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. 2023 Mar 7;24(2):e29. doi: 10.4142/jvs.22197

Isolation of feline panleukopenia virus from Yanji of China and molecular epidemiology from 2021 to 2022

Haowen Xue 1,†, Chunyi Hu 1,†, Haoyuan Ma 1, Yanhao Song 1, Kunru Zhu 1, Jingfeng Fu 1, Biying Mu 1, Xu Gao 1,✉
PMCID: PMC10071280  PMID: 37012037

Abstract

Background

Feline panleukopenia virus (FPV) is a widespread and highly infectious pathogen in cats with a high mortality rate. Although Yanji has a developed cat breeding industry, the variation of FPV locally is still unclear.

Objectives

This study aimed to isolate and investigate the epidemiology of FPV in Yanji between 2021 and 2022.

Methods

A strain of FPV was isolated from F81 cells. Cats suspected of FPV infection (n = 80) between 2021 and 2022 from Yanji were enrolled in this study. The capsid protein 2 (VP2) of FPV was amplified. It was cloned into the pMD-19T vector and transformed into a competent Escherichia coli strain. The positive colonies were analyzed via VP2 Sanger sequencing. A phylogenetic analysis based on a VP2 coding sequence was performed to identify the genetic relationships between the strains.

Results

An FPV strain named YBYJ-1 was successfully isolated. The virus diameter was approximately 20–24 nm, 50% tissue culture infectious dose = 1 × 10−4.94/mL, which caused cytopathic effect in F81 cells. The epidemiological survey from 2021 to 2022 showed that 27 of the 80 samples were FPV-positive. Additionally, three strains positive for CPV-2c were unexpectedly found. Phylogenetic analysis showed that most of the 27 FPV strains belonged to the same group, and no mutations were found in the critical amino acids.

Conclusions

A local FPV strain named YBYJ-1 was successfully isolated. There was no critical mutation in FPV in Yanji, but some cases with CPV-2c infected cats were identified.

Keywords: Cats, capsid protein, PCR, mutation, sequence analysis

INTRODUCTION

Feline panleukopenia virus (FPV), canine parvovirus (CPV), and mink enteritis virus are examples of familiar parvovirus members [1,2]. Animal parvoviruses, the genus parvovirus within the family parvoviral, are usually accountable for acute gastroenteritis and leukopenia in young animals. FPV was first identified in 1928 and was isolated in tissue culture in 1964 [3,4]. CPV surfaced as a canine pathogen in the late 1970s [5]. However, the origin of CPV is still unclear. Some studies suggest that FPV might be an ancestor of CPV [6,7].

FPV causes feline panleukopenia. This virus has been shown to infect non-domesticated cats and is known to cause all feline illnesses [8]. FPV is a 5,000 bp long single-stranded DNA virus. FPV has an open reading frame at the 5' and 3' ends of the genome, encoding non-structural proteins NS1 and NS2, respectively, and capsid proteins VP1 and VP2 [9,10]. The empty virus particles contain only VP1 and VP2. After completing the packaging and capsid assembly of the viral genome, VP2 is cleaved to produce VP3 [11]. The difference in several amino acid residues of VP2 proteins is known to cause differences in antigenicity and host range between CPV and FPV, affecting the virus’s surface structure and thereby distinguishing the two viruses [12,13,14]. Asn93, Ala103, and Asn323 are essential for CPV replication in canine cells, whereas Lys80, Asn564, and Ala568 are essential for FPV replication in feline cells. CPV-2a and CPV-2b differ from the original virulent strain CPV based on differences in amino acids at positions 87, 300, and 305 of the VP2 protein. The feline host range of the new antigenic types CPV-2a and CPV-2b are most likely determined by the changes in amino acids Met87Leu, Ala300Gly, and Asp305Tyr. The substitution of Asn426Asp differentiates CPV-2b from CPV-2a. In 2000, a novel CPV mutant was found in Italy. The VP2 of this novel mutant had an Asp426Glu mutation named CPV-2c [13]. Currently, CPV-2a, CPV-2b, and CPV-2c subtypes have been isolated from healthy cats and cats with plague [15,16,17]. Although FPV is very similar to CPV, the faster mutation rate of CPV makes it resemble an RNA virus. The CPV and FPV clades’ substitution rates are 1.7 × 10−4 and 9.4 × 10−5 substitutions/site/year, respectively [18]. Contrary to CPV, FPV has slowly mutated since it was discovered. Only one subtype is known, but the slow mutation rate does not affect its high threat to cats.

In this study, a strain of FPV from a cat with feline panleukopenia was isolated in an animal hospital in Yanji, China. The nucleotide sequence of the capsid protein 2 gene of the new isolation was determined compared with those of reference FPV and CPV strains. Yanji has a very developed dog and cat breeding industry, so we should pay more attention to the variation of FPV. There has never been any related investigation and research in the local area before, so an epidemiological survey was conducted in Yanji City, Jilin Province.

MATERIALS AND METHODS

Preliminary identification of clinical samples

A 6-month-old cat with vomiting and hematochezia was admitted to an animal hospital in Yanji. The cat was suspected of having panleukopenia. The breeder of the cat was questioned about the vaccination history. We learned that this cat had never been vaccinated against FPV. After dipping a cotton swab in the sample diluent, fecal samples are obtained in the cat’s rectum and blended equally with the diluent. Four drops of sample supernatant were collected using a sampling suction tube and inserted into the sample hole of FPV colloidal gold test paper (Anigen, Korea). The results were visualized after 5–10 min.

Virus isolation

The anal swabs of the sick cats were collected and vortexed in a 1.5 mL centrifuge tube containing 0.9% saline. The swabs were discarded, and the liquid was centrifuged for 10 min at 5,000 rpm. The supernatant was filtered with a 0.22 μm bacterial filter. The filtrate was inoculated in 90% F81 cells (preserved in our laboratory) cultured in a culture flask and placed in a 37°C, 5% CO2 incubator. F81 cells without virus inoculation were used as the blank control group. After five cell passages, the virus solution was harvested and stored in a refrigerator at −80°C for subsequent experiments.

Electron microscope observation

The 5th passage of the virus solution was concentrated and infiltrated into the copper mesh of the electron microscope and negatively stained with 2% phosphotungstic acid. Finally, the morphological properties of virus particles were examined.

The 50% tissue culture infectious dose (TCID50) determination of viruses

The 5th passage virus solution was diluted in a 10−1–10−10 gradient and inoculated into 96-well cell plates. The cells were grown at 37°C with 5% CO2 for 120 h. The TCID50 of the isolate was calculated using the Reed-Muench method.

Cloning and sequence analysis of the VP2 gene

According to the VP2 gene of FPV strain (accession number: M38246) registered in GenBank, primers were designed and synthesized using Oligo6.0 (Molecular Biology Insights, USA) to amplify the whole VP2 gene sequence (VP2-F: 5'-ATGAGTGATGGAGCAGTTCAAC-3'; VP2-R: 5'-GTATACCATATAACAAACCTTC-3'). The polymerase chain reaction (PCR) amplification process was as follows: pre-denaturation at 95°C for 5 min, followed by denaturation at 94°C for 30 sec, annealing at 57°C for 1 min, and extension at 72°C for 2 min.

A total of 35 reaction cycles were performed, and the final extension was done at 72°C for 10 min at 4°C. The expected length of the FPV VP2 gene was 1,932 bp. The gel recovery kit (Omega, USA) was used to recover the target gene following the manufacturer’s instructions. The target gene was connected to the pMD-19T simple vector (Takara, Japan), transforming into competent Trans5α (TransGen Biotech, China) cells. Escherichia coli was cultured, and the monoclonal colonies were selected. PCR identification was performed based on the primers mentioned above and reaction conditions. The positive colonies were expanded, cultured, and sent for sequencing (Comate Bioscience Co., Ltd., China).

Phylogenetic analysis of isolates

The sequencing results were sorted to find the complete VP2 gene sequence and compared with the sequence of reference strains in the GenBank database. The amino acid sequence of the VP2 gene was compared via DNAstar (DNASTAR, Inc., USA) and MEGA X (Mega Limited, New Zealand) software. Both homology and phylogenetic analysis were carried out.

Molecular epidemiology of FPV in Yanji City

From 2021 to 2022, 80 clinical samples of suspected FPV infection, including the above isolates, were gathered from each veterinary hospital in Yanji City. Vomiting, diarrhea, hematochezia, dehydration, and mental impairment were the clinical symptoms of probably infected cats. Except for the isolates mentioned above, 79 suspicious samples were discovered utilizing PCR amplification employing the above test procedures. Sequencing was performed on the positive samples. Using the DNAstar and MEGAX tools, the amino acid sequences of the obtained VP2 gene were homologically and phylogenetically analyzed.

RESULTS

Preliminary identification of clinical samples

There were red bands on the C-line and T-line of the FPV colloidal gold test paper, indicating that the feline tested positive for the FPV antigen. Therefore, the cat infected with FPV was diagnosed with feline panleukopenia.

Virus isolation

The cells showed cytopathic effects (CPEs) after 48 h of virus (5th passage) inoculation. Under the microscope, the cell morphology was round. Many adherent cells became non-adherent. No CPE was observed in uninoculated cells under the same culture conditions (Fig. 1).

Fig. 1. Microscopic observation of cell results. Amplified factor 100. (A) Virus-inoculated F81 cells; (B) Uninoculated F81 cells.

Fig. 1

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Electron microscope observation

The stained virus solution was placed under an electron microscope, and the virus particles were observed. There was no envelope structure outside. The diameter was approximately 20–24 nm. The particles were round, and the morphology was complete (Fig. 2). Therefore, the isolated FPV strain was identified as YBYJ-1.

Fig. 2. Electron microscopic observation results.

Fig. 2

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TCID50 determination of viruses

The TCID50 of the isolated strain was determined to be 1 × 10−4.94/mL. The virus was diluted 104.94 times and inoculated at 100 μL/well in a 96-well cell culture plate, which made half of the cells appear cytopathic.

Sequence analysis of the VP2 gene

The VP2 gene of the isolate was amplified, and the target DNA band was found at 1,932 bp.

The sequenced bands were cut using DNAstar software to obtain a 1,755 bp long DNA sequence. The amino acid sequences were compared with those of the FPV standard strain (GenBank: M38246). The amino acids at 10 sites (80, 87, 93, 103, 300, 305, 323, 426, 564, 568) that determine the host range and antigenic specificity of FPV were compared with the FPV standard strain (GenBank: M38246) and representative strains of each CPV subtype (Table 1). This study found that the significant amino acid sites of the viral strains identified were compatible with those of the FPV standard strain M38246. There was no significant difference.

Table 1. Comparison of amino acid mutations between YBYJ-1 isolated in this study and FPV and CPV subtypes.

Genotype GenBank Analysis of major amino acid sites
80 87 93 103 300 305 323 426 564 568
FPV (YBYJ-1) OM212011 K M K V A D D N N A
FPV M38246 K M K V A D D N N A
CPV2 M38245 R M N A A D N N S G
CPV2a EU659118 R L N A G Y N N S G
CPV2b M74849 R L N A G Y N D S G
CPV2c FJ005243 R L N A G Y N E S G
NewCPV2a U72695 R L N A G Y N N S G
NewCPV2b GQ379042 R L N A G Y N N S G
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FPV, feline panleukopenia virus; CPV, canine parvovirus; A, Ala; D, Asp; E, Glu; G, Gly; K, Lys; L, Leu; M, Met; N, Asn; R, Arg; S, Ser; V, Val; Y, Tyr.

Phylogenetic analysis of isolates

As a reference, FPV and CPV strains from Asia, Europe, and Oceania were used to compare the homology of VP2 gene sequences between this isolate and other known strains. Sequence homology analysis was performed by the MegAlign program in DNAstar software (Fig. 3). The results showed that the FPV YBYJ-1 isolate had high homology with the FPV strains from all over the world and relatively low homology with CPV. The FPV YBYJ-1 isolate shared 99.7% homology with the FPV type strain (GenBank: M38246). The Shanghai, China FPV reference strain (GenBank: MW811187) shared the isolate's highest degree of homology (99.8%). The Indian FPV reference strain (GenBank: MH559110) had the lowest degree of homology (97.4%). YBYJ-1 had much more homology with FPV than with CPV.

Fig. 3. The homology analysis of FPV isolates YBYJ-1 with some FPV and CPV-2 in the GenBank database. The FPV strains in this isolation are marked by blue boxes.

Fig. 3

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FPV, feline panleukopenia virus; CPV, canine parvovirus.

The Neighbor-Joining method constructed the phylogenetic tree using MEGA X software (Fig. 4). The results showed that the VP2 sequence of the isolate formed a monophyletic branch with some reference sequences in the GenBank database. Furthermore, it was not in the same branch as the reference sequence of CPV.

Fig. 4. The phylogenetic tree based on the complete VP2 sequences of FPV, together with CPV, was performed with the Neighbor-Joining method. Amino acid sequences were analyzed using the MEGA X software with a bootstrap test of 1,000 replicates. The red font represents the currently isolated FPV strain (YBYJ-1).

Fig. 4

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FPV, feline panleukopenia virus; CPV, canine parvovirus.

Sample collection and processing

This study collected 80 cases of suspected positive samples, including the above isolates. The VP2 gene of FPV was identified by PCR amplification. A total of 30 cases of PCR-positive samples, including the above isolates, were obtained. The detection rate was 37.5% (30/80). The VP2 gene of all positive samples was sequenced. The sequencing results were uploaded to the GenBank database to expand the information regarding FPV. Specific sample information is shown in Table 2.

Table 2. All feline panleukopenia virus-positive samples were detected in this epidemiological survey.

Name Age (mon) Clinical symptoms Vaccine history GenBank
1 (YBYJ-1) 6 Vomiting, hematochezia - OM212011
2 1 Fever, vomiting - OM322821
3 5 Vomiting, diarrhea - OM885373
4 3 Vomiting, hematochezia - OM885374
5 6 Dispirited, feverish - OM885375
6 2 Watery diarrhea - OM885376
7 3 Vomiting, sticky feces ○ OM885377
8 5 Vomiting, diarrhea + OM885378
9 8 Fever, hematochezia ○ OM885379
10 7 Dispirited, feverish - OM885380
11 4 Vomiting, diarrhea - OM885381
12 2 Diarrhea - OM885382
13 9 Vomiting, sticky feces - OM885383
14 5 Vomiting, diarrhea - OM885384
15 4 Fever, vomiting, diarrhea - OM918770
16 10 Vomiting, sticky feces ○ OM918771
17 5 Diarrhea, dehydration + OM918772
18 6 Fever, vomiting - OM918773
19 7 Vomiting, diarrhea - OM918774
20 15 Vomiting, hematochezia ○ OM918775
21 2 Watery diarrhea, vomiting - OM918776
22 5 Fecal sticky blood - OM918777
23 1 Watery diarrhea - OM918778
24 2 Vomiting, diarrhea - OM918779
25 7 Fever, vomiting, diarrhea ○ OM918780
26 3 Fever, vomiting - OM918781
27 8 Diarrhea, dehydration + OM918782
28 6 Fever, diarrhea ○ OM918783
29 9 Vomiting, fecal adhesion - OM918784
30 1 Vomiting, diarrhea - OM918785
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The first strain (YBYJ-1) was the above isolate.

-, unvaccinated vaccine; +, vaccines have been inoculated; ○, incomplete inoculation.

Phylogenetic analysis

Forty-three FPV reference strains and 17 CPV reference strains were collected, including 2 FPV vaccine strains. Combined with the 30 strains in this study, MEGAX software was used for homology analysis (Fig. 5) and phylogenetic analysis (Fig. 6). The results showed that among the 30 isolates in this study, three CPV had been identified unexpectedly. Comparing the critical amino acid sites found that the characteristics were consistent with those of CPV-2c (Leu87, Thr101, Tyr267, Ala297, Gly300, Tyr305, Ile324, Glu426, Val555). The binding sites of 27 strains of FPV were all conserved. Moreover, there was no key mutation. Additionally, the result showed the two amino acid sites with a high mutation probability (the amino acids at sites 91 and 101). Among the 27 FPVs, 22/27 (81%) had the Ala91Ser mutation, 2/27 (7%) had the Ala91Leu mutation, and all (100%) had the Ile101Thr mutation.

Fig. 5. Homology analysis of the investigated FPV-VP2 sequences and the nine reference strains. For our 39 sequences, FPV is marked in blue and CPV is marked in red.

Fig. 5

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FPV, feline panleukopenia virus; CPV, canine parvovirus.

Fig. 6. The phylogenetic tree based on the complete VP2 sequences of FPV, together with CPV, was performed with the Neighbor-Joining method. Amino acid sequences were analyzed using the MEGA X software with a bootstrap test of 1,000 replicates. The FPV can be divided into three gene groups; the orange background is group 1; the green background is group 2; the blue background is group 3, and the red background is the reference sequence of CPV. The symbols used to distinguish the different strains are as follows: the red triangular icon (▲) represents the vaccine strain of FPV, while the red circular icon (●) represents the FPV sample of this investigation.

Fig. 6

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FPV, feline panleukopenia virus; CPV, canine parvovirus.

Standard strains of FPV, vaccine strains and representative strains of each subtype of CPV were selected as a reference to analyze the homology with the 30 samples. The homology of strains 2, 15, and 26 with CPV was significantly higher than that of FPV. The homology between the 27 FPV and the FPV reference strains remained > 98%.

In the phylogenetic analysis, FPV was divided into three groups. Most of the 27 FPV strains in this survey belonged to group 3 (22/27, 81%). A small part belonged to group 2 (5/27, 18.5%). The two vaccination strains belonged to group 1, which was genetically distinct from the other 27 FPV viruses by a wide margin. Furthermore, the strains isolated in this survey shared a close genetic relationship with strains obtained from other provinces in China and relatively distant genetic relationships with strains from outside China.

DISCUSSION

In this study, an FPV was isolated and identified. After verification, the isolated strain was observed to be consistent with the characteristics of FPV. Next, the prevalence of FPV was investigated in Yanji, China, in the past 2 years. The result showed that FPV did not appear in the key mutation performance, but there were three cases of CPV infection in cats. FPV and CPV, which are very closely related viruses with a genome homology of 98%, are significant pathogens for domestic felines, canines, and various wild carnivorous species [4]. However, the critical difference between these two parvoviruses is that FPV varies slowly by random genetic drift. In contrast, CPV shows genomic substitution rates similar to those of the RNA viruses with values of approximately 10-4 substitutions/site/year under selection pressure [18,19].

An epidemiological investigation of local FPV infections showed that most cases of FPV infection were not vaccinated. The age of the infection was generally < 8 months (26/30, 86.7%). The VP2 variation study revealed that 27 of the 30 strains were consistent with the standard strain in 10 critical amino acid positions, dictating the viral characteristics. It also revealed that the FPV gene’s variation rate was sluggish, and the gene was relatively conserved. However, this study identified a high mutation rate of amino acid residues 91 and 101. Previous research has demonstrated considerable changes in antigenicity between FPV and CPV, governed by amino acid residues 93 and 101 of the VP2 protein [12]. In the VP2 protein’s tertiary structure, amino acids in the 50th to 100th position from Loop 1 play a crucial role in the antigenicity of the virus [20]. Furthermore, amino acid 91, with a high mutation rate, is located within the Loop 1 structure. Among them, the earliest isolated VP2 proteins of FPV (GenBank: M38246) and CPV (GenBank: M38245) have Ile at amino acid position 101. Almost all new isolates have mutated to Thr at amino acid 101 of the VP2 protein. Although 101 Thr is not in the Loop1 structure, it is very close to Loop1 in space, which inevitably affects the antigenicity of the virus. Regardless of how much FPV and CPV differ in the amino acid sequences of their VP2 genes, amino acids 80, 93, 103, 323, 564, and 568 are highly conserved [4,21]. According to some research, four crucial amino acids, 87, 300, 305, and 426, are also involved in host identification. Previous studies have shown that changes in the above 10 amino acids have the potential to alter host range, TfR binding, and antigenic structure in parvoviruses [20,22]. A 2020 study, for example, reported an FPV isolated from monkeys. The amino acids in FPV VP2 323 and 564 were identical to those in CPV. Mutations in these two amino acids may increase the FPV host range to include monkeys [23]. A new FPV strain isolated in this study was compared with the FPV standard strain (GenBank: M38246). There were no variations in these ten amino acid sites, indicating that the VP2 of this isolate was very conservative.

By comparing the homology between FPV and CPV, the result showed that the homology between the earliest isolated CPV strains and FPV was slightly higher than that between other CPV subtypes and FPV, which supported the viewpoint that FPV preceded CPV [6,7]. Although the genetic link between vaccine strains (GenBank: EU489360 and EU498361) and the local Chinese FPV is somewhat distant, they nonetheless have a significant protective efficacy. In this study, most diseased cats had never been vaccinated or received all of their immunizations. However, despite FPV vaccines, several cats from the sample source were still infected, which could be attributable to variances in physical fitness and living habits of cats or FPV infection while vaccinated but not yet operating.

The above variations of FPV sharply contrast with recent epidemiological studies on CPV. For example, recent studies in Australia have indicated that the dominant antigenic variant is shifting from CPV-2a to CPV-2b [24]. An epidemiological assessment of CPV in Japan in recent years revealed that the CPV-2b variant was dominant from 2014 to 2019. Japan, as an Asian country, was far from Australia, but the variance of CPV was similar [25]. This indicated a global trend in CPV evolution and prevalence. Surprisingly, three CPV-2c strains were finally confirmed in this investigation, showing that felines were among the CPV-2c host animals. We suspected this was caused by exposure to CPV-2c-infected dogs’ secretions or excretions. Previously, an epidemiological survey of CPV was conducted in Yanbian Prefecture, and the results revealed local transmission of CPV-2c [26]. This incident demonstrated that, while FPV was the ancestor of CPV, CPV mutation was more rapid and deadly.

The Yanbian Korean Autonomous Prefecture of Jilin Province borders Korea, Russia, and other nations, and the dog breeding industry is more developed in the area due to the traditional culture of Chinese Korean nationality. Yanji City, the capital of Yanbian Korean Autonomous Prefecture, is the economic and cultural hub of the region. The expanded dog breeding sector may result in a higher prevalence of CPV in the area. Because CPV may infect cats, the three incidences of CPV-2c infection in cats discovered in this study indicated that both FPV and CPV endangered the cats in Yanji City. Innovative vaccinations must be developed to avoid the potential large-scale spread of CPV and FPV.

Footnotes

Funding: This study was supported by Natural Science Foundation (20210101368JC) and “13th Five-Year” Science and Technology Project of Education Department of Jilin Province (JJKH20200521KJ) of Yanbian University, China.

Conflict of Interest: The authors declare no conflicts of interest.

Author Contributions:
  • Conceptualization: Xue H.
  • Data curation: Hu C, Ma H.
  • Formal analysis: Ma H.
  • Funding acquisition: Gao X.
  • Investigation: Hu C.
  • Methodology: Xue H.
  • Project administration: Song Y.
  • Resources: Zhu K.
  • Software: Xue H.
  • Supervision: Gao X.
  • Validation: Fu J.
  • Visualization: Mu B.
  • Writing - original draft: Xue H.
  • Writing - review & editing: Gao X.

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