綿羊和山羊住肉孢子蟲流行病學及分型研究進展

董 輝，陸瑤瑤，楊玉榮

DOI：10.3969/j.issn.1002-2694.2017.09.014

綿羊和山羊住肉孢子蟲流行病學及分型研究進展

董 輝，陸瑤瑤，楊玉榮1

動物住肉孢子蟲病可引起畜牧養殖業的經濟損失，影響食品質量安全，威脅人類健康。國際上已確定的綿羊(Ovisaries)住肉孢子蟲有4種：S.tenella、S.arieticanis、S.gigantea、S.medusiformis，山羊(Caprahircus)住肉孢子蟲有3種：S.capracanis、S.hircicanis、S.moulei。本文綜述綿羊和山羊住肉孢子蟲的生活史、國內和國際的流行情況、致病性、形態學特點和診斷方法，以期為中國綿羊和山羊住肉孢子蟲的生物學特征研究及其診斷分型提供有力基礎依據。

住肉孢子蟲；綿羊；山羊；流行病學；形態學；分型; 分子生物學

住肉孢子蟲(Sarcocystis)為頂復亞門，孢子蟲綱，真球蟲目，肉孢子蟲科，孢子蟲屬的一種原生性細胞內寄生蟲[1]。住肉孢子蟲在世界分布廣泛，人畜均會感染[2]。1843年Miescher第1次在鼠橫紋肌中發現了白色線狀的住肉孢子蟲包囊[3-4]，到目前為止在動物中一共發現有196種住肉孢子蟲[5]。住肉孢子蟲具有嚴格的宿主選擇性，其生活史需要在中間宿主和終末宿主中完成，中間宿主多為草食動物或者雜食動物，終末宿主多為肉食動物[6-7]。住肉孢子蟲可以在豬、牛和羊等中間宿主的肌肉形成包囊[8]，住肉孢子蟲蟲型和感染數量的不同，其致病性也具有明顯的差異，可引起家畜的厭食、流產、甚至死亡，人食用含住肉孢子蟲的肉后，會引起胃腸道疾病。羊住肉孢子蟲病可引起畜牧業經濟損失，降低肉品質量，危害公共健康[9]。本文綜述我國和國際上已確定的綿羊和山羊住肉孢子蟲的流行情況、生活史、形態學特點和分型、致病性以及分子學診斷方法，為深入研究國內綿羊和山羊住肉孢子蟲生物學特征提供有力依據。

1 生活史

住肉孢子蟲與哈蒙球蟲、弓形蟲和新孢子蟲的[10-12]生活史十分相似，分為有性生殖和無性生殖。以S.tenalla的生活史為例解釋綿羊和山羊住肉孢子蟲的生活史[4]。當犬科動物食入含有S.tenella包囊的組織后，包囊在胃和小腸內消化釋放出緩殖子，緩殖子在侵入小腸粘膜的過程中非常有活力，攝入包囊6 HPI(hours post inoculation)，可以在杯狀細胞內發現緩殖子。然后，緩殖子進入配子生殖階段，發育為雌、雄配子，其數量比約為95∶5，雌配子和雄配子受精后產生合子，合子外分泌囊壁形成卵囊。卵囊在腸壁內進行孢子化，每個孢子化的卵囊內含有兩個孢子囊，每個孢子囊內形成4個子孢子。孢子化的卵囊壁薄，易于破裂，游離的孢子囊會進入腸腔，隨終末宿主的糞便排出到外界的環境中[1]。當中間宿主綿羊誤食飼料和水中攜帶的S.tenella的卵囊，卵囊進入小腸后釋放出的子孢子經腸系膜和腸系膜淋巴結動脈，進入全身動脈血管內皮細胞完成第一代裂殖生殖(9～21 DPI)，然后進入全身毛細血管完成第二代裂殖生殖(16～40 DPI)，蟲血癥時間為14～32 DPI，然后裂殖子進入中樞神經組織、心臟形成包囊。

2 流行病學

2.1 世界各國的感染情況 綿羊和山羊住肉孢子蟲病在世界分布廣泛，文獻統計綿羊住肉孢子蟲病陽性率為31.42%～93.31%，山羊住肉孢子蟲病陽性率為28.30%～83.69%。國際上廣泛承認和確定的綿羊住肉孢子蟲有4種，S.tenella、S.arieticanis、S.gigantea、S.medusiformis。目前S.tenella、S.gigantea、S.arieticanis世界廣泛分布，S.medusiformis只在澳大利亞、新西蘭、伊朗和意大利有報道[7]。國際上廣泛承認和確定的山羊住肉孢子蟲有S.capracanis、S.hircicanis、S.moulei。山羊住肉孢子蟲在歐洲和北美洲文獻報道尚少。世界綿羊和山羊住肉孢子蟲感染和分布情況詳見表1。

表1 世界綿羊及山羊住肉孢子蟲病流行情況
Tab.1 Prevalence of Sarcocystis in sheep or goats from the world

宿主Host位置Location陽性率Positive%蟲型Species參考文獻References綿羊大洋洲93.31(990/1061)S.tenella、S.arieticanis、S.gigantea、S.medusiformis[1]歐洲31.42(3158/10051)S.tenella、S.arieticanis、S.gigantea、S.medusiformis[1,7][13]非洲54.67(621/1136)S.tenella、S.arieticanis[1]南美36.22(343/947)S.tenella、S.arieticanis、S.gigantea[1,14][12,15]北美67.40(1141/1693)S.tenella、S.arieticanis、S.gigantea[1]亞洲48.02(26061/54270)S.tenella、S.arieticanis、S.gigantea、S.medusiformis[1,4,8,10,16-87]山羊大洋洲28.33(17/60)—[1]非洲76.80(907/1181)S.capracanis[1]南美83.69(585/699)S.capracanis[1,14]亞洲53.89(5522/10246)S.capracanis、S.hircicanis、S.moulei[1,5,6,8,20,26,33,50,51,61,73,80,84,88-91]

2.2 在我國的流行情況 我國已確定的綿羊住肉孢子蟲有3種：S.tenella、S.arieticanis、S.gigantea，已確定的山羊住肉孢子蟲有3種：S.hircianis、S.capracanis、S.moulei。綿羊住肉孢子蟲病的陽性率在7.74%～100%，山羊住肉孢子蟲病的陽性率在9.73%～77.94%。根據已報道的綿羊和山羊住肉孢子蟲病的流行病學調查，統計中國綿羊和山羊的住肉孢子蟲病的分布情況，發現中國多地區羊感染住肉孢子蟲，且感染率較高，見表2。

表2 中國綿羊和山羊住肉孢子蟲流行病學調查
Tab.2 Epidemiological investigation of Sarcocystis in sheep and goats of China

宿主Host地區Region年份Year陽性率Positive%蟲型Species被檢組織Tissue檢測方法Method參考文獻Reference綿羊北京、河北199954.50(12/22)——MS,EM[26]甘肅19807.74(1152/14891)—MMS[80]黑龍江198591.82(359/391)—D,HGR,MS[81]河南1988-201611.60(105/905)S.arieticanis,S.tenellaD,E,H,MGR,MS,PS[25,48]遼寧1993-200027.83(59/212)—D,E,H,MGR,MS[43-45,82]內蒙199957.14(44/77)——MS,EM[26]青海1983-201561.34(7490/12210)S.tenella,S.gigantea,S.arieticanisD,E,H,MGR,PS,PS[27-31,36,37,39-42,46,47,49-74,76-79,83-87]新疆1985-199082.77(5418/6546)S.arieticanisD,H,S,M,GR,MS,PS[32-35,38,75]山羊北京、河北199957.60(19/33)——MS,EM[26]甘肅19809.73(114/1172)—MMS[80]內蒙199933.30(12/36)——MS,EM[26]青海1983-201373.52(261/355)S.mouleiD,E,H,MGR,MS[50,51,61,73,84,91]新疆1987-198842.00(5/12)—HMS[33]云南1999,201677.94(212/272)S.hircianis,S.capracanis—MS,PS,EM[5,26]

D: diaphragm 膈肌; E: esophagus 食道肌; H: heart 心肌; M: skeletal muscle 骨骼肌; —:未報道;

EM: electron microscope 電子顯微鏡; GR: Gross 肉眼觀察; MS: muscle squash 肌肉壓片; PS: paraffin section 石蠟切片

3 致病性

綿羊住肉孢子蟲S.tenella和S.arieticanis的終末宿主為犬科動物[7](表3)。S.tenella強致病性，綿羊感染后會出現厭食、體重減輕、貧血、產奶量降低、早產、流產、神經癥狀和死亡等[15,21]。S.arieticanis的致病性稍弱于S.tenalla[21]，感染S.arieticanis可以引起綿羊腹瀉、食欲下降、失去活動精神、毛發減少、虛弱等[4]。S.gigantea和S.medusiformis的終末宿主是貓科動物，對綿羊無致病性[7]，當組織間寄生的住肉孢子蟲包囊破裂時，引起肌肉的炎癥反應將影響肉的品質[15]。山羊住肉孢子蟲中，S.capracanis和S.hircicanis的終末宿主是犬科動物，S.capracanis致病性強于S.hircicanis，可以引起山羊體溫升高、體重減輕、流產和死亡[6]。S.moulei的終末宿主是貓科動物，無致病性[6]。

綿羊和山羊住肉孢子蟲對中間宿主的致病性高于終末宿主，通過犬科動物傳播的住肉孢子蟲的致病性要強于通過貓科動物傳播住的肉孢子蟲(對比見表3)。對于強致病性的S.tenella和S.arieticanis引起的羊住肉孢子蟲病，其感染嚴重程度與最初卵囊的攝入量、宿主的免疫狀態及營養狀態有關[4,7]，但強致病性的綿羊和山羊住肉孢子蟲對人沒有致病性。綿羊可以同時感染兩種類型的住肉孢子蟲(有致病性和無致病性的蟲型)[7]。

4 形態學特征

4.1 光學顯微鏡下的形態結構 很難根據臨床癥狀診斷住肉孢子蟲病[21]。2016年，Damboriarena就報道了綿羊食道肌大量隨機分布的白色橢圓形的S.gigantea包囊[15]，因為綿羊和山羊住肉孢子蟲的包囊通常寄生在肌肉組織。住肉孢子蟲與肌纖維平行，形態呈紡錘形、圓柱形、卵圓型等，顏色呈灰白色、乳白色。S.gigantea和S.medusiformis包囊可以通過肉眼觀察，S.tenella和S.arieticanis的包囊需要通過顯微鏡觀察。山羊住肉孢子蟲包囊均可以通過肉眼觀察。

蛋白酶可以將肌組織和包囊壁消化破解，釋放緩殖子，緩殖子呈月牙或香蕉型，通過光學顯微鏡可以檢查住肉孢子蟲的緩殖子[19,21]；組織學壓片技術可以觀察到宿主肌肉組織中非肉眼可見的住肉孢子蟲包囊[21]，當住肉孢子蟲的感染密度高時，組織學壓片方法優于其它方法[14]，住肉孢子蟲對宿主選擇和在組織器官內分布均有特異性，用光學顯微鏡觀察H&E染色的切片可以判定住肉孢子蟲包囊壁的薄厚并觀察包囊壁內的緩殖子[21]，所以結合組織學方法可以對住肉孢子蟲進鑒別和分型[25]。比如綿羊住肉孢子蟲中S.tenella是厚壁的住肉孢子蟲，寄生于綿羊的心肌和舌肌，S.arieticanis是薄壁的住肉孢子蟲，寄生于心肌，而S.gigantea和S.medusiformis為薄壁的住肉孢子蟲未寄生于心肌。

4.2 超微結構 住肉孢子蟲包囊壁由兩層構成，包囊外有囊壁和突起(Villar protrusions, VP)，內壁向內延伸形成隔，將囊腔分成小室，小室內有大量香蕉狀或腎形的緩殖子和母細胞。包囊壁的超微結構在不同類型的住肉孢子蟲中具有明顯的區別，目前為止住肉孢子蟲包囊壁的種類至少已有82種[1]。不同住肉孢子蟲包囊壁VP的類型有較大差別[1]，所以通過電子顯微鏡對比超微結構的差異是對住肉孢子蟲分型的一種有效方法[4]，也是住肉孢子分類學中最為認可的手段[7]。綿羊和山羊住肉孢子蟲形態特征見表3[1,5]。

表3 綿羊及山羊住肉孢子蟲形態特征
Tab.3 Morphology of the Sarcocystis in the sheep or goats

蟲型Species宿主Host肉眼Gross包囊大小和壁厚度Cystssize(mm)andWal(μm)突起類型Villarprotrusions分布Distribution致病性Pathogenicity膈肌D心肌H中樞神經系統CNS綿羊或山羊SheeporGoat人Human終末宿主DefinitiveHostsS.gigantea綿羊可見7.5×5薄壁<2Type21:菜花狀有無無無無家貓S.medusiformis可見8×0.2薄壁<2Type20:四邊形有無無無無家貓S.tenella不可見最長0.7厚壁1～3Type14:柵欄狀無有有強無家犬、狼、狐S.arieticanis不可見最長0.9薄壁<1Type7b:細絲狀有有無較強無家犬S.capracanis山羊可見1×0.1厚壁2-3Type14:柵欄狀有有有有無家犬、狼、狐S.hircicanis可見最長2.5薄壁<1Type7a:細絲狀有有無無無家犬S.moulei可見17×7厚壁3～4Type21:菜花狀有無無—無家貓

D: diaphragm 膈??；H: heart 心肌；CNS: central nervous system 中樞神經系統；S: sheep 綿羊；G: goat 山羊；Hu: human 人；—: 未報道

5 分子生物學分型

近年來隨著分子生物學技術的發展，關于住肉孢子蟲基因序列的研究主要集中在分子流行病學調查、分型研究和種系發育。目前，通過核糖體小亞基(18S rRNA)、核糖體大亞基(28S rRNA)鑒別住肉孢子蟲較為普遍[7]。內轉錄間隔區-ITS(Internal transcribed spacer)、線粒體細胞色素氧化酶Ⅰ-cox1(Cytochrome C oxidase subunit I)[5,93]也是良好的基因序列研究的選擇。已報道的關于綿羊和山羊住肉孢子蟲PCR引物序列，見表4。

6 討 論

國內對于住肉孢子蟲病的研究多集中在黃牛[94]、水牛，關于綿羊和山羊住肉孢子蟲的研究多集中于流行病學方面的研究，關于其生活史和其它生物學特征尚未完全證實。研究住肉孢子蟲，一方面是探究住肉孢子蟲的整體感染情況、季節動態變化、地理區域分布，另一方面是明確我國存在的住肉孢子蟲，對其分型，從而提高流行病學調查的信息多樣性和準確性，確定是否會對畜牧業及人類的食品安全造成威脅并有效控制該病。

表4 綿羊和山羊住肉孢子蟲PCR引物序列
Tab.4 Sequences of PCR primers of Sarcocystis in sheep or goats

序號NO.檢測方法Methods引物Primer片段大小Size(bp)蟲型Species參考文獻References1PCRSAD2F(5'-GGAAGCGATTGGAACC-3')300-350S.capracanis[6]18SrRNASAD2R(5'-CCTTGGTCCGTGTTTCA-3')2PCR1L(5'-CCATGCATGTCTAAGTATAAGC)-3')800S.tenella[14,88]3H(5'-GGCAAATGCTTTCGCAGTAG-3')3PCR-RFLPForward(5'-TTCTATGGCTAATACATGCG-3')722and242S.gigantea[19]Reverse(5'-CCCTAATCCTTCGAAACAGGA-3')901and63S.medusiformis4PCRForward(5'-CGCAAATTACCCAATCCTGA-3')700S.tenellaorS.arieticanis[12]Reverse(5'-ATTTCTCATAAGGTGCAGGAG-3')5Nest-PCRAP2(5'CCCGGGATCCAAGCTTGATCCTTCTGCAGGTTCACCTAC-3')530S.tenella[92]18SrRNAnested(5'-TTTGACTCAACACGGG-3')ST3(5'-CGTTGCCGCGCGTTAA-3')externalST1(5'-GGATCGCATTATGGTCAT-3')6Nest-PCRexternalSTA(5'-TTTCGCAAGGAAGAGGA-3')andSA2(5'-TGAAACGGCGCGTAGA-3')375S.arieticanis[92]18SrRNAinternal(5'-AGGGTTCGATTCCGGAG-3')SA1(5'-GCGGGAAGAGGAGAAT-3')7RT-PCRSar-F1(5'-GCACTTGATGAATTCTGGCA-3')600S.tenella[17]Sar-R1(5'-CACCACCCATAGAATCAAG-3')Sar-antisense:(5'-CCCTAATCCTTCGAAACAGGA-3')

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EpidemiologyandclassificationofSarcocystisinsheepandgoat

DONG Hui, LU Yao-yao, YANG Yu-rong

(CollegeofAnimalScienceandVeterinaryMedicine,HenanAgriculturalUniversity,Zhengzhou450002,China)

Sarcocystiscould cause significant economic losses of animal husbandry, and threaten to public health and the quality of food safety.S.tenella,S.arieticanis,S.giganteaandS.medusiformisare four speciesSarcocystisin sheep (Ovisaries). WhileS.capracanis,S.hircicanisandS.mouleiare three species ofSarcocystisin goat (Caprahircus). The life cycle, epidemiological, pathogenicity, morphological characteristics and diagnostic methods of sheep and goats were reviewed in this paper. The research of biological characteristics ofSarcocystisprovides a powerful basis for diagnosis in sheep and goat in China.

Sarcocystis; sheep; goat; epidemiology; morphology; classification; molecular biology

Yang Yu-rong, Email: yangyu7712@sina.com

國家重點研發計劃(2016YFD0500707)，河南省高校科技創新人才支持計劃(17HASTIT038)資助項目

楊玉榮, yangyu7712@sina.com

河南農業大學牧醫工程學院, 鄭州 450002

R382.3

：A

：1002-2694(2017)09-0828-09

2017-03-23編輯：劉岱偉

Supported by the National Key Research and Development Program of China (No. 2016YFD0500707) and the Program for Science and Technology Innovation Talents in Universities of Henan Province (No. 17HASTIT038)