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Journal of Clinical Microbiology, December 1999, p. 3940-3945, Vol. 37, No. 12
0095-1137/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
Adenoviruses from Human Immunodeficiency
Virus-Infected Individuals, Including Two Strains That Represent
New Candidate Serotypes Ad50 and Ad51 of Species B1 and D,
Respectively
Jan C.
De
Jong,1,*
Anton G.
Wermenbol,1
Marja W.
Verweij-Uijterwaal,1
Kees W.
Slaterus,2
Pauline
Wertheim-Van
Dillen,2
Gerard J. J.
Van
Doornum,3
Saye H.
Khoo,4 and
John C.
Hierholzer5
Research Laboratory of Infectious Diseases,
National Institute of Public Health and the Environment (RIVM), 3720 BA
Bilthoven,1 and Laboratory of Medical
Microbiology, Academic Medical Center,2 and
Municipal Health Laboratory,3 Amsterdam,
The Netherlands; Department of Infectious Diseases, North
Manchester General Hospital, Manchester, United
Kingdom4; and Respiratory and Enteric
Virus Branch, Center for Infectious Diseases, Centers for Disease
Control and Prevention, Atlanta, Georgia5
Received 3 May 1999/Returned for modification 9 July 1999/Accepted 13 September 1999
 |
ABSTRACT |
Adenovirus (Ad) isolates from a large number of human
immunodeficiency virus (HIV)-infected individuals were compared
serologically and genetically with Ad isolates from immunocompetent
patients. Between 1982 and 1994, stool and urine samples from 137 subjects with AIDS hospitalized in The Netherlands yielded 143 Ad
strains. Forty additional Ad strains were obtained from 35 HIV-positive patients in Manchester, United Kingdom, in 1992 and 1993. Of these 183 HIV-associated Ad strains, 84% belonged to species D and 3% belonged
to species C. These strains were compared with 2,301 Ad strains
collected during general diagnostic examinations in The Netherlands
from 1973 to 1992. Of the latter strains, 5% belonged to species D and
49% belonged to species C. Two of the Ads isolated from fecal
specimens of AIDS patients represent new serotypes: candidate Ad
serotype 50 (prototype strain, Wan) of subspecies B1 and candidate Ad
serotype 51 (prototype strain, Bom) of species D. The DNA restriction
enzyme patterns of strains Wan and Bom differed from the patterns of
all established prototypes.
| |
INTRODUCTION |
Genera of the adenovirus (Ad) family
have been subdivided into numerous serotypes. As reported by Francki et
al. (8), "A serotype is defined on the basis of its
immunological distinctiveness, as determined by quantitative
neutralization with animal antisera (from other species). A
serotype has either no cross-reaction with others or shows a
homologous-to-heterologous titer ration of >16 in both directions. If
neutralization shows a certain degree of cross-reaction between two
viruses in either or both directions (homologous-to-heterologous titer
ratio of eight or 16), distinctiveness of serotype is assumed if: (i)
the hemagglutinins are unrelated, as shown by lack of cross-reaction on
hemagglutination inhibition; or (ii) substantial
biophysical/biochemical differences of DNAs exist."
To date, 49 serotypes of human Ads have been recognized (16)
and grouped into six species (formerly called subgenera) (3) on the basis of their hemagglutinating properties and biophysical and
biochemical criteria: species A, B (subdivided into subspecies B1 and
B2), C, D, E, and F (19). The seven most recently described serotypes all belong to species D and were first isolated from human
immunodeficiency virus (HIV)-infected patients (13, 16). For
reasons still not understood, many patients with AIDS shed Ads that are
rarely or never isolated from immunocompetent individuals (10, 13,
14). In the present paper, we describe Ad strains isolated from
stool and urine specimens of patients with AIDS and compare them with
Ad isolates obtained from immunocompetent patients during a similar
time frame. We also describe two new serotypes isolated from the AIDS
patients; we propose the names Ad serotype 50 (Ad50) (subspecies B1)
and Ad51 (species D) for the two new serotypes.
| |
MATERIALS AND METHODS |
Origins of virus strains.
Prototype Ad strains were obtained
from the American Type Culture Collection (Manassas, Va.). Wild-type Ad
strains were recovered from several hospitals in both The Netherlands
and Manchester, United Kingdom. From 1973 to 1992, 2,301 Ads were
isolated at the general virus diagnostic laboratory of the Dutch
National Institute of Public Health and the Environment (Rijksinstituut voor Volksgezondheid en Milieuhygiëne [RIVM]) from clinical
samples taken from immunocompetent patients living in The Netherlands, with each isolate originating from a different patient. Isolation and
typing procedures remained essentially unchanged during the 20-year
period. The number of isolates from clinical specimens, which were
mainly sent by hospital-based physicians, varied between 67 and 200 per
year. Nine Ad isolates could not be typed, mainly because they seemed
to be mixtures of viruses belonging to different serotypes. Their
separation proved difficult and their characterization would therefore
be too time-consuming. It cannot be excluded that one of the strains
represents a new serotype.
Between 1982 and 1994 in The Netherlands, 143 Ad infections were
established by virus isolation from 115 AIDS patients hospitalized at
the Academic Medical Center and the Municipal Health Laboratory, both
in Amsterdam, and from 22 AIDS patients in other hospitals in The
Netherlands. Four patients were infected with two Ad serotypes, and one
patient was infected with three Ad serotypes. At North Manchester
General Hospital, Manchester, United Kingdom, 40 Ad infections were
established by virus isolation from stool and urine samples from 35 HIV-positive patients in 1992 and 1993; two different serotypes were
isolated from five samples (14). Together, these 183 HIV-associated Ad strains form the subject of the present study.
Origins of antisera.
Antisera were raised in rabbits by
conventional procedures (7). Essentially, HEp-2 cell-grown
virus preparations made in serum-free Eagle minimal essential medium
were purified by extraction with Arcton 113 fluorocarbon, mixed with
Freund's incomplete adjuvant, and injected intramuscularly into
rabbits four times at weekly intervals. The animals were boosted 1 month later with Arcton 113 fluorocarbon-purified virus and were bled
10 days after that. Reference horse antisera were prepared at the
Centers for Disease Control and Prevention (CDC) as described
previously (12).
Serological analysis.
All strains were serotyped at RIVM by
virus neutralization (VN) assays; many strains were further analyzed by
hemagglutination inhibition (HI) tests. VN and HI assays were performed
as described previously (5-7, 18). VN tests were conducted
with human diploid embryonic lung fibroblasts (strain GaBi) growing in
96-well microplates unless indicated otherwise. In accordance with the
usual practice for Ads (17), in VN assays the cell cultures
were inoculated with a virus dose that caused 100% of the cells to
show cytopathic effects after 7 days of incubation at 37°C. HI assays
were performed in microplates with either rat or rhesus monkey
erythrocytes where appropriate.
Genetic purification and DREA.
Virus strains were
genetically purified by two consecutive passages at terminal dilution
in human diploid fibroblasts (strain GaBi). Tenfold dilution series
were inoculated onto tube cultures of GaBi cells with 10 tube cultures
per dilution. After inoculation, the cells were incubated for 4 to 6 weeks in roller drums at 37°C. Positive tubes with the highest
dilution yielding any growth were then subcultivated. If two tubes were
positive at the same dilution, the tube with the latest-appearing
cytopathic effect was selected. If more than two tubes were positive at
the same dilution, the passage was repeated. A number of strains were
characterized by DNA restriction enzyme analysis (DREA) as described
previously (18).
| |
RESULTS |
Comparison of Ad serotypes circulating among immunocompetent and
HIV-infected individuals.
The Ad species and serotype
distributions among the subjects varied according to HIV infection,
which in most patients had advanced to AIDS (Tables
1 and 2).
Ads from HIV-infected patients generally belonged to species D; certain
serotypes were particularly related to the condition of AIDS, namely,
serotypes 9, 17, 20, 22, 23, 26, 27, 42 to 49, and 51 (Table 2). Only
rarely were Ads from immunocompetent patients among these serotypes.
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TABLE 1.
Ad isolates by site and species from non-HIV-infected and
HIV-infected individuals from The Netherlands and the
United Kingdom
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TABLE 2.
Ad infections by species and serotype of non-HIV-infected
patients from The Netherlands and HIV-infected patients from The
Netherlands and Manchester, United Kingdoma
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Deviant Ads from HIV-infected patients.
During the typing
procedures, a number of unusual isolates that presented typing problems
were detected. They may have represented as yet unknown Ad serotypes
and are described below.
(i) Subspecies B1 candidate Ad50: strain Wan.
Ad strain Wan
was isolated from a fecal sample taken in January 1988 from a
34-year-old man with diarrhea who was hospitalized with AIDS at a
hospital in Amsterdam. Strain Wan grew exceptionally well in GaBi
cells, yielding crude cell lysates with infectious virus titers up to
109 50% tissue culture infective doses per ml. The virus
was genetically purified by passages at terminal dilution. In the VN
tests, none of the 49 rabbit antisera to the established Ad prototype
strains and the rabbit antiserum to strain Bom (see below) reacted with strain Wan to titers higher than 0.01 the homologous titers (data not
shown). Weak cross-reactivities were observed with Ad21 (subspecies B1)
and Ad14, Ad34, and Ad35 (subspecies B2), and all were below the
threshold of 1/16 the homologous VN titers (Table
3). Conversely, rabbit anti-Wan antiserum
did not react with any of the 49 prototype strains or with strain Bom
with a VN titer higher than 0.01 the homologous titer (data not shown).
A low VN titer was found only with Ad21 (Table 3).
Strain Wan agglutinated erythrocytes from rhesus monkeys. According to
differential hemagglutination (HA) subgrouping, this
strain could be
classified as HA subgroup 1B (
9,
11). In
the HI tests, the
strain could not be clearly distinguished from
Ad21 (subspecies B1) or
from Ad34 and Ad35 (subspecies B2) when
antiserum to the Ad21 prototype
strain was used (Table
4). The
phenomenon
that a strain belonging to serotype
x is reacting in
HI
assays like prototype
y was reported before (
13,
20) and
was observed extensively in the present study (data not
shown).
In view of the serotype definition for Ad and the behavior in
the VN assays, this observation is not taxonomically significant.
Only
a low HI titer to strain Wan was observed with antiserum
to Ad34, and
no reactivity was detected with antisera to the other
members of
species B (see Table
6). Conversely, rabbit antiserum
to strain Wan
inhibited the HA of Ad21, Ad34, and Ad35 to titers
that differed only
fourfold or less from the homologous titer.
By DREA with restriction enzyme
SmaI, strain Wan produced
eight bands (Fig.
1), confirming its
allocation to species B (
19).
By using five restriction
enzymes, DREA patterns were determined
for strain Wan and the Ad14 and
Ad21 prototype strains (Fig.
1).
The patterns proved to be different
from those of the Ad1 to Ad41
prototype strains (
1), the
Ad42 prototype strain (
21), the
Ad43 to Ad47 prototype
strains (
13), and to Ad47 and Ad48 prototype
strains
(
16).
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FIG. 1.
DREA of strain Wan (Ad50) and some related strains of
species B. Lanes of electrophoresis gels: m, molecular weight markers;
1, Ad50 prototype strain Wan; 2, Ad21 prototype strain; 3, Ad14
prototype strain.
|
|
Earlier, strain Wan was examined by a novel PCR method for species
identification of human Ads and was found to belong to
subspecies B1
(
15) (Table
2). Recently, the two extreme ends
of the hexon
gene, which together comprise 872 nucleotides, were
sequenced and were
compared with the same regions of all eight
established species B
prototype strains. In this analysis, the
regions of strain Wan proved
to be identical to those of the Ad21
prototype strain (subspecies B1)
and different at a total of 84
to 95 nucleotide positions from the
corresponding regions of the
other seven prototype strains of species B
(
4). This is in
line with the identical reactivities of
strain Wan and Ad21 prototype
strain in HI tests and the classification
of strain Wan as subspecies
B1 in the species-specific Ad
PCR.
(ii) Species D candidate Ad51: strain Bom.
Ad strain Bom was
isolated at a hospital in Amsterdam from a stool sample taken in June
1989 from a 51-year-old male AIDS patient with fever,
Pneumocystis carinii pneumonia, and diarrhea. The patient
died in February 1991. This strain grew readily in GaBi cells and
epithelial cell lines such as HEp-2 cells. It was genetically purified
by passages at terminal dilution. In the VN assays, all of the 49 rabbit antisera to the Ad prototypes and the rabbit antiserum to strain
Wan reacted with strain Bom to titers lower than 0.01 the homologous
titers (data not shown). The same was true for rabbit antiserum to
strain Bom when titrated against the 49 prototype strains and strain
Wan. The CDC reference horse antisera to 29 prototype strains of
species D, i.e., all species D prototype strains except the Ad48 and
Ad49 prototype strains, were also titrated against strain Bom. The most
reactive of these antisera were those against Ad33, Ad43, and Ad44,
which showed 32- to 64-fold lower titers to strain Bom than to the
corresponding homologous viruses (Table
5). The recently proposed serotypes Ad48
and Ad49 did not show any cross-reactivity with strain Bom. Together,
these results demonstrate the uniqueness of strain Bom in the VN tests
and its position as a candidate new prototype of species D.
Strain Bom agglutinated erythrocytes from rats. According to the
differential HA subgrouping scheme of Hierholzer (
9,
11),
this strain could be classified as HA subgroup 2E. In the HI tests,
strain Bom did not react with antisera to the Ad serotypes of
species D
except with antisera to the Ad43 prototype strain and
weakly with
antisera to the Ad27, Ad44, Ad48, and Ad49 prototype
strains (Table
6). Horse anti-Ad43 serum reacted with
strain
Bom to roughly the same HI titer as to Ad43 strain 1373; the
Ad43
prototype strain (strain 1309) did not hemagglutinate
satisfactorily
in our hands and thus could not be used in the HI tests.
Conversely,
antiserum to strain Bom reacted in HI assays only with Ad43
strain
1373 and Ad49 strain Sak (but not with the Ad49 prototype strain
itself) and weakly with the Ad27, Ad44, and Ad48 prototype strains.
Apparently, strain Bom shares its fiber antigen with Ad43 strain
1373 and Ad49 strain Sak.
By DREA with restriction enzyme
SmaI, strain Bom produced 15 bands (Fig.
2), confirming its allocation
to species D (
19).
With five restriction enzymes, DREA
patterns were determined for
strains Bom, Ben (Ad48), and Kam (Ad49),
the Ad48 prototype strain,
and the Ad49 prototype strain (Fig.
2). The
DREA patterns of strain
Bom proved different from those of the Ad1 to
Ad41 prototype strains
(
1), the Ad42 prototype strain
(
21), the Ad43 to Ad47 prototype
strains (
13),
and the Ad47 and Ad48 prototype strains (
16).
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FIG. 2.
DREA of strain Bom (Ad51) and some related strains of
species D. Lanes of electrophoresis gels: m, molecular weight markers;
1, Ad51 prototype strain Bom; 2, Ad48 prototype; 3, strain Ben (Ad48);
4, Ad49 prototype; 5, strain Kam (Ad49).
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(iii) Subspecies B1: Ad21 variant strain Wek.
Ad strain Wek
could not be typed in the VN assays with rabbit antisera to all 49 serotypes or horse antisera to the subspecies B1 prototype strains.
However, rabbit antisera to strain Wek did neutralize the Ad21
prototype strain to a titer that was 40 times higher than the VN titer
to strain Wek itself (Table 3). Apparently, strain Wek is an Ad21
strain with a low avidity for VN antibodies, but with a VN
antibody-inducing capacity similar to that of the Ad21 prototype
strain. Strain Wek did not react with horse antiserum to the Ad21
prototype strain. This was not unexpected, however, because the
strength of this antiserum did not allow the detection of titers more
than 32-fold lower than the homologous titer. In the HI tests, strain
Wek could not be distinguished from the Ad21 prototype strain (Table
4).
(iv) Species D: Ben-like strains.
In the VN tests, a group of
17 closely related strains was identified as Ad48, although strain Ben,
which is representative of these viruses, differed significantly from
the Ad48 prototype strain in these assays. Antiserum to strain Ben,
however, showed a fivefold higher VN titer to the Ad48 prototype strain
than to the homologous virus (Table 5). Apparently, strain Ben is a
less "avid" variant of Ad48. In the HI tests, strain Ben reacted
like the Ad27 prototype strain (Table 6).
(v) Species D: Kam-like strains.
Another group of deviant
strains comprised 22 viruses. We identified the strains of this group
as Ad49. The representative strain, Kam, was isolated from a fecal
specimen of a 1-year-old boy with bronchopneumonia in Amsterdam in
1975. This strain belongs to Ad49 but deviated in the VN tests from the
Ad49 prototype strain in one direction, showing a homologous
titer-to-heterologous titer ratio of 20 when the Ad49 prototype strain
was tested against Kam antiserum (Table 5). Since strain Kam did not
hemagglutinate in our hands, strain Sak, which was closely related to
strain Kam in the VN assays, was used in the HI assays. It reacted like the Ad43 prototype strain (Table 6).
(vi) Species D: Aus-like strains.
Another potentially new
serotype was represented by strain Aus. It was isolated from a stool
sample of an HIV-infected Australian patient in 1991. Rabbit antiserum
to the Ad44 prototype strain demonstrated an almost 100-fold lower VN
titer to strain Aus than to the homologous strain, and rabbit antiserum
to strain Aus differentiated the two viruses even by a ratio of 640. Horse antiserum from the CDC to the Ad44 prototype strain, however,
showed only a fourfold lower VN titer to strain Aus than to the
homologous strain (Table 5). Strain Aus was therefore classified as
Ad44. It did not display HA activity in our tests.
| |
DISCUSSION |
This study confirms the results presented in earlier papers
(10, 13, 14) reporting that most of the Ads infecting the gastrointestinal tracts of HIV-infected patients represent serotypes or
intermediate serotypes of species D that are rarely isolated from
clinical specimens of immunocompetent patients or of patients suffering
from other kinds of immunodeficiencies. Typical AIDS-associated Ad
serotypes include types 9, 17, 20, 22, 23, 26, 27, and 42 to 51 (Table
2). The cause of this predilection is not known. It has been suggested
that the long-term infection characteristic for AIDS patients may
provide the opportunity for mutations to occur within a strain or for
recombinational events between coinfecting serotypes to take place and
could explain the unusual frequency and variety of deviating Ad strains
in the gastrointestinal tracts of such individuals (10).
Alternatively, these patients may be more likely to develop symptomatic
Ad infection and may thus be more likely to be examined by virological
analysis, although the pathogenic significance of Ad infections in AIDS
patients is unclear and asymptomatic infection is not uncommon
(10, 14).
Another explanation for the emergence of novel Ad serotypes from AIDS
patients may be a more quantitative one. As is apparent from Table 2,
even the "typical" AIDS-associated Ads are not strictly confined to
this group of patients, nor has it been established that they circulate
more frequently among such patients. In this regard, we note that data
on the Ad serotype distributions in the guts of non-HIV-infected adults
are scanty. At the general diagnostic department of RIVM, for instance,
a total of 1,478 Ad strains were typed during the period from 1981 to
1992. Only seven of these strains were isolated from fecal specimens of
non-HIV-infected patients ages 25 to 59 years. Perhaps, therefore, the
"new" Ads have just come to light since stool samples from that
particular age group are now examined more frequently because AIDS
patients frequently suffer from intestinal disorders of various
etiologies. Possibly, nucleotide sequence analysis can produce evidence
for and against these various hypotheses (2).
Some typing problems were encountered during the present study. A few
arose from the phenomenon that in VN assays horse anti-Ad antisera are
generally less discriminatory than rabbit antisera. For example, strain
Aus of species D was a novel serotype in the VN tests with rabbit
antisera, while it belonged to Ad44 in the VN assays with reference
horse antisera from CDC (Table 5). The definition of Ad serotype does
not specify the animal species in which the antisera to be used in the
VN assays should be prepared (see the introduction). There are
arguments, therefore, to call strain Aus a new serotype. To avoid
confusion, however, we think that it is sensible to create a new
serotype only when it proves to be novel in VN assays with both kinds
of antisera. The practical problem is that antisera for routine Ad
typing are usually prepared in rabbits, whereas the widely used CDC
reference antisera, instrumental for the recognition of new serotypes,
were prepared in horses. In routine typing work, therefore, Ad strains
like Aus will remain untypeable.
Another kind of typing problem was presented by Ad21 strain Wek. For
unknown reasons, strain Wek escaped significant neutralization by
anti-Ad21 antiserum. It was recognized as belonging to serotype 21 only
with the aid of rabbit antiserum to strain Wek (Table 3), which is not
available in routine typing laboratories.
On the basis of their uniqueness in the VN assays, we propose that
strains Wan and Bom be considered prototypes of Ad50 and Ad51,
respectively. Their weak cross-reactivities in the VN and HI assays
with members of species B and D, respectively, their capacity to
agglutinate rat and monkey erythrocytes, and the number of bands
produced with the restriction enzyme SmaI confirm that they
belong to species B and D, respectively. Molecular evidence showed that
strain Wan belongs to subspecies B1 and is closely related to the Ad21
prototype strain of this subspecies.
It is striking that the last nine new Ad serotypes were identified in
HIV-infected subjects. One might speculate that still more new Ad types
will be detected among these immunocompromised individuals in the
future. PCR-based methods may be helpful for tracking down such
viruses, especially when they would not be readily growing, like the
fastidious serotypes Ad40 and Ad41 (6), or even not
cultivable at all. In the latter case, VN assays are not possible and
an alternative taxonomic concept based on sequence data must be
developed to express the uniqueness of such viruses. For cultivable
Ads, the current type definition seems appropriate from a medical point
of view. Immunity to Ads appears to be closely linked to the presence
of neutralizing serum antibodies, and the application of gene therapy
with Ad vectors may be seriously hindered by such antibodies.
| |
ACKNOWLEDGMENTS |
We thank M. J. Cardosa and D. Perera for allowing us to use
their nucleotide sequence data for Ad species B, A. S. Bailey for
providing the AIDS-associated Ad strains from Manchester, and D. Sanders for retrieving data for Ad isolates obtained at RIVM from the
data files of the Institute.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Erasmus
University Rotterdam, Faculty of Medicine, Department of Virology, Dr.
Molewaterplein 50, 3015 GE, Rotterdam, The Netherlands. Phone: 31-10 408 8067. Fax: 31 10 408 9485. E-mail:
jc.de.jong{at}wxs.nl.
| |
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Journal of Clinical Microbiology, December 1999, p. 3940-3945, Vol. 37, No. 12
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Copyright © 1999, American Society for Microbiology. All rights reserved.
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Abstract
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