![[Feedback]](/icons/banner/feedbackACT.gif){kind=icon}
![[For Subscribers]](/icons/banner/subscriberACT.gif){kind=icon}
![[Archive]](/icons/banner/archiveACT.gif){kind=icon}
![[Search]](/icons/banner/searchACT.gif){kind=icon}
![[Contents]](/icons/banner/tocACT.gif){kind=icon}
Previous Article | Next Article 
Journal of Clinical Microbiology, November 1998, p. 3248-3254, Vol. 36, No. 11
Department of Molecular Genetics and
Microbiology, University of New Mexico, Albuquerque, New
Mexico1;
Epidemiology and Biostatistics Program,
Received 30 April 1998/Returned for modification 12 June
1998/Accepted 4 August 1998
This study compared the performances of three human papillomavirus
(HPV) detection tests with specimens collected by three alternative
procedures. The HPV tests included the Hybrid Capture Tube test (HCT),
the microplate-based Hybrid Capture II test (HC II), and the MY09-MY11
L1 consensus primer PCR-based assay. Initial cervical specimens were
collected from study subjects with a broom device, and after
Papanicolaou smears were made, residual specimens were placed into
PreservCyt (PC), a liquid cytology medium. A second specimen was
collected from each subject and placed into Digene Specimen Transport
Medium (STM). The device for collection of the second specimen
alternated with consecutive subjects between a conical cytology brush
and a Dacron swab. At the 1.0-pg/ml cutoff, the results of the HC II
agreed well with those of the PCR. Specifically, when PCR data were
restricted to the types found by the HC II (HPV types 16, 18, 31, 33, 35, 39, 45, 51, 52, 56, 58, 59, and 68), there was greater than 90%
agreement between the HC II and PCR results with both STM and PC. At a
lower cutoff (0.2 pg/ml), HC II-positive results increased further,
especially when the test was applied to the PC specimens. However,
false-positive HC II results were more often observed at the 0.2-pg/ml
cutoff. HC II yielded the highest HPV positivity with specimens placed into PC, followed by specimens collected with a conical brush and
placed into STM and, last, by those collected with a Dacron swab and
placed into STM. Our results demonstrate the utility of both the STM
and PC specimen collection methods and show good agreement between the
HC II and PCR.
Certain human papillomaviruses
(HPVs) are responsible for the development of cancer and its precursor
lesion cervical intraepithelial neoplasia (4, 24, 30). The
potential role of HPV testing in cervical cancer screening programs has
been under consideration for several years (8-10, 21, 31)
and is felt to be promising for women with atypical squamous cells of
undetermined significance.
Commercial availability of HPV detection systems in the United States
has been limited. The first-generation Hybrid Capture Tube test (HCT;
Digene Corporation, Silver Spring, Md.) has been used as an HPV
detection test and is the only HPV DNA test approved by the U.S. Food
and Drug Administration (5, 23, 29, 33, 35). A
second-generation assay with increased analytical sensitivity and a
more efficient kit format has recently been developed. This new test,
currently under consideration by the U.S. Food and Drug Administration,
is named the Hybrid Capture II test (HC II). The hybrid capture
technique is based on the formation of RNA-DNA hybrids between HPV DNA
that may be present in clinical specimens and complementary unlabeled
HPV RNA probes. The RNA-DNA hybrids are captured and immobilized by
antihybrid antibodies. Immobilized hybrids are reacted with a
monoclonal antibody reagent that is conjugated to alkaline phosphatase,
and the complexes are detected via a chemiluminescent substrate
reaction. In HCT, a tube luminometer is employed, whereas in HC II, a
microplate luminometer reads the light output and displays the assay
results as relative light units (RLU). HPV positivity or negativity is
based on comparison to a standard positive reference (RLU of a clinical
specimen divided by the mean RLU of three positive calibrator
references).
The HCT Probe B cocktail detects a limited number of high-risk HPV
types, including HPVs 16, 18, 31, 33, 35, 45, 51, 52, and 56, and has
been reported to have a diagnostic sensitivity similar to that of the
Papanicolaou (Pap) smear (6). HC II detects HPV types at an
increased sensitivity compared to that of HCT (23). In
addition, probes for HPV types 39, 58, 59, and 68 have been added to
the HC II Probe B group. One potential advantage of this test is that
it may provide a semiquantitative measure of viral load (8, 9, 11,
16, 23, 31, 32). It has been suggested that viral load may lend
prognostic and diagnostic value (13, 20).
To date, investigators in most reported HCT-based studies have used a
Dacron swab to collect cervical cells into 1.0 ml of Specimen Transport
Medium (STM; Digene Corporation) (31, 34, 35). Recently, a
conical cytology brush has been used to collect cervical cells. This
modification was made with the expectation that the brush would
increase the number of cells obtained and thus provide a specimen with
an increased concentration of HPV.
As HPV test formats and specimen collection devices have continued to
evolve, new liquid specimen collection media have also become available
for routine use in Pap smear screening. Recently, a new technique that
employs the collection of cervical cells into PreservCyt (PC) liquid
cytology medium, from which ThinPrep (Cytyc, Boxborough, Mass.)
thin-layer slides are produced, has been introduced. This method has
received approval for clinical use from the U.S. Food and Drug
Administration (22, 33). An advantage of using a liquid
cytology medium for the collection of cervical specimens is that
multiple diagnostic tests can be performed with a single sample. For a
cervical diagnosis within the atypical squamous cells of undetermined
significance category, HPV testing can be performed on the temporarily
stored Pap smear specimen without the cost of a clinical follow-up
visit. Accordingly, HPV testing of specimens in PC has recently been
approved by the U.S. Food and Drug Administration.
This study compares HPV detection in specimens collected by three
different means. These three methods are under consideration as HPV
sampling strategies for routine clinical use. HPV detection in these
specimens was evaluated by comparing the first-generation HCT, the
prototype second-generation HC II, and a widely used PCR assay based on
the MY09-MY11-HMB01 primer set. PCR was performed only on the specimens
collected in PC. The selected L1 consensus primer PCR-based method
detects a broad spectrum of anogenital HPV types that include, but are
not limited to, HPVs 6, 11, 16, 18, 26, 31, 33, 34, 35, 39, 45, 51, 52, 53, 54, 55, 56, 57, 58, 59, 61, 62, 64, 66, 67, 68, 70, 72, 73, IS39,
MM4 (also called W13B), MM7 (also called P291), MM8 (also called P155),
MM9 (also called P238a), CP6108, CP8061, and CP8304 (1-3,
25).
Study population and collection of specimens.
Figure
1 summarizes the cervical specimen
collection and HPV testing strategies. Two hundred eight specimens were
selected from specimens collected in a prospective population-based
natural-history study of 9,175 women conducted in Costa Rica
(17). The median age of these women was 37 years. Cervical
diagnoses were virtually all within normal limits but included a small
number of low-grade abnormalities (n = 10). This cohort
consisted of women with past histories or no history of squamous
intraepithelial lesions. Initial specimens were collected from all 208 women with a broom device (Cervex Brush; Unimar, Wilton, Conn.) for the
Pap smear. Following the preparation of a conventional Pap smear,
residual cells on each broom device were placed into ~20 ml of PC
liquid cytology medium (Cytyc). Approximately half of the 208 women had
a second cervical specimen collected with a Dacron swab and placed into 1.0 ml of STM. The remaining women had a second cervical specimen collected with a conical brush (Medical Packaging Corporation, Camarillo, Calif.) into 0.6 ml of STM. These two collection methods were alternated between consecutive patients. Specimens collected in PC
and STM were stored at ambient temperature and PCR and dot blot-based HPV testing methods.
The PCR and dot
blot analyses were performed at the University of New Mexico. Aliquots
for PCR testing were taken prior to HC II analyses of these specimens.
The laboratory was unaware of the clinical statuses and HCT and HC II
results of the study subjects.
0095-1137/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
Comparison of PCR- and Hybrid Capture-Based Human
Papillomavirus Detection Systems Using Multiple Cervical Specimen
Collection Strategies
ABSTRACT
Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
INTRODUCTION
Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
MATERIALS AND METHODS
Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
20°C, respectively, until processing.
View larger version (18K):
[in a new window]
FIG. 1.
Flowchart illustrating the cervical specimen collection
and HPV testing strategies.
20°C until
amplification.
-globin primer system was coamplified with
the HPV consensus primers. Positive and negative PCR controls were
included with each amplification. PCRs were conducted in a Perkin-Elmer
model 9600 thermocycler with the following amplification profile: an
initial 95°C AmpliTaq Gold activation for 9 min; 40 cycles of a
95°C denaturation for 1 min, a 55°C annealing for 1 min, and a
72°C terminal extension for 1 min; and a 72°C final extension for 5 min. Amplimers were analyzed by ethidium bromide-stained agarose gel
electrophoresis.
HPV typing analyses were carried out by dot blot hybridization and with
biotinylated HPV type-specific oligonucleotide probes as previously
described (1). PCR products were denatured and applied to
replicate nylon membranes (3.5 µl per well) with dot blot apparatuses
(Bio-Rad Laboratories, Hercules, Calif.). A collection of previously
characterized HPV PCR products (3.5 µl) were applied as HPV
type-specific controls. The membranes were hybridized at 53°C
overnight with biotinylated HPV type-specific oligonucleotide probes
for HPVs 6 or 11, 16, 18, 26, 31, 33, 35, 39, 40, 42, 44, 45, 51, 52, 53, 54, 55, 56, 57, 58, 59, 66, 68, 73 (P238A), MM4 (W13B), MM7 (P291),
and MM8 (P155). Probes for HPV types 26 and MM8 and types 40 and 42 were pooled as pairs during hybridization. A -globin probe was used
to assess specimen adequacy. Following hybridization, membranes were
washed at 56 to 57°C to remove nonspecifically bound probe.
Immobilized probes were detected with streptavidin-horseradish peroxidase (Vector, Burlingame, Calif.) and Enhanced Chemiluminescent Substrate (Amersham, Arlington Heights, Ill.). Blots were exposed to
Kodak X-Omat AR 5 film for an initial 10 min, followed by a second 2-h
or overnight exposure. The resulting data were analyzed manually by two
observers and recorded on a database spreadsheet. Discrepant results
were independently arbitrated.
All specimens positive for PCR by gel electrophoresis that did not bind
to any of the HPV type-specific oligonucleotide probes were subjected
to restriction fragment length polymorphism (RFLP) analysis as
previously described (3). The resulting RFLP profiles were
compared to known HPV type profiles, and the HPV types were designated.
The RFLP results were subsequently confirmed by an independent
PCR-based detection method (15).
Hybrid capture-based HPV testing methods. All hybrid capture testing of clinical specimens was performed at Digene Corporation. The laboratory technicians were unaware of the clinical statuses and HPV PCR results of the study subjects.
Cervical specimens collected in STM (0.6 and 1.0 ml) were processed according to the manufacturer's HCT or HC II package insert. Briefly, one-half volume of NaOH-based denaturation reagent was added to each sample, which was then mixed vigorously and incubated at 65°C for 45 min. Seventy-five microliters of the denatured specimen was removed for analysis by HC II, and 150 µl was removed for HCT. The HC II Probe B cocktail contains RNA probes for high-risk HPV types 16, 18, 31, 33, 35, 39, 45, 51, 52, 56, 58, 59, and 68. HPV positivity by HC II was determined with 0.2-, 0.5-, 1.0-, and 10.0-pg/ml detection cutoff limits. HCT used a single fixed 10.0-pg/ml assay cutoff and did not include RNA probes for HPVs 39, 58, 59, and 68. Specimens collected into PC were analyzed by HC II as follows. A 2-ml aliquot was removed from each specimen and placed into a microcentrifuge tube and centrifuged at 13,000 × g for 15 min. The supernatant was carefully aspirated, and the pellet was resuspended in 50 µl of STM. Twenty-five microliters of denaturation reagent was added, and the specimens were denatured for 45 min at 65°C. From this point, the remainder of the HC II procedure was identical to that applied to the STM specimens.Data analyses.
Agreement was measured by both absolute
agreement and Cohen's kappa statistic (
), a measure of the
agreement between two methods in excess of that due to chance
(12). Approximate 95% confidence intervals (CIs) were
computed with an asymptotic variance and critical values from the
normal distribution. Proportions were compared with exact P
values for the Pearson chi-square test. Statistical significance was
achieved when the P value of the test was less than 0.05. All analyses were performed with SAS version 6.12 software
(28).
| |
RESULTS |
|---|
|
Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
|
|---|
HPV DNA positivity. The overall HPV DNA positivity was 24.5% by PCR (any HPV type), and when the test was restricted to the 13 cancer-associated HPV types present in the HC II Probe B cocktail, the HPV DNA positivity was 12.5%. In comparison, the overall HPV DNA positivity was as follows for different media, cutoffs, and tests: 22.1% by HC II of specimens in PC at the 0.2-pg/ml cutoff, 13.9% by HC II of specimens in STM at the 0.2-pg/ml cutoff, 13.0% by HC II of specimens in PC at the 1.0-pg/ml assay cutoff, 11.5% by HC II of specimens in STM at the 1.0-pg/ml cutoff, and 7.2% by HCT testing of specimens in STM.
HCT versus HC II. Results of the HCT and HC II at the 10.0-pg/ml assay cutoff were equivalent for Dacron swab and conical brush specimens and revealed that, at this assay cutoff, the level of detection of HC II was nearly equivalent to that of the HCT, with a kappa value of 0.90 (95% CIs = 0.79 and 1.00). In addition, HPV detection was only slightly greater by HC II than by HCT (8.7 versus 7.2% positive) and the difference was not statistically significant.
Dacron swab versus conical brush. HPV DNA detection by HC II was greater for specimens obtained with the conical brush than for specimens obtained with the Dacron swab at 0.2-, 0.5-, and 1.0-pg/ml assay cutoffs (Table 1). However, these differences were not statistically significant. Since specimens were collected alternately with a conical brush and Dacron swab from consecutive patients, differences in HPV positivity may actually reflect chance differences in the prevalence of HPV among the two groups of women, despite randomization. This possible explanation was supported by the results of HC II when it was applied to the PC specimens. A higher HPV positivity was observed with PC specimens from women from whom a second specimen was obtained with a conical brush than with PC specimens from women from whom the second specimen was obtained with a Dacron swab.
|
= 0.60) was largely attributable to the
much greater HPV DNA positivity obtained with the PC specimens (22.1%
in PC versus 13.9% in STM). Agreement was better for the group of
specimens obtained with a conical brush than for those obtained with a
Dacron swab at the 1.0-, 0.5-, and 0.2-pg/ml HC II assay cutoffs.
However, the kappa statistics were not significantly different.
HC II versus PCR. Initial comparisons of HC II and PCR results included PCR detection of only those HPV types included in the HC II Probe B cocktail. When HC II was compared to the PCR method with PC specimens, the kappa values were 0.47 (95% CIs = 0.32 and 0.62), 0.59 (95% CIs = 0.43 and 0.74), and 0.63 (95% CIs = 0.47 and 0.79) for HC II assay cutoff values of 0.2, 0.5, and 1.0 pg/ml, respectively (Fig. 2). Agreement was actually slightly better when results of HC II from STM specimens were compared to the PCR results from PC specimens (kappa values, 0.69, 0.70, and 0.68 for HC II cutoff levels of 0.2, 0.5, and 1.0 pg/ml, respectively). Agreement between HC II and PCR for the group of women sampled with a conical brush was greater than for the group sampled with a Dacron swab, and the kappa values were significantly different at the 0.2-, 0.5-, and 1.0-pg/ml HC II cutoff levels (P = 0.02, 0.04, and 0.03, respectively).
|
|
|
| |
DISCUSSION |
|---|
|
Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
|
|---|
It has been proposed that HPV DNA testing might be used as an adjunct in the management of women with minor cytological abnormalities (8, 10, 18, 21, 26). This study set out to compare different specimen collection methods for HPV testing. In addition, it was important to compare results of HPV testing of specimens in PC liquid cytology medium by well-established HPV testing methods and to further characterize the newly available HC II HPV method. We compared two hybrid capture methods (HCT and HC II) and L1 consensus PCR for HPV DNA testing, using specimens collected in both STM and PC.
Results by HC II were in excellent agreement with results by HCT at the 10.0-pg/ml cutoff, illustrating the correspondence of the two hybrid capture HPV tests. Also, as expected, when HCT was compared to HC II at the 1.0-, 0.5-, and 0.2-pg/ml assay cutoffs, the agreement progressively decreased. As previously reported (23), a 1.0-pg/ml cutoff can routinely be used in HC II, reflecting an approximately 10-fold increase in sensitivity over that of HCT. It is anticipated that the increased sensitivity may improve the clinical utility of this second-generation HPV hybrid capture test.
The conical brush STM collection method may be an improvement over the Dacron swab STM collection method. This is suggested by both the increase in overall HPV DNA detection and the higher correlation of HC II data from STM conical brush specimens with HC II and PCR data from PC specimens.
Although collection with a conical brush appeared to result in higher HPV DNA detection by HC II than collection with a Dacron swab, further analyses of results stratified by STM sampling device demonstrated a potential problem with subject randomization. When the subjects were separated into two groups based on STM collection device and analyses were limited to those specimens collected in PC, the HC II data showed a higher prevalence of HPV and correlated significantly better with PCR data from the group of women who had an STM sample collected with a conical brush (data not shown). Because the PC specimen was collected prior to the STM specimen, the device used in the second specimen collection should not have affected the initial specimen. Therefore, the apparent difference between these two sampling methods may be due to a chance difference in subjects. However, there was no obvious difference in the ages of and clinics attended by the two groups of women for Pap smear diagnosis. In addition, the samples were collected in a random manner.
Two recent studies reported reasonable correlation between PCR and HCT HPV assay results (7, 34). However, neither of these previous studies used PC. Some of the disagreement between PCR and HC II results may be attributed to the use of separate PC aliquots that were processed and tested at two laboratory sites. In other words, the level of agreement may have been higher if both tests were performed with the same aliquot.
The HC II detection cutoff value represents the relative light unit reading above which samples are considered positive. There is uncertainty as to which HC II cutoff is best in terms of accuracy and clinical utility. The comparison of results of HC II and PCR with PC specimens demonstrated a good correlation at 0.5- and 1.0-pg/ml HC II cutoffs. In contrast, at the 0.2-pg/ml HC II cutoff, the kappa value was only fair (0.47). However, the comparison to PCR results with STM specimens at 0.2 pg/ml resulted in a kappa value of 0.69, indicating good agreement. Our data suggested that, for specimens collected in PC, an HC II cutoff of about 1.0 pg/ml was optimal and that the use of a 0.2-pg/ml HC II cutoff introduced a measurable level of false positivity. This increase in background at the 0.2-pg/ml HC II cutoff was observed only with PC specimens, which implies that there was a higher level of nonspecific detection for samples collected in PC than for those collected in STM.
For specimens collected in STM, use of a 0.2-pg/ml HC II cutoff leads to an apparent increase in the level of HPV positivity compared to the levels produced with the 0.5- and 1.0-pg/ml HC II cutoffs. When using this specimen collection medium, an HC II threshold of less than 1.0 pg/ml might be optimal and suggests that the HPV DNA detection ability of HC II is approaching that of the MY09-MY11-HMB01 PCR method. Sensitivities for PCR and HC II were equivalent when analyses were restricted to the HPV types included in the HC II Probe B cocktail. Additional studies are necessary to evaluate the detection limits of HC II and to compare results with results of sensitive PCR detection methods that distinguish a broad spectrum of HPV types.
Based on the PCR results from matched specimens, cross-reactivity of the HC II Probe B cocktail with phylogenetically related HPV types was observed. When these and additional HPV types were included in HC II and PCR and the results were compared, the kappa statistics and percentages of agreement decreased, partially because HC II detected some of these HPVs. The HPV types not represented by the HC II Probe B group but detected by HC II at a 1.0-pg/ml assay cutoff included HPVs 53, 66, 67, 73, CP6108 (27), and CP8061 (27). In addition, HPVs 53 and 67 were also detected at a 10.0-pg/ml HC II cutoff. It should be noted that limited data are available to assess cervical disease risk for some of these rarer HPV types. Differences in HC II HPV detection endpoints for various cross-reactive HPVs may contribute to the decreases in agreement. These differences in HC II HPV type-specific sensitivities will result in a lower overall comparability with the sensitivity of M409-11-MMB01 PCR with probes that detects these additional HPV types. The clinical relevance of the HC II Probe B cocktail's cross-reactivities with some low-risk HPVs remains to be fully determined.
| |
ACKNOWLEDGMENTS |
|---|
This work was funded in part by a contract to C. M. Wheeler from the National Institutes of Health, RFP-NCI-CA-CN-55044-07.
We thank Michele Manos for her continuing helpful advice. We acknowledge the superb Costa Rican study team and the data processing excellence of Julie Buckland and Kay Helgesen at IMS.
| |
FOOTNOTES |
|---|
* Corresponding author. Mailing address: University of New Mexico, School of Medicine, Department of Molecular Genetics and Microbiology, 915 Camino de Salud NE, Albuquerque, NM 87131-5276. Phone: (505) 272-9151. Fax: (505) 277-5273. E-mail: cwheeler{at}salud.unm.edu.
Present address: International Agency for Research against Cancer,
Lyon, France.
| |
REFERENCES |
|---|
|
Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
|
|---|
| 1. | Bauer, H. M., and M. M. Manos. 1993. PCR detection of genital human papillomavirus, p. 407-413. In D. H. Persing, T. F. Smith, F. C. Tenover, and T. J. White (ed.), Diagnostic molecular microbiology. ASM Press, Washington, D.C. |
| 2. | Bauer, H. M., Y. Ting, C. E. Greer, J. C. Chambers, C. J. Tashiro, J. Chimera, A. Reingold, and M. M. Manos. 1991. Genital human papillomavirus infection in female university students as determined by a PCR-based method. JAMA 265:472-476[Abstract]. |
| 3. | Bernard, H. U., S. Y. Chan, M. M. Manos, C. K. Ong, L. L. Villa, H. Delius, C. L. Peyton, H. M. Bauer, and C. M. Wheeler. 1994. Identification and assessment of known and novel human papillomaviruses by polymerase chain reaction amplification, restriction fragment length polymorphisms, nucleotide sequence, and phylogenetic algorithms. J. Infect. Dis. 170:1077-1085[Medline]. |
| 4. |
Bosch, F.,
M. M. Manos,
N. Muñoz,
M. Sherman,
A. M. Jansen,
J. Peto,
M. H. Schiffman,
V. Moreno,
R. Kurman, and K. V. Shah.
1995.
Prevalence of human papillomavirus in cervical cancer: a worldwide perspective.
J. Natl. Cancer Inst.
87:796-802 |
| 5. |
Brown, D. R.,
J. T. Bryan,
H. Cramer, and K. H. Fife.
1993.
Analysis of human papillomavirus types in exophytic condylomata acuminata by hybrid capture and Southern blot techniques.
J. Clin. Microbiol.
31:2667-2673 |
| 6. | Cavuslu, S., C. Mant, W. G. Starkey, J. M. Bible, C. Biswas, B. Kell, P. Rice, J. M. Best, and J. Cason. 1996. Analytic sensitivities of Hybrid-Capture, consensus and type-specific polymerase chain reactions for the detection of human papillomavirus type 16 DNA. J. Med. Virol. 49:319-324[Medline]. |
| 7. | Cope, J. U., A. Hildesheim, M. H. Schiffman, M. M. Manos, A. T. Lörincz, R. D. Burk, A. G. Glass, C. Greer, J. Buckland, K. Helgesen, D. R. Scott, M. E. Sherman, R. J. Kurman, and K.-L. Liaw. 1997. Comparison of the Hybrid Capture Tube test and PCR for detection of human papillomavirus DNA in cervical specimens. J. Clin. Microbiol. 35:2262-2265[Abstract]. |
| 8. | Cox, J. T., A. T. Lörincz, M. H. Schiffman, M. E. Sherman, A. Cullen, and R. J. Kurman. 1995. Human papillomavirus testing by Hybrid Capture appears to be useful in triaging women with a cytologic diagnosis of atypical squamous cells of undetermined significance. Am. J. Obstet. Gynecol. 172:946-954[Medline]. |
| 9. | Cuzick, J., G. Terry, L. Ho, T. Hollingworth, and M. Anderson. 1994. Type-specific human papillomavirus DNA in abnormal smears as a predictor of high-grade cervical intraepithelial neoplasia. Br. J. Cancer 69:167-171[Medline]. |
| 10. | Ferenczy, A. 1995. Viral testing for genital human papillomavirus infections: recent progress and clinical potentials. Int. J. Gynecol. Cancer 5:321-328. [Medline] |
| 11. | Ferenczy, A., E. Franco, J. Arseneau, T. C. Wright, and R. M. Richart. 1996. Diagnostic performance of Hybrid Capture human papillomavirus deoxyribonucleic acid assay combined with liquid-based cytologic study. Am. J. Obstet. Gynecol. 175:651-656[Medline]. |
| 12. | Fleiss, J. L. 1981. Statistical methods for rates and proportions, p. 212-236. John Wiley and Sons, New York, N.Y. |
| 13. | Franco, E. L., L. L. Villa, H. Richardson, T. Rohan, and A. Ferenczy. 1997. Epidemiology of cervical human papillomavirus infection, p. 14-22. In E. L. Franco, and J. Monsonego (ed.), New developments in cervical cancer screening and prevention. World Health Organization/EUROGIN monograph. Blackwell Scientific Publications Ltd., Oxford, United Kingdom. |
| 14. | Gravitt, P. E., and M. M. Manos. 1992. Polymerase chain reaction-based methods for the detection of human papillomavirus DNA, p. 121-133. In N. Muñoz, F. X. Bosch, K. V. Shah, and A. Meheus (ed.), The epidemiology of cervical cancer and human papillomavirus. International Agency for Research against Cancer, Scientific Publications, Lyon, France. |
| 15. |
Gravitt, P. E.,
C. L. Peyton,
R. J. Apple, and C. M. Wheeler.
1998.
Genotyping of 27 human papillomavirus types by using L1 consensus PCR products by a single-hybridization, reverse line blot detection method.
J. Clin. Microbiol.
36:3020-3027 |
| 16. | Hall, S., A. Lörincz, F. Shah, M. E. Sherman, F. Abbas, G. Paull, R. J. Kurman, and K. V. Shah. 1996. Human papillomavirus DNA detection in cervical specimens by Hybrid Capture: correlation with cytologic and histologic diagnoses of squamous intraepithelial lesions of the cervix. Gynecol. Oncol. 62:353-359[Medline]. |
| 17. | Herrero, R., M. H. Schiffman, C. Bratti, A. Hildesheim, I. Balmaceda, M. E. Sherman, M. Greenberg, F. Cardenas, V. Gomez, K. Helgensen, J. Morales, M. Hutchinson, L. Mango, M. Alfaro, N. W. Potischman, S. Wacholder, C. Swanson, and L. A. Brinton. 1997. Design and methods of a population-based natural history study of cervical neoplasia in a rural province of Costa Rica: the Guanacaste project. Pan Am. J. Public Health 1:362-375. |
| 18. |
Herrington, C. S.,
M. F. Evans,
F. M. Charnock,
W. Gray, and J. O. McGee.
1996.
HPV testing in patients with low grade cervical cytological abnormalities: a follow up study.
J. Clin. Pathol.
49:493-496 |
| 19. | Hildesheim, A., M. H. Schiffman, P. E. Gravitt, A. G. Glass, C. E. Greer, T. Zhang, D. R. Scott, B. B. Rush, P. Lawler, M. E. Sherman, R. J. Kurman, and M. M. Manos. 1994. Persistence of type-specific human papillomavirus infection among cytologically normal women. J. Infect. Dis. 169:235-240[Medline]. |
| 20. |
Ho, G. Y. F.,
R. D. Burk,
S. Klein,
A. S. Kadish,
C. Chang,
P. Palan,
J. Basu,
R. Tachezy,
R. Lewis, and S. Romney.
1995.
Persistent genital human papillomavirus infection as a risk factor for persistent cervical dysplasia.
J. Natl. Cancer Inst.
87:1365-1371 |
| 21. | Jenkins, D., C. Sherlaw-Johnson, and S. Gallivan. 1996. Can papillomavirus testing be used to improve cervical cancer screening? Int. J. Cancer 65:768-773[Medline]. |
| 22. | Lee, K. R., R. Ashfaq, G. G. Birdsong, M. E. Corkill, K. M. McIntosh, and S. L. Inhorn. 1997. Comparison of conventional Papanicolaou smears and a fluid-based, thin-layer system for cervical cancer screening. Obstet. Gynecol. 90:278-284[Abstract]. |
| 23. | Lörincz, A. 1996. Hybrid capture method for detection of human papillomavirus DNA in clinical specimens. Papillomavirus Rep. 7:1-5. |
| 24. | Lörincz, A. 1987. Oncogenic association of specific human papillomavirus types with cervical neoplasia. J. Natl. Cancer Inst. 79:671-677. |
| 25. | Manos, M. M., Y. Ting, D. K. Wright, A. J. Lewis, T. R. Broker, and S. M. Wolinsky. 1989. Use of polymerase chain reaction amplification for the detection of genital human papillomaviruses. Cancer Cells 7:209-214. |
| 26. | Mansell, M. E., L. Ho, G. Terry, A. Singer, and J. Cuzick. 1994. Semi-quantitative human papillomavirus DNA detection in the management of women with minor cytologic abnormalities. Br. J. Obstet. Gynaecol. 101:807-809[Medline]. |
| 27. | Peyton, C. L., and C. M. Wheeler. 1994. Identification of five novel human papillomavirus sequences in the New Mexican triethnic population. J. Infect. Dis. 170:1089-1092[Medline]. |
| 28. | SAS Institute Inc. 1996. SAS/STAT software: changes and enhancements through release 6.11, p. 219-230. SAS Institute Inc., Cary, N.C. |
| 29. | Schiffman, M. H., N. B. Kiviat, R. D. Burk, K. V. Shah, R. W. Daniel, R. Lewis, J. Kuypers, M. M. Manos, D. R. Scott, M. E. Sherman, R. J. Kurman, M. H. Stoler, A. G. Glass, B. B. Rush, I. Mielzynska, and A. T. Lörincz. 1995. Accuracy and interlaboratory reliability of human papillomavirus DNA testing by hybrid capture. J. Clin. Microbiol. 33:545-550[Abstract]. |
| 30. |
Schiffman, M. H.,
H. M. Bauer,
R. N. Hoover,
A. G. Glass,
D. M. Cadell,
B. B. Rush,
D. R. Scott,
M. E. Sherman,
R. J. Kurman,
S. Wacholder,
C. K. Stanton, and M. M. Manos.
1993.
Epidemiologic evidence showing that human papillomavirus infection causes most cervical intraepithelial neoplasia.
J. Natl. Cancer Inst.
85:958-964 |
| 31. | Schneider, A., D. M. Zahm, R. K. Kirchmayr, and V. L. Schneider. 1996. Screening for cervical intraepithelial neoplasia grade 2/3: validity of cytologic study, cervicography, and human papillomavirus detection. Am. J. Obstet. Gynecol. 174:1534-1541[Medline]. |
| 32. | Shah, K. V., L. Solomon, R. Daniel, S. Cohn, and D. Vlahov. 1997. Comparison of PCR and Hybrid Capture methods for detection of human papillomavirus in injection drug-using women at high risk of human immunodeficiency virus infection. J. Clin. Microbiol. 35:517-519[Abstract]. |
| 33. | Sherman, M., M. Schiffman, A. Lörincz, R. Herrero, M. Hutchinson, C. Bratti, D. Zahniser, J. Morales, A. Hildesheim, K. Helgensen, D. Kelly, M. Alfaro, F. Mena, I. Balmaceda, L. Mango, and M. Greenberg. 1997. Cervical specimens collected in liquid buffer are suitable for both cytologic screening and ancillary human papillomavirus testing. Cancer 81:89-97[Medline]. |
| 34. | Smits, H. L., L. J. M. Bollen, S. P. Tjong-a-Hung, J. Vonk, J. V. D. Velden, F. J. W. Ten Kate, J. A. Kaan, B. M. Mol, and J. T. Schegget. 1995. Intermethod variation in detection of human papillomavirus DNA in cervical smears. J. Clin. Microbiol. 33:2631-2636[Abstract]. |
| 35. | Sun, X., A. Ferenczy, D. Johnson, J. Koulos, O. Lungu, R. Richart, and T. Wright. 1995. Evaluation of the Hybrid Capture human papillomavirus deoxyribonucleic acid detection test. Am. J. Obstet. Gynecol. 173:1432-1437[Medline]. |
This article has been cited by other articles:
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| Antimicrob. Agents Chemother. | Clin. Microbiol. Rev. |
|---|---|
| Clin. Vaccine Immunol. | ALL ASM JOURNALS |
|---|
