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15.Molecular epidemiology of rabies in Guangxi Province, south of China


Journal of Clinical Virology 39 (2007) 295–303

Molecular epidemiology of rabies in Guangxi Province, south of China
Qi Liu a , Yi Xiong b , Ting Rong Luo a,? , You-Chuan Wei a , Song-Jian Nan a , Fang Liu a , Yan Pan a , Li Feng a , Wei Zhu a , Ke Liu a , Jian-Gang Guo b , Hua-Ming Li b
a

College of Animal Science and Technology, Guangxi University, 100 Daxue Road, Nanning 530004, Guangxi, China b Guangxi Vererinary Prevention and Quarantine Center, Nanning 530001, Guangxi, China Received 12 December 2006; received in revised form 19 April 2007; accepted 19 April 2007

Abstract Background: Surveillance data for rabies in Guangxi Province in China showed that human rabies cases have gradually increased since 1996. Objective: To evaluate the epidemiology of rabies at the molecular level and provide suggestions for effective prevention of rabies in Guangxi. Study design: Since 2000, 1569 brains from suspected rabid animals were collected from different areas of Guangxi. Rabies virus was isolated from 42 samples. RT-PCR was used to amplify a 455 nucleotide segment of the 3 -terminal of the N gene. The sequencing data from that segment was used for phylogenetic analysis. Results: Nucleotide homology comparisons and phylogenetic tree analysis based on this sequence indicated that all the rabies virus isolates from Guangxi belonged to genotype 1 and could be divided into four groups. Groups I, II and IV included 23, 10 and 8 isolates, respectively. These had nucleotide homologies of 97.1–100%, 98.2–100% and 99.1–99.6%, respectively. Only the GXN119 strain belonged to group III. Group I had two group-speci?c mutations: T90N and E110D. Group II had one group-speci?c mutation of T42S. Conclusions: This study showed that rabies virus isolates from Guangxi have a close genetic relationship and topographical distribution. ? 2007 Elsevier B.V. All rights reserved.
Keywords: Rabies; N gene; Nucleotide homology; Molecular epidemiology

1. Introduction Rabies is a serious disease that continues to threaten many mammals in Asian countries and other areas of the world (Fishbein and Robinson, 1993; Pastoret, 2002; Hemachudha et al., 2002; Warrell and Warrell, 2004). WHO estimated human mortality from endemic canine rabies to be 55,000 deaths per year in Asia and Africa, with 56% of the deaths occurred in Asia. The majority (84%) of these deaths occur in rural areas (WHO Technical Report Series, No. 931). Most Asian countries remain endemic for canine rabies. Wildlife rabies plays a very minor role in south and south-east Asia, but exists in some species, including bats (Wilde et al., 2005). In Europe, the United Kingdom has been considered rabies-free
Abbreviations: RT-PCR, reverse-transcription polymerase chain reaction; N, nucleocapsid ? Corresponding author. Tel.: +86 771 3236103; fax: +86 771 3236103. E-mail address: trluo@tom.com (T.R. Luo). 1386-6532/$ – see front matter ? 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.jcv.2007.04.021

since 1902, although in 2002 a man died in Scotland after contracting European bat lyssavirus rabies (Fooks et al., 2003). In the United States, during the 1950s, there was a dramatic decline of the number of cases of rabies in domestic animals as a result of dog vaccination campaigns (Aubert, 1994; Fogelman et al., 1993; Krebs et al., 1993; Krebs et al., 1995). In Latin America, canine rabies and wild rabies, especially transmitted by hematophagous and insectivorous bats, have emerged as problems. Since 2000 the molecular epidemiology of rabies has been published from Africa: Zimbabwe (Sabeta et al., 2003), Botswana (Johnson et al., 2004a), Sudan (Johnson et al., 2004b), and South Africa (Nel et al., 2005); South America: Venezuela (Mattos et al., 1996), Argentina (Cisterna et al., 2005), Bolivia (Favi et al., 2003), Brazil (Ito et al., 2003), and Colombia (Hughes et al., 2004); Mexico (Flisser et al., 2002); and Trinidad (Wright et al., 2002). The N gene of the rabies virus is most often the target for genetic analysis and adaptive evolution analysis because the gene is highly conversed (Holmes et al., 2002). Kissi reported

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genetic polymorphism in the rabies virus N gene in 69 rabies isolates from various part of the world. These were partially sequenced and compared to 13 representative isolates of the six lyssavirus genotypes (Kissi et al., 1995). Smith reported on the molecular epidemiology and historical relationships of rabies virus using a limited sequence analysis of the N gene of 87 isolates from Europe, Africa, North America, and South America (Smith et al., 1992). Ito and Susetya reported on the phylogenetic analysis of rabies virus in Thailand based on two variable regions of the N gene (Ito et al., 1999; Susetya et al., 2003). In China, several papers about rabies virus were reported recently (Meng et al., 2007; Tang et al., 2005; Zhang et al., 2005; Zhang et al., 2006). Guangxi, a southern Province of China, has a severe rabies epidemic. Human rabies cases in Guangxi increased from 16 in 1995 to 79 in 2000. Almost all of the deaths were attributed to dog bites. Bai reported the nucleotide sequences of the G gene of a Guangxi street strain, CGX89-1, in 1993 (Bai et al., 1993). Gu carried out the molecular epidemiological characterization of eight isolates of rabies virus from Guangxi by cloning and sequencing the fragment of rabies virus N gene (Gu et al., 2001). We now provide additional information about the molecular epidemiology of rabies in Guangxi since 2000, using brain samples collected from rabid dogs and other animals from different areas of Guangxi. The analysis was performed by partially sequencing the N gene.

2.3. Cloning nucleocapsid (N) gene A 3 -terminal fragment of the N gene was cloned with the primers RHN3 (5 -ACAGACAGCGTCAATTGCAAAGC3 ) and RHN4 (5 -TCGGATTGACGAAGATCTTGCTC-3 ), which ampli?ed nucleotides 1–455. The PCR products were cloned into the vector pMD18-T and sequenced by Takara Corp. Sequence information from both strands was aligned and edited using the Vision X program. 2.4. Phylogenetic analysis Phylogenetic analysis was carried out on 455 nucleotides of the 3 -terminal of the N gene of the isolates (Table 1) and in conjunction with some strains from the GenBank database that were obtained from other countries. Alignments of homologous sequences were made with the Clustal method of the MegAlign program of the DNAStar Version 7.0 package (DNASTAR Inc., USA). A neighbor-joining (NJ) tree for all the DNA sequences were constructed under the Kimura 2-parameter model using MEGA3.1 software (Kumar et al., 2004). Phylogenetic relationships of sequences were further con?rmed by maximum likelihood in PHYML (Guindon and Gascuel, 2003) and by Bayesian analysis in mrbayes-3.1.2 (Huelsenbeck et al., 2001; Ronquist and Huelsenbeck, 2003), respectively. For maximum likelihood analysis, the model of HKY85 was used (Hasegawa et al., 1985). The transition/transversion ratio and proportion of invariable sites were estimated by maximizing the likelihood of the phylogeny. For Bayesian analyses, four Monte Carlo Markov Chains (MCMC) were simultaneously run for 1,200,000 generations, saving a tree every 100 generations. Posterior probability (PP, shown as percentage) for Bayesian analyses and bootstrap values (BP) for trees assessed relative support for monophyletic groups.

2. Materials and methods 2.1. Virus isolates One thousand ?ve hundred and sixty-nine animal brain samples were obtained from 14 cities in Guangxi from October 2000 to April 2005. Five samples were from rabid cattle, and two from rabid pigs that were bitten by rabid dogs. Eleven samples were from symptomatic rabid dogs with hypersalivation, hydrophobia, aerophobia, or biting animals. One sample was from a normal stray cat, and 1550 samples were from clinically normal dogs. These were obtained from the local stray dogs or from the local commercial butchers, with permission of the Food and Drug Administration. The brain samples were subjected to RT-PCR and then the wild rabies virus strains were isolated using the mouse inoculation test (MIT). 2.2. Reverse-transcription polymerase chain reaction (RT-PCR) Total viral RNA was extracted from original host brain or mouse brain using Trizol (Invitrogen, CA, USA) following the manufacturer’s instructions. RT-PCR ampli?cation for diagnosis was carried out with the primers RHN1 (5 -CTACAATGGATGCCGAC-3 ) and RHN2 (5 TTGCTCAACCTATACAGAC-3 ).

3. Results 3.1. Detection and isolation of rabies virus RT-PCR performed on 1569 animal brain samples identi?ed ?ve rabies-positive samples from rabid cattle, two from rabid pigs, and 11 from rabid dogs. Twenty-three samples from 1550 normal dogs and one from a normal cat were also found to be positive. Rabies viruses were isolated from these RT-PCR-positive samples by MIT (Table 1). 3.2. Sequences of 455 nucleotides of the 3 -terminal of the N gene A 455 nucleotide segment of the 3 -terminal of the N gene was sequenced. The homology of the sequences was at least 84.5% among the 42 rabies virus isolates. Based on their homology, the rabies virus isolates were divided into four groups. Group I included 23 isolates with nucleotide

Q. Liu et al. / Journal of Clinical Virology 39 (2007) 295–303 Table 1 Origin of rabies virus strains and isolation date Isolates GXN119 GX102 GX201 GXLA GX074 GX08 GX09 GXBM GX014 GXB03 GX120 GX219 GX123 GX173 GX174 GXGL GX304 GX01 GX091 GX195 GX260 GX019 GXHX GXSL GXPX GX506 GX508 GX509 GX510 GXWXp GXcat GXGG GXNniu GXQZ GX441 GX442 GX443 GX452 GX496 GX520 GX0510 GXBS Original city(County) Nanning (Jiangnan) Nanning Nanning Nanning (Longan) Baise (Debao) Qinzhou (Pubei) Qinzhou (Pubei) Hechi (Bama) Chongzuo (Pinxiang) Yulin (Bobai) Yulin (Rongxian) Guigang (Qintang) Yulin (Fumian) Nanning (Rongning) Nanning (Rongning) Guilin (Yangshuo) Fangchenggang(Fangchengqu) Guilin (Lingchun) Liuzhou (Luzhuai) Wuzhou (Chuangwu) Laibin (Binzhouqu) Beihai (Hepu) Nanning (Hengxian) Nanning (Shanglin) Chongzuo (Pinxiang) Chongzuo (Longzhou) Chongzuo (Longzhou) Chongzuo (Longzhou) Chongzuo (Longzhou) Wuxuan Beihai Guigang (Pingnan) Nanning Qinzhou (Qinnan) Liuzhou (Liucheng) Liuzhou (Liujiang) Nanning (Hengxian) Hezhou (Zhongshan) Nanning (Qingxiuqu) Chongzuo (Fushui) Liuzhou (Rongan) Baise Animal species Clinically normal dog Clinically normal dog Clinically normal dog Rabid dog Clinically normal dog Clinically normal dog Clinically normal dog Rabid dog Clinically normal dog Clinically normal dog Clinically normal dog Clinically normal dog Clinically normal dog Clinically normal dog Clinically normal dog Rabid cattle Rabid cattle Rabid dog Rabid dog Clinically normal dog Rabid cattle Clinically normal dog Rabid dog Rabid cattle Rabid dog Clinically normal dog Clinically normal dog Clinically normal dog Clinically normal dog Rabid pig Clinically normal cat Rabid dog Rabid cattle Rabid dog Rabid dog Rabid dog Rabid pig Clinically normal dog Clinically normal dog Clinically normal dog Rabid dog Clinically normal dog Isolation date October 2000 May 2002 May 2002 January 2003 February 2003 March 2003 March 2003 March 2003 April 2003 May 2003 May 2003 June 2003 July 2003 July 2003 July 2003 January 2004 March 2004 May 2004 July 2004 October 2004 December 2004 January 2005 March 2005 March 2005 March 2005 March 2005 March 2005 March 2005 March 2005 March 2005 April 2005 April 2005 April 2005 April 2005 April 2005 April 2005 April 2005 April 2005 April 2005 April 2005 April 2005 April 2005

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GenBank accession number DQ 866111 DQ 866088 DQ 866093 DQ 866116 DQ 866107 DQ 866108 DQ 866109 DQ 866115 DQ 866106 DQ866080 DQ 866089 DQ 866113 DQ 866090 DQ 866091 DQ 866092 DQ 866083 DQ 866117 DQ 866105 DQ 866110 DQ 866112 DQ 866114 DQ 866087 DQ 866119 DQ 866120 DQ 866085 DQ 866099 DQ 866100 DQ 866101 DQ 866102 DQ 866121 DQ866081 DQ866082 DQ 866084 DQ 866086 DQ 866094 DQ 866095 DQ 866096 DQ 866097 DQ 866098 DQ 866103 DQ 866104 DQ 866118

homology of 97.1–100%; Group II included 10 isolates with nucleotide homology of 98.2–100%; only the GXN119 strain belonged to group III; Group IV included eight isolates with nucleotide homology of 99.1–99.6% (Table 2). 3.3. Phylogenetic tree analysis of Guangxi rabies virus isolates Phylogenetic tree analysis was carried out to determine the genetic relationships among the rabies virus isolates based on the nucleotide sequences of the N gene (Fig. 1). We also compared the sequences of the isolates from Guangxi with rabies sequences in the GenBank database. The isolates were divided into four distinct clusters consistent with the four groups above based on their homology. Group I also contained one strain, CTN, from Shandong Province. Group III

contained the unique isolate GXN119 from Guangxi and one isolate from Thailand. Group IV contained eight isolates from Guangxi, and the ?xed strains ERA, SAD, and PV. The isolates in groups I, II, III from Guangxi were located closely together. Two isolates, MRV from a mouse in Henan and DRV from a deer in Jilin of China, were included into other branches. None of the isolates from Guangxi was closely related to strains from other areas in Asia: India, Sri Lanka, Korea, and Iran. However, the isolate MRV from Henan province was closely related to vaccine strains CVS, HEPFluly, and isolate 8702IRA from Iran. 3.4. Amino acid mutations of rabies virus isolates Comparison of the fragments of the N protein of the isolates with that of the ERA strain over a 151 residues segment

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Table 2 Homologies of N gene of rabies virus isolates from Guangxi provincea

Q. Liu et al. / Journal of Clinical Virology 39 (2007) 295–303

a

The upper ?gures indicate the homologies of nucleotide sequence, the lower ?gures indicate the homologies of deduced amino acid sequence.

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Fig. 1. Phylogenetic tree on N gene of rabies virus isolates from Guangxi.

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Fig. 2. Amino acid mutations of rabies virus isolates from Guangxi isolates from Guangxi.

, indicates the speci?c mutations of amino acid on the deduced N protein of rabies virus

indicated that two speci?c amino acid substitutions at positions 90 and 110 occurred in group I: T90N and E110D. In group II, the threonine in ERA was replaced by serine (T42S). Eight isolates in group IV showed a unique substitution, P58S, commonly with the other three groups (Fig. 2). 3.5. Geographical distribution of rabies virus isolates from Guangxi This analysis determined the geographical distribution of rabies virus in Guangxi. Isolates of group I were prevalent in the south-eastern area of Guangxi. Isolates of group II were mainly found in the western area. Isolates of group IV were mainly found in the south of Guangxi (Fig. 3). Nanning city had isolates of all four groups, and the Chongzuo city had isolates of three groups.

4. Discussion Molecular epidemiology based on sequence analysis of the rabies N gene differentiated genetic groups of rabies

viruses. The extent of sequence divergence between them provides a quantitative measure of their relationship. The molecular epidemiology of rabies in China has been reported years (Gu et al., 2001; Meng et al., 2007; Zhang et al., 2006). Gu divided eight isolates from Guangxi only into three groups by analyzing N gene and Meng divided 39 isolates from different provinces of China into four groups by analyzing the full length of G gene. In this study, we cloned and sequenced the 3 -terminal region, nucleotides 1–455, of 42 isolates. This region includes the fragment 99–405, as reported by Kissi (Kissi et al., 1995). The homologies of the 42 isolates based on the region 1–455 indicated that they belonged to genotype 1 and could be divided into four groups: I, II, III, and IV. In Meng’s analysis, group I consisted primarily of samples from Anhui, Hunan, Hubei, and Jiangsu Provinces. Only two isolates Yue 1 and N11 from Guangxi Province lay on a separate branch within group I. This group is similar to group II in our investigation. Group II, including the isolates from Chongqing and Ningxia in the centre of China, was independent. Group III comprised two isolates from Guangxi together with a vaccine strain CTN from Shandong, and this group is consistent with our group I, because our group I also included

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301

Fig. 3. Geographical distribution of rabies virus isolates from Guangxi, The distribution of rabies virus isolates in group I ( and group IV ( ).

); group II (

); group III (

);

the strain CTN. However, in our analysis, group I included the majority of rabies virus isolates from the south-eastern area of Guangxi. Meng’s group IV included CHI1-BK from a deer, MRV from a mouse in Henan and DRV from a deer from Jilin; and concluded several laboratory and vaccine strains. Our research also showed that eight isolates, including one from a normal cat, mapped to the southern area of Guangxi, and to group IV with vaccine strains. The unique isolate GXN119 from Nanning, together with the isolate 8738tha from Thailand, was placed into group III. This ?nding is different from that of Meng’s report (Meng et al., 2007). Transmission of rabies by asymptomatic animals is an intriguing possibility. In India a dog that had no detectable antibody was found to excrete rabies virus intermittently

in its saliva over 30 months (Veeraraghavan et al., 1968). In Ethiopia rabies virus was isolated repeatedly from 0.5% of asymptomatic, naturally infected dogs (Fekadu, 1972). And street rabies virus was isolated from saliva of 0.3% of healthy dogs in Nigeria (Aghomo and Rupprecht, 1990). It is noteworthy that 23 rabies virus isolates were collected from normal dogs without clinical symptoms. Our statistical data showed RT-PCR positive rate for rabies virus in clinically normal dogs has gradually increased from 2001 to 2005 (data not shown). These rabies virus carriers, clinically normal dogs, are dangerous to humans and other animals. This phenomenon might be due to the incubation period of rabies. Because the incubation period of rabies is the most variable among viral infections of the CNS, the range is from 7 days

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to more than 6 years (Hemachudha et al., 1991; Hemachudha and Phuapradit, 1997; Smith et al., 1991). The mechanism is need to further study. We compared the nucleotide sequences of isolates from different parts of the world obtained from the GenBank database with those of 43 isolates from China, including 42 isolates from Guangxi and one isolate from Shandong Province. Phylogenetic analysis based on 455 nucleotides of the 3 -terminal of the N gene in this study indicated that the rabies viruses from Guangxi are distantly related to isolates from surrounding countries such as India, Sri Lanka, and North Korea (Fig. 1). Although rabies isolates in the same geographic area tend to constitute a group, the unique isolate GXN119 from a clinically normal dog brain in Nanning, together with isolate 8738tha from Thailand, constituted group III. The identity of nucleotides between both isolates was 95.8%, and homology of deduced amino acid was 96.7%. Further study on how the isolate GXN119 transmit to/or where it come from, in order to explain the relationship between the isolate GXN119 from Guangxi and the isolate 8378tha from Thailand. Comparison of the deduced amino acid sequences of the isolates with that of ERA showed that proline at position 58 became serine in all 42 isolates. Thirty-four isolates of groups I, II, and III had six common mutations: H26Y, C40S, S61N, V95L, G106D, and P135S. Group I had two groupspeci?c mutations: T90N and E110D. Group II had one group-speci?c mutation: T42S (Fig. 2). The rabies virus isolates from Guangxi varied in topographical distribution. These observations may be explained by the fact that Guangxi acts as a transfer station, playing an important role in national commercial activity. Commodities, including animals, from eastern regions such as Guangdong, Hainan, and Hong Kong must pass through Guangxi on their way to western regions such as Yunnan, Guizhou, and Sichuan, and vice versa. Eight isolates from the southern area of Guangxi belonged to group IV. These isolates were obtained from brain samples from seven clinically normal dogs and one clinically normal cat. Interestingly, the isolates did not cause neural symptoms clinically when they were injected into the brain of mice (data not shown). According to their nucleotide homology, these isolates are very close to the ?xed strains ERA, SAD and PV. This is the new presentation of molecular epidemiological data of rabies in the Guangxi of China. Compared with reports of Gu and Meng (Gu et al., 2001; Meng et al., 2007), our research revealed that rabies viruses in Guangxi exist a close genetic relationship and geographical distribution. Isolates of group I were prevalent in the south-eastern area of Guangxi. Isolates of group II were mainly found in the western area. Isolates of group IV were mainly found in the south of Guangxi (Fig. 3). All indications are that the rabies epidemic in dogs will continue to spread in the foreseeable future in Guangxi. The infection cycle is mainly maintained in dogs, but occasionally spills over to other species such as cattle, cats, and pigs. The importance of this study is that this

molecular epidemiological data might provide suggestions for more effective prevention of rabies in Guangxi.

Con?icts of interest We declare no con?ict of interest.

Acknowledgements We are grateful to the local veterinary stations for their cooperation in carrying out the study and for their valuable support in collecting samples. The study is supported by grant from The National Basic Research Program (973 Program) of China (2005CB523003); by the Scienti?c Research Foundation for Returned Overseas Chinese Scholars, State Education Ministry ([1998]–679); and by The Key Technology R&D Program of Guangxi Province (Guikegong 0537008-3C).

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