鳥類弓形蟲基因型研究進展

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剛地弓形蟲(Toxoplasmagondii)是地域分布廣、宿主多、生活史復(fù)雜、危害大的一種重要人獸共患寄生蟲。據(jù)估計全世界約有1/3的人感染弓形蟲[1]。鳥類、嚙齒類、哺乳類，甚至海洋動物皆可作為弓形蟲的宿主[2]。人體弓形蟲感染主要有3種途徑：攝入含有包囊的生的或未熟肉類；食入被卵囊污染的食物或飲水；以及經(jīng)胎盤的垂直傳播。由于感染率之高，剛地弓形蟲在歐美被列為繼沙門菌(Salmonella)和李斯特菌(Listeria)之后的第三大致死性食源性疾病的病原體[3]。一個多世紀(jì)以來，研究人員對弓形蟲的研究熱情始終不減，一是因為弓形蟲引起的家養(yǎng)動物(如羊、豬、牛、雞等)的疾病和流產(chǎn)導(dǎo)致重大的經(jīng)濟損失，嚴(yán)重影響制約畜牧養(yǎng)殖業(yè)的發(fā)展；二是感染動物成為人獸共患病的感染來源，危害公共衛(wèi)生安全；三是免疫力低下人群(HIV/AIDS患者、惡性腫瘤長期化療患者等)的隱性感染可激活為急性活動性感染并引發(fā)腦炎、肺炎和眼病等嚴(yán)重疾病，可導(dǎo)致患者死亡；孕期感染弓形蟲可致不良妊娠結(jié)局或新生兒先天性弓形蟲?。凰氖枪蜗x生活史需要轉(zhuǎn)換宿主，各生活史階段的蟲體形態(tài)不同，為研究寄生物與宿主/細(xì)胞之間的相互作用提供了良好模型[4]。

隨著弓形蟲的基因組測序的完成，以及人獸分離株的逐漸增多，已發(fā)現(xiàn)各地區(qū)的人獸分離蟲株存在種內(nèi)遺傳結(jié)構(gòu)(基因型)差異。目前為止，弓形蟲數(shù)據(jù)庫中已經(jīng)報告并記錄的基因型有232個(http://toxodb.org/toxo)。分型所用方法多采用多位點 PCR-RFLP，遺傳標(biāo)志從早年的1-6個，到目前[SAG1，(5′+3′)SAG2，SAG3，BTUB，GRA6，c22-8，c29-2，L358，PK1和Apico]10個位點。針對于國內(nèi)外的研究者用于蟲體分離的宿主標(biāo)本多包括野生動物(高原鼠兔和野鼠)、流浪貓、家兔、家豬、市售豬肉、寵物犬以及人體等，鳥類的弓形蟲株基因型報道總體相對較少。自2003年起，Dubey等針對于分布于全球不同國家和地區(qū)的散養(yǎng)家雞的流行情況、基因型進行一些研究報道。人工養(yǎng)殖的雞、鴨、鵝、鴿子以及鵪鶉、鴕鳥、寵物鳥等有少量報道。近年來，Su等對黑雁(Brantacanadensis)、疣鼻天鵝(Cygnusolor)等有遷徙習(xí)性珍稀候鳥極少報道。在中文文獻數(shù)據(jù)庫中尚未對于鳥類弓形蟲基因型的綜述文獻，本文針對目前報道的家養(yǎng)禽類、觀賞鳥類，以及自然野生珍稀鳥類的弓形蟲株基因型做簡要概述，為鳥類弓形蟲株種群結(jié)構(gòu)信息提供參考。

1 家養(yǎng)禽類弓形蟲株基因型

目前，針對于散養(yǎng)家雞的報道相對于其他鳥類較多。自2003年起，Dubey等開始對散養(yǎng)家雞(Gallusdomesticus)弓形蟲的流行情況、遺傳基因進行研究，樣本來源于巴西、美國、墨西哥、葡萄牙、印度、伊朗、剛果、馬里等分布于世界南美洲、北美洲、歐洲、亞洲、非洲五大洲的國家和地區(qū)。來自全球的22個國家散養(yǎng)家雞的弓形蟲流行情況，文中報道的檢測方法大多運用Dubey建立的改良凝集試驗(MAT)，通過采集雞大腦、心臟和血液等組織和成分，進行抗體水平測定。本文所收集總的報道有4120個樣本，其中總的陽性樣本為1460個，平均陽性感染率44.1%。其中，按照區(qū)域來分，五個大洲的平均陽性感染率依次為南美洲(54.0%)、北美洲(46.1%)、歐洲(42.5%)、非洲(33.3%)、亞洲(31.3%)。針對于全球五個大洲散養(yǎng)家雞的弓形蟲感染陽性率比較分析可以看出，美洲、歐洲地區(qū)相對偏高，非洲、亞洲相對偏低。綜合分析可能有以下原因：一是歐美國家和地區(qū)生活人口的飲食習(xí)慣和生活方式不同，人的弓形蟲感染率高于亞非地區(qū)；二是歐美國家和地區(qū)由于研究鳥類弓形蟲起步較早，研究的范圍、發(fā)表論文和報道數(shù)據(jù)要多于亞非國家和地區(qū)?？傮w而言，散養(yǎng)家雞的弓形蟲感染率相對較高，平均約為50%，特別是在一些農(nóng)村衛(wèi)生條件差，散養(yǎng)家禽和貓等多種動物混養(yǎng)的地區(qū)更高。弓形蟲是一種土源性、食源性寄生蟲，貓為其終末宿主，散養(yǎng)在空曠土地上的家雞因為貓的活動、土壤啄食、混合飲水等途徑感染，嚴(yán)重危害公共衛(wèi)生安全，須引起高度重視。此外，值得一提的是，本文中所參考的文獻，對于鳥類弓形蟲研究，在采集樣本時多選取鳥類的腦、心臟、血液等組織和成分，因弓形蟲在這幾個組織和成分相對富集，獲取蟲體的概率相對較高。

全球南美洲、北美洲、歐洲、亞洲、非洲五個大洲報道的關(guān)于散養(yǎng)家雞的弓形蟲感染基因型多為常見經(jīng)典的Ⅰ型、Ⅱ型和Ⅲ型，來自全球的22個國家和地區(qū)，除歐洲、亞洲地區(qū)沒有出現(xiàn)Ⅰ型弓形蟲外，當(dāng)?shù)厣B(yǎng)家雞弓形蟲感染均存在Ⅰ型、Ⅱ型和Ⅲ型，其中南美洲的巴西、智利分別出現(xiàn)Ⅰ-Ⅱ型、Ⅰ-Ⅲ型弓形蟲混合基因型，非洲的烏干達同時出現(xiàn)Ⅰ-Ⅱ-Ⅲ和Ⅰ-Ⅱ型弓形蟲混合基因型，歐洲的葡萄牙報道出現(xiàn)獨特的基因型模式弓形蟲感染(ToxoDB:#254)?；旌匣蛐秃头堑湫突蛐筒挥嬋雰?nèi)，從Ⅰ型、Ⅱ型和Ⅲ型占比情況來看，南美洲Ⅰ型、Ⅱ型和Ⅲ型數(shù)量為84、29、77，Ⅰ型、Ⅲ型可能為優(yōu)勢基因型。北美洲Ⅰ型、Ⅱ型和Ⅲ型數(shù)量為16、9、64，Ⅲ型遠(yuǎn)超其他基因型。歐洲沒有報道Ⅰ型，Ⅱ型、Ⅲ型數(shù)量為51、8，Ⅱ型的數(shù)量遠(yuǎn)遠(yuǎn)多于Ⅲ型。亞洲、非洲地區(qū)Ⅲ型的數(shù)量居多。從全球五大洲的數(shù)量綜合來看，Ⅰ型、Ⅱ型、Ⅲ型分別為101、111、230，Ⅰ型、Ⅱ型持平，Ⅲ型約為Ⅰ型、Ⅱ型的兩倍，Ⅲ型可能為全球散養(yǎng)家雞感染弓形蟲的優(yōu)勢基因型(表1)。

目前，除散養(yǎng)家雞外，人工養(yǎng)殖的禽類主要有散養(yǎng)家鴨、家鵝、鵪鶉、鴕鳥等，對于禽類的報道非常少，對于來自埃及、伊朗、馬來西亞、美國、中國五個國家報道的散養(yǎng)家鴨、家鵝主要的弓形蟲基因型為Ⅰ型、Ⅱ型、Ⅲ型。Casagrande等[35]報道在巴西農(nóng)場養(yǎng)殖的鵪鶉的弓形蟲基因型為#87。Langoni等[36]發(fā)現(xiàn)屠宰場的鴕鳥基因型為#206，與一個先前報道引起巴西患者先天性弓形蟲病(tgosbr1，ToxoDB#206)的基因型一致，支持了鴕鳥為弓形蟲污染環(huán)境的哨兵。Zhu等[37]報道中國常見的鵪鶉感染弓形蟲的基因型為Toxo#9，與中國哺乳動物、嚙齒類動物感染的主要優(yōu)勢基因型Chinese 1，即Toxo#9一致，為監(jiān)測和控制鵪鶉的弓形蟲的感染情況提供依據(jù)(表2)。

表1 全球分布散養(yǎng)家雞的弓形蟲病流行情況和基因型概況
Tab.1 Prevalence and genotype of toxoplasmosis in free-range chickens (Gallus domesticus) distributed around the world

LocationTimeSampleRatioRateGenotypeRatioToxoDBReferenceBrazil2003H，BR16/4040．0%I/Ⅲ7/6Dubeyetal[5]Brazil2003H67/9669．8%I/Ⅲ34/13Dubeyetal[6]Brazil2006H，BR15/2853．6%I/Ⅲ/I?Ⅱ17/1/3Brandaoetal[7]Brazil2006H，BR33/5066．0%I/Ⅲ14/10Dubeyetal[8]Brazil2007H，BR39/8446．4%——Dubeyetal[9]Brazil2010H42/5084．0%Ⅱ/Ⅲ5/15#59/#62Dubeyetal[10]Argentin2003H，BR19/2965．5%I/Ⅱ/Ⅲ1/1/7Dubeyetal[11]Argentin2005H25/6141．0%I/Ⅱ/Ⅲ4/3/10Dubeyetal[12]Peru2004H13/5026．0%I/Ⅲ7/3Dubeyetal[13]Chile2006H，BR47/8555．3%Ⅱ/Ⅲ/I?Ⅲ17/4/1Dubeyetal[14]Guyan2007H，BR50/7665．8%I/ⅢDubeyetal[15]Venezuela2005H，M16/4634．8%Ⅱ/Ⅲ3/10Dubeyetal[16]AmericaH，BR，BL，20/11816．9%Ⅱ/Ⅲ5/14Dubeyetal[17]America2006H，BR60/14441．7%I/Ⅲ5/1Dubeyetal[18]America2006H，BR84/9885．7%I/Ⅱ/Ⅲ6/3/6Dubeyetal[19]Mexico2004H，BR，BL13/2086．3%I/Ⅲ1/5Dubeyetal[20]Grenada2005H，M53/10252．0%I/Ⅱ/Ⅲ5/1/29Dubeyetal[21]Guatemala2005H，BR，M37/5074．0%I/Ⅲ3/5Dubeyetal[22]Austria2005H302/83036．4%Ⅱ33Dubeyetal[23]Portugal2006H，M61/22527．1%Ⅱ/Ⅲ8/4Dubeyetal[24]Portugal2015BRⅡ/Ⅲ/A7/4/4#1#3/#2Vermaetal[25]Italy2008H，BR41/6464．1%II3Dubeyetal[26]India2003H，BR，BL，133/74117．9%Ⅱ/Ⅲ2/5#1/#2Dubeyetal[27]SriLanka2005H，BR39/10039．0%Ⅱ/Ⅲ6/6Dubeyetal[28]Iran2007H，M23/4551．1%Ⅲ6Ziaetal[29]Iran2013T41/24117．0%Ⅱ/Ⅲ8/33Khademvatetal[30]Egypt2003H，BR，BL49/12140．5%Ⅱ/Ⅲ3/17Dubeyetal[31]Congo2005H，M25/5050．0%I/Ⅱ/Ⅲ1/1/8Dubeyetal[32]Mali2005H，BR5/4810．4%Ⅱ/Ⅲ2/4Dubeyetal[32]Kenya2005BR4/3013．3%Ⅱ1Dubeyetal[32]Ugandan2008BR40/8547．1%I?Ⅱ?Ⅲ/I?Ⅱ2/3Lindstrometal[33]Ethiopia2013H48/12538．4%Ⅱ1#1Tilahunetal[34]Total1460/412044．1%I/Ⅱ/Ⅲ101/111/230

Note: H, Heat; BR, Brain; BL, Blood; M, Muscle; A, Atypical; -, Mixed genotype.

表2 主要禽類的弓形蟲基因型
Tab.2 Genotype of Toxoplasma gondii in main birds

HostLocationTimeTissueGenotypeToxoDBReferenceDucksEgypt2003H，BR，BL，ⅢDubeyetal[31]DucksIran2007H，MⅢZiaetal[29]DucksMalaysi2013I/ⅡPuvanesuaranetal[38]DomesticgooseUSA2007H，BR，BLⅡDubeyetal[39]DomesticgeeseChina2013BR，BLⅡRongetal[40]QuailsBrazilian2015M#87Casagrandeetal[35]QuailsChina2017MChinese1#9Zhuetal[37]OstrichesBrazilian2015H，BLAtypical#206Langonietal[36]

Note: H, Heat; BR, Brain; BL, Blood; M, Muscle; A, Atypical.

2 觀賞鳥類弓形蟲株基因型

鳥類是人們旅游觀賞的重要寵物之一，主要的觀賞鳥類有原鴿、黑蓋、孔雀、鸚鵡、鴉類等。塞爾維亞、葡萄牙報道的原鴿弓形蟲基因型有典型的Ⅰ型、Ⅱ型、Ⅲ型。Chen等[41]報道在中國福建野生動物園的黑蓋、孔雀和虎皮鸚鵡的三種寵物鳥進行檢測，其弓形蟲基因型分別為ToxoDB#9、ToxoDB#2和ToxoDB#10，表明野生動物園寵物鳥存在弓形蟲傳播風(fēng)險。Salant等[42]報道來自以色列的散養(yǎng)寒鴉、家鴉弓形蟲基因型均為Ⅱ型，結(jié)論表明人口密度和鴉類弓形蟲感染率呈現(xiàn)正相關(guān)。Cooper等[43]研究發(fā)現(xiàn)澳大利亞的牡丹鸚鵡感染弓形蟲后，出現(xiàn)嚴(yán)重的神經(jīng)系統(tǒng)癥狀，肉眼檢查發(fā)現(xiàn)腦出血，脾腫大，肝炎，右心室增厚等。腦病變組織切片海綿狀變化，有彌漫性、非化膿性腦炎。弓形蟲基因型為非典型II型，該基因型先前澳大利亞野生動物有記錄，表明弓形蟲可通過環(huán)境途徑傳播(表3)。

表3 人工飼養(yǎng)觀賞鳥的弓形蟲基因型
Tab.3 Artificial feeding ornamental bird Toxoplasma gondii genotype

HostLocationTimeTissueGenotypeToxoDBReferencePigeonsSerbia2014H，BRⅡ/ⅢMarkovicetal[44]PigeonsPortugal2014BL，TI/Ⅱ/ⅢVilaresetal[45]PigeonsPortugal2008BRI/Ⅱ/ⅢWaapetal[46]Black?cappedChina2015H，TChinese1#9Chenetal[41]PeacockChina2015H，T#2Chenetal[41]BudgerigarChina2015H，T#10Chenetal[41]CorvusmonedulaIsraeli2013BR，TⅡSalantetal[42]CorvussplendensIsraeli2013BR，TⅡSalantetal[42]LovebirdAustralia2015BR#3，II?ACooperetal[43]

Note: H, Heat; BR, Brain; BL, Blood; M, Muscle; A, Atypical.

3 野生珍稀鳥類弓形蟲株基因型

目前，全球報道的野生珍稀鳥類約20種左右，根據(jù)《世界自然保護聯(lián)盟》(IUCN)瀕危物種紅色名錄(IUCN.Org:https://www.iucn.org/)、《國家保護有益的或者有重要經(jīng)濟、科學(xué)研究價值的陸生野生動物名錄》、《國家重點保護野生動物名錄》等法律法規(guī)及其公約的相關(guān)規(guī)定，將目前報道的感染弓形蟲的野生珍稀鳥類進行歸類，明確其所受保護的等級，為后續(xù)的野生珍稀鳥類弓形蟲基因型研究及其保護提供一定參考[47]。表4所列的自然野生珍稀鳥類，大多為重點保護野生動物，其感染弓形蟲為地區(qū)散發(fā)，時有報道，發(fā)病的鳥類數(shù)量通常為個例。自然珍稀鳥類弓形蟲基因型大多為典型Ⅱ型、Ⅲ型，Ⅰ型相對較少。此外，Su等[48]報道的美國夏威夷黑雁(Brantasandvicensis)被列入2012年《世界自然保護聯(lián)盟》(IUCN)瀕危物種紅色名錄“易?！?VU)的受威脅級別，發(fā)現(xiàn)其弓形蟲基因型為ToxoDB#261、ToxoDB#262。Aubert等[49]報道的法國灰林鸮(Strixaluco)在我國為國家二級保護動物，其弓形蟲基因型為Ⅱ型。Dubey等[50]報道的哥斯達黎加彩虹巨嘴鳥(Ramphastossulfuratussulfuratus)，其弓形蟲基因型非克隆系典型Ⅰ型、Ⅱ型，還發(fā)現(xiàn)Ⅲ變異型，為ToxoDB#52首次報道弓形蟲從彩虹巨嘴鳥分離。Zhu等[51-53]報道的中國新疆地區(qū)的七彩山雞(PhasianuscolchicusLinnaeus)、家麻雀(Passerdomesticus)，中國蘭州地區(qū)的家麻雀(Passerdomesticus)以及中國吉林地區(qū)的黃雀(Carduelisspinus)、小云雀(Alaudagulgula)的弓形蟲基因型均為為Ⅱ變異型，花臉鴨(Anasformosa)為Chinese 1型，ToxoDB#9，其中黃雀、小云雀和花臉鴨均被列入列入中國國家林業(yè)局2000年8月1日發(fā)布的《國家保護有益的或者有重要經(jīng)濟、科學(xué)研究價值的陸生野生動物名錄》(表4)。

表4 自然野生珍稀鳥類的弓形蟲基因型
Tab.4 Genotype of Toxoplasma gondii in natural wild rare birds

LevelHostLocationTimeTissueGenotypeToxoDBReferenceIC?2013?LCCanadageesAmerica2004TⅢDubeyetal[54]IC?2012?LCMuteswanAmerica2013HⅢ#2#216Suetal[55]IC?2013?LC4CanadageeseAmerica2016HII/III#1#2#4#266Vermaetal[56]IC?2012?VUHawaiianGeeseAmerica2016BL，T#261#262Suetal[48]IC?2013?LCWoodpeckerAmerica2007BRⅢGerholdetal[57]IC?2012?LCWoodpeckerNorway2014BR，TⅡJokelainenetal[58]IC?2012?LCSturnusvulgarisIran2013TⅡ/ⅢKhademvatanetal[30]IC?2014?LCTawnyOwlFrance2008BRIIAubertetal[49]IC?2012?LCToucanCostaRica2008BR，BLnon?clonalI，#52Dubeyetal[50]GuineafowlBrazil2011BLⅡDubeyetal[59]IC?2012?LCPheasanChina2012MII?V#3Zhuetal[51]IC?2012?LCGallusgallusNicaraguaBLI，II，III，#52ToxoDBColumbaliviaIran2013TⅡ/ⅢKhadeetal[30]CT?2010?LCEareddovesBrazil2014BL，T#1#6#17Barrosetal[60]IC?2013?LCHouseChina2012MII?V#3Zhuetal[51]IC?2013?LCHouseChina2013H，BR，LUII?V#3Zhuetal[52]IC?2013?LCHouseIran2013TⅡ/ⅢKhadeetal[30]IC?2009?LCEurasianSiskinChina2015BRII?V#3Zhuetal[53]IC?2012?LCOrientalSkylarkChina2015BRII?V#3Zhuetal[53]IC?2012?LCAnasformosaChina2015H，LUChinese1#9Zhuetal[53]IC?2012?LCTreesparrowsChina2012MI#10Zhuetal[51]IC?2013?LCRedhawkAmerica2013BRI/Ⅱ#10/#5Suetal[61]IC?2013?LCGriffonvulturesIsraeli2013BR，TⅡSalantetal[42]

Note: H, Heat; BR, Brain; BL,: Blood; M, Muscle; LU, Lung; A, Atypical; V, Variant;

ICUNCEP-IC, World Conservation Union Catalog of endangered species; LC, 低危; VU, 易危;

CTWPSUESS-CT, Catalog of terrestrial wildlife protected by the state or useful in economic and scientific research

4 小 結(jié)

目前，關(guān)于鳥類弓形蟲基因型的研究報道相對較少，鳥類作為弓形蟲傳播的重要的中間宿主動物群體，目前針對于鳥類弓形蟲主要基因型中散養(yǎng)家雞Ⅰ型、Ⅱ型、Ⅲ型均有，其中Ⅲ型居多；散養(yǎng)家鴨、家鵝、鵪鶉、鴕鳥等主要禽類以及原鴿、黑蓋、孔雀、鸚鵡、鴉類等觀賞鳥類，有典型的Ⅰ型、Ⅱ型、Ⅲ型以及chinese1型；雁雀等野生珍稀鳥類，出現(xiàn)典型的Ⅱ型、Ⅲ型以及Ⅱ型非典型基因型，其基因型豐富度較高。

鳥類弓形蟲的研究雞、鴨、鵝等禽類是人類動物源性食品主要來源之一，觀賞飼養(yǎng)鸚鵡、鴿子等動物人工寵物鳥類成為人們旅游觀光、休閑娛樂方式之一，鳥類弓形蟲的感染率、基因型、毒力的研究對于公共衛(wèi)生、食品安全、旅游行業(yè)具有重要意義。對于野生珍稀遷徙候鳥的弓形蟲的基因種群結(jié)構(gòu)、毒力相關(guān)因子、傳播路線途徑、種間遺傳進化等是未來研究的熱點。隨著鳥類弓形蟲基因型研究的不斷深入和拓展，相關(guān)的種群結(jié)構(gòu)等生物信息將逐步得以豐富。

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