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Objective: Rapid, high-volume screening programs are needed as part of cervical cancer prevention in China. Methods: In a 5-day screening project in Inner Mongolia, 3345 women volunteered following a community awareness campaign, and self-swabbed to permit rapid HPV testing. Two AmpFire™ HPV detection systems (Atila Biosystems) were sufficient to provide pooled 15-HPV type data within an hour. HPV+ patients had same-day digital colposcopy (DC) performed by 1 of 6 physicians, using the EVA™ system (MobileODT). Digital images were obtained and, after biopsy of suspected lesions for later confirmatory diagnosis, women were treated immediately based on colposcopic impression. Suspected low- grade lesions were offered treatment with thermal ablation (Wisap), and suspected high-grade lesions were treated with LLETZ. Results: Of 3345 women screened, 624 (18.7%) were HPV+. Of these, 88.5% HPV+ women underwent same-day colposcopy and 78 were treated. Later consensus histology results obtained on 197 women indicated 20 CIN2+, of whom 15 were detected and treated/referred at screening (10 by thermal ablation, 4 by LLETZ, 1 by referral). Conclusions: Global control of cervical cancer will require both vaccination and screening of a huge number of women. This study illustrates a cervical screening strategy that can be used to screen-and-treat large numbers of women. HPV self-sampling facilitates high-volume screening. Specimens can be tested rapidly, promoting minimal loss-to-follow-up. Specifically, the AmpFire™ system used in this study is highly portable, simple, rapid (92 specimens per 65 min per unit), and economical. Visual triage can be performed on HPV+ women with a portable digital colposcope that provides magnification, lighting, and a recorded image. Diagnosis and appropriate treatment remain the most subjective elements. The digital image is under study for deep-learning based automated evaluation that could assist the management decision, either by itself or combined with HPV typing. * Correspondence: email@example.com Centers for Vulvovaginal Disease, Washington, DC, USA Full list of author information is available at the end of the article © The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Goldstein et al. Infectious Agents and Cancer (2020) 15:64 Page 2 of 7 Introduction Inner Mongolia. Accordingly, techniques such as Infection with human papillomavirus (HPV) is a leading visualization with acetic acid (VIA) and HPV testing cause of cancer among women worldwide with approxi- have been studied as alternative methods. mately 500,000 new cervical cancer cases and 250,000 The prevalence of HPV varies amongst different ethnic deaths each year . Cervical cancer is caused by per- and geographic regions [11, 12]. In China, the prevalence sistent infection with a group of carcinogenic HPV geno- and genotype distributions of HPV are well documented. types (HPV16, 18, 31, 33, 35, 39, 45, 51, 52, 56, 58, 59, HPV genotypes 16, 18, 52 and 58 are the most common and probably HPV68) . The importance of cervical cancer-causing types amongst Chinese women, with dif- cancer is accentuated by the relatively young average age fering distribution rates throughout the country. The at incidence and death. prevalence of high-risk HPV within Inner Mongolia Cervical cancer screening strategies have evolved from ranges from 14.5–36.0%, and this varies significantly be- cytology-based to HPV-based . Following the identifi- tween different ethnicities [13–15]. cation of HPV as the cause of cervical cancer and the This study demonstrates the feasibility of a rapid, development of sensitive HPV tests, HPV-based screen- high-volume screening approach that combines self- ing permits the extension of screening intervals and in- sampled HPV testing and digital colposcopy triage to creased impact per number of lifetime screens . reach unscreened populations, as exemplified by Inner Without compromising yield of disease, self- Mongolia, China. sampling can increase participation and reach of cer- vical cancer screening programs. Self-sampling is Methods comparable to clinician-obtained sampling for HPV- This is a cross-sectional analysis using data from women based screening, is well accepted in many populations, attending a same-day, high-volume screening demon- and has been incorporated into screening programs to stration in Inner Mongolia, China. Women were con- improve coverage [4, 5]. tacted and, following an awareness campaign, 3345 Currently, there are no national cervical cancer screen- agreed to participate and provided consent (Fig. 1). Par- ing programs in China and only 10–30% of Chinese ticipants were female, 30–65 years old, who provided women report having ever had cervical cancer screening consent to participate in the study. We excluded women . Although incidence and mortality rates (15.3/100, who: knew or thought they might be pregnant, were un- 000 and 4.6/100,000, respectively) are moderately high, able to provide informed consent, were seriously ill, had the population is so large that every year, there are ap- a gross cervical mass, history of previous treatment for proximately 100,000 new cervical cancer cases and 30, cervical cancer, or complete hysterectomy, or had cer- 000 deaths in China . In general, women living in vical cancer screening in the past 5 years. rural areas are less likely to report ever having had cer- During a 6-day period in May 2019 that consisted of 4 vical cancer screening and mortality rates from cervical clinic days and 2 travel days, 3345 Chinese women aged cancer are up to 48% higher [6, 8–10]. 30 to 65 were screened in three different medical clinics The Inner Mongolia Minority Autonomous Region in the Inner Mongolia Minority Autonomous Region. (Inner Mongolia), is a vast territory that stretches in a IRB approval was obtained from United Family Hospitals great crescent for 1500 miles across northern China. Investigational Review Board, Beijing, China. Local Inner Mongolia was part of the ancient Silk Road region health officials notified and registered potential partici- and is bordered to the north by Mongolia and Russia. pants in the preceding weeks. The vast majority of Inner Mongolia is a geographically diverse and relatively women had never been screened for cervical cancer. underdeveloped province, with a population of over 24 After obtaining informed consent, participants received million in the 2010 census. Forty-nine ethnic groups live a brief explanation of HPV and cervical cancer via a pre- in Inner Mongolia though the majority are Mongolian recorded video, as well as instructions on how to obtain or Han. Additional ethnicities include Manchu, Hui, a self-sampled vaginal specimen. Daur, Ewenki, Oroqen, and Korean. More than 58% of We screened 460–990 women per day (Fig. 2). The the population lives in rural areas. first 79 arrivals were referred directly to colposcopy after Due to the level of development, complex geography, self-sampling, without awaiting the test results, to make and dispersed population across the rural parts of the best use of the physicians’ time. This provided a subset majority of Inner Mongolia, the conventional, multi-step of 69 HPV-negative referrals. Subsequently, only HPV- screening process for cervical cancer is not feasible. The positive women were referred for colposcopic traditional process of screening with cytology, colpos- examination. copy, biopsy and subsequent treatment of women diag- Self-collected vaginal specimens were collected using nosed with cervical precancer is too resource and dry brushes and tested for 15 high-risk HPV (HPV16, expertise-intensive for low-income, vast regions such as HPV18, or a pool of 13 types including HPV31, 33, 35, Goldstein et al. Infectious Agents and Cancer (2020) 15:64 Page 3 of 7 Fig. 1 Study population 39, 45, 51, 52, 53, 56, 58, 59, 66, 68) on site using two lesions, lesions with course mosaicism or punctuation, AmpFire™ (Atila Biosystems, California) machines run- and lesions with sharp borders were considered suspi- ning concurrently. While waiting for test results, women cious for CIN2 + . The limitations of visual assess- participated in a joint breast cancer screening effort. All ment for grading are acknowledged and discussed below. women positive for high-risk HPV (hrHPV+) results If DC was positive for cervical abnormalities (sus- were contacted via text message and returned for colpo- pected CIN1+), patients underwent cervical biopsy of scopic examination the same day or the following day. the exocervix using a SoftBiopsy™ (Histologics, Califor- Digital Colposcopy (DC) was performed with the EVA nia) brush for subsequent confirmatory diagnosis, but system 90 s after the application of acetic acid. All DC were treated presumptively with thermocoagulation or was performed by one of six physicians and the EVA loop electrosurgical excision procedure (LLETZ) the system was used to obtain 1–3 DC images per patient. same day. The SoftBiopsy™ (Histologics, California) Thin acetowhite lesions were considered suspicious for brush obtains tissue from the entire exocervix to be CIN1. Thick acetowhite lesions, rapidly appearing processed in a single slide. Compared with multiple bi- opsies from biopsy forceps, it is faster to obtain tissue from multiple areas of the exocervix and it causes less trauma and bleeding, making it easier to perform ther- mocoagulation (if needed) immediately after biopsy. Thermocoagulation was performed when DC findings were suspicious for CIN1 lesions using one of two differ- ent thermocoagulation systems: C3 thermo-coagulator (WISAP, Germany) or TC thermocoagulator™ (Cure Medical, Utah). A LLETZ was performed when findings were highly suspicious for CIN2+ or when thermal abla- tion was not technically possible. If no acetowhite changes were seen and the entire transformation zone was visible, the patients were in- formed of the findings and not immediately treated. Re- Fig. 2 Health camp approach in the Inner Mongolia Minority peat HPV testing in 1 year was advised; although the Autonomous Region, Photo acknowledgement: Adam Qin availability of such follow-up was recognized not to be Goldstein et al. Infectious Agents and Cancer (2020) 15:64 Page 4 of 7 assured, immediate treatment in the absence of a visible Table 1 General information of the screened residences in three areas in Inner Mongolia lesion was judged not to be warranted. If the transform- ation zone was not fully visible on DC or if the lesion Areas extended in the endocervical canal, endocervical curet- Balinyouqi Aershan Molidawa Total tage (ECC) was performed. Age Overall, at colposcopy, clinician colposcopic impres- 30 ~ 34 76 (8.3) 5 (2.6) 55 (5.5) 136 (6.4) sion led to 216 women biopsied and, of those, 84 imme- 35 ~ 39 143 (15.7) 15 (7.8) 235 (23.4) 393 (18.5) diately treated. Immediate treatment included thermal 40 ~ 44 157 (17.2) 32 (16.6) 237 (23.6) 426 (20) ablation, LLETZ, and none (including women who re- 45 ~ 49 222 (24.3) 46 (23.8) 268 (26.7) 536 (25.2) fused treatment and those treated later, based on histo- logic results). All biopsy specimens were subsequently 50 ~ 54 153 (16.8) 60 (31.1) 152 (15.1) 365 (17.2) processed, and read twice, by two pathologists (QXB, 55 ~ 59 116 (12.7) 31 (16.1) 44 (4.4) 191 (9) JF). The original histopathologic diagnoses included 60 ~ 64 45 (4.9) 4 (2.1) 14 (1.4) 63 (3) CIN1, CIN1–2, CIN2, CIN2–3, CIN3, and inadequate. Mean 46.2 ± 8.0 48.4 ± 6.2 44.0 ± 6.7 45.4 ± 7.4 For this research analysis, precancer case status among Ethnicity the HPV-positive women was defined as follows: CIN3 Han 540 (59.1) 148 (75.1) 681 (67) 1369 (64.4) by either pathologist or CIN2 by both pathologists. The remaining adequate samples were considered <CIN2. Meng 344 (37.7) 39 (19.8) 44 (4.3) 427 (20.1) The few women with unanticipated high-grade lesions Da 0 (0) 0 (0) 189 (18.6) 189 (8.5) (CIN2+) were later contacted with their histology results unknown 29 (3.2) 10 (5.1) 103 (10.1) 139 (6.3) and were counseled to follow up at the regional hospital Parity for appropriate management. As mentioned, while 0 4 (0.4) 3 (1.6) 13 (1.3) 20 (0.9) women were waiting for the results of their HPV tests, 1 393 (43.6) 157 (84) 553 (55) 1103 (51.9) they were screened for breast cancer with a portable ultrasound unit (results reported separately). Through- 2 442 (49.1) 22 (11.8) 376 (37.4) 840 (39.5) out the screening and treatment process, for educational ≥ 3 60 (6.7) 5 (2.6) 63 (6.3) 128 (6.1) purposes, local doctors and nurses were taught colpos- unknown 2 (0.2) 0 (0) 0 (0) 2 (0.1) copy techniques by the visiting physicians and received training to evaluate DC images. cases received treatment: 10 by thermal ablation, 4 by Results LLETZ, 1 by referral. We notified the clinicians of the 5 Using self-sampled HPV testing, 3345 women were untreated cases for follow-up after the program ended. screened. Most women screened were ethnically Han (64.4%) and Meng (20.1%) (Table 1). The majority Discussion (63.7%) were ages 35–49. As its main conclusion, this study showed that large- HPV-positive women (624, 18.7%) were invited for scale cervical cancer screening efforts are feasible using colposcopy and 552 attended the medical examination. self-sampling and rapid HPV testing. Availability of re- Colposcopic impression was inadequate for 20.8%. Of sults within 2 h of collection made it possible for a the rest, 78.5% impressions were normal and not requir- single-visit screen and treat program. ing biopsy. Among the 20 CIN2+ cases, we saw the expected The characteristics of the 197 HPV-positive women strong relationship between HPV positivity and presence that underwent colposcopy and had a biopsy are listed of precancer, with some insights on partial HPV geno- in Table 2. Biopsies were collected with SoftBiopsy® typing. However, our evaluation of absolute sensitivity of brush (44.2%), ECC (52.8%), or both (3%). the HPV test was imperfect, because most HPV-negative From the 78 women who received treatment, 71 women did not receive colposcopic evaluations. HPV (89.7%) were treated with thermal ablation and 7 (9.0%) DNA negativity typically predicts an extremely low risk with LLETZ. of prevalent or incipient cervical cancer (or even precan- This rapid, high-volume program yielded 0.60% of pre- cer) . cancer (20 out of 3345) in the screening population. As the success of cervical cancer screening programs From the 20 cases identified by histology, 10 were in- has dramatically decreased the rates of cervical cancer in fected with HPV16, 1 with HPV18, and 8 with other developed nations, the global burden of this disease falls types (HPV status was unknown for 1 case) (Table 3). mainly in areas of limited resources. It is estimated that Thus, we observed the expected increased risk associated the number of 35–64-year-old women in rural China ex- with HPV16 and HPV18. Fifteen of the 20 HPV-positive ceeds 150 million. As the vast majority of these women Goldstein et al. Infectious Agents and Cancer (2020) 15:64 Page 5 of 7 Table 2 Descriptive statistics for HPV-positive women with for women in China to obtain self-collected HPV speci- biopsies taken (n = 197) mens, which then undergo rapid testing. Self-swabbing Frequency n (%) for HPV appears to be acceptable to Chinese women, re- gardless of their ethnicity. HPV results Rapid testing is a critical aspect of this model as it al- 16 33 (17.2) lows for same-day treatment. The highly portable iso- 18 16 (8.3) thermal PCR based HPV AmpFire™ testing system takes Others 143 (74.5) 1 h to run 94 specimens and provides partial genotyping (another test kit is available for complete typing). It is Colposcopy impression minimally labor intensive and does not require a high degree of technical expertise to run. The self-swab speci- High 21 (10.7) mens can be stored dry (without collection media) and Low 72 (36.5) the reagents can be stored at room temperature for sev- Inadequate 104 (52.8) eral weeks. Furthermore, the price per specimen is ap- Biopsy taken proximately $US 7 and the same system can be used to Brush 87 (44.2) test for other sexually transmitted infections. ECC 104 (52.8) The second component of this proposed model is to perform DC on all HPV+ women with a highly portable Both 6 (3.0) DC system. Our program included 6 physicians, a level Histology of expert involvement that is often not available. Given CIN2+ 20 (10.2) the huge number of women in China who have never < CIN2 176 (89.8) been screened as compared to the number of physicians Treatment available, DC is a modality that could be performed (if Thermoablation 70 (89.7) authorized) by mid-level providers such as nurses or midwives. Digital images obtained have excellent reso- LLETZ 7 (9.0) lution and areas of question can be magnified for better Referral 1 (1.3) interpretation. In addition, captured images can be used None 119 for continued education of mid-level providers, and the Includes 1 multiple infection with HPV types 16 and 18 images can be sent electronically, through a secure, cloud-based portal, to an expert colposcopist for con- have never been screened, strategies must be developed sultation of difficult cases. that allow for the screening and treating of large num- Our study supports assistive technology to aid clinical bers of women. We demonstrate a screen-and-treat decision making based on human visual impression. model that is low-cost, rapid, and capable of being im- Even when performed by experienced specialists, colpo- plemented on a large scale, as evidenced by the ability to scopic impression shows subjectivity and limited reliabil- screen 3345 women in less than one week. The authors ity or inter-observer agreement . In addition to its have previously described a similar strategy for cervical inherent subjectivity, it requires highly trained human cancer screening in the Yunnan Province . resources that are not available in some settings. The first component of this model consists of self- Ongoing efforts using Automated Evaluation (AVE) of obtained HPV specimens for rapid testing. It is practical the cervix show promising results using archived images from a consortium of sites [19, 20]. AVE has been evalu- ated for cervical cancer screening in the general popula- Table 3 Histology by HPV status for women with biopsies taken (n = 216) tion and as triage of HPV positive tests. When used as an aid to VIA (possibly in combination with HPV type), HPV status Histology it might improve risk stratification of screening and CIN2+ <CIN2 Total n (col %) n (col%) n (col%) triage, minimizing the subjectivity of human visual interpretation. 16+ 10 (50.0%) 23 (11.7%) 33 (15.3%) The third component of this screen-and-treat model is 18+ 1 (5.0%) 15 (7.7%) 16 (7.4%) to use the clinical impression obtained from the DC im- Other hrHPV+ 8 (40.0%) 135 (68.9%) 143 (66.2%) ages, perhaps assisted by AVE, to determine immediate Unknown type 1 (5.0%) 4 (2.0%) 5 (2.3%) and appropriate treatment. Thermocoagulation is inex- HPV- (controls) 0 (0.0%) 19 (9.7%) 19 (8.8%) pensive, highly portable, and a highly effective treatment Total 20 196 216 modality for cervical intraepithelial lesions caused by Includes 1 multiple infection with HPV types 16 and 18 HPV. Goldstein et al. Infectious Agents and Cancer (2020) 15:64 Page 6 of 7 Cervical cancer screening programs could be com- Tierney O’Keefe: none to report. Cathy Sebag: Was an employee of MobileODT during the data collection. bined with same-day vaccination efforts for HPV and Lior Lobel: Was an employee of MobileODT during the data collection. other medical interventions. For example, we combined Anna Zhao: employee, United Foundation for China’s Health, a non-profit cervical and breast screening as part of the same 501(c)3 corporation. Yan Ling Lu: none to report. program. The screening model proven to be feasible by this ef- Author details 1 2 fort is promising, but might not be widely applicable at Centers for Vulvovaginal Disease, Washington, DC, USA. Peking University 3 4 Cancer Hospital, Beijing, China. Yale University, New Haven, CT, USA. Duke the present time. The health camp approach (Fig. 2) is, University, Durham, NC, USA. United Family Hospitals, Beijing, China. by its nature, crowded and might be contraindicated 6 7 Medical College of Wisconsin, Milwaukee, WI, USA. Division of Cancer until social gathering is again safe. Where social distan- Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Rockville, MD, USA. New Age Women’s Health, Miami, Florida, USA. cing remains a priority due to COVID-19, cervical 9 10 Annapolis Dermatology Center, Annapolis, MD, USA. Bellingham Bay cancer prevention efforts will need to be adjusted 11 Family Medicine, Bellingham, WA, USA. Pacific Northwest Urology accordingly to maintain a net benefit for participants, as Specialists, Bellingham, WA, USA. Scripps College, Claremont, California, USA. MobileODT, Tel Aviv, Israel. discussed by Ajenifuja et al. in a companion article. 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J Med Virol. 2018;90(1):148–56. 501(c)3 corporation. Shareholder in MobileODT. 14. Wang MZ, Feng RM, Wang S, et al. Clinical performance of human Maria Demarco, Mark Schiffman, Didem Egemen, Kanan Desai: NCI has papillomavirus testing and visual inspection with acetic acid in primary, received cervical screening supplies and results at no cost from several combination, and sequential cervical Cancer screening in China. Sex Transm companies (Roche, BD, Qiagen, MobileODT) for independent evaluations of Dis. 2019;46(8):540–7. test performance. 15. Ji Y, Ma XX, Li Z, Peppelenbosch MP, Ma Z, Pan Q. The burden of human Sarah Bedell: none to report. papillomavirus and chlamydia trachomatis Coinfection in women: a large Janet Gersten: none to report. cohort study in Inner Mongolia, China. J Infect Dis. 2019;219(2):206–14. Gail Goldstein: Is a board member of the Gynecologic Cancers Research 16. Gage JC, Schiffman M, Katki HA, et al. 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Infectious Agents and Cancer – Springer Journals
Published: Oct 22, 2020
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