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Genotype of Varicella-zoster virus isolated in Jiangsu, China

Virology Journal volume 21, Article number: 264 (2024) Cite this article

Abstract

Objective

To analyze the genotypes of VZV in Jiangsu province to identify vaccine strains and wild strains, providing a molecular biological background for the effective prevention and control of varicella.

Method

Stratified sampling was used to collect herpes fluid or throat swab from patients diagnosed with varicella. ORF22 was carried out, and the restriction enzyme site of ORF38, ORF54 and ORF62 were detected.

Results

All 207 virus strains were Clade 2 type by sequencing the PCR products of ORF22. The sequencing results showed that five SNP sites changed compared to the Dumas reference strain(Clade 1). From A to G at 37,902, from T to c at 38,055, from A to C at 38,081, and from G to A at 38,177, from G to A at 39,394. The prevalent VZV genotypes in Jiangsu is consistent with the P-Oka. The restriction enzyme site analysis of PCR amplification products from ORF38 (PstI), ORF54 (BglI), ORF62 (SmaI) showed that all 207 virus strains were wild-type. There were two different types of the wild strains, and 183 strains (88.4%) were PstI (+), BglI (+), SmaI (-). The wild strains between different regions showed no significant differences (χ2 = 0.05, P = 0.982).

Conclusions

The prevalent VZV genotypes are Clade 2 and the prevalent virus strains are wild strains in Jiangsu Province, the primary wild strain observed is mainly PstI (+), BglI (+), SmaI (-).

Introduction

Varicella-zoster virus (VZV) belongs to family Herpesviridae and is a member of subfamily Alphaherpesvirinace, which is a highly conserved double stranded DNA virus and only infects only infects humans [1]. Its genome is 125 kb in length and with 74 open reading frames (ORF) coding at least 71 genes [2]. The variation between different strains is only 0.1%, which is manifested as manifested as single nucleotide polymorphisms (SNPs) [3]. Varicella is typically a self-limiting disease, but it may still lead to serious complications [4, 5].

Genotyping of VZV helps understand viral diversity, recombination, evolution and transmission. At present, some molecular biology techniques such as genome sequencing, SNPs, and restriction fragment length polymorphism (RFLP) have been applied to determine the genotype of VZV and distinguish vaccine strains from wild strain [6,7,8,9]. According to the international nomenclature of the VZV genotype, VZV can be divided into five major genotypes (Clade 1–5) and two tentative genotypes to be confirmed (Clade VI and VII) [10]. Genotyping method based on SNPs in ORF22 is currently widely used to discriminate different VZV viral clades [11]. In previous study, PstI restriction enzyme site in ORF38 and BglI restriction enzyme site in ORF54 were analyzed by RFLP to identify the vaccine strain [6]. Restriction enzyme site of VZV wild-type strains prevalent in different regions vary. Vast majority of VZV wild-type strains in Europe and North America contain a PstI restriction site in ORF38 [12], while only 20% of the wild strains in the United States and the United Kingdom contain a BglI restriction site in ORF54 like Oka vaccine strain [13]. However, there are some limitations to differentiate Oka vaccine from wild-type VZV strain in circulation with PstI restriction endonuclease. Therefore, amplification of specific fragments of ORF62 with SmaI restriction endonuclease can distinguish Oka-like and non-Oka like wild strain from Oka vaccine strain [6].

While the live attenuated varicella vaccine (Oka strain) is widely available globally and has been proven to be the most effective measure for the prevention and control of varicella [14,15,16], our previous study revealed a high proportion of breakthrough varicella cases in Jiangsu Province [17]. Additionally, there was no available information on the circulating genotype of VZV in Jiangsu Province. The aim of our study is to determine the genotype of VZV and explore the reasons for higher proportion of breakthrough varicella by molecular epidemiology method in Jiangsu Province, east coast of China.

Materials and methods

Patients and clinical samples

According to the geographical location, the whole province was divided into three regions: the north, the middle, and the south. Two cities from each region were selected, respectively, and patients clinically diagnosed with varicella from September to October 2019 were included in this study. Finally, the research sites were Xishan District and Wujin District in the south, Rugao City and Xinghua City in the middle, and Ganyu County and Siyang Country. Patients’ information, including age, gender, date of rash onset, and history of varicella vaccination, was collected. Herpes fluid or throat swabs of patients were collected by the local general hospital or community health center and sent to the Jiangsu Provincial Center for Disease Control and Prevention for storage in a -40 °C freezer. This study was approved by the Jiangsu Provincial Center for Disease Control and Prevention Ethics Committee.

DNA extraction and polymerase chain reaction (PCR)

Viral DNA of VZV was extracted from patient’s herpes liquid or throat swabs using a highly efficient DNA extraction kit (QIAGEN Bio, Inc., Shanghai, China). PCR amplification was carried out in a 25-ul reaction mixture including 2X PrimesSTAR® RMax DNA Polym.erase (Takara Bio, Inc., Beijing, China), 0.2 μm of each primer and sterilized distilled water. To determine the genotype of VZV, we amplified the 447-bp fragment of VZV ORF22. In order to distinguish VZV vaccine strain from wild strain, the target fragment amplification of ORF38, ORF54, and ORF62 was performed. The primers used in PCR are shown in Table 1. The condition for PCR reaction was as follows: A denaturation cycle at 98℃ for 4 min, 35 cycles of 98℃ for 10 s, annealing at 55℃ for 5 s and extension at 72℃ for 5 s, followed by a final extension at 72℃ for minutes. PCR amplification of this study was performed with gradient PCR.

Table 1 Primers uses for amplifying the fragments in VZV
Full size table

Sequencing and restriction enzyme reaction

The PCR product of the 447-bp fragment of ORF22 was sent to the Shanghai Shenggong Biomedical Co., Ltd for sequencing. The sequencing results were analyzed with MEGA X (https://www.megasoftware.net/). The sequencing data was compared with the Dumas strain (Genbank No. X04370), and the VZV genotype was determined by analyzing six SNPs sites (37902,38019,38055,38081,38177,39394).

The restriction endonuclease digestion was a 20 ul mixture including 10 ul of PCR products, 1 ul of restriction endonuclease (PstI, BglI, SmaI; Takara Bio Inc.), 2ul of the accompanying 10X buffer, and 7 ul of Dnase-and-Rnase-free water. PCR amplificates were purified before digestion and the DNA concentration was measured in order to always use the same concentrations during digestion. The reaction mixtures were incubated at 37 ℃ for 3 h for PstI and BglI and 30 ℃ for 3 h for SmaI. The digested products of three restriction endonuclease were analyzed by capillary electrophoresis.

Statistical analysis

Pearson chi-square test was used for comparison of categorical data. A p-value < 0.05 was considered statistically significant. All statistical analyses and drawing were performed with R 4.3.0(R Foundation for Statistics).

Results

Patients’ characteristics

A total of 207 patients with varicella were included. There were 81 cases in the south, 66 cases in the middle and 60 cases in the north. The median age of the patients was 6.9 years old(range interquartile,5.8–9.2). Among them, 105 (50.7%) were male patients and 100 (48.3%) had a history of one-dose varicella vaccination, the average interval after varicella vaccination was 6.1 years. The patients’general information was showed in Table 2.

Table 2 General information of varicella patients
Full size table

Genotype of VZV

The sequencing results of the PCR product of ORF22 showed that all 207 virus strains were Clade 2. Five SNP sites changed compared with the Dumas reference strain(Clade 1) according to the sequencing results. From A to G at 37,902, from T to c at 38,055, from A to C at 38,081, and from G to A at 38,177, from G to A at 39,394(Table 3). The prevalent VZV genotype in the Jiangsu Province was consistent with the P-Oka.

Table 3 Genotype of varicella-zoster virus identified in this study
Full size table

Restriction fragment length polymorphism (RFLP)

The product of ORF38(647-bp) was cleaved into fragments of 290-bp and 357-bp by PstI. The product of ORF54(497-bp) was cleaved into fragments of 241-bp and 256-bp by BglI. The product of ORF62(268-bp) was cleaved into fragments of 79-bp,153-bp and 36-bp fragments by SmaI. (Fig. 1). 207 strains of virus strains were all wild strains. There were two different types of the wild strains, 24 strains (11.6%) were PstI (+), BglI (+), SmaI (+), and 183 strains (88.4%) were PstI (+), BglI (+), SmaI (-)(Table 4). The wild strains between different regions showed no significant difference (χ2 = 0.05, P = 0.982) (Fig. 2).

Fig. 1
figure 1

DNA fragments after amplification by PCR based on ORF 38,54,62 and digestion by restriction endonucleases. (M: size marker)

Full size image
Fig. 2
figure 2

Distribution of two different types of the VZV wild strains in Jiangsu Province. * type1: PstI ＋，BglI＋，SmaI＋; type2: PstI ＋，BglI＋，SmaI－

Full size image
Table 4 Genotype of the VZV strains in the present study and other studies
Full size table

Conclusion

Studies have shown that evolution occurs between different VZV genotypes [18], and it is of great significance to monitor VZV virus strains. VZV genotype distribution may be affected by many factors including climate, virus-host interactions, migration, etc [19]. In this study, the genotypes of 207 virus strains in Jiangsu Province were analyzed to identify vaccine strains and wild virus strains, providing a molecular biological basis for the prevention and control of varicella in Jiangsu Province.

In this study, all of the 207 virus strains in Jiangsu province were Clade 2, which was consistent with a study by Liu on 19 VZV genotypes in Anhui Province [3]. Similarly, studies on VZV genotypes in Shanghai showed that Clade 2 was also the main VZV in Shanghai [19,20,21]. Jiangsu, Wuhan, Anhui and Shanghai are all plain areas along the Yangtze River basin with typical temperate monsoon climate. This suggests that the distribution of VZV genotypes in China has significant geographical characteristics. Combined with studies from Japan and Korea, the main VZV strain circulating in Southeast Asia was Clade 2 type [22, 23]. Globally, the distribution of VZV genotypes has obvious regional specificity, and there are differences among various regions. Unlike from Southeast Asia where Clade 2 is predominant, in South Asia such as India, Clade 4 and Clade 5 are dominant genotypes [12]. While Clade 4 is rare in China, a VZV genotype study in Guangdong detected three cases of Clade 4. This may be due to the fact that Guangdong is located on the southern border of China and there is a high level of outbound movement of people and the possibility of exposure to Clade 4. Peter reported that Clade 4 may be formed due to the recombination of Clade 1 and Clade 2 [24]. According to the international common nomenclature, Clade 1 and Clade 3 are the major epidemic virus strains in Europe and America, while Clade 4 and Clade 5 are the major epidemic genotypes in Africa and spread with African immigrants [10]. A Spanish study with a high proportion of African immigrants showed that Spain had 29% of Clade 5 [12].

In this study, all 207 virus strains collected from Jiangsu province were wild ones. Among them, most (88.4%) of the wild strain ORF38, ORF54, ORF62 showed PstI (+), BglI (+), SmaI (-) as the restriction enzyme cutting sites of PCR products. This is the same as other studies in China [3, 19, 20]. PstI (+), BglI (+) and SmaI (-)type wild strains are the main prevalent wild strains in China.In addition, PCR products of wild strains ORF38, ORF54 and ORF62 (11.6%) showed PstI (+), BglI (+) SmaI (+), which was consistent with the results of a study on VZV gene in Yunnan [1]. This wild strain of PstI (+), BglI (+), SmaI (+) is not common in China, and it was only found in this study and the study in Yunnan. The restriction sites of varicella vaccine strain V-Oka were PstI -, BglI (+), SmaI (+) [10]. Studies have shown that PstI (+), BglI (+), SmaI (-)are the restriction sites of some other wild strains in tropical and subtropical climates in Africa and Asia [25]. PstI (-), BglI (+), SmaI (+) vaccine strains and the main endemic PstI (+), BglI (+), SmaI (-) wild strains exist simultaneously in the environment of Jiangsu region. The wild strains of PstI (+), BglI (+), SmaI (+) are formed through interaction and evolution between two different virus strains. In addition, Jiangsu has a developed economy and a high mobility of foreign population, which may be caused by inflow of population from Yunnan, leading to this type of cycle. The distribution of ORF38, ORF54 and ORF62 PCR products had certain regional differences. PstI (+), BglI (-), SmaI (-)showed the restriction sites of major wild strains prevalent in Europe and the United States [25, 26]. The presence of the BglI locus on ORF54 can be used to identify wild strains prevalent in Europe, America, Asia and Africa. However, the study found changes in VZV strains in Europe and the United States. In the United States, RFLP studies showed that only 10.5% of virus strains had BglI restriction sites in the 1980s, however, this increased to 18.2% in the 1990s [27]. In Germany, the PCR product BglI (+) of ORF54 virus strain isolated from 1997 to 2001 was 6%, compared with 21% in 2006 [25]. The increase in THE VZV strain OF BglI (+) was caused by migration from Asia and Africa.In this study, all VZV were wild strains, 48.3% of the cases had a history of varicella vaccination, and vaccination of varicella vaccine may not be able to prevent VZV wild strain varicella infection.In addition, people with a history of varicella vaccination had an average inoculation interval of 6.1 years, and the wild virus type of varicella infection may be caused by immune failure or weakened immunity.

In summary, Clade 2 was the main VZV gene prevalent in Jiangsu, and the wild strain was the wild strain, which was mainly PstI (+), BglI (+), SmaI (-) type. This study provided baseline information for further understanding of the distribution of VZV genotypes in Jiangsu, and VZV molecular epidemiological surveillance is necessary for the control of VZV infection.

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Acknowledgements

We greatly appreciate the help we received from the Jiangsu Center for Disease Control and Prevention (CDC), the Changzhou CDC and the Wujin CDC.

Funding

This work was supported by the “333” Project of Jiangsu Province, grant number BRA2017538.

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Author notes

  1. Yong Wang, Lei Zhang and Mengqi Bian contributed equally to this work.

Authors and Affiliations

  1. Department of General Surgery, Northern Jiangsu People’s Hospital, Yangzhou, Jiangsu Province, 225001, China

    Yong Wang & Jun Ren

  2. Department of Expanded Programme on Immunization, Jiangsu Provincial Center for Disease Control and Prevention, Nanjing, Jiangsu Province, 210009, China

    Lei Zhang, Hongxiong Guo, Zhiguo Wang, Ying Hu, Xiuying Deng & Xiang Sun

  3. Department of Otorhinolaryngology, Northern Jiangsu People’s Hospital, Yangzhou, Jiangsu Province, 225001, China

    Mengqi Bian

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Contributions

Yong Wang: designed the study, conducted data collection and analysis, wrote the first and subsequent drafts of the manuscript; Lei Zhang and Mengqi Bian: participated in the research design; Zhiguo Wang: data collection; Hongxiong Guo: Experimental guidance; Ying Hu and Xiuying Deng: experiments; Xiang Sun and Jun Ren: critically reviewed and provided extensive feedback on all drafts of the manuscript. All authors approved the final version of the manuscript for submission.

Corresponding authors

Correspondence to Xiang Sun or Jun Ren.

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Ethical approval

The studies involving varicella patients were reviewed and approved by the ethical review committee of Jiangsu Provincial Center for Disease Control and Prevention (JSJK2019-B004-02).

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The authors declare no competing interests.

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Wang, Y., Zhang, L., Bian, M. et al. Genotype of Varicella-zoster virus isolated in Jiangsu, China. Virol J 21, 264 (2024). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12985-024-02543-3

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