⅰ含量（ng/g） LC3Ⅱ含量（ng/g） LC3Ⅱ/LC3Ⅰ 阴性对照组 5 2.4±0.6 1.0±0.7 1.26±0.44 4.5±0.4 3.8±1.2 阳性对照组 5 6.6±1.1 1.2±0.8 1.07±0.31 6.1±0.7a 6.0±1.5a 实验组 5 10.0±2.4ab 7.9±1.9ab 0.79±0.14a 8.9±0.7ab 11.7±2.7ab F值 46.73 60.56 2.80 67.95 22.87 P值 <0.001 <0.001 0.100 <0.001 <0.001 注：阴性对照组采用常规换药,阳性对照组采用卡波姆凝胶换药,实验组采用海藻糖凝胶换药；LC3为微管相关蛋白轻链3；与阴性对照组比较,aP<0.05；与阳性对照组比较,bP<0.05
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Table 4. 3组大鼠伤后6 d全层皮肤缺损创面组织中2种胶原蛋白占比及其比值的比较（
组别 样本数 总胶原蛋白占比（%） Ⅰ型胶原蛋白占比（%） Ⅲ型胶原蛋白占比（%） Ⅰ型胶原蛋白/Ⅲ型胶原蛋白 阴性对照组 5 22±10 18±9 4.4±1.6 11.6±2.2 阳性对照组 5 31±9 23±8 8.3±2.2a 4.2±1.3a 实验组 5 32±6 23±7 11.6±2.2ab 2.8±0.7ab F值 1.78 0.61 15.86 10.71 P值 0.211 0.559 <0.001 0.002 注：阴性对照组采用常规换药,阳性对照组采用卡波姆凝胶换药,实验组采用海藻糖凝胶换药；与阴性对照组比较,aP<0.05；与阳性对照组比较,bP<0.05
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Table 5. 3组新西兰白化模型兔耳创面愈合后30 d瘢痕组织的增生及胶原蛋白情况比较（
组别 样本数 表皮厚度（μm） 真皮厚度（μm） 总胶原蛋白占比（%） Ⅰ型胶原蛋白占比（%） Ⅲ型胶原蛋白占比（%） Ⅰ型胶原蛋白/Ⅲ型胶原蛋白 阴性对照组 6 11.8±1.4 168±10 40±7 31.6±5.7 7.6±1.7 4.1±0.9 阳性对照组 6 11.7±1.8 141±7a 42±6 33.6±5.1 8.2±1.0 4.3±0.5 实验组 6 11.4±1.2 103±9ab 41±5 26.5±2.9b 14.7±3.5ab 1.9±0.4ab F值 0.12 86.31 0.17 3.65 15.84 24.14 P值 0.887 <0.001 0.842 0.051 <0.001 <0.001 注：阴性对照组采用常规换药,阳性对照组采用卡波姆凝胶换药,实验组采用海藻糖凝胶换药；与阴性对照组比较,aP<0.05；与阳性对照组比较,bP<0.05
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