Evidence of pestivirus RNA in human virus vaccines
Ryô Harasawa1994, Journal of Clinical Microbiology
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We examined live virus vaccines against measles, mumps, and rubella for the presence of pestivirus RNA or of pestiviruses by reverse transcription PCR. Pestivirus RNA was detected in two measles-mumps-rubella combined vaccines and in two monovalent vaccines against mumps and rubella. Nucleotide sequence analysis of the PCR products indicated that a modified live vaccine strain used for immunization of cattle against bovine viral diarrhea is not responsible for the contamination of the vaccines.
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Live virus vaccines for human use, 29 monovalent vaccines against measles, mumps, rubella or polio, eight polyvalent vaccines against measles-mumps-rubella and one bacterial polyvalent vaccine against Streptococcus pneumoniae, were tested by reverse transcriptase-nested PCR for the presence of petivirus or pestivirus RNA. Twenty-four samples were selected from European manufacturers, ten were from U.S.A. and four from Japan. Five (13.1%) out of 38 tested samples were positive for pestivirus RNA. Three vaccines (rubella and two measles) were from Europe and two (mumps and rubella) from Japan. The 5'-untranslated genomic region of the contaminant pestivirus RNA were amplified by reverse transcription-PCR and sequenced. Analyses based on primary nucleotide sequence homology and on secondary structures, characteristic to genotypes, revealed that the cDNA sequences belonged to bovine viral diarrhea virus (BVDV). A cDNA sequence, detected from one measles sample, belonged to BVDV-1b genotype. Pestiviral cDNA detected from the Japanese mumps and rubella vaccine samples, belonged to the BVDV genotypes 1a and 1c, respectively. Analysis on two cDNA sequences detected from measles and rubella vaccine samples from Europe showed their appurtenance to a new genotype, BVDV-1d. These findings indicate that contamination by animal pestivirus may occur in biological products for human use.
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JOURNAL OF CLINICAL MICROBIOLOGY, June 1994, p. 1604-1605
0095-1 137/94/$04.00+0
Copyright C) 1994, American Society for Microbiology
Vol. 32, No. 6
Evidence of Pestivirus RNA in Human Virus Vaccines
RYO HARASAWA* AND TETSUO TOMIYAMA
Animal Center for Biomedical Research and Branch Hospital, Faculty of Medicine,
The University of Tokyo, Bunkyo-ku, Tokyo 113, Japan
Received 6 December 1993/Returned for modification 7 February 1994/Accepted 7 March 1994
The presence of pestiviruses in cell cultures and in fetal
bovine serum has long been a recognized problem not only in
laboratories but also among vaccine manufacturers (9). Therefore, it is quite possible for an adventitious pestivirus to be
present in live virus vaccines prepared from pestivirus-contaminated master seed virus stocks and/or cell cultures. Procedures
currently in use to detect the adventitious pestivirus in biological products are culture methods and immunological assays.
Detection of pestivirus contamination in viral vaccines has
been hampered because most (99%) of the pestivirus strains
are noncytopathic in cell cultures. Immunological assays are
sometimes incapable of direct detection of low-titer contamination of pestiviruses in vaccines. Therefore, the culture
methods and immunological assays are not perfect for detection of pestivirus contamination in viral vaccines. To our
knowledge, there is no publication available concerning pestivirus contamination in viral vaccines for human use. This
report represents the first evidence of contamination with
pestivirus RNA or pestiviruses in live human virus vaccines
from licensed manufacturers.
We examined five commercial monovalent or combined live
vaccines against measles, mumps, and rubella for pestivirus
contamination by reverse transcription PCR with nested
primer pairs to amplify the 5' noncoding region conserved
among viral genomes of the genus Pestivirus. The PCR primers
used for the first- and second-round amplifications were selected from published sequences (1, 2, 7, 13) and have no
significant nucleotide homology to the genomes of other virus
genera reported so far. A single dose of each lyophilized
vaccine was dissolved in 200 [lI of reconstituent supplied with
the vaccine and subjected to RNA extraction with an RNAzol
B extraction kit (Biotecx Laboratories, Inc., Houston, Tex.).
The RNA was subsequently used for cDNA synthesis and
nested PCR as described previously (4). The first-round primers Fl [5'-ATGCCC(AfT)(C/T)AGTAGGACTAGC-3'] and
Rl (5'-ACTCCATGTGCCATGTACAG-3') amplified an approximately 285-bp product, and the second-round primers F2
[5'-AGTCGTCAGT(A/G)GTTCGA C-3'] and R2 (5'-CTCT
GCAGCACCCTATCA-3') amplified an approximately 155bp product, from the pestivirus cDNA. PCR experiments were
repeated two times for each vaccine in separate laboratories.
Nucleotide sequences of the second-round PCR products were
determined by the method of Sanger et al. (14).
*
Corresponding author. Mailing address: Animal Center for Biomedical Research, Faculty of Medicine, The University of Tokyo,
Bunkyo-ku, Tokyo 113, Japan. Fax: 81-3-3816-5680.
1604
The presence of specific pestivirus RNA was apparent on
the gels after the second-round PCR of the monovalent
vaccines against mumps and rubella and of the two measlesmumps-rubella combined vaccines (Fig. 1). The source of
contamination is currently unknown. The measles and mumps
vaccines were prepared in primary chicken embryo cell cultures and the rubella vaccine was prepared in primary rabbit
kidney cell cultures. All the cell cultures used for vaccine
production were supplemented with fetal bovine serum.
Among animals, pigs and ruminants are natural hosts for
pestiviruses, which include the causative agents of hog cholera
in pigs, border disease in sheep and goats, and mucosal disease
or bovine viral diarrhea in cattle. Bovine viral diarrhea virus
(BVDV) or BVDV RNA in the fetal bovine serum that is used
to grow the host cells used for the preparation of the vaccines
might be a source of contamination, because the mumps
vaccine prepared in primary chicken embryo cells was positive
for the pestivirus RNA. The nucleotide sequences of the PCR
products indicated that the contaminants in the viral vaccines
are distinct from the BVDV vaccine strain 12, which has been
4890-.
267v.2
..234
g194
<118
FIG. 1. Second-round PCR products of pestivirus cDNA resolved
by 4 to 20% gradient polyacrylamide gel electrophoresis. Lane A,
BVDV strain 12 used as a positive control; lanes B and C, measlesmumps-rubella combined vaccines produced by different manufacturers; lane D (negative), a measles vaccine; lane E, a rubella vaccine;
lane F, a mumps vaccine; lane G, a live canine parvovirus vaccine used
as a negative control. The outer lanes on both sides contain molecular
size markers with sizes indicated in base pairs. The significance of weak
extra bands appearing in the positive lanes is unknown.
Downloaded from http://jcm.asm.org/ on July 24, 2020 by guest
We examined live virus vaccines against measles, mumps, and rubella for the presence of pestivirus RNA or
of pestiviruses by reverse transcription PCR. Pestivirus RNA was detected in two measles-mumps-rubella
combined vaccines and in two monovalent vaccines against mumps and rubella. Nucleotide sequence analysis
of the PCR products indicated that a modified live vaccine strain used for immunization of cattle against
bovine viral diarrhea is not responsible for the contamination of the vaccines.
VOL. 32, 1994
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used in Japan (Fig. 2). Thus, cattle vaccinated with a modified
live BVDV strain do not seem to be a source of the BVDV
contamination of fetal bovine serum.
Although it has not been established that BVDV infections
cause specific symptoms in humans, infantile gastroenteritis
associated with excretion of pestivirus antigens (19) and microcephaly in infants who were born to mothers seropositive
for pestiviruses (10) have been reported. Serum antibodies
against BVDV have been detected in humans who had no
contact with potentially infected animals (3, 18). Since noncytopathic biotypes of BVDV are capable of incorporating the
host cellular RNA into their genomes (8, 11), pestivirus
contamination would raise another issue with regard to the
safety of live virus vaccines produced in continuous cell lines
which are potentially oncogenic. Use of continuous cell lines as
cell substrates for the production of human biologicals has
been approved by the WHO Study Group (17). There is no
evidence presented in this paper to substantiate contamination
of the human virus vaccines with infectious pestiviruses, but
iatrogenic infections have been reported for veterinary virus
vaccines contaminated with infectious pestiviruses (5, 6, 15,
16). It is important to avoid the risk of contamination of human
viral vaccines. In conclusion, we suggest that human viral
vaccines be examined for the presence of adventitious pestiviruses by PCR, which will provide an additional assurance of
safety because of its sensitivity. PCR will be particularly useful
when it complements other tests (12) such as culture methods
or immunological assays.
Nucleotide sequence accession numbers. The nucleotide
sequence data first presented in this paper will appear in the
DDBJ, EMBL, GSDB, and NCBI nucleotide sequence data
bases with the following accession numbers: D26051, D26050,
D26052, D26048, and D26049 for sequences A, B, C, E, and F,
respectively, in Fig. 2.
We thank Richard 0. Roblin of the American Type Culture
Collection for critical review of the manuscript.
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1. Collett, M. S., R. Larson, C. Gold, D. Strick, D. K. Anderson, and
A. F. Purchio. 1988. Molecular cloning and nucleotide sequence of
the pestivirus bovine viral diarrhea virus. Virology 165:191-199.
2. Deng, R., and K. V. Brock. 1992. Molecular cloning and nucleotide
sequence of a pestivirus genome, non-cytopathic bovine viral
diarrhea virus strain SD-1. Virology 191:867-879.
3. Giangaspero, M., G. Wellemans, E. Vanopdenbosch, A. Belloli,
and A. Verhulst. 1988. Bovine viral diarrhea. Lancet ii:110.
4. Harasawa, R., K. Hikiji, H. Tanabe, Y. Takada, and H. Mizusawa.
1993. Detection of adventitious pestivirus in cell cultures by
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Res. Commun. 12:215-220.
5. Kreeft, H. A. J. G., I. Greser-Wilke, V. Moennig, and M. C.
Horzinek 1990. Attempts to characterize bovine viral diarrhea
virus isolated from cattle after immunization with a contaminated
vaccine. Dtsch. Tierarztl. Wochenschr. 97:63-65.
6. Loken, T., J. Krogsrud, and I. Bjerkas. 1991. Outbreaks of border
disease in goats induced by a pestivirus-contaminated orf vaccine,
with virus transmission to sheep and cattle. J. Comp. Pathol.
104:195-209.
7. Meyers, G., T. Rumenapf, and H.-J. Thiel. 1989. Molecular cloning
and nucleotide sequence of the genome of hog cholera virus.
Virology 171:555-567.
8. Meyers, G., T. Rumenapf, and H.-J. Thiel. 1989. Ubiquitin in a
togavirus. Nature (London) 342:491.
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10. Potts, B. J., J. L. Sever, N. R. Tzan, D. Huddleston, and G. A.
Elder. 1987. Possible role of pestiviruses in microcephaly. Lancet
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11. Qi, F., J. F. Ridpath, T. Lewis, S. R. Bolin, and E. S. Berry. 1992.
Analysis of the bovine viral diarrhea virus genome for possible
cellular insertions. Virology 189:285-292.
12. Robertson, J. S. 1991. New molecular approaches for detecting
viral genomes. Dev. Biol. Stand. 75:205-209.
13. Roehe, P. M., M. J. Woodward, and S. Edwards. 1992. Characterization of p20 gene sequences from a border disease-like pestivirus
isolated from pigs. Vet. Microbiol. 33:231-238.
14. Sanger, F., S. Nicklen, and A. R. Coulson. 1977. DNA sequencing
with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA
74:5463-5467.
15. Vannier, P., Y. Leforban, R. Carnero, and R. Cariolet. 1988.
Contamination of a live virus vaccine against pseudorabies (Aujeszky's disease) by an ovine pestivirus pathogen for the pig. Ann.
Rech. Vet. 19:283-290.
16. Wensvoort, G., and C. Terpstra. 1988. Bovine viral diarrhea virus
infections in piglets born to sows vaccinated against swine fever
with contaminated vaccine. Res. Vet. Sci. 45:143-148.
17. WHO Study Group. 1987. Acceptability of cell substrates for
production of biologicals. W. H. 0. Tech. Rep. Ser. 747:1-29.
18. Wilks, C. R., G. Abraham, and D. K. Blackmore. 1989. Bovine
pestivirus and human infection. Lancet i:107.
19. Yolken, R., E. Dubovi, F. Leister, R. Reid, J. Almeido-Hill, and M.
Santosham. 1989. Infantile gastroenteritis associated with excretion of pestivirus antigens. Lancet i:517-520.
Downloaded from http://jcm.asm.org/ on July 24, 2020 by guest
FIG. 2. Nucleotide sequence alignment of the second-round PCR products. A, B, C, E, and F are the sequences of the products shown in the
corresponding lanes in Fig. 1. Homologous sequences are shown in white on black. The nucleotide sequence numbers are given from a consensus
alignment. Primer sequences for the second-round PCR are indicated by arrows. Dashes represent spaces between adjacent nucleotides introduced
for maximum alignment.
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