Chinese Journal of Animal Nutrition >

2023 , Vol. 35 >Issue 5: 3333 - 3341

DOI: https://doi.org/10.12418/CJAN2023.309

RESEARCH PAPER

Effects of Apriona swainsoni Larvae on Gastrointestinal Motility and Gastrointestinal Hormone Secretion of Mice with Functional Dyspepsia

  • CHENG Yaoyun , 1 ,
  • SU Lan 2 ,
  • ZHOU Weiqing 3 ,
  • HE Zhenyu 4 ,
  • XU Huachao , 1, *
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  • 1 College of Forestry and Biotechnology, Zhejiang A&F University, Hangzhou 311300, China
  • 2 Lingfeng Subdistrict Office, Anji County, Zhejiang Province, Huzhou 313000, China
  • 3 Forestry Bureau of Chunan County, Zhejiang Province, Chunan 311700, China
  • 4 People’s Government of Zhouxiang Town, Ningbo 315300, China
*professor, E-mail:

Received date: 2022-10-21

  Online published: 2023-05-11

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Abstract

This experiment was conducted to study the effects of Apriona swainsoni (A. swainsoni) larvae on body weight, gastrointestinal motility function and gastric hormone levels of mice with functional dyspepsia. After adaptive feeding for 5 days, ninety specific pathogen free (SPF) grade ICR mice were randomly divided into normal group, model group, domperidone group (10 mg/kg), low A. swainsoni larvae low (4%), medium (8%) and high concentration group (12%), with 15 mice per group. Except for the normal group, the FD mouse model of the other groups was established by irregular feeding combined with intraperitoneal injection of L-arginine (L-Arg). After the successful establishment of FD mouse model, the mice in the domperidone group (10 mg/kg BW domperidone), and A. swainsoni larvae low (4% A. swainsoni larvae suspension), medium (8% A. swainsoni larvae suspension) and high concentration (12% A. swainsoni larvae suspension) groups were given the corresponding drugs with the intragastric volume 0.2 mL per day, normal group and model group were given the same volume of normal saline. The body weight at the beginning of modeling, the end of modeling and the end of intervention of the mice was recorded. After 7 days of continuous intragastric administration, mice were killed after intragastric administration of semi-solid paste with carbon powder, and the whole stomach and small intestine of mice were removed to calculate the gastric emptying rate and intestinal propulsion rate; the levels of serum gastrin (GAS) and motilin (MTL) in mice were determined by enzyme-linked immunosorbent assay (ELISA); the pathological changes of gastric tissue of mice were observed by hematoxylin-eosin (HE) staining. The results showed that the body weight, gastric emptying rate and intestinal propulsion rate of mice in the model group were significantly decreased (P<0.05), and the levels of GAS and MTL in serum were significantly decreased compared with the normal group (P<0.05); compared with the model group, the body weight, gastric emptying rate and small intestinal propulsion rate in the A. swainsoni larvae low, middle and high concentration groups were significantly increased (P<0.05), the levels of GAS and MTL in serum were significantly increased (P<0.05), meanwhile, the body weight of mice was significantly increased (P<0.05). There was no difference in gastric histopathology among all groups. In conclusion, irregular diet combined with intraperitoneal injection of L-Arg can successfully establish FD mouse model; A. swainsoni larvae can promote gastrointestinal motility and improve FD of mice, and its mechanism may be related to the increase of serum GAS and MTL levels.

Key words： Apriona swainsoni larvae; functional dyspepsia; gastrointestinal motility; motilin; gastrin

Cite this article

CHENG Yaoyun , SU Lan , ZHOU Weiqing , HE Zhenyu , XU Huachao . Effects of Apriona swainsoni Larvae on Gastrointestinal Motility and Gastrointestinal Hormone Secretion of Mice with Functional Dyspepsia[J]. Chinese Journal of Animal Nutrition, 2023 , 35(5) : 3333 -3341 . DOI: 10.12418/CJAN2023.309

消化不良(dyspepsia)表现为上腹出现慢性或复发性的不适或疼痛、恶心、早饱感等症状,其中60%为功能性消化不良(functional dyspepsia,FD),即未能对其症状做出明确的器质性或生化性解释[1]。FD发病率由于社会环境、个体、诊断标准等因素不同存在较大差异,目前FD在全世界范围的发病率为5%~20%,在我国消化类疾病中确诊为FD的病患数量高达50%[2-3]。FD发病原因众多,如胃肠运动功能障碍、内脏敏感性增高,情绪低落等,且幽门螺杆菌感染与FD之间存在联系[4]。由于其发病率高、症状多样化、复发性强的特点目前临床多以经验治疗为主。斗米虫是指寄生在云实树中的天牛幼虫,在古代有一斗米换一头虫的说法,故名斗米虫,其主要种为锈色粒肩天牛(Apriona swainsoni)和桑天牛(Apriona germari),在我国分布广泛,属于危害能力较强的蛀干害虫,更是优良的药用资源昆虫。斗米虫体内含有抗菌蛋白、几丁质,具有较好的食用与药用价值。《本草纲目》《神农本草经》《中国药典》等古籍对斗米虫的功效均有记载,斗米虫在江浙一带有多年食用历史,是提高免疫力、抗病毒、抗肿瘤、治疗癌症的珍贵药用资源昆虫,且其对治疗小儿疳积、食欲不振有显著功效[5⇓-7]。孙媭[8]利用MTT法、流式细胞术等方法研究发现,斗米虫蛋白对人胃癌细胞MFC和小鼠乳腺癌细胞4T1有抑制作用,此外,该蛋白还能抑制4T1细胞的迁移率,并诱导4T1及MFC细胞凋亡,具有一定的体外抗肿瘤活性。侯沛颖等[9]研究证明斗米虫蛋白在乳腺癌荷瘤小鼠体内具有抗肿瘤活性。Wu Chen[10]研究发现,斗米虫包含所有人体必需氨基酸,其不饱和脂肪酸中n-6/n-3比率较低,在预防心血管疾病方面有很大潜力。斗米虫的脂溶性组分和水提物对于肿瘤细胞都有抑制作用。高诗琪等[11]研究发现,斗米虫抗菌肽粗提液对金黄色葡萄球菌和枯草芽孢杆菌有抑制作用;何振宇等[12]研究发现,斗米虫可以有效提高小鼠血清中淀粉酶(AMS)、脂肪酶(LPS)和乳酸脱氢酶(LDH)的活性,改善胃肠消化功能并提高胃肠免疫力。王丽红[13]发现,FD患者会出现胃动力不足,经和胃汤治疗后能调节胃动素、胃泌素分泌,改善胃动力,促进胃肠蠕动。斗米虫作为中药食用历史悠久,且无毒性[14],是具有较好发展前景的保健食品和药用昆虫。关于斗米虫对胃肠作用的试验研究较少,斗米虫对于FD的治疗目前多应用于民间。斗米虫对于胃肠运动的影响以及对胃肠激素是否存在调节作用值得深入研究。因此,本文在建立FD小鼠模型的基础上,探究斗米虫对FD小鼠胃排空率和小肠推进率的影响,检测小鼠血清胃肠激素含量,判断其是否对FD小鼠具有治疗作用,为进一步开发斗米虫食药用功能,确定其最适剂量提供理论基础。

1 材料与方法

1.1 试验动物及分组

无特定病原体(SPF)级ICR小鼠90只,雌性,体重(20±2) g,动物合格证号:SCXK(浙)2018-0010。试验于浙江农林大学进行,饲养环境温度21~25 ℃,相对湿度45%~65%,昼夜明暗交替时间为12 h。本试验的各项操作均经浙江农林大学伦理委员会审核并予以通过(伦理审核号ZAFUAC2022011)。将90只ICR雌性小鼠随机分为6组,分别为正常组、模型组、多潘立酮组以及斗米虫低、中、高浓度组,每组15只。

1.2 试验材料

多潘立酮片(批号H10910003)为西安杨森制药有限公司产品,左旋精氨酸(L-Arg)、4%多聚甲醛固定液、羧甲基纤维素、苏木素-伊红(HE)染液试剂盒为承勒科技(杭州)有限公司产品,胃泌素(gastrin,GAS)试剂盒、胃动素(motilin,MTL)试剂盒为武汉纯度生物科技有限公司产品。
碳末半固体糊:在128 mL水中加入8 g奶粉、5 g羧甲基纤维素、4 g糖、4 g淀粉、1 g活性炭,配制成150 mL的半固体糊,约150 g。
不同浓度斗米虫混悬液:斗米虫200条,体质量1.6~2.0 g,虫龄5龄,属于老熟幼虫,由江西上饶斗米虫养殖基地提供。将斗米虫放入-80 ℃冰箱中冷冻处死后,随即使用冷冻干燥机脱水干燥至恒重,然后加入液氮在研钵中研磨至粉末状,经过高压灭菌后加入生理盐水配成浓度分别为4%(低浓度)、8%(中浓度)、12%(高浓度)的斗米虫混悬液备用。

1.3 试验方法

对除正常组外的其余组小鼠进行造模。适应性饲养5 d后,参照文献[15⇓⇓-18]以及预试验,采用不规律进食结合L-Arg腹腔注射的方式建立FD动物模型,以2 d进食、1 d禁食为循环,共10 d,第11、12天腹腔注射0.1 g/kg BW L-Arg;正常组小鼠则腹腔注射体积相等的生理盐水进行替代。对各组造模小鼠的日常状态(体重、饮水量、饮食量、毛发光泽度和个体活跃度)进行观测,待造模结束后从每个组随机选取5只小鼠处死,测定小鼠的小肠推进率和胃排空率,以此为FD造模成功指标。造模成功后,隔天对多潘立酮组(10 mg/kg BW[19],溶于生理盐水)与斗米虫低(4%斗米虫混悬液)、中(8%斗米虫混悬液)、高浓度组(12%斗米虫混悬液)小鼠给予相应药物,灌胃体积每天0.2 mL,正常组与模型组灌胃相等体积的生理盐水,共7 d。记录小鼠体重变化。末次给药后禁食24 h,每只小鼠灌胃0.5 g碳末半固体糊,30 min后眼球采血,室温自然凝固15 min后,4 ℃、2 500 r/min离心20 min,取血清冻存待测。

1.4 小鼠体重测定及一般状态观察

在开始造模时、造模后和干预结束时,称重记录小鼠体重,观察其毛发光泽度和个体活跃程度情况。

1.5 小鼠胃排空及小肠推进功能测定

小鼠眼球采血后脱颈处死,剖开腹腔,分别对小鼠贲门和幽门进行结扎,取出全胃拭干后称重,然后沿着大弯处剪开,暴露胃内容物,采用4 ℃的生理盐水冲洗干净后再次滤纸拭干,并称取胃净重,计算胃内容物排空率。剖腹后取小鼠全段小肠,记录小肠的全段长度和碳末半固体糊在小肠中的移动长度,计算小肠推进率。相关计算公式如下:
胃排空率(%)=[1-(胃全重-胃净重)/碳末半固体糊重]×100;
小肠推进率(%)=(碳末半固体糊的移动距离/小肠全长)×100。

1.6 小鼠胃组织病理学观察

取部分胃组织,经生理盐水冲洗后,在4%多聚甲醛中浸泡固定2 d,然后制作石蜡切片,切片依次苏木素染色、伊红染色后脱水、中性树胶封片,进行显微镜观察及图像采集分析。

1.7 小鼠血清胃肠激素水平检测

取待测血清样本,按照酶联免疫吸附测定(ELISA)试剂盒(武汉纯度生物科技有限公司)说明书操作,检测小鼠血清中MTL和GAS水平。

1.8 数据处理与分析

使用SPSS 25.0软件对数据进行统计学处理与分析,数据结果采用“平均值±标准差”表示,P<0.05时认为有显著差异。

2 结果

2.1 各组小鼠一般状态变化

造模期间,正常小鼠精神状态良好,活动度高,被毛色白且密集具有光泽,粪便呈灰黑色颗粒状,含水量低,较硬;造模小鼠出现食欲减少,活跃程度降低,喜聚集,嗜睡,并出现弓背、竖毛现象,毛色逐渐失去光泽,粪便含水量增加。给药后,多潘立酮组与斗米虫低、中、高浓度组小鼠上述症状逐渐改善、消失。

2.2 各组小鼠体重的比较

由表1可知,造模开始时,各组小鼠体重均无显著差异(P>0.05);造模结束时,造模的5组之间小鼠体重无显著差异(P>0.05),但均较正常组显著减轻(P<0.05);给药干预结束时,与模型组相比,多潘立酮组和斗米虫低、中、高剂量组小鼠体重均显著增高(P<0.05),正常组小鼠体重显著高于其余5组(P<0.05),多潘立酮组与斗米虫低、中、高浓度组之间无显著差异(P>0.05)。
表1 各组小鼠体重的比较

Table 1 Comparison of body weight of mice among all groups g

项目
Items		 造模开始时
At the beginning of
modeling		 造模结束时
At the end of
modeling		 干预结束时
At the end of
intervention
正常组Normal group 22.24±0.64 28.91±1.13a 30.51±1.64a
模型组Model group 22.30±0.85 25.17±1.15b 26.13±0.85c
多潘立酮组Domperidone group 22.39±0.27 25.62±0.77b 28.52±0.80b
斗米虫低浓度组
A. swainsoni larvae low concentration group		 22.42±0.50 25.93±0.72b 29.12±1.30b
斗米虫中浓度组
A. swainsoni larvae medium concentration group		 22.13±0.58 25.41±0.82b 29.10±1.47b
斗米虫高浓度组
A. swainsoni larvae high concentration group		 22.49±1.14 25.59±0.97b 29.01±0.94b

同列数据肩标无字母或相同字母表示差异不显著(P>0.05),不同小写字母表示差异显著(P<0.05)。下表同。

In the same column, values with no letter or the same letter superscripts mean no significant difference (P>0.05), while with different small letter superscripts mean significant difference (P<0.05). The same as below.

2.3 各组小鼠胃排空及肠推进功能的比较

由表2可知,与模型组相比,各治疗组的小鼠胃排空率均显著提高(P<0.05),其中多潘立酮组胃排空率最高,斗米虫中浓度组小鼠的胃排空率与正常组和多潘立酮组无显著差异(P>0.05),但显著高于斗米虫低、高浓度组(P<0.05)。多潘立酮组的小肠推进率最高,显著高于模型组以及斗米虫低、中浓度组(P<0.05);与模型组相比,斗米虫低、中、高浓度的小肠推进率均显著提高(P<0.05),且斗米虫各浓度组与正常组无显著差异(P>0.05)。
表2 各组小鼠胃排空及肠推进功能的比较

Table 2 Comparison of gastric emptying and intestinal propulsion function of mice among all groups %

项目
Items		 胃排空率
Gastric emptying rate		 小肠推进率
Intestinal propulsion rate
正常组Normal group 88.60±6.60ab 87.37±9.85ab
模型组Model group 47.40±6.80d 54.27±6.20c
多潘立酮组Domperidone group 93.30±0.27a 94.31±5.16a
斗米虫低浓度组A. swainsoni larvae low concentration group 68.40±9.13c 78.77±10.45b
斗米虫中浓度组A. swainsoni larvae medium concentration group 89.00±3.80ab 85.73±6.59b
斗米虫高浓度组A. swainsoni larvae high concentration group 86.60±5.82b 89.36±8.26ab

2.4 各组小鼠胃组织病理学观察

经过光镜观察HE染色切片发现各组小鼠的胃组织肌层、浆膜层、黏膜层及黏膜下层结构清晰,均未见明显的坏死、变性、增生、化生、萎缩等病理学改变,符合构建FD动物模型的要求。

2.5 各组小鼠血清胃肠激素水平的比较

由表3可知,与正常组相比,模型组小鼠血清GAS、MTL水平显著降低(P<0.05);与模型组相比,斗米虫低、中、高浓度组与多潘立酮组小鼠血清GAS水平均有不同程度升高,其中多潘立酮组血清MTL、GAS水平均为最高,且血清MTL水平显著高于其他各组(P<0.05),血清GAS水平显著高于斗米虫低、中浓度组和模型组(P<0.05);斗米虫高浓度组血清GAS水平与正常组无显著差异(P>0.05),但显著高于斗米虫低、中浓度组和模型组(P<0.05),斗米虫低、中浓度组和模型组之间无显著差异(P>0.05);斗米虫各浓度组间,血清MTL水平随斗米虫混悬液浓度的升高显著升高(P<0.05),斗米虫高浓度组血清MTL水平相较正常组与多潘立酮组无显著差异(P>0.05)。
表3 各组小鼠血清胃肠激素水平的比较

Table 3 Comparison of serum gastrointestinal hormone levels of mice among all groups μg/mL

项目Items 胃泌素GAS 胃动素MTL
正常组Normal group 476.76±43.47b 305.05±22.49a
模型组Model group 241.83±30.80cd 201.09±2.67d
多潘立酮组Domperidone group 571.20±67.37a 312.15±17.63a
斗米虫低浓度组A. swainsoni larvae low concentration group 278.44±59.13c 210.10±16.83c
斗米虫中浓度组A. swainsoni larvae medium concentration group 334.67±40.87c 245.64±15.06b
斗米虫高浓度组A. swainsoni larvae high concentration group 510.31±40.07b 300.10±11.16a

3 讨论

患有FD的人数众多,是临床最常见的疾病之一[20]。FD病因复杂,易复发,且因缺乏器质性、系统性或代谢性疾病的相关证据,目前临床对于患者治疗的方式多以缓解其不良症状为主。目前FD的罹患无确切病因,导致建立FD的动物模型种类繁多,其主要表现为出现体重下降、食欲不振、精神萎靡,且胃肠组织无病理学变化[21]。L-Arg可以在一氧化氮合成酶(nitric oxidative synthase,NOS)的作用下与分子氧合成可以对胃肠道产生抑制性的一氧化氮(nitric oxide,NO),减少胃窦指数,但对降低胃排空效果甚微,且效果受进食影响[17,22]。本研究采用不规律进食联合L-Arg腹腔注射的方法构建FD小鼠模型,在试验中造模小鼠出现胃动力下降,饮食量、体重减少等症状,胃肠组织未出现器质性病变,是一种安全有效的造模方式。
FD患者中,存在胃固体排空延缓、近端胃及胃窦运动异常、内脏敏感性增高、幽门十二指肠运动协调失常等胃肠动力障碍的症状超过半数[23]。目前胃肠动力障碍为罹患FD的主要评判依据,本研究通过对FD小鼠灌胃斗米虫混悬液,发现斗米虫具有提高FD小鼠胃排空率、小肠推进率的功效,能够有效促进胃肠蠕动,增加胃肠运动功能。图1显示各组小鼠的胃组织均未发生病理改变,符合FD无器质性病变的症状,也体现斗米虫的安全性较高,未对小鼠机体造成损害。在有关治疗FD的相关研究中,郭令飞等[24]发现,香砂六君子汤合半夏泻心汤可以通过调节血清白细胞介素-6(interleukin-6,IL-6)、降钙素基因相关肽(calcitonin gene related peptide,CGRP)、神经肽S受体1(neuropeptide S receptor 1,NPSR1)水平,改善临床症状,提高胃肠动力。王香香等[25]基于线粒体自噬于Pink1/Parkin信号通路探讨柴胡疏肝散的对FD大鼠的功效,发现其可减少胃窦组织的线粒体肿胀,抑制Cajal间质细胞(interstitial cells of Cajal,ICCs)线粒体自噬,来增加FD大鼠的胃肠动力功能。齐美欣等[26]发现,柴胡疏肝散有效部位组方能显著增加胃排空率、小肠推进率,提高胃促生长素(Ghrelin)和MTL分泌水平,上调闭锁小带蛋白-2(zonula occluden-2,ZO-2)蛋白表达水平,有效提高胃肠动力。本研究结果与上述研究所得结果基本一致,表明斗米虫对于FD小鼠具有增强其胃肠动力功能的作用。
图1 各组小鼠胃组织切片(苏木精-伊红染色)

A:正常组;B:模型组;C:多潘立酮组;D:斗米虫低浓度组;E:斗米虫中浓度组;F:斗米虫高浓度组。

Fig.1 Sections (HE staining) of gastric tissue of mice in all groups

A: normal group; B: model group; C: domperidone group; D: A. swainsoni larvae low concentration group; E: A. swainsoni larvae medium concentration group; F: A. swainsoni larvae high concentration group.

随着近年来研究的深入,脑肠轴越来越受到学者们的关注。脑肠轴是中枢神经系统与胃肠道的链接,脑肠轴功能对胃肠道的调节功能影响深远,可以双向调节中枢神经系统与胃肠道[27]。出现FD则是神经系统传导出现异常,具体表现为脑肠信号传导与脑肠肽分泌异常。GAS和MTL都脑肠肽,其中GAS是由胃窦组织和十二指肠黏膜中G细胞分泌的一种胃肠激素,可以刺激消化系统组织细胞分泌胃酸,促进胃肠道黏膜生长和胃窦组织收缩[28-29];MTL是Mo由细胞分泌,可以促进胃平滑肌的收缩,刺激消化道电活动[30]。彭昊等[31]研究认为,血清GAS、MTL能显著影响胃肠动力功能,改善血清GAS、MTL水平能够改善重症患儿的胃肠动力障碍,加速胃排空;李晓玥等[32]发现,和胃汤能够通过调节胃肠激素和脑肠肽分泌,促进胃排空率,有效缓解FD主要症状;李莉等[33]通过研究FD大鼠胃组织线粒体功能,发现柴胡疏肝散可能通过恢复胃组织线粒体功能,抑制线粒体自噬来提高体内胃肠激素水平,纠正胃动力功能障碍;龙兴瑶[34]研究表明,蚕蛹油可以促进便秘小鼠肠胃蠕动,提高血清GAS、MTL水平,增加抗氧化酶血清超氧化物歧化酶(superoxide dismutase,SOD)、过氧化氢酶(catalase,CAT)、谷胱甘肽过氧化物酶(glutathione peroxidase,GSH-Px)活性,能有效预防便秘。本研究表明,灌胃斗米虫混悬液可显著提高小鼠血清GAS、MTL水平,与上述研究结果相类似,说明斗米虫具有调节脑肠肽水平来改善胃肠动力促进胃肠排空的作用。
斗米虫无毒,在民间有叠加食用的方式。本研究针对斗米虫对FD小鼠的治疗效果进行了初步探究,发现斗米虫能够改善其胃肠道运动功能,提高血清胃肠激素水平,有效恢复体重。本试验中FD小鼠的胃肠动力功能随斗米虫混悬液浓度的升高而提高,小鼠的血清胃肠激素水平也与斗米虫混悬液浓度呈正相关,斗米虫的药效是否会因剂量进一步增加而提高还有待后续深入研究。FD为多因素致病,近年研究发现内质网应激在FD中起重要作用[35],机体发生内质应激后,会引起细胞自噬或其他反应,导致FD的发生。斗米虫是否存在通过抑制细胞自噬来改善内质网应激的机制还需要进行相关研究。斗米虫是一种具有极大开发价值潜力的食药用昆虫资源,其对于FD是否存在更深层次的作用机理和最大剂量的上限也有待进一步研究。

4 结论

斗米虫能显著提高FD小鼠的体重、胃排空率、小肠推进率,且对FD小鼠血清GAS、MTL水平有提高作用,说明斗米虫对于FD小鼠的胃动力障碍具有一定的治疗效果,且对胃动力功能的提高作用随高斗米虫混悬液浓度的升高而增强。

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