王雪潔 馮京海

(中國(guó)農(nóng)業(yè)科學(xué)院北京畜牧獸醫(yī)研究所，動(dòng)物營(yíng)養(yǎng)學(xué)國(guó)家重點(diǎn)實(shí)驗(yàn)室，北京 100193)

家禽的腸道包括十二指腸、空腸、回腸、盲腸和直腸，是營(yíng)養(yǎng)物質(zhì)消化、吸收的主要位點(diǎn)。家禽的腸道約占體重的1.5%，但其長(zhǎng)度約是體長(zhǎng)的6倍。腸道內(nèi)腔環(huán)形皺襞以及腸絨毛使小腸表面積擴(kuò)大了20～30倍，有效地增強(qiáng)了小腸的吸收功能[1]。同時(shí)腸道也是家禽能量消耗的主要組織，飼料中6.0%～8.0%的能量由家禽腸道消耗[2]。另外，家禽腸道中棲息著大量微生物，其中包括大量由飼料和飲水進(jìn)入的病源微生物，因此腸道上皮組織也是家禽抵御病源菌的重要屏障[3]。維持腸道正常的結(jié)構(gòu)和功能對(duì)于家禽的生長(zhǎng)和健康十分關(guān)鍵。熱應(yīng)激影響家禽的健康和產(chǎn)長(zhǎng)性能，研究發(fā)現(xiàn)熱應(yīng)激導(dǎo)致肉雞生長(zhǎng)性能顯著下降[4]，以及禽類(lèi)解偶聯(lián)蛋白mRNA表達(dá)量下降[5]。同時(shí)熱應(yīng)激還影響肉仔雞免疫器官的發(fā)育，損傷小腸形態(tài)結(jié)構(gòu)[6]，改變盲腸菌群多樣性[7]。熱應(yīng)激是影響家禽腸道結(jié)構(gòu)和功能的一個(gè)重要因素。熱應(yīng)激影響家禽腸道的形態(tài)以及腸黏膜的完整性。熱應(yīng)激影響腸道的結(jié)構(gòu)可能與多種因素有關(guān)，例如熱應(yīng)激引起的采食量下降、腸道血流量減少等。本文針對(duì)熱應(yīng)激影響家禽腸道結(jié)構(gòu)的研究進(jìn)行總結(jié)，并從采食量、血流量、微生物等方面探討熱應(yīng)激影響家禽腸道的機(jī)制，以期加深對(duì)于熱應(yīng)激影響家禽腸道健康的認(rèn)識(shí)。

1 熱應(yīng)激對(duì)家禽腸道結(jié)構(gòu)的影響

1.1 腸道形態(tài)

環(huán)境高溫影響家禽的腸道絨毛高度。Deng等[8]發(fā)現(xiàn)，34 ℃熱應(yīng)激12 d可導(dǎo)致蛋雞回腸和盲腸絨毛高度縮短。Song等[9]觀察到33 ℃每天應(yīng)激10 h，連續(xù)應(yīng)激20 d，肉雞的空腸絨毛高度縮短。張少帥等[6]發(fā)現(xiàn)，31 ℃應(yīng)激14 d顯著降低了空腸和回腸的絨毛高度。其他研究也在肉雞[10-11]和豬[12-14]上獲得相似發(fā)現(xiàn)。然而Quinteriro-Filho等[15]發(fā)現(xiàn)，31 ℃應(yīng)激10 h對(duì)肉雞空腸絨毛高度沒(méi)有顯著影響。Burkholder等[16]發(fā)現(xiàn)，30 ℃應(yīng)激24 h對(duì)肉雞回腸和盲腸的絨毛高度無(wú)顯著影響。這可能是由于環(huán)境溫度較低或應(yīng)激持續(xù)時(shí)間較短所致。Hao等[17]發(fā)現(xiàn)，36 ℃應(yīng)激5 h對(duì)肉雞空腸絨毛高度沒(méi)有顯著影響，但應(yīng)激10 h后絨毛高度與隱窩深度的比值顯著降低。另外，不同腸段對(duì)于高溫的敏感性可能存在差異。30 ℃應(yīng)激14 d顯著降低了肉雞空腸遠(yuǎn)端絨毛高度，但不影響近端絨毛高度[18]。

環(huán)境高溫影響家禽腸道隱窩深度的報(bào)道不一。Song等[9]觀察到高溫導(dǎo)致肉雞的空腸隱窩深度加深。Quinteriro-Filho等[15]發(fā)現(xiàn)，高溫對(duì)肉雞空腸隱窩深度沒(méi)有顯著影響。而B(niǎo)urkholder等[16]發(fā)現(xiàn)，高溫引起肉雞回腸和盲腸的隱窩深度變淺。Al-Fataftah等[10]同樣發(fā)現(xiàn)，高溫導(dǎo)致肉雞腸道隱窩深度下降。另外在豬上也同樣發(fā)現(xiàn)，高溫導(dǎo)致腸道隱窩變淺[12-13]。高溫對(duì)家禽腸道隱窩深度的不同影響可能與熱應(yīng)激的強(qiáng)度和持續(xù)時(shí)間有關(guān)。Pearce等[14]證明，隨熱應(yīng)激時(shí)間延長(zhǎng)，豬腸道隱窩深度先加深，然后逐漸變淺。

腸道絨毛的高度受到成熟上皮細(xì)胞凋亡脫落、幼稚上皮細(xì)胞遷移以及隱窩干細(xì)胞增殖的共同影響。環(huán)境高溫降低家禽腸道絨毛高度可能與促進(jìn)成熟上皮細(xì)胞的凋亡有關(guān)。Yu等[13]在電子顯微鏡下觀察到，高溫造成豬空腸絨毛頂端損傷，上皮細(xì)胞脫落，導(dǎo)致絨毛高度縮短。Yu等[19]的體外試驗(yàn)也發(fā)現(xiàn)，提高培養(yǎng)溫度可導(dǎo)致腸上皮細(xì)胞(IEC-6)的凋亡增加。腸道隱窩深度可能與隱窩內(nèi)干細(xì)胞的增殖活性有關(guān)。Yamauchi等[20]發(fā)現(xiàn)，腸道隱窩干細(xì)胞的增殖可能對(duì)高溫更加敏感。熱應(yīng)激初期家禽可能通過(guò)代償性的促進(jìn)隱窩內(nèi)干細(xì)胞的增殖活性，以恢復(fù)絨毛頂端上皮細(xì)胞的脫落。隨著家禽逐漸適應(yīng)熱應(yīng)激，隱窩深度可能恢復(fù)，而熱應(yīng)激進(jìn)一步持續(xù)可能由于營(yíng)養(yǎng)攝入減少等原因?qū)е赂杉?xì)胞增殖抑制，隱窩變淺。

1.2 黏膜完整性

環(huán)境高溫影響家禽腸道的絨毛高度和隱窩深度，不僅抑制腸道影響營(yíng)養(yǎng)物質(zhì)的消化、吸收[21]，還會(huì)影響腸道黏膜的完整性，增加病原微生物感染的幾率。黃淑成等[22]研究報(bào)道，38 ℃應(yīng)激10 h后肉雞血漿中內(nèi)毒素的含量呈極顯著的升高。Pearce等[14]也發(fā)現(xiàn)，35 ℃高溫下豬血漿中內(nèi)毒素的含量顯著升高。Hall等[23]和Lim等[24]在小鼠上也有相似發(fā)現(xiàn)。內(nèi)毒素進(jìn)入體內(nèi)后刺激免疫系統(tǒng)，導(dǎo)致血液中白細(xì)胞介素-1(IL-1)、腫瘤壞死因子(TNF)-α等細(xì)胞因子的含量升高[25-26]。Deng等[8]發(fā)現(xiàn)，34 ℃下蛋雞血漿中TNF-α、IL-1的含量顯著升高。Bouchama等[27]在人上也有相似發(fā)現(xiàn)。內(nèi)毒素是來(lái)源于革蘭氏陰性菌細(xì)胞壁脂多糖的大分子復(fù)合物，其相對(duì)分子質(zhì)量約為1×106～20×106，正常情況下只有微量的脂多糖通過(guò)腸道上皮細(xì)胞間的緊密連接或受體介導(dǎo)的胞吞跨細(xì)胞膜轉(zhuǎn)運(yùn)進(jìn)入動(dòng)物體內(nèi)[26]，因此高溫導(dǎo)致家禽血液中內(nèi)毒素和細(xì)胞因子含量的升高，間接表明腸道的完整性受損。Song等[9]利用尤斯灌流室(Ussing chamber)直接證實(shí)，33 ℃熱暴露20 d導(dǎo)致肉雞空腸黏膜通透性顯著增加，表現(xiàn)為跨上皮電阻值(TER)下降，大分子物質(zhì)的滲透性增強(qiáng)。在小鼠和豬上也有相似發(fā)現(xiàn)[14,28-29]。Dokladny等[30]體外研究發(fā)現(xiàn)，提高培養(yǎng)溫度導(dǎo)致Caco-2細(xì)胞之間的緊密連接受損。Yu等[13]通過(guò)電子顯微鏡也觀察到，熱應(yīng)激導(dǎo)致豬空腸細(xì)胞緊密連接形態(tài)發(fā)生改變。上述研究結(jié)果均表明高溫降低了腸道黏膜的完整性。

高溫降低腸道黏膜的完整性可能與肥大細(xì)胞有關(guān)。Deng等[8]發(fā)現(xiàn)，高溫增加了蛋雞腸道上皮組織中肥大細(xì)胞的數(shù)量。肥大細(xì)胞釋放的生物活性物質(zhì)如類(lèi)胰蛋白酶和組胺等可以增強(qiáng)上皮組織的通透性[31-32]。高溫影響?zhàn)つさ耐暾钥赡芘c緊密連接蛋白的表達(dá)和分布有關(guān)。Ikari等[33]體外研究發(fā)現(xiàn)，高溫抑制緊密連接蛋白ZO-1蛋白的表達(dá)，并且誘導(dǎo)ZO-1蛋白由細(xì)胞膜向細(xì)胞質(zhì)轉(zhuǎn)移。Dokladny等[30]也發(fā)現(xiàn)，提高培養(yǎng)溫度降低了ZO-1蛋白的表達(dá)。但Dokladny等[34]發(fā)現(xiàn)，高溫上調(diào)了Occludin蛋白的表達(dá)，推測(cè)可能與腸道上皮代償性的保護(hù)反應(yīng)有關(guān)。Pearce等[14]發(fā)現(xiàn)高溫影響豬腸道ZO-1、Occludin、Claudin 3等緊密連接蛋白mRNA的表達(dá)，表現(xiàn)為先降低后升高的趨勢(shì)，進(jìn)一步證實(shí)了這一推測(cè)。另外，環(huán)境高溫提高家禽血液中IL-1、TNF-α等細(xì)胞因子的含量[8]，影響肌球蛋白輕鏈激酶的表達(dá)[14]，進(jìn)一步引起肌球蛋白輕鏈磷酸化，調(diào)控肌動(dòng)蛋白細(xì)胞骨架的收縮，導(dǎo)致緊密連接打開(kāi)，增加小腸滲透性[35-38]，這可能也是高溫?fù)p傷腸道黏膜完整性的機(jī)制之一。

高溫影響腸上皮黏膜的完整性，增加了病原菌感染的幾率。Burkholder等[16]觀察到，30 ℃熱暴露24 h會(huì)增加肉雞腸道中沙門(mén)氏菌的附著。Quinteiro-Filho等[39-40]發(fā)現(xiàn)熱應(yīng)激提高沙門(mén)氏菌在肉雞盲腸和嗉囊上的定植，以及移位進(jìn)入肉雞的脾臟、肝臟和骨髓中，表明高溫降低了肉雞對(duì)沙門(mén)氏菌感染的抵抗。另外，由于上皮完整性的受損，內(nèi)毒素進(jìn)入家禽的循環(huán)系統(tǒng)，進(jìn)一步激活局部和系統(tǒng)免疫，使能量和營(yíng)養(yǎng)物質(zhì)由生長(zhǎng)轉(zhuǎn)向產(chǎn)生急性期蛋白和其他免疫調(diào)控因子，從而抑制畜禽生長(zhǎng)[41-42]，這可能是高溫影響家禽健康和生長(zhǎng)的關(guān)鍵原因。

2 熱應(yīng)激影響家禽腸道功能

2.1 采食量下降

環(huán)境高溫對(duì)于腸道結(jié)構(gòu)的影響可能與高溫降低采食量有關(guān)。張彩霞等[43]發(fā)現(xiàn)，限飼70%顯著降低了肉雞十二指腸絨毛高度。但劉路路等[44]發(fā)現(xiàn)，同樣限飼70%并沒(méi)有顯著影響黃羽肉雞十二指腸、空腸和回腸的絨毛高度和隱窩深度，這可能因?yàn)辄S羽肉雞生長(zhǎng)速度較慢，對(duì)于短時(shí)間限飼不敏感。Yamauchi等[45]發(fā)現(xiàn)，饑餓應(yīng)激會(huì)導(dǎo)致蛋雞十二指腸和空腸絨毛高度降低。Nuez等[46]發(fā)現(xiàn)，60%限飼顯著降低了仔豬小腸絨毛高度和隱窩深度。Ferraris等[47]總結(jié)了限飼或營(yíng)養(yǎng)不足對(duì)于腸道的影響，認(rèn)為限飼嚴(yán)重影響腸道黏膜的結(jié)構(gòu)和轉(zhuǎn)運(yùn)功能，增加腸道對(duì)于大分子的滲透性，導(dǎo)致腸道絨毛的萎縮。Garriga等[18]研究了高溫對(duì)肉雞腸道結(jié)構(gòu)和功能的影響，同時(shí)利用采食量配對(duì)的方法研究采食量降低的效應(yīng)。研究發(fā)現(xiàn)，采食配對(duì)組同樣降低了肉雞空腸遠(yuǎn)端的絨毛高度。Pearce等[14]在豬上的研究也發(fā)現(xiàn)了相似結(jié)果，且采食配對(duì)組脂多糖的滲透率有升高趨勢(shì)。這些研究結(jié)果表明，熱應(yīng)激對(duì)于腸道結(jié)構(gòu)的影響部分是由于采食量下降引起的。

2.2 體溫升高

環(huán)境高溫對(duì)于腸道結(jié)構(gòu)的影響可能與動(dòng)物體溫升高有關(guān)。體外研究發(fā)現(xiàn)，提高培養(yǎng)溫度顯著抑制上皮細(xì)胞IEC-6的增殖，誘導(dǎo)上皮細(xì)胞的凋亡[19]，影響Caco-2細(xì)胞之間的緊密連接[27]。熱應(yīng)激導(dǎo)致豬[13]和大鼠[19]的直腸溫度升高。推測(cè)直腸溫度升高可能影響腸道上皮細(xì)胞的增殖和緊密連接，誘導(dǎo)上皮細(xì)胞凋亡，從而影響家禽腸道結(jié)構(gòu)。另外，Bouchama等[27]觀察到中暑病人直腸溫度升高，血液中TNF、IL-1和內(nèi)毒素含量均顯著升高，而體溫下降后TNF、IL-1和內(nèi)毒素的含量也隨之下降，這一發(fā)現(xiàn)間接表明體溫升高可能與腸道結(jié)構(gòu)變化有關(guān)。

2.3 腸道血流量減少

高溫環(huán)境下，動(dòng)物為了增加散熱，提高體表的血流量，導(dǎo)致腸道等組織的血流量下降[48-49]。血流量長(zhǎng)時(shí)間減少可能引起腸道上皮細(xì)胞缺氧[23]、ATP耗竭、乳酸積聚、細(xì)胞功能紊亂，最終導(dǎo)致上皮細(xì)胞壞死和脫落，降低腸道絨毛高度，損害腸道上皮的完整性[38,48]。

2.4 腸道微生物

環(huán)境高溫對(duì)于腸道的影響可能與腸道微生物有關(guān)。彭騫騫等[7]采用16S rDNA PCR-變性梯度凝膠電泳(DGGE)技術(shù)，發(fā)現(xiàn)31 ℃持續(xù)高溫影響肉雞盲腸菌群的結(jié)構(gòu)和多樣性。隨熱應(yīng)激持續(xù)時(shí)間延長(zhǎng)，對(duì)蛋雞十二指腸、空腸和回腸優(yōu)勢(shì)細(xì)菌菌群組成的影響越顯著，同時(shí)腸道絨毛高度和隱窩深度下降也越明顯[50]。熱應(yīng)激減少肉雞腸道中腸桿菌科的數(shù)量，增加鏈球菌屬和葡萄球菌屬的數(shù)量[51]，增加沙門(mén)氏菌等病原菌在腸道中的定植[16,39-40]。腸道中的病原菌可以刺激腸道免疫細(xì)胞和上皮細(xì)胞分泌炎性細(xì)胞因子如TNF、IL-1等，進(jìn)一步引起肌球蛋白輕鏈磷酸化，導(dǎo)致小腸上皮緊密連接打開(kāi)，增加小腸滲透性[35-36]。Song等[9]研究發(fā)現(xiàn)，高溫降低了腸道中乳酸桿菌和雙歧桿菌的數(shù)量，增加大腸桿菌和梭菌的數(shù)量，而高溫環(huán)境下飼喂益生菌，增加了肉雞腸道中乳酸菌和雙歧桿菌數(shù)量，同時(shí)也提高了肉雞腸道絨毛高度，促進(jìn)緊密連接蛋白的表達(dá)，表明高溫對(duì)肉雞腸道結(jié)構(gòu)和功能的影響可能與腸道微生物組成變化有關(guān)。目前有關(guān)高溫影響腸道微生物組成的研究相對(duì)較少，對(duì)于高溫通過(guò)微生物影響腸道結(jié)構(gòu)和功能的機(jī)制還不清楚。

3 小 結(jié)

綜上所述，熱應(yīng)激影響家禽腸道的結(jié)構(gòu)，降低腸黏膜的完整性，抑制腸道免疫功能。熱應(yīng)激對(duì)家禽腸道的影響可能和采食量降低、體溫升高、腸道血流量減少以及腸道微生物改變有關(guān)。熱應(yīng)激影響家禽腸道的結(jié)構(gòu)和功能，進(jìn)一步影響家禽的生長(zhǎng)和健康。

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