Sexually Transmitted Diseases:
Concordance of Self-Collected and Clinician-Collected Swab Samples for Detecting Human Papillomavirus DNA in Women 18 to 32 Years of Age
Winer, Rachel L. PhD*; Feng, Qinghua PhD†; Hughes, James P. PhD‡; Yu, Mujun MD, PhD†; Kiviat, Nancy B. MD†; O'Reilly, Sandra BS*; Koutsky, Laura A. PhD*
From the Departments of *Epidemiology, †Pathology, and ‡Biostatistics, University of Washington, Seattle, Washington
Financial support for this study was provided by NIH A1-38383 and 5T32AI007140-24.
Correspondence: Rachel L. Winer, PhD, University of Washington HPV Research Group, Lake Union Place, Suite 300, 1914 N 34th Street, Seattle, WA 98103. E-mail: email@example.com.
Received for publication April 24, 2006, and accepted July 21, 2006.
Objective: The objective of this study was to determine whether self- and clinician-collected samples are comparable for human papillomavirus (HPV) detection.
Study Design: Three hundred seventy-four women aged 23 to 32 (population 1) and 211 women aged 18 to 25 (population 2) contributed self-collected vaginal and clinician-collected cervical and vulvovaginal samples for HPV DNA testing. Eighty-six women mailed in self-collected samples.
Results: Agreement between self-collected vaginal and clinician-collected combined cervical/vulvovaginal samples was excellent (population 1:92.0%, κ = 0.81; population 2: 96.4%, κ = 0.88), but self-collected samples were more concordant with clinician-collected cervical samples in population 2 (κ = 0.84) than population 1 (κ = 0.65) (P = 0.01). Age-adjusted HPV prevalence was slightly lower in mailed-in (21.5%) than in-clinic self-collected samples (26.8%).
Conclusions: The combined clinician-collected cervical/vulvovaginal sample is most sensitive for detecting all female genital tract HPV infections. HPV concordance between cervical and vaginal samples may be better for newer infections. Larger studies are needed to determine whether mailed-in self-samples are as effective as those collected in a clinical setting.
TESTING FOR HUMAN PAPILLOMAVIRUS (HPV) DNA is more sensitive than cytology for detecting high-grade squamous intraepithelial lesions (SIL) and invasive cervical cancer.1 Self-collected samples for HPV testing could be effective in increasing cervical cancer screening coverage and participation in HPV vaccine trials, especially if they could be collected in nonclinical settings. Discordant results between self-collected vaginal samples and clinician-collected cervical samples may reflect differences in HPV detection or prevalence in the vagina versus the cervix rather than differences between self- versus clinician-collected sampling methods. We evaluated concordance between self-collected vaginal swab samples and clinician-collected cervical and vulvovaginal swab samples, as well as concordance between clinician-collected cervical and vulvovaginal swab samples, in a population of women in their mid-20s to early 30s and in a population of women in their late teens to mid-20s. We also evaluated whether mailed-in samples were comparable to in-clinic self-collected samples for detecting HPV DNA.
Materials and Methods
Women in population 1 (aged 23–32 years during follow up; mean age, 27.9 years; standard deviation [SD], 2.1) had been recruited 5 to 10 years earlier to participate in a longitudinal study of genital HPV infection when they were students at the University of Washington. Current addresses were available for 543 of the 603 women in the original cohort (90.0%), and at the time of this report, 374 (approximately 69% of women receiving letters) were ultimately reenrolled. Participants were scheduled for up to 2 clinic visits between April 2001 and January 2005, and participants who were not able to physically return for a follow-up visit had the option of mailing in a self-collected sample.
Women in population 2 (aged 18–25 years during follow up; mean age, 20.7 years; SD, 1.9) were newly recruited to participate in a longitudinal study of genital HPV infection. Letters of invitation were mailed to 18- to 22-year-old female students who were eligible to participate if they had never had vaginal intercourse with a male partner or if their first intercourse had occurred within the past 3 months. A total of 211 women (88.7% of 238 eligible women receiving letters) were enrolled, and clinic visits were scheduled every 4 months between December 2000 and August 2005. All study participants provided written informed consent, and all study protocols and procedures were reviewed and approved by the University of Washington Human Subjects Division.
At each visit, demographic, medical, and sexual history information was collected through a face-to-face interview with a nurse practitioner and participants were given a kit for self-collecting a genital specimen for HPV DNA analysis. The kit consisted of a 15.2-cm prescored Dacron-tipped swab (identical to that used by the study clinician), a covered tube containing 1 mL of specimen transport medium (STM; Digene Diagnostics, Gaithersburg, MD), a plastic cup, a plastic bag, and latex gloves. The kit also included illustrated instructions explaining how to perform the self-collection: “Open the tube. Put it in the cup. Put the tube in the cup so that the liquid inside the tube doesn't spill. Take the Q-tip out of its wrapper. Gently push the Q-tip up into your vagina while holding your labia apart. Insert the Q-tip as far as it will go without hurting, as you would with a tampon. Turn the Q-tip inside your vagina 3 full turns. As you rotate the Q-tip, keep it as far inside your vagina as you can. Take the Q-tip out of your vagina. Take out the Q-tip while you hold your labia apart. Put the Q-tip in the tube. Break off the end of the Q-tip so that you can close the cap tightly. Put the closed tube into the plastic bag. Throw out the broken end of the Q-tip and your gloves. Wash your hands.” The specimen was collected without supervision in an examination room. Women performing the self-collection at home were mailed an identical self-collection kit, and the study clinician administered a telephone interview to collect demographic, medical, and sexual history information and instructed women to collect and mail the sample by Federal Express the same day.
After the in-clinic self-collection, a nurse practitioner performed a standardized pelvic examination. Separate cervical and vulvovaginal prescored Dacron-tipped swab specimens were collected into separate tubes containing 1 mL STM for HPV DNA analysis. In addition, cervical cytology specimens were obtained using a cytobrush to collect cellular material from the endocervical canal and a plastic spatula to collect cells from the squamocolumnar junction and ectocervix. Colposcopic inspection of the vulva, vagina, and cervix was performed, and all women with cytologic or colposcopic evidence of high-grade SIL or repeated cytology showing low-grade SIL or atypical squamous cells of undetermined significance (ASCUS) were referred for colposcopically directed biopsy. Genital warts and other cervical and vaginal infections detected during study examinations were treated according to standard protocols.
Polymerase chain reaction (PCR) methods have been described previously.2 Self-collected samples, clinician-collected cervical samples, and clinician-collected vulvovaginal samples were analyzed separately. DNA was isolated using the QIAamp DNA blood mini column (Qiagen, Inc., Valencia, CA) according to the manufacturer's protocol. One 250th of each sample was amplified and 10 μL of PCR products were dotted onto nylon filters and probed with a biotin-labeled generic probe. Specimens positive by generic probe were typed using the Roche reverse line-blot assay (Roche Molecular Systems, Inc., Alameda, CA). Positive samples and β-globin were first amplified simultaneously using the PGMY09/PGMY11 consensus primers. Seventy microliters of denatured PCR product were added to each well of an Amplicor typing tray containing 3 mL of preheated hybridization solution and a strip containing oligonucleotide probes for β-globin and 37 HPV types. Types 16, 18, 26, 31, 33, 35, 39, 45, 51, 52, 53, 56, 58, 59, 66, 67, 68, 73, and 82 were classified as high risk (HR) and types 6, 11, 40, 42, 54, 55 (a subtype of 44), 57, 61, 62, 64 (a subtype of 34), 69, 70, 71, 72, 81, 83, 84, and CP6108 were classified as low risk (LR).3,4 Samples hybridizing with the generic probe but not with a type-specific probe were classified as negative. Samples negative for β-globin DNA were considered insufficient for analysis.
Cytology specimens were reviewed by a cytotechnologist and all smears showing abnormalities were reviewed by the study pathologist. Findings were classified according to the Bethesda system5 as normal, ASCUS, low-grade SIL, or high-grade SIL. Biopsy tissue was diagnosed as showing cervical intraepithelial neoplasia (CIN) grade 1, 2, or 3. None of the women developed cytologic or histologic evidence of invasive cervical cancer.
Comparisons of HPV DNA results were made among in-clinic self-collected samples, clinician-collected cervical samples, clinician-collected vulvovaginal samples, and combined clinician-collected cervical/vulvovaginal samples. A combined clinician-collected cervical/vulvovaginal sample was defined as positive if either the cervical or vulvovaginal specimen was positive and negative if both specimens were negative. An adjusted McNemar test6 was used to compare the proportions of HPV DNA-positive results between samples while accounting for correlation of multiple samples within subjects. The concordance of HPV DNA detection between sampling modalities was assessed using an unweighted κ statistic to determine the percentage agreement beyond that expected by chance,7 and jackknife estimation was used to compute the variance while accounting for correlation within subjects. A z statistic was used to compare κ statistics between populations. A z statistic was also used to compare the age-adjusted proportions of HPV DNA-positive results among in-clinic and mailed-in self-collected specimens from women in population 1. In population 2, logistic regression was used to assess whether the number of prior self-collections was associated with the likelihood of type-specific positive agreement (defined as testing positive for a specific HPV type in both samples) between self-collected samples and clinician-collected samples (cervical, vulvovaginal, and combined cervical/vulvovaginal). Robust variance estimates were used to account for correlation within subjects.
Two hundred ninety-six of the 374 women in population 1 completed at least one in-clinic visit, contributing a total of 338 in-clinic self-collected samples, 340 clinician-collected cervical samples, and 340 clinician-collected vulvovaginal samples for HPV DNA testing. In addition, 86 women mailed in 88 self-collected samples. Eight women completed one in-clinic visit and mailed in one self-collected sample. The 211 women in population 2 contributed a total of 1,168 self-collected samples, 1,162 clinician-collected cervical samples, and 1,169 vulvovaginal samples. None of the enrolled women refused to perform the self-collection, and there were no reports of prescored swabs breaking during self-collection. The proportion of all samples that were insufficient for HPV DNA analysis by PCR was 1.1% and did not vary by population, sampling method, or location of collection.
In both populations, HPV was most likely to be detected in the clinician-collected combined cervical/vulvovaginal sample followed by the clinician-collected vulvovaginal sample, the self-collected sample, and the clinician-collected cervical sample. These trends were similar for HR HPV and multiple-type infections (see Table 1).
The agreement between sampling modalities was moderate to excellent in population 1 (percent agreement: 86.5–95.7%, κ 0.65–0.92) and excellent in population 2 (percent agreement: 94.9–98.8%, κ 0.84–0.96) (Table 2). Within each population, agreement was slightly higher when restricting to detection of HR HPV types, but the differences were not statistically significant (data not shown). Agreement was higher in population 2 than in population 1 for comparisons of HPV in clinician-collected cervical samples versus self-collected samples (P = 0.01), clinician-collected cervical samples versus clinician-collected vulvovaginal samples (P = 0.03), and clinician-collected cervical samples versus clinician-collected combined cervical/vulvovaginal samples (P = 0.08). Self-collected samples were more concordant with clinician-collected vulvovaginal samples than with clinician-collected cervical samples in population 1, but only slightly more concordant in population 2. Within both populations, combined clinician-collected cervical/vulvovaginal samples were more concordant with clinician-collected vulvovaginal samples than with clinician-collected cervical samples. Clinician-collected cervical samples were similarly concordant with both self-collected samples and clinician-collected vulvovaginal samples within both populations (see Table 2).
Type-specific positive agreement was generally higher in population 2 than in population 1. Within each population, type-specific positive agreement with self-collected samples was highest for vulvovaginal samples followed by combined clinician-collected cervical/vulvovaginal samples and clinician-collected cervical samples (see Table 3).
In population 1, although the age-adjusted prevalence of HPV infection in mailed-in self-collected samples tended to be slightly lower than the age-adjusted prevalence estimates in in-clinic clinician-collected samples, no statistically significant differences were observed (Table 4). Women who mailed in their samples were slightly older than women who self-collected in the clinic (28.5 vs. 27.7; P <0.01) and were as likely to have been HPV-positive at their last clinic visit on the original study (23.2% vs. 21.4%; P = 0.73). Since their last visit on the original study, women who mailed in their samples reported a higher average number of pregnancies (0.70 vs. 0.41, P <0.01), a slightly higher number of new sex partners (2.6 vs. 2.0; P = 0.18), and were slightly more likely to have had an abnormal Pap smear (23.2% vs. 16.3%; P = 0.15).
Eight cases of CIN 2 to 3 were detected over the course of the study, including 3 cases of CIN 3 and one case of CIN 2 in population 1 and 4 cases of CIN 2 in population 2. At the visit before biopsy, HR HPV types were detected in 8 of 8 (100%) clinician-collected vulvovaginal samples, 7 of 8 (87.5%) clinician-collected cervical swab samples, and 6 of 8 (75%) in-clinic self-collected swab samples. One woman with CIN 3 was negative for HR HPV on the self-collected sample only, and another woman with CIN 3 was negative for HR HPV on both the clinician-collected cervical and self-collected samples.
In population 2, the number of prior self-collections was positively associated with the likelihood of type-specific positive agreement between self-collected swabs and clinician-collected vulvovaginal swabs (odds ratio [OR] for each increase of one prior self-collection = 1.21; 95% confidence interval [CI] = 1.09–1.33). No statistically significant associations between the number of prior self-collections and likelihood of type-specific positive agreement were observed for comparisons between self-collected swabs and clinician-collected cervical (OR for each increase of one prior self-collection = 0.99; 95% CI = 0.88–1.12) or clinician-collected combined cervical/vulvovaginal (OR for each increase of one prior self-collection = 1.09; 95% CI = 0.97–1.23) swabs.
Most previous studies evaluating HPV concordance between self- and clinician-collected samples have been conducted among women referred for colposcopy or otherwise deemed to be at high-risk for cervical neoplasia.8–18 In contrast, the women in the current study were at low risk for cervical neoplasia and may be more representative of women participating in routine screening or in future HPV vaccination and transmission studies. Our overall concordance estimates between self- and clinician-collected samples are comparable to or higher than those reported by other studies using similar sampling techniques.10,11,15,17–19
Sampling both the cervix and vulva–vagina was the most effective method for detecting HPV infections in the female genital tract. Sampling either site alone (whether by self- or clinician-obtained methods) underestimated the frequency of infection. Nonetheless, in situations in which clinician-performed sampling is not feasible, self-collected vaginal samples may be a viable alternative. Consistent with previous reports of higher rates of HPV detection in self-collected vaginal samples than clinician-collected cervical samples,10,14,15,18–21 we observed that HPV infections were more likely to be detected in vaginal samples (either self-collected or clinician-collected) than in cervical samples. The larger surface area of the vaginal mucosa relative to the cervix may correspond to enhanced detection of infected vaginal cells8 or increased prevalence of infection in the vagina. HPV-infected cervical cells may also shed into the vagina and be detected in vaginal samples. Furthermore, in this study, a portion of self-collected vaginal samples likely included cells directly sampled from the ectocervix, because the instructions were to insert the swab “as far as it will go without hurting” before rotating. Both self-collected vaginal samples and clinician-collected vulvovaginal samples were highly concordant with combined clinician-collected samples of the cervix and vulva–vagina, suggesting that vaginal samples provide a good approximation of HPV infections in the genital tract. Furthermore, the ability of women to effectively self-collect samples is supported by the high concordance between self- and clinician-collected vaginal samples.
The prevalence of HPV infection was higher in the population of older, more sexually experienced women. Concordance between sampling modalities, however, was higher in the younger population of women who were recruited before or close to their sexual debut with the most pronounced differences observed for comparisons between vaginal (either self- or clinician-collected) and cervical samples. This suggests that concordance between the cervix and the vagina may be better for more recently acquired HPV infections as a result of higher levels of detectable virus.22 (We have also observed a positive association between increasing levels of cervical HPV 16 and 18 E7 RNA and likelihood of type-specific positive concordance between cervical and vaginal samples (RL Winer, unpublished data). The excellent concordance rates observed in the younger population suggest that self-collected vaginal swabs would be highly effective in natural history or vaccine surveillance studies conducted among women at risk for acquiring new HPV infections. Women in the younger population, who self-collected more samples than the women in the older population (average number of samples per woman: 5.6 vs. 1.1), may also have had more opportunity to master the self-collection technique. The positive association between number of prior self-collections and increased likelihood of type-specific positive agreement between self-collected and clinician-collected vulvovaginal samples (but not between self-collected samples and clinician-collected cervical or combined cervical/vulvovaginal samples) suggests that experience with the self-collection technique may improve test performance. Nonetheless, our data also suggest that women with no prior self-collection experience are able to accurately self-collect samples, because concordance between self-collected vaginal and clinician-collected vulvovaginal samples was still excellent among both the older women and the younger women at their first visit (κ = 0.85).
The slightly lower prevalence of HPV DNA detected in the mailed versus in-clinic self-collected samples raises some concern about the feasibility of mailed-in samples. The difference may have been partially attributable to age, given that women who mailed in their samples were on average 9 months older than women who collected their samples in the clinic and that women testing negative for HPV DNA in in-clinic self-samples were on average 9 months older than women testing HPV-positive (P < 0.01). Indeed, after age adjustment, differences in prevalence between mailed versus in-clinic self-collected samples decreased, although did not completely disappear. The high rate of β-globin positivity in both mailed-in and in-clinic samples is encouraging and suggests that the quality of mailed-in specimens was equivalent to those collected in the clinic. Harper et al23 previously reported 100% β-globin positivity in mailed-in samples self-collected at home, and Brown et al20 also reported high rates of β-globin positivity in vaginal swab samples self-collected at home and transported by study personnel (as well as increased HPV detection in vaginal samples self-collected at home compared with clinician-collected cervical samples). It is possible, however, that women collecting their samples at home were less meticulous in adhering to the self-collection instructions or that the self-sampling procedure is more difficult to perform outside of the clinical setting. Because mailed-in self-collects were only solicited when women were unable to return for a clinical examination, we did not have paired samples on the same women and were therefore unable to assess concordance between in-clinic self-collected and mailed-in self-collected samples. In future studies, it would be worthwhile to have women self-collect samples both at home and in the clinic on the same day.
Consistent with most previous studies,15,24–27 self-collected swab samples detected a high proportion of HR HPV infections in women with histologically confirmed CIN 2 to 3, but were not as sensitive as clinician-collected cervical samples. For use in cervical cancer screening programs, directed cervical swabs seem to offer the optimal balance between sensitivity and specificity. Nonetheless, although our sample was small, these and other data suggest that a cervical cancer screening strategy that incorporates self-sampling for HR HPV could be a reasonable alternative in situations in which it is not possible to have a clinician obtain the sample for HR HPV DNA testing.
Other limitations of our study should be noted. Both populations of women were relatively young and of high socioeconomic status and therefore our results may not be generalizable to older populations of women or women of lower socioeconomic status. In addition, other studies have shown that using 2 sequential swabs may increase the sensitivity of self-sampling for HPV DNA,8,9 and other collection devices such as tampons (which require more complicated DNA extraction procedures10) and brushes have also been evaluated.8,9,12,14,16,21,27–29 Because our goal was to develop a method that would be easy for the patient to use and the laboratory to process, we decided to have women self-collect only one swab. Finally, because in-clinic self-samples were always collected before clinician-collected samples, it was not possible to assess any potential effect of sampling order. Because there has been some suggestion that more exfoliated cells might be collected by a first swab than by subsequent swabs,10,30 it may be worthwhile to randomize sampling order in future studies.
In conclusion, vaginal swab samples self-collected in a clinical setting are comparable to clinician-collected samples for detecting HPV DNA but may underestimate the frequency of HPV infection. Although mailed-in samples do not appear to be as effective as in-clinic self-collected samples for detecting HPV DNA, future studies should evaluate potential ways to improve the sensitivity of self-samples collected in a nonclinical setting. As a screening tool, self-collected swabs may be a viable alternative in situations in which clinician-performed sampling is not feasible and could be effective in increasing screening coverage. Furthermore, with the recent availability of prophylactic HPV vaccines, it is increasingly important to develop phase IV studies to investigate transmission dynamics and determine the population-level impact of vaccines on the prevalence of HPV types that are and are not targeted by vaccines. For these types of surveillance studies, in which detection of all HPV types in the genital tract is the goal, combined clinician-collected cervical and vulvovaginal sampling would be most sensitive, but self-samples may be a reasonable alternative.
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