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Levi S. Downs, Jr., MD Levi S. Downs, Jr., MD
Cervical Cancer Screening:Cervical Cancer Screening:New ApproachesNew Approaches
, ,, ,
Disclosures & images
During the previous 12 months, I have been a consultant for and received honoraria from Merck.
Images are attributed where appropriateNumerous images are utilized from :
ABS: Apgar, Brotzman, Spitzer. Colposcopy, 2nd Ed., 2008
ASCCP Modern Colposcopy, 2nd Ed., 2004
Unlabeled images are from the University of MichiganUnlabeled images are from the University of Michigan
All ASCCP Guidelines are from:Wright TC, Massad S, Dunton CJ, et al. J Lower Genital Tract Disease, 2007; 11: 201-222 and 2007; 11: 223-239
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ObjectivesObjectives
Early detection or prevention of cervical cancer
Prevent mismanagement of screening
Discuss current cervical screening guidelines:
ACS/ASCCP/ASCP Consensus American Cancer Society, American Society for Colposcopy and Cervical Pathology, American Society for Clinical Pathology. Obstet Gynecol 2012; 120: 1222-38
ACOGACOG P ti B ll ti #131 N b 2012ACOG Practice Bulletin #131, November 2012
U.S. Preventive Services Task ForceAnn Int Med 2012; 156: 880-91
Discuss ASCCP 2006 screening guidelinesRevisions due March 2013
Outline
The original Pap test
Better understanding of etiology and natural history
Evolution of cervical cancer screening
The newest guidelines for screening
3
Median Age of Events Associated withMedian Age of Events Associated withCervical Infection by HR HPVCervical Infection by HR HPV
Menarche
1st intercourse1st intercourse
High-risk HPV Infection
ASC-US or LSIL and HPV positive
Pap normal, HPV (-), Type specific antibody (+)
CIN 3/ Carcinoma in situ, HPV (+)
10 15 20 25 30 35 40 45 50
Microinvasive cancer, HPV (+)
Invasive HPV(+)
Evolution of the Pap Test
PublicationsPublications
1917 ”A rhythmical ‘heat period’ in guinea pigs”in guinea pigs
1928 “New cancer diagnosis”
1933 “The sexual cycle in the human female as revealed by vaginal smears”
1941 Publication of “The diagnostic value of gvaginal smears in carcinoma of the uterus”
1949 Widespread introduction of the Pap test begins
Image from US Postal Service
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Cervical Cytology
Normal LSIL HSIL (CIN2)
HSIL (CIS) Invasive SCC
ASCUS
The Good News About Pap Tests:Cervical Cancer Mortality, 1950-2004
5-year mortality per5 year mortality, per 100,000 Caucasian females
American Cancer Society Statistical Report
5
Annual contribution to squamous cervical cancer Annual contribution to squamous cervical cancer screening failure in USAscreening failure in USA
Why does screening fail?
% #
Never screened 50% 6280>5 yrs since screened 10% 1260False Negative Pap 30% 3770Errors in follow up 10% 1260
Total 100% 12,560
Sawaya Obstet Gynecol 1999
Retrospective Study of Cervical Cancers Diagnosed at Kaiser Northern California
Have causes of screening failures changed since 1999?
Pap results 3-36 months prior to diagnosis, N=833
Failure to screen
No Pap 464 56%
No visit: 19%
1-2 visits 18%
>3 visits 63%
Failure in detection: 1st Pap WNL 263 32%
Failure to follow-up: 1st Pap abnormal 106 13%
Leyden MA, Manos M, Kinney W et al JNCI 2005;97:67583
6
System Failures Leading to Cervical Cancer Diagnosis
Health care providersdo not screen women
at visitsPatient does not get
Women do notcome in for
appropriate therapy
Patient gets cervical cancer
screeningColposcopy for
abnormal screennot done
Courtesy of Connie Trimble, MD, Johns Hopkins University School of Medicine, Baltimore, MD
Who are the rarely and never screened?
G % P t t
Proportion of Women Receiving Cervical Cancer Screening,National Health Interview Survey, United States, 2000
Group % Pap test
past 3 years
All women 82%
Insured
Yes
No
85%
62%
Country of birthCountry of birth
US born
Foreign born in U.S. <10 yrs
83%
61%
Swan et al, Cancer. 2003;97:1528-40
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Prevalence of pap tests during last 3 years by education level in the U.S.
https://www.cdc.gov/nchs/data/hus/hus07.pdf
2007. Health US 2007.CDC, National Center for Health Statistics.
How good is the Pap Test?How good is the Pap Test?
Meta-analyses: Biopsy proven CIN 2,3
Sens. Spec.Fahey 49% 62%Follen-Mitchell 67% 77%Nanda 51% 97%
Nanda K et al. Ann Intern Med 2000;132:810-9
Nanda 51% 97%
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Pap Test Evolution
AHCPR tAHCPR report on
Evaluation of Cervical Cytology
Meta-analysis of existing literature
Sensitivity
Conventional pap 51%
Liquid cytology 80%
AHCPR, Evaluation of Cervical Cytology, 1999
Conventional vs. Liquid Cytology: Another Meta-analysis
Arbyn et al, Obstet Gynecol 2008; 111: 167-77
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What has been done to improve screening?
Screening Interval
3 y 2 y 1 y
Decrease in incidence 51% 57% 70%Decrease in mortality 57% 61% 72%Decrease in simple hyst 44% 50% 64%Decrease in rad hyst 43% 50% 67%Decrease in rad hyst 43% 50% 67%Decrease in radiation 58% 65% 73%
AHCPR Evaluation of Cervical Cytology, 1999
Pap Test Evolution
Cost / life-year saved vs. no screening
Screening Interval Liquid ConventionalScreening Interval Liquid Conventional
One year $17,600 $13,271
Two years $8,882 $6,368
Three years $5,918 $4,079
ComparisonComparison
Mammogram cost / life-year saved is $50,000
AHCPR, Evaluation of Cervical Cytology, 1999
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Pap Test Evolution
1995 Automated re-screening system approved by FDA
1996 thin-layer cytology system approved by FDA
1997 Cell location system approved by FDA
1998 Computer assisted primary screening device approved by FDApp y
2001 The Bethesda System of nomenclature
2006 HPV Vaccine approved by FDA
“Finding lesions” is not the objective of screening?!
We can’t tell which lesions will progress
Emphasis should be placed on:
Persistent HPV infections
CIN 3 (no margin for error)
Persistent CIN 2 and CIN 2,3 in non-adolescent womenadolescent women
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What is the rationale for combined What is the rationale for combined screening with HPV test plus Pap?screening with HPV test plus Pap?
++
Premise for clinical use of HPV
Most HPV infections are transient—especially in young womenespecially in young women
Precancerous changes (HSIL) result from persistent HPV infections
Absence of HPV highly predictive of absence of CIN
12
Cumulative incidence of HPVinfection from time of coitarche
Moscicki AB et al. J Adol Health 2005;37:S1-S9
The Probability of Clearing anHPV Infection
708090
10203040506070
Ho GYF et al, NEJM 1998; 328: 423-428
010
0 1 to 6 6 to 12 12 to 18
Months Since Positive Test
13
HPV Prevalence and Cervical Cancer - Incidence by Age
25
30
Hi risk HPV
30
0
5
10
15
20
25 Hi risk HPVCancer
25
15
10
5
0
Sellors et al. CMAJ. 2000;163:503.
Ries et al. Surveillance, Epidemiology and End Results (SEER) Cancer Stats NCI, 1973-1997. 2000.
0
15-1
9
20-2
4
25-2
9
30-3
4
35-3
9
40-4
4
45-4
9
50-5
4
0
Prevalence of HPV by Age Manchester, U.K.
)P
erce
ntag
e H
PV
(+
Peto et al Br. J. Cancer (2004:91:942-53)
Age Group
14
4550
Prevalence of HPV types in females, ages 14-59, United States, 2003-2004 (NHANES)
51015202530354045
Pre
vale
nce
%
Low Risk
High Risk
05
14-19 20-24 25-29 30-39 40-49 50-59
Age, yrs
Dunne E, et al., JAMA, 2007
Sensitivity and specificity to diagnose CIN3 Sensitivity and specificity to diagnose CIN3
Cytology threshold LSIL or ASC-US X2
HR-HPV testing by HC2
Sens Spec Refer NPV
Pap 57.2% 89.9% 11.6% 98.4%Pap 57.2% 89.9% 11.6% 98.4%
HR-HPV 90.8% 72.6%72.6% 29.4% 99.6%
Kulasingam et.al. JAMA 2002;288:1749-57
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The Portland Kaiser Study 20,810 women followed for up to 122 months Over 45 mo incidence of CIN 3+ = 4 54% if HPV+
Combined HPV and Pap Testing Combined HPV and Pap Testing
Over 45 mo, incidence of CIN 3+ = 4.54% if HPV+ or Pap > ASC-US. If both neg, incidence = 0.16%
Efficacy of Pap (> ASC), HR-HPV, and Pap +HPV to predict CIN3+ within 45 mo.
Sensitivity PPV NPVPap + HPV 86.4% 4.54 99.8499.84ap 86 % 5 99 899 8Pap alone 49.2% 9.63 99.47HPV 75.4% 4.40 99.76
Sherman et.al. JNCI 2003;95:46-52
HPV Testing Requirements
Tests must be analytically and clinically validated
Proven acceptable reproducibility, clinical sensitivity, specificity, PPV and NPV for cervical cancer and CIN2/3
Based on FDA approval and/or publication in peer-reviewed scientific literature
Restrict testing to high risk HPV types Restrict testing to high risk HPV types
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FDA approved screening and triage
The first FDA approved test was:Hybrid Capture 2® (hc2), using a solution hybridization
th d T l d i l di HR
Low-risk
6, 11, 42, 43, 44
Because this is a cervical cancer triage test, HPV testing for ASC management and primary screening should be by high-risk panel only
method. Two panels were approved, including a HR panel with 13 types.
High-risk
16, 18, 31, 33, 35, 39, 45, 51, 52, 56, 58, 59, 68
FDA approved screening and triage
The second FDA approved test wasCervista® HPV HR, using an isothermal enzymatic DNACervista HPV HR, using an isothermal enzymatic DNA amplification process. The test detects 14 HR types.
High-risk
16, 18, 31, 33, 35, 39, 45, 51, 52, 56, 58, 59, 66, 68
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FDA approved screening and triage
The FDA approved type-specific testing in 2009: pp yp p gCervista® HPV 16/18
Pitfalls of HPV DNA Testing
Positive HPV at any point in time may be from infection destined to resolve
HC2® reports “positive” at threshold of 1 pg/ml (5000 viral copies)
Report of “equivocal” or “indeterminate” if the levels approach thresholdNo clear next step – most labs recommend repeat
After cytology ~4-5% of specimens have i ffi i t li id f HPV t tiinsufficient liquid for HPV testing
HC2® and Cervista® have differing thresholds. The clinician should be aware of the potential impact upon clinical management.
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Negative HPV identifies a very low
Validation of Co-Testing and Screening Intervals
identifies a very low risk group, whether cytology is negative or not
Kaiser Study
N=331818 women age > 30 in prospective> 30 in prospective co-testing study
Katki HA, et al. Lancet Oncol 2011; 12: 663
HPV testing finds more women at high5-year risk of cancer or pre-cancer
Test 5 year Excess HPV Pap 5 year ExcessTest Result
5-year Risk
Excess Risk
HPV+ 7.6% 7.4%
RR 38HPV- 0.2%
Pap+ 4.7% 4.3%
RR 11 7Pap- 0 4%
HPV Test
Pap Test
5-year Risk
Excess Risk
HPV+ Pap+ 12% 6%
RR 2HPV+ Pap- 6%
HPV- Pap+ 0.9% 0.7%
RR 4 5HPV- Pap- 0 2%RR 11.7Pap 0.4% RR 4.5 HPV- Pap- 0.2%
Katki HA, et al. Lancet Oncol 2011; 12: 663
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Proportion of CoProportion of Co--Test Results inTest Results in331,061 Kaiser Patients over 30331,061 Kaiser Patients over 30
2 4%
3.7% 1.4%
92.5%
2.4%
Discordant
Katki HA, et al. Lancet Oncol 2012; 12: 663
Kaiser Northern California % Pap-/HPV
94 1%
813,000 co-tests
86 8%
89.3%90.4%
91.4%
92.3%
93.5%94.3%
94.1%
93.6%
93.3%
92.5%
Total = 90.9%
% P
ap-/
HP
V-
86.8%%
Castle PE, et al. Five-year experience of human papillomavirus DNA and Papanicolaou test co-testing. Obstet Gynecol 2009;113:595–600
20
Percent of women Pap Normal / HPV positive
Kaiser/Northern California N = 813,000 co-tests
% P
ap-/
HP
V+
Total = 3.90%
6.76%
3.08%
2.89%
2.72%
2.56%
2.59%
3.81%5.01%
2.94%
2.87%
3.02%
Castle PE, et al. Obstet Gynecol 2009
What About HPV (+) and Cytology (-) ?
Rates of HPV persistence - 6 mos:Rates of HPV persistence 6 mos:
Clavel - France: 40%
Cuzick - England: 55%
Kinney-Kaiser @12 mo: 35%
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HPV (+) and Cytology (-)
Risk for CIN 2+ at 6 mos:
Cl l F 4 2%Clavel - France: 4.2%
Cuzick - England: 2.8%
Wright – South Africa: 7.8%
Clavel C et al Br J Cancer 2001;84:1616 1623Clavel C et al. Br J Cancer 2001;84:1616–1623Cuzick J et al. BMJ 2003;362:1871-76Wright TC et al. JAMA 2000;283:81-6
Proportion of CoProportion of Co--Test Results inTest Results in331,061 Kaiser Patients over 30331,061 Kaiser Patients over 30
2 4%
3.7% 1.4%
92.5%
2.4%
Katki HA, et al. Lancet Oncol 2012; 12: 663
Baseline Pap %Neg 96.2
ASC-US 2.6LSIL 0.76AGUS/NOS 0.23ASC-H/HSIL/SCC 0.25
22
Risk of Future CIN 3: Baseline HPV & Pap Test Concordance
Summary of Portland DataLorincz et al. Arch Pathol Lab Med 2003; 127: 959-968
BaselineStatus
N Woman yrs follow-
up
CIN 3N
Rate/100Woman Years
RR(95% CI)
Pap -HPV +
2561 10758 63 0.596 10.6410.64(7.3(7.3--15.5)15.5)
Pap -HPV -
17594 86210 48 0.056 1.0
Association of Initial Pap Abnormalities with Histology
Kaiser study
N=331
818 women age > 30 in prospective co-testing study
ASC-H/HSIL/SCC
LSILHPV+/Pap-
HPV+/ASC-US
AGUS/NOSLSIL
p
0 1 2 3 4 5
Years since enrolment
Katki HA, et al. Lancet Oncol 2011; 12: 663
23
Rate of cervical cancer following negative HPV test or normal Pap
For all women with normal Pap test:For all women with normal Pap test: 7.5 cervical cancers per 100,000 women / year
For all women HPV-negative: 3.8 cervical cancers per 100,000 women / year
For all women HPV-negative who also had a normal Pap test: 3 2 cervical cancers pernormal Pap test: 3.2 cervical cancers per 100,000 women / year
Katki HA, et al. Lancet Oncol 2011; 12: 663
Cumulative Risk Of Invasive Disease Based on Initial Co-Test
Kaiser Study
N=331,818 women age > 30 in prospective co-testing study
Katki HA, et al. Lancet Oncol 2011; 12: 663
24
W th 21 Y
Updated Consensus Guidelines:When to begin screening
Women younger than 21 Years:
1. Saslow et al. ACS/ASCCP/ASCP. CA Cancer J Clin 2012; 62: 147-72 and AJCP 2012; 137: 516 – 542.
2. Moyer VA, et al. USPSTF. Ann Int Med 2012; 156: 880-913. ACOG Practice Bulletin #131, November 20124. NCCN Cervical Cancer Screening Guideline v. 2-2012.
www.NCCN.org
Rationale for Beginning Screening at Age 21Cervical Cancer Incidence by Age Group
USCS*, 1998-2002
Age Rate per 100,0000-19 0.120-29 4.530-39 13.940-49 16.550-64 15.465+ 14.6All ages 9.4
*United States Cancer Statistics includes data from CDC’sNational Program of Cancer Registries and NCI’s
Surveillance, Epidemiology and End Results Program.
Saraiya M et al. Obstet Gynecol 2007;109:360-70.
25
Women older than 65 Years:
Updated Consensus Guidelines:When to cease screening
Screening should not be resumed for any reason, even if a woman reports having a new sexual partner.
Do not screen1. Saslow et al. ACS/ASCCP/ASCP. CA Cancer J Clin 2012; 62:
147-72 and AJCP 2012; 137: 516 – 542.2. Moyer VA, et al. USPSTF. Ann Int Med 2012; 156: 880-913. ACOG Practice Bulletin #131, November 20124. NCCN Cervical Cancer Screening Guideline v. 2-2012.
www.NCCN.org
Cessation of Screening
Adequate negative prior screening
is defined as:
3 consecutive negative cytology results
2 consecutive negative co-tests done within the 10 years before stopping screening with the most recent test within 5 years.y
26
Evidence of adequate negative prior screening is not required
Updated Consensus Guidelines:Women with prior hysterectomy
Evidence of adequate negative prior screening is not required (all but USPST). Screening should not be resumed for any reason, including if a woman reports having a new sexual partner.
1. Saslow et al. ACS/ASCCP/ASCP. CA Cancer J Clin 2012; 62: 147-72 and AJCP 2012; 137: 516 – 542.
2. Moyer VA, et al. USPSTF. Ann Int Med 2012; 156: 880-913. ACOG Practice Bulletin #131, November 20124. NCCN Cervical Cancer Screening Guideline v. 2-2012.
www.NCCN.org
Rationale for Stopping after Hyst
Vaginal cancer rate 7/million/year
663 vag cuff Paps needed to find one VAIN
2066 women followed after hyst for average 89 months:
3% had VAIN, 0 had cancer
Risk of Pap abnormality after hyst = 1%.
Comparable to risk of breast cancer in men Comparable to risk of breast cancer in men for which screening not recommended
Pearce KF et al. NEJM 1996;335:1559-62
Piscitelli JT et al. AmJOG 1995;173:424-30
27
Updated Consensus Guidelines:Women with prior HPV Vaccination
Recommended screening practices should not change on the basis of HPV vaccination
1. Saslow et al. ACS/ASCCP/ASCP. CA Cancer J Clin 2012; 62: 147-72 and AJCP 2012; 137: 516 – 542.
2. Moyer VA, et al. USPSTF. Ann Int Med 2012; 156: 880-913. ACOG Practice Bulletin #131, November 20124. NCCN Cervical Cancer Screening Guideline v. 2-2012.
www.NCCN.org
Not addressed
Both liquid-based and conventional smears are acceptable
Updated Consensus Guidelines:Screening Frequency
Both liquid based and conventional smears are acceptable. Co-testing should NOT be performed for women under age 30. Recommendations NOT intended for women with HIV,
immunocompromise, or in utero DES exposure
1. Saslow et al. ACS/ASCCP/ASCP. CA Cancer J Clin 2012; 62: 147-72 and AJCP 2012; 137: 516 – 542.
2. Moyer VA, et al. USPSTF. Ann Int Med 2012; 156: 880-913. ACOG Practice Bulletin #131, November 20124. NCCN Cervical Cancer Screening Guideline v. 2-2012.
www.NCCN.org
28
C t ti “ f d” d t l “ t bl ” b ll b t
Updated Consensus Guidelines:Screening Frequency
Co-testing “preferred” and cytology “acceptable” by all but USPSTF Recommendations NOT intended for women with HIV,
immunocompromise, or in utero DES exposure
1. Saslow et al. ACS/ASCCP/ASCP. CA Cancer J Clin 2012; 62: 147-72 and AJCP 2012; 137: 516 – 542.
2. Moyer VA, et al. USPSTF. Ann Int Med 2012; 156: 880-913. ACOG Practice Bulletin #131, November 20124. NCCN Cervical Cancer Screening Guideline v. 2-2012.
www.NCCN.org
2006 ASCCP Guideline for Co-test Follow-up
Wright TC, et al. J Lower Genital Tract Disease, 2007; 11: 201-222 and 223-239
29
Updated ASCCP Guideline for Co-test Follow-up
Wright TC, et al. J Lower Genital Tract Disease, 2007; 11: 201-222 and 223-239
UpdatesSaslow. CA Cancer J Clin 2012; 62: 147
RoutineCo-test in5 years
What is the recommended strategy to incorporate HPV-type Specific Testing?
There is no role for testing for low risk HPV ttypes
Testing for HPV 16/18 was approved in March 2009 by the FDA
Individuals with HPV 16 or 18 are at much higher risk of developing HSIL or cancer
30
Percent of Squamous and AdenoCaof Cervix Due to HPV 16 or 18
90 86%
100
HPV 16 or 18
40
50
60
70
8070%
3030%
All other types
Munoz N et al. Int J Cancer 2004;111:278-85. [Evidence Level B]
Castellsague X et al. J Natl Cancer Inst 2006;98:303-15. [Evidence Level B]
0
Squamous cell carcinoma Adenocarcinoma
10
20 14%
Cumulative Incidence of CIN 3+ After Single HPV+Followed for 10 years Among Women > 30
HPV 16HPV 16
HPV 18
HR-HPV other than 16/18
HPV neg
Khan MJ et al. JNCI 2005;97:1072-9.
31
Changes of HPV Type Prevalence by Lesion Severity
HPV Types in CIN 2, CIN 3 and Cervical CancerIceland, 1990-1994 and 1999-2003
Sigurdsson K et al. Int J Cancer 2007;2682-2687
What is the recommended strategy to incorporate HPV-type Specific Testing?
32
What is the recommended strategy to incorporate HPV-type Specific Testing?
UpdatesSaslow. CA Cancer J Clin 2012; 62: 147
Co-test5 years
Colposcopy
Fundamental Principles
The goal of cervical cancer screening is the identification and treatment oftrue cervical cancer precursors
Persistent hi-risk HPV, CIN2 and CIN3 are accepted as cervical cancer precursors
Transient HPV infection, LSIL, and CIN1 are not considered cervical cancer precursorsprecursors
33
The biggest gain in reducing cervical cancer incidence and mortality would be achieved by
Conclusion
incidence and mortality would be achieved by increasing screening rates among women who have not been screened or who have not been screened regularly. . .
ACS, 2002
Recommendation Caveats
Clinicians, patients, payers, IRBs, and the courts should never view recommendations as dictatesshould never view recommendations as dictates. Strong recommendations based on high-quality evidence will not apply to all patients.
Users of guidelines may reasonably conclude that following guidelines will be a mistake for some patients.
However, screening in excess of guidelines has been shown to cause potential harm to patients and to increase cost without sound justification
34
What might a futurescreening strategy include?
New Biomarkers may enhance our ability to detect cancer precursors, e.g. DNA methylationdetect cancer precursors, e.g. DNA methylation of cell adhesion molecule 1, or expression of p16ink4A
When the HPV vaccine is fully deployed, the alteration of disease prevalence will greatly decrease the PPV of Pap testing. It is likely that primary screening will be based on HPV testingprimary screening will be based on HPV testing
2008 ASCCP Biannual Meeting
Questions?
35
Citation SummaryABS: Apgar, Brotzman, Spitzer. Colposcopy, 2nd Ed., 2008
ACOG Practice Bulletin #131: Screening for Cervical Cancer, November 2012
ACS/ASCCP/ASCP Consensus Conference of American Cancer Society, American Society for Colposcopy andCervical Pathology American Society for Clinical Pathology Obstetrics & Gynecology 2012: 120: 1222-38Cervical Pathology, American Society for Clinical Pathology. Obstetrics & Gynecology 2012: 120: 1222 38.
ASCCP Modern Colposcopy, 2nd Ed., 2004
ASCCP Copyright 2004, 2009 American Society for Colposcopy and Cervical Pathology. All rights reserved.
Arbyn et al. Obstet Gynecol 2008; 111: 167-77
Castellsague X et al. J Natl Cancer Inst 2006; 98:303-15 [Evidence Level B]
Castle PE, et al. Five-year experience of human papillomavirus DNA and Papanicolaou test co-testing. ObstetGynecol 2009; 113:595-600
Clavel C et al. Br J Cancer 2001; 84:1616-1623
Connie Trimble, MD, Johns Hopkins University School of Medicine, Baltimore, MD
Cuzick J et al. BMJ 2003; 362: 1871-76
Dunne E, et al. JAMA 2007, 297(8): 813-819. doi:10.1001/jama.297.8.813
Ho GYF et al. NEJM 1998; 328: 423-428
Citation Summary (continued)
Katki HA, et al. Lancet Oncol 2012; 12:663 Khan MJ et al. JNCI 2005; 97:1072-9
Kulasingam et al. JAMA 2002; 288: 1749-57
Leyden MA, Manos M, Kinney W, et al. JNCI 2005; 97:67583Leyden MA, Manos M, Kinney W, et al. JNCI 2005; 97:67583
Moscicki AB et al. J Adol Health 2005; 37:S1-S9
Moyer VA, et al. USPSTF, Ann Int Med 2012; 156: 880-91
Munoz N et al. Int J Cancer 2004; 111:278-85. [Evidence Level B]
NCCN Cervical Cancer Screening Guideline v. 2-2012, www.NCCN.org
Nanda K et al. Ann Intern Med 2000; 132:810-9
National Center for Health Statistics, Health, US, 2007, Centers for Disease Control and Prevention, d / h /d t /h /h 07 dfwww.cdc.gov/nchs/data/hus/hus07.pdf
Pearce KF et al. NEJM 1996; 335:1559-62
Peto et al. Br. J. Cancer (2004:91:942-53)
Piscitelli JT et al. AmJOG 1995; 173:424-30
36
Citation Summary (continued)
Saraiya M et al. Obstet Gynecol 2007; 109:360-70
Saslow et al. ACS/ASCCP/ASCP Cancer J Clin 2012; 62: 147-72 and AJCP 2012; 137: 516-542
Sellors et al. CMAG. 2000; 163.503
Sherman et al. JNCI 2003; 95:46-52
Sigurdsson K et al. Int J Cancer 2007; 2682-2687
Swan et al, Cancer. 2003:1528-40
Wright TC, et al. JAMA 2000; 283:81-6
Wright TC, Massad S, Dunton CJ, et al. Journal of Lower Genital Tract Disease 2007, 11:201-22; 11:223-239.
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