Number 40 n June 1, 2011

Liquid-based Cytology Test Use by Office-based
 

Physicians: United States, 2006–2007
 by Esther Hing, M.P.H., Division of Health Care Statistics, National Center for Health Statistics;
 

and Mona Saraiya, M.D., M.P.H., and Katherine B. Roland, M.P.H., Division of Cancer Prevention and Control,
 

National Center for Chronic Disease Prevention and Health Promotion
 

Abstract

Background—In the United States, liquid-based cytology (LBC) has become

a common screening method for cervical cancer. However, the extent of LBC

use, and how it varies by patient and practice characteristics, is unknown.

Objective—This report describes the ordering and provision of Papanicolaou

(Pap) tests, with a major focus on the extent to which LBC has supplanted

conventional cytology. The type of Pap test is examined for visits made to

primary care physicians in 2006–2007 by females aged 15–64.

Methods—Estimates of Pap test cytology use (both LBC and conventional)

are based on combined data from the 2006–2007 National Ambulatory Medical

Care Survey (NAMCS), an annual nationally representative survey of visits to

nonfederal office-based physicians in the United States, as well as on information

reported by sample physicians in Cervical Cancer Screening Supplements fielded

as part of NAMCS during the same years.

Results—In 2006–2007, LBC was used in approximately 75% of Pap tests

for which the type of cytology was known. LBC was less likely to be used for

Medicare patients than for privately insured patients, although LBC use did not

vary significantly according to the other patient or practice characteristics

examined.

Conclusion—The high percentage of LBC use by office-based physicians in

2006–2007 confirms the widespread use of this screening method among primary

care providers, as has been reported in the literature.

Keywords: physician visits • cervical cancer screening

Introduction

In the United States, liquid-based

cytology (LBC) has rapidly become a

common method used in cervical

cancer screening (1–4). Its popularity

with both medical professionals and

insurance companies may be related to

the ease of microscopic interpretation

and the potential for performing

additional medical tests on the same

sample (2,5,6). This popularity may

also be attributable to direct marketing

to physicians, to patients, and to

laboratories (1). However, limited

information is available on the extent of

LBC use and how use varies by patient

and practice characteristics; previous

studies (1,3,4) were based on selected

specialties or were conducted in limited

geographic areas. This report examines

the type of cytology test ordered or

provided at primary care visits to

office-based physicians made by females

aged 15–64 in the United States in

2006–2007.

U.S. DEPARTMENT OF HEALTH AND HUMAN SERVICES 

Centers for Disease Control and Prevention 

National Center for Health Statistics 
Page 2 National Health Statistics Reports n Number 40 n June 1, 2011

Methods

All data were obtained from the

National Ambulatory Medical Care

Survey (NAMCS), conducted by the

Centers for Disease Control and

Prevention’s (CDC) National Center for

Health Statistics. NAMCS is a national

probability sample survey of visits to

nonfederal office-based physicians

selected from the master files of the

American Medical Association and the

American Osteopathic Association. In

2006, NAMCS began including a

separate stratum—community health

centers (CHCs)—which produced an

additional sample of up to 250

clinicians. NAMCS utilizes a multistage

probability sample design involving

patient visits within physician practices

among 112 geographic primary sampling

units. Sampled physicians were asked to

complete Patient Record Forms (PRFs)

for a systematic random sample of up to

30 office visits occurring during a

randomly assigned 1-week reporting

period. For each sampled visit, a sample

weight is computed that takes into

account all stages of the survey design

as well as physician response. The

2006–2007 unweighted response rate

was 60.3%, with 65,963 PRFs

completed (7,8).

This report examines the type of

cytology—LBC, conventional, or

unspecified—provided or ordered at

visits to office-based physicians in

primary care specialties [general/family

practice, obstetrics-gynecology (ob-gyn),

internal medicine, and pediatrics] for

females aged 15–64 who had a

Papanicolaou (Pap) test (n = 1,667).

The weighted percentage of cytology

test visits where type of cytology

was originally reported as unspecified

was 19.4%. The percentage of

PRFs abstracted by a Census field

representative rather than by someone in

a physician’s office was higher for visits

with unspecified type of cytology

(79.6%) than for visits with known type

(44.9%). Physician responses to the

2006 and 2007 Cervical Cancer

Screening Supplements (CCSS) to

NAMCS were used to edit the

unspecified responses. CCSS is

sponsored by CDC’s Division of Cancer

Prevention and Control to examine

provider practices regarding cervical

cancer screening. CCSS is selfadministered in physician offices as part

of NAMCS, and all physician specialties

in this study were eligible for CCSS.

Using this information, 181 of the 365

visits with unspecified cytology type

were inferred to equal the type of

cytology reported to be used by sample

physicians in CCSS. When physicians in

CCSS reported using both methods,

unspecified tests were not changed.

After editing, 10.4% of cytology test

visits remained unspecified (weighted).

Physician characteristics examined

included practice size (solo, 2–5

physicians, 6–10 physicians, or 11 or

more physicians), physician specialty

[ob-gyn, general or family practice, or

other (e.g., internal medicine or

pediatrics)], practice ownership

[physician or group practice, health

maintenance organization (HMO), CHC,

or other ownership], and location of the

practice (geographic region and

metropolitan statistical area status).

Patient characteristics included age and

race, expected payment source, reason

for visit (preventive or not), and whether

a human papillomavirus (HPV) test was

ordered or provided at the sample visit.

Bivariate differences in the type of

cytology test, by selected patient and

practice characteristics, were examined

using chi-square tests of association at

the α = 0.05 level, with Bonferroni

adjustments for multiple comparisons.

If chi-square tests were statistically

significant, a post hoc t-test procedure

was used to make pairwise comparisons

of type of cytology used between

different categories of practice or patient

characteristics. Significant results from

the post hoc procedure are reported

here. Differences in types of cytology

(controlling for patient and provider

characteristics) were analyzed in a

logistic regression model, with LBC

compared with conventional cytology as

the dependent variable. All estimates

were obtained using SUDAAN software

to account for the complex sample

design of NAMCS (9).

Results

In 2006–2007, females aged 15–64

made an estimated 210 million visits to

primary care physicians annually.

Cytology screening was performed at

12.5% (26.2 million) of these visits

(data not shown). Approximately 67.2%

of tests used LBC, 22.3% used

conventional cytology, and 10.4% had

unspecified type of cytology. The

percentage of tests using LBC varies

according to assumptions made about

the nature of the unspecified tests. If the

unspecified tests are assumed to use

conventional cytology, 67.2% of

cytology tests use LBC; however, if the

same tests are assumed to use LBC,

77.7% of all cytology tests use LBC.

If unspecified tests are assumed to be

missing at random (i.e., if only tests of

known type are included in the

denominator), 75.1% of tests use LBC.

NAMCS estimates that assume

unspecified tests use LBC (81.2% for

ob-gyns compared with 69.6% for

family physicians) or are missing at

random (79.3% for ob-gyn and 65.6%

for family physicians) are more

consistent with previous study estimates

(80%–82% LBC among ob-gyns and

75% among family physicians) (1,5,6)

than are estimates assuming that the

unspecified tests use conventional

cytology (72.2% for ob-gyns and 58.0%

for family physicians). In the analysis

that follows, tests with unspecified

cytology were assumed to be randomly

distributed and were therefore deleted.

Among visits with known type of

cytology, a significant bivariate

association between type of test and

physician specialty was found (p < 0.05)

(Table 1). Ob-gyns were significantly

more likely to order LBC (79.3%) than

other primary care physicians (63.0%–

65.6%) (p < 0.05 in both cases). Practice

ownership was also associated with

LBC provision (p < 0.05): CHCs

ordered fewer LBC tests (51.1%) than

physician- and group-owned practices

(77.5%) (p < 0.05). Although the overall

effect of patient’s primary expected

payment source was only marginally

significant (p = 0.06), privately insured

females were significantly more likely
National Health Statistics Reports n Number 40 n June 1, 2011	 Page 3

to have LBC (77.2%) than females

enrolled in Medicare (50.0%) (p < 0.05).

Results of a logistic regression for

LBC relative to conventional cytology

are presented in Table 2. Relative to

visits with conventional cytology tests,

females enrolled in Medicare [odds ratio

(OR) = 0.28; 95% confidence interval

(CI) = 0.12–0.65] had lower odds of

having LBC tests than females relying

on private insurance, all else remaining

constant. Practice ownership, region,

metropolitan statistical area status,

patient age, race, HPV test provision,

and preventive care visits were unrelated

to LBC use in the model. A logistic

regression model that included all

unspecified tests and assumed that they

were all LBC had virtually identical

results (data not shown).

Discussion

For six decades, cytology testing

has been used to detect precancerous or

early cancerous changes in the

cervix (6). Although in 2003 the U.S.

Preventive Services Task Force (10)

cited insufficient evidence to

recommend LBC over conventional

cytology for cervical cancer screening,

LBC has become the most common

testing method. In the present nationally

representative study of outpatient visits

for 2006–2007, approximately 75% of

cytology tests were liquid-based

(assuming missing cytology type was

missing at random). This finding is

consistent with LBC’s rapid replacement

of conventional cytology as the most

common screening method for cervical

cancer.

Although significant bivariate

associations were found between LBC

use and physician specialty and practice

ownership, these associations were not

significant when simultaneously

controlled for in a multivariate logistic

regression. These bivariate findings are,

however, consistent with results from

provider surveys that show that

providers who practice in environments

where resources are scarce, or providers

managed by a larger organization, may

be more likely to use the less expensive

conventional Pap (11,12). Although the

model for the present study found that

Medicare patients were less likely to

have LBC relative to conventional

cytology tests (when controlling for all

other practice and patient

characteristics), this finding requires

further research.

LBC tests are more expensive than

conventional Pap tests. In 2005,

Medicare reimbursement was

approximately $15 for a conventional

Pap test and $27 for LBC (6). The

higher cost of LBC screenings has put

financial pressure on public screening

programs for underserved females, such

as the National Breast and Cervical

Cancer Early Detection Program.

Because clinics providing services for

the program had a difficult time

contracting with providers and

laboratories that performed conventional

Pap tests, the program changed its

reimbursement policy to allow payment

for a Pap test at the higher Medicare

rate for LBC, provided the LBC

screening was only done biennially (6).

The data have certain limitations.

First, the fact that 10.4% of tests had

unspecified type of cytology means that

it is not possible to provide a precise

national estimate of the percentage of

cytology visits with LBC compared with

conventional cytology. Even with this

limitation, the study confirms the

widespread use of LBC among

primary care providers, based on a

nationally representative sample of

office visits during 2006–2007.

Although the ease of conducting HPV

testing on the remaining LBC sample

has been cited as an advantage of

LBC, evidence of comparable

sensitivity and specificity of LBC

and conventional cytology suggests

no advantage of one method over

the other for detecting cervical

cancer (13–15). HPV testing can also

be conducted at lower cost with

conventional cytology through

co-collection (12). These findings raise

questions about the impact of frequent

use of LBC on health care costs (5).

References

1.	 Rappaport KM, Forrest CB,

Holtzman NA. Adoption of liquidbased cervical cancer screening

tests by family physicians and

gynecologists. Health Serv Res

39(4 pt 1):927–47. 2004.

2.	 Yabroff KR, Saraiya M, Meissner HI,

Haggstrom DA, Wideroff L, Yuan G,

et al. Specialty differences in primary

care physician reports of Papanicolaou test screening practices: A

national survey, 2006 to 2007. Ann

Intern Med 151(9):602–11. 2009.

3.	 Noller KL, Bettes B, Zinberg S,

Schulkin J. Cervical cytology

screening practices among

obstetrician-gynecologists. Obstet

Gynecol 102(2):259–65. 2003.

4.	 Saint M, Gildengorin G, Sawaya GF.

Current cervical neoplasia screening

practices of obstetrician/gynecologists

in the U.S. Am J Obstet Gynecol

192(2):414–21. 2005.

5.	 Schiffman M, Solomon D. Screening

and prevention methods for cervical

cancer. JAMA 302(16):1809–10.

2009.

6.	 National Breast and Cervical

Cancer Early Detection Program,

Cervical Cancer Expert Panel.

White paper on technologies for the

early detection of cervical neoplasia

[online]. 2005. Available from:

http://www.hhs.state.ne.us/womens

health/docs/CCEPWhitePaper.pdf.

7.	 National Center for Health Statistics.

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documentation [online]. Hyattsville,

MD. 2008. Available from:

ftp://ftp.cdc.gov/pub/Health_Statistics/

NCHS/Dataset_Documentation/

NAMCS/doc06.pdf.

8.	 National Center for Health Statistics.

2007 NAMCS Micro-data file

documentation [online]. Hyattsville,

MD. 2010. Available from:

ftp://ftp.cdc.gov/pub/Health_Statistics/

NCHS/Dataset_Documentation/

NAMCS/doc07.pdf.

9.	 SUDAAN, release 9.0.1 [computer

software]. Research Triangle Park,

NC: RTI International. 2005.

10. U.S. Preventive Services Task

Force. Screening for cervical cancer:

Recommendations and rationale

[online]. AHRQ Publication
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No. 03–515A. 2003. Available from:

http://www.uspreventiveservices

taskforce.org/3rduspstf/cervcan/

cervcanrr.pdf.

11. Saraiya M, Irwin KL, Carlin L, Chen

X, Jain N, Benard V, Montano DE.

Cervical cancer screening and

management practices among

providers in the National Breast and

Cervical Cancer Early Detection

Program (NBCCEDP). Cancer

110(5):1024–32. 2007.

12. Castle PE, Fetterman B, Poitras N,

Lorey T, Shaber R, Kinney W.

Five-year experience of human

papillomavirus DNA and

Papanicolaou test cotesting. Obstet

Gynecol 113(3):595–600. 2009.

13. Arbyn M, Bergeron C, Klinkhamer P,

Martin-Hirsch P, Siebers AG, Bulten

J. Liquid compared with

conventional cervical cytology: A

systematic review and meta-analysis.

Obstet Gynecol 111(1):167–77. 2008.

14. Siebers AG, Klinkhamer PJ, Grefte

JM, Massuger LF, Vedder JE,

Beijers-Broos A, et al. Comparison

of liquid-based cytology with

conventional cytology for detection

of cervical cancer precursors: A

randomized controlled trial. JAMA

302(16):1757–64. 2009.

15. ACOG Committee on Practice

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National Health Statistics Reports n Number 40 n June 1, 2011 Page 5

Table 1. Distribution of cytology test visits, and type of test, for females aged 15–64, by selected characteristics:

United States, 2006–2007

Selected characteristic1

Distribution of

selected

characteristics

among visits with

known type of

cytology test Total

Percent distribution of

cytology test visits by type2

LBC3 Conventional

All visits (n = 1,483) ............................... 100.0 100 75.1 24.9

Practice size4 ( p = 0.102)

Solo. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

2–5 physicians ..................................

6–10 physicians .................................

11 or more physicians .............................

28.4

43.5

21.7

6.4

100

100

100

100

86.0

72.4

71.6

56.7

*14.0

27.6

28.4

43.3

Physician specialty ( p = 0.033)

Obstetrics or gynecology ............................

General or family practice ...........................

Other primary. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

70.8

21.1

*8.1

100

100

100

79.3

65.6

63.0

20.7

34.4

37.0

Practice ownership ( p = 0.020)

Physician or group................................

Health maintenance organization ......................

Community health center ...........................

Other ownership . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

79.9

*2.5

3.1

14.5

100

100

100

100

77.5

*30.6

51.1

74.7

22.5

69.4

48.9

*25.3

Geographic region ( p = 0.144)

Northeast .....................................

Midwest . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

South. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

West . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

18.3

20.2

41.9

19.6

100

100

100

100

75.6

72.7

81.6

63.1

24.4

27.3

18.4

36.9

MSA5 status ( p = 0.212)

MSA ........................................

Non-MSA . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

90.5

9.5

100

100

76.5

62.0

23.5

38.0

Patient age ( p = 0.136)

15–24 years....................................

25–44 years....................................

45–64 years....................................

15.6

47.1

37.4

100

100

100

72.1

78.1

72.6

27.9

21.9

27.4

Patient race ( p = 0.137)

White . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

Black . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

Other . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

80.1

15.5

4.5

100

100

100

76.5

70.9

64.1

23.5

29.1

35.9

Primary payment source ( p = 0.064)

Private insurance ................................

Medicare6 .................. ..................

Medicaid or SCHIP7 ............... ...............

All other sources .................................

81.2

1.9

6.9

10.0

100

100

100

100

77.2

50.0

65.3

69.1

22.8

50.0

34.7

30.9

HPV8 DNA test ordered or provided ( p = 0.405)

Yes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

No. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

9.4

90.6

100

100

80.7

74.5

*19.3

25.5

Preventive care reason for visit ( p = 0.517)

Yes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

No or unknown ..................................

80.2

19.8

100

100

75.8

72.4

24.2

27.6

* Figure does not meet standards of reliability or precision.
 1

p values refelct chi-square test of association between type of test and characteristic.
 2

Excludes 10.4% of cytology tests with type unspecified.
 3

LBC is liquid-based cytology.
 4

Includes imputed practice size for 0.1% of visits.
 5

MSA is metropolitan statistical area.
 6

Includes patients dually eligible for Medicare and Medicaid.
 7

SCHIP is State Children’s Health Insurance Program.
 8

HPV is human papillomavirus.
 

SOURCE: CDC/NCHS, National Ambulatory Medical Care Survey, 2006–2007.
Page 6 National Health Statistics Reports n Number 40 n June 1, 2011

Table 2. Adjusted odds ratio for liquid-based cytology test, and 95% confidence interval among visits made to primary care physicians

with known type of cytology test, for females aged 15–64 who had a Pap test, by selected characteristics: United States, 2006–2007

Selected characteristic

Adjusted odds ratio

for LBC1

95% confidence

interval

Practice size2

Solo .............................................

3–5 physicians .......................................

6–10 physicians ......................................

11 or more physicians ..................................

Reference

0.43

0.40

0.30

. . .

0.17–1.10

0.15–1.08

0.07–1.34

Physician specialty

Obstetrics or gynecology.................................

General or family practice ................................

Other primary .......................................

Reference

0.74

0.54

. . .

0.33–1.70

0.25–1.17

Practice ownership

Physician or group ....................................

Health maintenance organization ...........................

Community health center ................................

Other ownership . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

Reference

0.26

0.61

0.88

. . .

0.04–1.75

0.26–1.39

0.32–2.42

Geographic region

Northeast ..........................................

Midwest . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

South ............................................

West . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

Reference

0.91

1.11

0.53

. . .

0.24–3.49

0.40–3.11

0.18–1.56

MSA3 status

MSA . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

Non-MSA . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

2.15

Reference

0.69–6.76

. . .

Patient age

15–24 years ........................................

25–44 years ........................................

45–64 years ........................................

Reference

1.30

1.06

. . .

0.83–2.03

0.66–1.70

Patient race

White. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

Black. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

Other. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

Reference

0.70

0.83

. . .

0.39–1.26

0.46–1.52

Primary payment source

Private insurance .....................................

Medicare4 .................... ....................

Medicaid or SCHIP5 ................. .................

All other sources......................................

Reference

0.25

0.64

0.81

. . .

0.10–0.60

0.32–1.25

0.45–1.44

HPV6 DNA test ordered or provided

Yes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

No ..............................................

1.23

Reference

0.48–3.15

. . .

Preventive care reason for visit

Yes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

No or unknown.......................................

1.20

Reference

0.68–2.11

. . .

. . . Category not applicable. 1

LBC is liquid-based cytology. Based on 1,483 visits with known type of cytology test.

2

Includes imputed practice size for 0.1% of visits.

3

MSA is metropolitan statistical area.

4

Includes patients dually eligible for Medicare and Medicaid.

5

SCHIP is State Children’s Health Insurance Program.

6

HPV is human papillomavirus.

SOURCE: CDC/NCHS, National Ambulatory Medical Care Survey, 2006–2007.
Page 8 National Health Statistics Reports n Number 40 n June 1, 2011

Suggested citation

Hing E, Saraiya M, Roland KB. Liquid-based

cytology test use by office-based physicians:

United States, 2006–2007. National health

statistics reports; no 40. Hyattsville, MD:

National Center for Health Statistics. 2011.

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source, however, is appreciated.

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