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Molecular epidemiology of rabies in Indonesia

Molecular epidemiology of rabies in Indonesia
Molecular epidemiology of rabies in Indonesia

Virus Research 135(2008)144–149

Contents lists available at ScienceDirect

Virus

Research

j o u r n a l h o m e p a g e :w w w.e l s e v i e r.c o m /l o c a t e /v i r u s r e

s

Molecular epidemiology of rabies in Indonesia

Heru Susetya a ,Makoto Sugiyama a ,b ,?,Akio Inagaki b ,Naoto Ito a ,b ,Gatot Mudiarto c ,Nobuyuki Minamoto a ,b

a

The United School of Veterinary Sciences,Department of Veterinary Medicine,Faculty of Applied Biological Sciences,Gifu University,1-1Yanagido,Gifu 501-1193,Japan b

Laboratory of Zoonotic Diseases,Department of Veterinary Medicine,Faculty of Applied Biological Sciences,Gifu University,1-1Yanagido,Gifu 501-1193,Japan c

Virology Unit,Animal Drug Assay and Certi?cation Laboratory,Bogor,Indonesia

a r t i c l e i n f o Article history:

Received 20September 2007

Received in revised form 3March 2008Accepted 4March 2008

Available online 16April 2008

Keywords:Rabies virus

Reverse transcriptase polymerase chain reaction

Molecular epidemiology Indonesia

a b s t r a c t

In order to clarify the genetic relationships and dynamics of rabies viruses that are epidemic in Indonesia,we determined and analyzed 1307nucleotides of nucleoprotein genes of 34rabies ?eld isolates collected from Sumatra,Java,Kalimantan,Sulawesi and Flores islands.Results of phylogenetic analysis indicated that rabies isolates in Indonesia formed one cluster,were of Asian lineage,and were closely related to a rabies isolate in China rather than to rabies isolates in Thailand,India or Sri Lanka.Rabies isolates in Indonesia were divided into three phylogroups (ID1,ID2and ID3)that included seven lineages.There was a correlation between phylogroup and geographical distribution of the isolates.Isolates in four lineages (SC1,SC2,SC3and ST)of the ID1phylogroup were mainly present in Sumatra.Isolates in the ST lineage were distributed widely in Sumatra,while isolates in the SC1,SC2and SC3lineages were limited to central Sumatra.ID2and ID3phylogroups included one lineage (JA)and two lineages (KS and SF),respectively.Results of phylogenetic analysis and historical background suggest that rabies viruses in China might have been transferred to Indonesia and spread to each island due to human activities.

?2008Elsevier B.V.All rights reserved.

1.Introduction

Rabies virus is distributed worldwide and causes lethal viral encephalitis in a wide range of host species.Although all mammals are susceptible to rabies infection,the vector species that transmit the virus to humans are limited to several canid and feline species and chiropteran species.

As a member of the Lyssavirus genus,rabies virus has a single-stranded RNA genome of approximately 12kb containing N,P,M,G and L genes encoding nucleoprotein,phosphoprotein,matrix pro-tein,glycoprotein and polymerase protein,respectively (Bourhy et al.,1992,1993).The development in recent years of molecular methods of analysis such as reverse transcription and polymerase chain reaction (RT-PCR)and techniques for sequencing rabies genes has led to a better understanding of the distribution and genetic characteristics of rabies virus at both the global level (Smith et al.,1992;Kissi et al.,1995)and regional levels (David et al.,2000;Nadin-Davis et al.,1994;Nishizono et al.,2002;Liu et al.,2007).

?Corresponding author at:Laboratory of Zoonotic Diseases,Department of Veterinary Medicine,Faculty of Applied Biological Sciences,Gifu University,1-1Yanagido,Gifu 501-1193,Japan.Tel.:+81582932948;fax:+81582932948.

E-mail address:sugiyama@gifu-u.ac.jp (M.Sugiyama).Rabies has existed since at least the nineteenth century in Indonesia.Epidemiological form of rabies in Indonesia is urban rabies,in which domestic dogs act as the main reservoir.Despite the implementation of a campaign against dogs to eliminate rabies in 1989,rabies is still prevalent in Sumatra,Kalimantan,Sulawesi and Flores islands;there have been no reported cases of rabies in Java since 2000(information from Directorate Gen-eral of Livestock Production in Indonesia).In Indonesia,135cases of human deaths due to rabies and 3349cases of post-exposure treatment for rabies were reported in 1999(http://www.who.int/emcdocuments/rabies/whocdscsreph200210.html ).However,there is little information on epidemics of rabies and dynamics of rabies viruses in Indonesia.Smith et al.(1992)reported that two rabies virus strains,one isolated from a dog and one from a human in Java,genetically belonged to the Asian group.How-ever,this information is not suf?cient for use in epidemiology of rabies in Indonesia because Indonesia consists of more than 13,000islands and there is no genetic information on rabies viruses in other endemic areas of Indonesia.Genetic information on rabies viruses in endemic areas is important to trace the dynamics of rabies infection and eradicate rabies from Indonesia.In this study,we sequenced 1307nucleotides of the N gene of rabies virus iso-lates from ?ve islands in Indonesia and analyzed the phylogenetic relationships between these isolates and rabies strains originating

0168-1702/$–see front matter ?2008Elsevier B.V.All rights reserved.doi:10.1016/j.virusres.2008.03.001

H.Susetya et al./Virus Research135(2008)144–149145

Table1

Rabies?eld viruses from Indonesia used in this study

Island Area Location Identi?cation number Year Animal origin Accession number

Sumatra Northern Medan SN00-142000Dog AB154235

Deli Serdang SN00-032000Dog AB154234 Central Bukittinggi SC02-902002Dog AB154243

Bukittinggi SC97-011997Dog AB154233

Bukittinggi SC02-892002Dog AB154231

Bukittinggi SC01-662001Civet cat AB154213

Bukittinggi SC01-742001Cat AB154209

Bukittinggi SC02-792002Dog AB154229

Bukittinggi SC02-822002Cat AB154211

Bukittinggi SC01-702001Tiger AB154242

Bute SC01-632001Dog AB154228

Bukittinggi SC02-872002Monkey AB154224

Bukittinggi SC01-652001Deer AB154214

Bukittinggi SC01-732001Cattle AB154212

Bukittinggi SC01-682001Cat AB154208

Padang SC00-362000Dog AB154226

Tj.Mutiara SC00-452000Dog AB154227

Bukittinggi SC02-832002Dog AB154230

Bukittinggi SC01-752001Cat AB154210

Bukittinggi SC02-912002Dog AB154232

Pesisir Selatan SC00-122000Dog AB154225 Southern Rejanglebong SS01-212001Dog AB154238

Bengkulu SS01-132001Dog AB154237

Java Western Cirebon JA97-051997Dog AB154220

Kalimantan Eastern unknown KL00-182000Dog AB154221

unknown KL97-031997Dog AB154223

Tapin KL01-272001Dog AB154222

Sulawesi Northern Manado SW97-041997Dog AB154241 Southern unknown SW02-222002Dog AB154240

Pangkep SW01-112001Dog AB154239

Flores Ende FL01-062001Dog AB154215

Flores FL97-011997Dog AB154218

Flores timur FL02-082002Dog AB154216

Sikka Fl02-102002Dog AB154217

from other regions in the world.Based on the results,the dynamics of rabies viruses in Indonesia are discussed.

2.Materials and methods

2.1.Sample collection

A total of thirty-four brain samples from twenty-?ve dogs,four cats,a cow,a civet cat,a deer,a monkey and a tiger were used for genetic analysis in this study(Table1).The brain samples from dogs were collected in Sumatra,Java,Kalimantan,Sulawesi and Flo-res islands of Indonesia.The samples from the other animals were collected in central Sumatra.The civet cat was a wild animal and the others were domestic animals.After these animals had bitten humans or had shown signs of rabies,they were diagnosed as hav-ing rabies from the results of?uorescent antibody tests(Dean et al.,1996)carried out by the Animal Diseases Investigation Centers of Indonesia.

2.2.RT-PCR

Total RNA was extracted from each brain specimen using a Mag Extractor RNA Kit(TOYOBO,Osaka,Japan).The comple-mentary DNA(cDNA)of the rabies genome was synthesized by using Ready-To-GoYou-Prime First-Strand Beads(Amersham Pharmacia,NJ,U.S.A)with positive sense primer RHN-19(5 -AAAATGTAACACCT CTACAATG-3 )acting at positions from52 to73(based on the nucleotide number of the viral genome of Nishigahara strain[Ito et al.,2001]).In the?rst step,the cDNA of N gene was ampli?ed by PCR using PCR Beads(Amer-sham Pharmacia)with primer RHN-19and negative sense primer RHNS-8(5 -AGGGAGACTGTCCACTTCTATAGG-3 )acting at positions from1641to1664.This?rst PCR ampli?ed a DNA fragment of1613bp.The second PCR was performed by using posi-tive sense primer RHN-17(5 -TTCAAAGTCAATAATCAGGTGG-3 ,at positions from92to113)and negative sense primer RHNS-3(5 -TCAGGATTGACAAACATTTTGCTC-3 at positions from1517to1540), which gave a DNA fragment of1454bp.The pro?les of the?rst and second PCRs consist of an initial denaturation for5min at95?C, followed by40cycles of denaturation for30s at95?C,reanneal-ing for1min at50?C,and elongation for2min at72?C,and a?nal incubation for5min at72?C.

2.3.Direct sequencing

Ampli?ed cDNA was employed for direct sequencing with Cy5-labeled primers RTNSEQ1(5 -AGAATCAGGAGTGATCTTGTCTCC-3 , negative sense,at positions from368to391),RTNSEQ2(5 -CTATTTGGGAGAAGAGTTTTTTGG-3 ,positive sense,at positions from1099to1122),RTNSEQ3(5 -GCTGGAACCTACGACATGTTTTTC-3 ,positive sense,at positions from689to712),and RTNSEQ4 (5 -GCCCTGAGCAGTCTTCATAAGCAG-3 ,negative sense,at posi-tions from762to785).After puri?cation of the second PCR product using an UltraClean kit(MO BIO,CA,U.S.A),a cycle sequencing reaction was carried out by using an AutoCycle Sequencing Kit (Amersham Pharmacia).Sequencing products were analyzed by

146H.Susetya et al./Virus Research 135(2008)

144–149

Fig.1.A phylogenetic tree based on sequences of 1307nucleotides of N genes from rabies viruses.Nucleotide sequences of 34Indonesian isolates were determined in this study.The sequences of ten representative isolates were used for this phylogenetic tree.The remaining sequences were obtained from the GenBank database (country or strain/animal origin/year,accession number).The tree was constructed by using the Clustal X program.The genetic distances between nodes are proportional to branch lengths.Numbers at nodes are bootstrap probabilities that were calculated using 1000replicates.Horizontal lines indicate degree of nucleotide difference.ID1,2and 3indicate each phylogroup classi?ed in Fig.2.

using an ALF DNA Sequencer (Amersham Pharmacia).The N gene target sequence was 1307b,corresponding to the nucleotides at positions 114to 1420of the viral genome of Nishigahara strain (Ito et al.,2001).2.4.Genetic analysis

A 1307-nucleotide sequence of the N gene of the isolates from Indonesia was compared phylogenetically with those of strains from other regions in the world,the information being obtained from the GenBank database.Phylogenetic analysis was performed by the neighbor-joining method using Clustal X (Larkin et al.,2007).The bootstrap probabilities were calculated using 1000replicates.

3.Results

3.1.RT-PCR and nucleotide sequence of N gene (nt 114–1420)A speci?c PCR product (1454bp)was ampli?ed from all of the samples used in this study (data not shown).Nucleotide sequences (1307b)of the N genes (nt 114–1420)of 34rabies isolates (Table 1)were determined and compared with those of 20iso-lates from other regions or three vaccine strains (see Fig.1).Rabies isolates in Indonesia showed 88.4–90.2%,86.1–88.4%,85.9–87.4%and 86.2–87.4%nucleotide homologies to those in China,Thai-land,India and Sri Lanka,respectively.They showed comparatively low nucleotide similarities (85.5–86.7%,85.2–86.6%,85–86.6%and 8

4.9–86.0%)to rabies isolates from Mexico,USA and Africa and the

H.Susetya et al./Virus Research135(2008)144–149

147

Fig.2.A radical phylogenetic tree based on sequences of1307nucleotides of N genes of rabies?eld isolates in Indonesia.Thirty-four isolates in Indonesia determined in this study and one isolate in China obtained from the Gen Bank database were used for analysis.The tree was generated using the Clustal X program.The genetic distances between nodes are proportional to branch lengths.Numbers at nodes are bootstrap probabilities that were calculated using1000replicates.Horizontal lines indicate degree of nucleotide difference.ID1,2and3indicate each phylogroup.SC1,SC2,SC3,ST,JA,SF and KS represent each lineage.Animal species from which each isolate derived were indicated with identi?cation number.All isolates without indication of the species were derived from dogs.

Nishigahara vaccine strain,respectively.The nucleotide homologies dropped to74.2–75.4%compared to Duvenhage virus,a genotype IV rabies related virus.Nucleotide and amino acid sequences among isolates in Indonesia were94.4–100%and97.5–100%homologous, respectively.

3.2.Phylogenetic analysis

Phylogenetic analysis based on the N gene sequences(1307b)of Indonesia isolates and street viruses from various parts of the world revealed that all rabies isolates in Indonesia formed one cluster and belonged to Asian lineage(Fig.1).Rabies isolates in Indonesia are more closely related to four isolates in China,which were found in Jiangsu,Henan,Hunan and Guizhou provinces in2004(Zhang et al.,2006),than to isolates from Thailand,India or Sri Lanka.The rabies viruses in Indonesia were divided into three phylogroups designated as ID1,ID2and ID3(Fig.2).Phylogroup ID1consists of three lineages(SC1,SC2and SC3)and one lineage(ST)formed by isolates from Sumatra.Phylogroup ID2consists of one lineage(JA) formed by an isolate from a dog in Java.Phylogroup ID3consists of two lineages(KS and SF)formed by isolates from eastern areas of Indonesia,Kalimantan,Sulawesi and Flores islands.The

bootstrap

Fig.3.Geographical distribution and proposed dynamics of rabies?eld isolates in Indonesia.SC1,SC2,SC3,ST,JA,SF and KS represent each lineage determined by phylogenetic analysis based on nucleotide sequences(see Fig.2).

148H.Susetya et al./Virus Research135(2008)144–149

values supported the lineage association except for the node of ST and SC1,of which value was only188.Isolates from two cats,one deer and one monkey belonged to lineage SC1.Isolates from two cats and one civet cat belonged to lineage SC2.An isolate from a cow belonged to lineage SC3.There was no speci?c genetic relationship among isolates obtained from domestic and wild animals.

3.3.Geographic distribution

The geographical distribution of the genetic lineages of rabies virus in Indonesia is shown in Fig.3.Isolates of ST lineage in the ID1phylogroup showed a large geographic distribution in Sumatra. Isolates of SC1,SC2and SC3lineages in the ID1phylogroup were distributed restrictedly in central Sumatra.An isolate of JA lineage in the ID2phylogroup was present in Java.Two remaining lineages (KS and SF)in the ID3phylogroup were found in the eastern area of Indonesia.Isolates of KS lineage were distributed in Kalimantan and Sulawesi and those of SF lineage were distributed in Sulawesi and Flores islands.

4.Discussion

Based on the N gene sequence,phylogenetic relationships among rabies viruses could be examined and distinguished more easily and closely than by using monoclonal antibodies or other conventional methods.We previously employed550b(Ito et al., 1999)or512b(Susetya et al.,2003)of the rabies N gene for examin-ing genetic relationships of rabies isolates in Thailand and reported that rabies?eld isolates in Thailand have a close genetic relation-ship to an isolate from China as a member of an Asian lineage.In this study,1307-nucleotide sequence of N gene was used to deter-mine the genetic relationships of rabies?eld isolates in Indonesia. Better results for bootstrap values were obtained by using1307b of the gene than by using550b or512b of the N gene(data not shown).The results of this study con?rmed that all isolates from Indonesia belong to Lyssavirus genotype1,the genotype of classical rabies virus.

When compared with the same gene regions of rabies isolates from various countries in the world,isolates from Indonesia made a cluster with an Asian lineage and were more closely related to an isolate from China than to isolates from Thailand,India or Sri Lanka. This genetic relationship between the isolates from Indonesia and China is supported by88.4–90.2%nucleotide homologies.Based on limited sequence analysis of the N gene,it has been reported that one isolate from Anhui of China and two isolates from Java of Indonesia belonged to the same group(Smith et al.,1992),and isolates in Indonesia were closely related genetically to the iso-lates from Philippines and China(Sugiyama and Ito,2007).It is known that many Chinese people had migrated to Indonesia from China for work or trading.The genetic data and historical facts sug-gest that rabies street viruses in China might have been transferred to Indonesia through dogs brought by humans who had migrated (Fig.3).

We showed by phylogenetic analysis that there are three rabies phylogroups that have been maintained endemically in Indone-sia.There was a correlation between phylogroup and geographical distribution of the isolates(Fig.3).Isolates in the ID1,ID2and ID3phylogroups were distributed in Sumatra,Java and the three islands(Kalimantan,Sulawesi and Flores),respectively.In the ID1 phylogroup,while the rabies viruses belonging to ST lineage were pandemic throughout Sumatra,the viruses belonging to the other three lineages(SC1,SC2and SC3)were endemic in central Sumatra. The viruses of the latter three lineages,which had been maintained among dogs in central Sumatra,spread not only to domestic ani-mals but also to a wild civet cat.Many people have kept dogs for hunting wild boar in the jungles of central Sumatra.Since there is a local superstition that dogs injected with rabies vaccine become less aggressive for hunting,some people do not want their dogs to be vaccinated.This may be the reason for the maintenance of rabies viruses in dogs in some areas of central Sumatra.We found that domestic animals other than dogs,including cats,a cow,a deer,a monkey and a tiger,were infected with rabies virus in central Suma-tra.This means that rabies virus in rabid dogs easily disseminated to other animals and humans in central Sumatra.The detection of rabies virus in a wild civet cat raises the possibility that rabies may appear as a sylvatic type in Indonesia in the future.

The ID2phylogroup consisted of an isolate collected in1997in Java,where rabies was thought to have been almost eradicated. Smith et al.(1992)reported the nucleotide sequences of part of the N gene of two isolates from Java collected in1989.In this study,phylogenetic analysis using the limited region of the N gene revealed that these two isolates belonged to a JA lineage(data not shown).These results suggest that rabies viruses in a JA lineage were endemic in Java from1989until at least1997.

The ID3phylogroup consisted of isolates from Kalimantan, Sulawesi and Flores islands.Rabies viruses in KS and SF lineages of the ID3phylogroup were found in eastern areas of Indonesia.An SF lineage is formed by isolates from Sulawesi and Flores islands. No cases of rabies had been reported in Flores until1997.It is thought that a?sherman brought infected dogs from southeast Sulawesi to East Flores island(Windiyaningsih et al.,2004).The results of sequencing show a close genetic relationship between isolates from the two islands,supporting the above report.Results obtained in Kalimantan and Sulawesi also raise the possibility that rabies viruses were transferred between the two islands by human activities in a manner similar to that in the case of Sulawesi and Flores islands.

We studied in detail the molecular epidemiology of rabies in Indonesia for the?rst time by using many rabies isolates origi-nating from several animals and geographical areas.The?ndings suggest that rabies viruses in China might have been transferred to Indonesia and spread to each island with human activities.The results should be useful for tracing the route of rabies transmission and for establishing measures to eliminate rabies in Indonesia. Acknowledgments

This study was supported in part by grants-in-aid for scienti?c research from the Ministry of Education,Culture,Sports,Science and Technology,Japan(nos.16658120,17255010and17405044) and a grant-in-aid for scienti?c research(The21st Century center-of-Excellence Program)from the Ministry of Education,Culture, Sports,Science and Technology,Japan(E-1).

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英语中的比较级与最高级 详解

比较级与最高级 1.as...as 与(not) as(so)...as as...as...句型中,as的词性 第一个as是副词,用在形容词和副词的原级前,常译为“同样地”。第二个as是连词,连接与前面句子结构相同的一个句子(相同部分常省略),可译为“同..... He is as tall as his brother is (tall) . (后面的as 为连词) 只有在否定句中,第一个as才可换为so 改错: He is so tall as his brother.(X) 2.在比较状语从句中,主句和从句的句式结构一般是相同的 与as...as 句式中第二个as一样,than 也是连词。as和than这两个连词后面的从句的结构与前面的句子大部分情况下结构是相同的,相同部分可以省略。 He picked more apples than she did. 完整的表达为: He picked more apples than she picked apples. 后而的picked apples和前面相同,用did 替代。 He walked as slowly as she did.完整表达为: He walked as slowly as she walked slowly. she后面walked slowly与前面相同,用did替代。

3.谓语的替代 在as和than 引导的比较状语从句中,由于句式同前面 主句相同,为避免重复,常把主句中出现而从句中又出现的动词用do的适当形式来代替。 John speaks German as fluently as Mary does. 4.前后的比较对象应一致 不管后面连词是than 还是as,前后的比较对象应一致。The weather of Beijing is colder than Guangzhou. x than前面比较对象是“天气”,than 后面比较对象是“广州”,不能相比较。应改为: The weather of Bejing is colder than that of Guangzhou. 再如: His handwriting is as good as me. 应改为: His handwriting is as good as mine. 5.可以修饰比较级的词 常用来修饰比较级的词或短语有: Much,even,far,a little,a lot,a bit,by far,rather,any,still,a great deal等。 by far的用法: 用于强调,意为“...得多”“最最...”“显然”等,可修饰形容词或副词的比较级和最高级,通常置于其后,但是若比较级或最高级前有冠词,则可置于其前或其后。

五年级上册成语解释及近义词反义词和造句大全.doc

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二年级语文的、地、得用法教案

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(二)其次,我们来看提土“地”的用法。通常提土“地”的后面往往跟的是表示动作的词,也就是动词,我们 用算式表示就是“地+动词”。 比如:仔细地看,大声地说,慢慢地走。看,提土地后 面的看、说、走都是表示动作的词。 现在我们再来举几个例子:快速地跑,用力地抓,认真 地读,快活地游着,积极地参加,早早地离开,自由自在地 飞翔,一次又一次地握手、迅速地包围、沙沙地直响、斩钉 截铁地说、用力地踢、仔细地看……。也就是说,提土“地”前面的词语一般用来说明提土“地”后面的动作怎么样。 (三)最后,我们来看双人“得”的用法。双人“得” 前面多数是表示动作的词或词语,少数是形容词,我们用算 式表示就是“动词(形容词)+得”。比如:玩得开心,红得发紫,吃得好,大得很,跳得高,急得满头大汗,“玩、吃、跳”这些是动词,“大、红、急”这些是形容词,后面都得 用双人“得”。 现在我们再来举几个例子:玩得刺激,看得仔细,唱得 好听,写得端正,举得高高的,说得真精彩,气得双脚直跳、理解得十分深刻、乐得合不拢嘴、惊讶得目瞪口呆……。也 就是说,双人“得”后面的词语一般用来补充说明双人“得”前面的动作怎么样。 二、“的、地、得”用法补充说明:

英语中的比较级和最高级

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的地得的用法和区分

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多媒体课件、录屏软件 八、教学设计与过程 开场白: 同学们好!今天我们一起来学习“的、地、得”的正确用法。首先我们来了解一下它们的区别。 1、相同之处:原来它们都是念轻声“de”,都是结构助词,起连接作用。 2、不同之处:在书面语中要写成三个不同的字,而且它们的搭配及用法也各不相同。 (1)怎么样的什么 (2)怎样样地干什么 (3)干得怎么样 下面我们就来学习一下它们的正确用法。 白勺“的”的结构是用“形容词或名词或代词+的+名词”来表示,而我们最常见,用得最多的还是“形容词+的+名词”的结构。 而土也“地”的用法可以用“形容词+地+动词”的结构来表示。 双人“得”是用“动词+得+形容词”的结构来表示 3、练习巩固 (1)形近区分 静静(的)河面静静(地)写字欢乐(的)山谷

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