Research

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ONCOLOGY

Microinvasive adenocarcinoma of the cervix

Lori Spoozak, MD; Sharyn N. Lewin, MD; William M. Burke, MD; Israel Deutsch, MD;
Xuming Sun, MS; Thomas J. Herzog, MD; Jason D. Wright, MD
OBJECTIVE: We compared the outcomes of microinvasive squamous

cell carcinoma and adenocarcinoma of the cervix and examined the

safety of fertility-conserving treatment.
STUDY DESIGN: The Surveillance, Epidemiology, and End Results da-

tabase was used to identify all women with stage IA1 and IA2 cervical
carcinoma diagnosed from 1988 to 2005. The treatment and outcomes
of women with adenocarcinomas were compared with squamous cell
carcinomas.
RESULTS: A total of 3987 women including 988 with adenocarcinomas

(24.8%) were identified. Women with adenocarcinoma were more often

white and were younger (P .05 for all). Survival for stage IA1 adeno-

carcinomas (hazard ratio, 0.79; 95% confidence interval, 0.212.94)

was similar to that of women with squamous cell tumors. For stage IA2
tumors, survival was similar for squamous cell and adenocarcinomas
(hazard ratio, 0.51; 95% confidence interval, 0.18 1.47). For stage
IA1 and IA2 adenocarcinomas, survival was similar for conization and
hysterectomy.
CONCLUSION: Survival is similar for microinvasive adenocarcinomas

and squamous cell carcinomas. Conization appears to be adequate

treatment for microinvasive adenocarcinoma.
Key words: adenocarcinoma of the cervix, fertility conserving
treatment, microinvasive squamous cell carcinoma

Cite this article as: Spoozak L, Lewin SN, Burke WM, et al. Microinvasive adenocarcinoma of the cervix. Am J Obstet Gynecol 2012;206:80.e1-6.

he incidence of invasive adenocarcinoma of the cervix is increasing.

Population-based estimates now suggest
that adenocarcinomas account for more
than a quarter of all newly diagnosed cervical cancers in the United States.1,2 In
certain racial and ethnic groups, adeno-

From the Division of Gynecologic Oncology,

Department of Obstetrics and Gynecology
(Drs Spoozak, Lewin, Burke, Herzog, and
Wright and Ms Sun); the Department of
Radiation Oncology (Dr Deutsch), College
of Physicians and Surgeons, Columbia
University, and Herbert Irving
Comprehensive Cancer Center (Drs Lewin,
Deutsch, Herzog, and Wright and Ms Sun),
New York, NY.
Received May 20, 2011; revised June 18,
2011; accepted July 15, 2011.
The authors report no conflict of interest.
Presented at the 42nd annual meeting on
Womens Cancer of the Society of
Gynecologic Oncologists, Orlando, FL, March
6-9, 2011.
Reprints: Jason D. Wright, MD, Division of
Gynecologic Oncology, Department of
Obstetrics and Gynecology, Columbia
University College of Physicians and Surgeons,
161 Fort Washington Ave., 8th Floor, New
York, NY 10032. jw2459@columbia.edu.
0002-9378/$36.00
2012 Mosby, Inc. All rights reserved.
doi: 10.1016/j.ajog.2011.07.029

80.e1

carcinomas have increased by nearly

50%.3 Whether the prognosis for adenocarcinomas differs from that of squamous cell carcinomas has long been
debated.4-9
Microinvasive carcinomas of the cervix are tumors with 5 mm or less of stromal invasion and 7.0 mm or less of lateral
extension.10 These neoplasms are associated with an excellent prognosis, and
many women with these tumors are candidates for conservative, uterine-preserving treatments.11
Traditionally the classification of microinvasive cervical cancer has been limited to squamous cell carcinomas.10 In
2009, the International Federation of
Gynecology and Obstetrics (FIGO) staging system for cervical cancer was revised
so that microinvasive adenocarcinomas
were staged using the same criteria as microinvasive squamous cell carcinomas.10
Although the risk of parametrial spread
and nodal metastasis in women with microinvasive adenocarcinomas appears to
be low, radical hysterectomy is often
considered the treatment of choice for
these lesions.12-14 This aggressive treatment is in spite of the fact that a number
of studies have suggested that survival
for women with adenocarcinomas and
less than 5 mm of cervical invasion is excellent.12-21 In addition to operative

American Journal of Obstetrics & Gynecology JANUARY 2012

morbidity, radical hysterectomy results

in loss of fertility that can be particularly
problematic because many women with
adenocarcinomas are young. To date,
there have been few data directly comparing the outcomes of microinvasive
adenocarcinomas and squamous cell
carcinomas.
Given the uncertainty regarding the
behavior of microinvasive adenocarcinoma of the cervix, we performed a population-based analysis to determine the
natural history of microinvasive cervical
adenocarcinoma. Specifically we compared the outcomes of women with microinvasive squamous cell carcinoma
and adenocarcinoma and examined the
safety of fertility-conserving treatment.

M ATERIALS AND M ETHODS

The National Cancer Institutes Surveillance, Epidemiology, and End Results
(SEER) database was utilized. SEER is a
population-based cancer registry that includes approximately 26% of the US
population.22 SEER is composed of a
number of geographically distinct tumor
registries. The demographic characteristics of the SEER registries have been previously characterized and reported.23
Data from SEER 17 registries was uti-

Oncology

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TABLE 1

Association between tumor histology and

demographic and clinical characteristics

Characteristic

Squamous cell
(n 2999)

Adenocarcinoma
(n 988)

Age at diagnosis, y

P value
.05

.....................................................................................................................................................................................................................................

40

1428

(47.6)

493

(49.9)

41-65

1319

(44.0)

435

(44.0)

65

252

(8.4)

60

(6.1)

.....................................................................................................................................................................................................................................
.....................................................................................................................................................................................................................................
..............................................................................................................................................................................................................................................

.0001

Race

.....................................................................................................................................................................................................................................

White

2341

(78.1)

846

(85.6)

Black

359

(12.0)

43

(4.4)

Other

299

(10.0)

99

(10.0)

.....................................................................................................................................................................................................................................
.....................................................................................................................................................................................................................................
..............................................................................................................................................................................................................................................

Year of diagnosis

.41

.....................................................................................................................................................................................................................................

1988-1993

487

(16.2)

146

(14.8)

1994-1999

869

(29.0)

279

(28.2)

2000-2005

1643

(54.8)

563

(57.0)

.....................................................................................................................................................................................................................................
.....................................................................................................................................................................................................................................
..............................................................................................................................................................................................................................................

SEER registry

.05

.....................................................................................................................................................................................................................................

West

1502

(50.1)

539

(54.6)

Central

759

(25.3)

229

(23.2)

East

738

(24.6)

220

(22.3)

.....................................................................................................................................................................................................................................
.....................................................................................................................................................................................................................................
..............................................................................................................................................................................................................................................

.0001

Marital status

.....................................................................................................................................................................................................................................

Married

1466

(48.9)

613

(62.0)

Single

1347

(44.9)

341

(34.5)

186

(6.2)

34

(3.4)

.....................................................................................................................................................................................................................................
.....................................................................................................................................................................................................................................

Unknown

..............................................................................................................................................................................................................................................

.0001

Tumor grade

.....................................................................................................................................................................................................................................

266

(8.9)

297

(30.1)

545

(18.2)

216

(21.9)

285

(9.5)

65

(6.6)

1903

(63.5)

410

(41.5)

.....................................................................................................................................................................................................................................
.....................................................................................................................................................................................................................................
.....................................................................................................................................................................................................................................

Unknown

..............................................................................................................................................................................................................................................

Stage

.19

.....................................................................................................................................................................................................................................

IA1

1610

(53.7)

554

(56.1)

IA2

1389

(46.3)

434

(43.9)

.....................................................................................................................................................................................................................................
..............................................................................................................................................................................................................................................

.0001

Treatment

.....................................................................................................................................................................................................................................

Conization

784

(26.1)

182

(18.4)

2215

(73.9)

806

(81.6)

.....................................................................................................................................................................................................................................

Hysterectomy

..............................................................................................................................................................................................................................................

.0001

Lymphadenectomy

.....................................................................................................................................................................................................................................

Yes

913

(30.4)

535

(54.2)

No

2086

(69.6)

453

(45.9)

.....................................................................................................................................................................................................................................
..............................................................................................................................................................................................................................................

Radiation

1.00

.....................................................................................................................................................................................................................................

Yes

176

(5.9)

58

(5.9)

No

2823

(94.1)

930

(94.1)

.....................................................................................................................................................................................................................................
..............................................................................................................................................................................................................................................

Spoozak. Microinvasive cervical adenocarcinoma. Am J Obstet Gynecol 2012.

Research

lized. The study received approval from

the Columbia University Institutional
Review Board.
Women with invasive adenocarcinomas
and squamous cell carcinomas treated between 1988 and 2005 were selected. Patients with adenosquamous carcinomas
were excluded. Clinical and pathologic
data including age at diagnosis (40, 4165, and 65 years of age), race (white,
black, other), grade (1, 2, and 3), and marital status (married and single) were examined. Year of diagnosis was stratified as
1988-1993, 1994-2005, and 2000-2005 for
analysis.
Patients were categorized based on the
geographic area of residence within the
United States at the time of diagnosis as:
central (Detroit, Iowa, Kentucky, Louisiana, and Utah), eastern (Connecticut;
New Jersey; Atlanta, GA; and rural Georgia), and western (Alaska; California;
Hawaii; Los Angeles, CA; New Mexico;
San Francisco, CA; San Jose, CA; and Seattle, WA).
Each patients primary treatment was
classified as either conization or hysterectomy (extrafascial and radical). In addition, whether lymph node sampling
was performed and the presence of nodal
metastasis were recorded for each patient. The extent of disease codes were
used to classify each patients stage based
on the 2009 staging criteria of the FIGO.
Patients with stage IA1 tumors had stromal invasion of 3 mm or less and 7 mm
or less of lateral spread, whereas those
with IA2 tumors had 3-5 mm of stromal
invasion and 7 mm or less of lateral
spread. The vital status of each patient
was recorded.
Frequency distributions between categorical variables were compared using 2
tests. Cox proportional hazards models
were developed to examine stage-specific
survival. In the Cox proportional hazards
analyses, we modeled the cancer-specific
hazard ratios while controlling for other
prognostic variables. The effect of histology on survival was also examined using
Kaplan-Meier analysis and compared using the log-rank test. All analyses were performed with SAS version 9.2 (SAS Institute
Inc, Cary, NC).

JANUARY 2012 American Journal of Obstetrics & Gynecology

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Oncology

R ESULTS
A total of 3987 women including 988 with
adenocarcinomas (24.8%) and 2999 with
squamous cell carcinomas with microinvasive disease (75.2%) were identified. The
demographic and clinical variables of the
cohort are displayed in Table 1. Stage IA1
tumors were noted in 554 of the women
with adenocarcinomas (56.1%) and in
1610 of those with squamous neoplasms
(53.7%), whereas 43.9% of women with
adenocarcinomas and 46.3% of those with
squamous cell carcinomas had stage IA2
tumors (P .19). Women with adenocarcinoma were more often white (85.6% vs
78.1%), were younger at diagnosis, and
were more likely to be married (P .05 for
all). Conization was the primary treatment
in 26.1% of women with squamous cell
carcinomas and in 18.4% of patients with
adenocarcinomas (P .0001).
Lymph node sampling was performed
in 913 women with squamous cell carcinomas (30.4%) and in 535 patients with
adenocarcinomas (54.2%) (Table 1).
Among patients with stage IA1 tumors,
nodal metastases were noted in 3.8%
(95% confidence interval [CI], 2.1
6.3%) of squamous cell carcinomas and
in 0.7% (95% CI, 0 2.6%) of adenocarcinomas (Table 2). For women with
stage IA2 neoplasms, nodal disease was
identified in 3.0% (95% CI, 1.7 4.8%)
of those with squamous cell carcinomas
and in 0.8% (95% CI, 0 1.8%) of
women with adenocarcinomas.
Survival was then examined. KaplanMeier analysis revealed no difference in
cancer-specific survival for women with
stage IA1 cervical cancer based on histology (P .15) (Figure 1). In a multivariable
Cox proportional hazards model, cancerspecific survival for women with stage IA1
adenocarcinomas (hazard ratio [HR],
0.79; 95% CI, 0.212.94) was similar to
that of women with squamous cell tumors
(Table 3). Among women with stage IA1
tumors, the only predictors of survival
were advanced age and nodal metastasis.
Survival was similar whether treatment
consisted of hysterectomy or conization
(HR, 1.84; 95% CI, 0.66 5.17).
Likewise, for women with stage IA2 tumors, Kaplan-Meier analysis showed no difference in cancer-specific survival based on
80.e3

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TABLE 2

Lymph node metastasis stratified by histology and stage

Squamous cell

Adenocarcinoma

Variable

Nodes sampled

Metastasis

Nodes sampled

Metastasis

Stage IA1

371

3.8% (2.16.3)

274

0.7% (0.02.6)

Stage IA2

542

3.0% (1.74.8)

261

0.8% (0.01.8)

..............................................................................................................................................................................................................................................
..............................................................................................................................................................................................................................................

The 95% confidence intervals are shown in parentheses.

Spoozak. Microinvasive cervical adenocarcinoma. Am J Obstet Gynecol 2012.

histology (P .40) (Figure 2). In the multivariable analysis, cancer-specific survival for
IA2 adenocarcinomas (HR, 0.51; 95% CI,
0.181.47)wassimilartothatofwomenwith
squamous cell carcinomas (Table 3). Survival was similar for hysterectomy and
conization (HR, 0.87; 95% CI, 0.332.26).
Five year survival was then examined
stratified by histology, stage, and treatment
(Table 4). Among women with stage IA1
tumors, 5 year survival was similar for
conization and hysterectomy for both
squamous cell carcinomas and adenocarcinomas. For patients with stage IA1 adenocarcinomas, 5 year survival was 96.9%

(95% CI, 94.0 98.4%) for hysterectomy

compared with 98.8% (95% CI, 91.5
99.8%) for conization. For women with
stage IA2 squamous cell tumors, survival
for hysterectomy (96.3%; 95 CI, 94.8
97.4%) was superior to that of conization
(90.2%; 95% CI, 85.8 93.2%). Five year
survival for women with stage IA2 adenocarcinomas was similar for hysterectomy
(98.2%; 95% CI, 88.199.7%) and conization (97.8%; 95% CI, 95.199.0%).

C OMMENT
Our analysis suggests 2 major findings for
microinvasive cervical cancer. First, out-

FIGURE 1

Kaplan-Meier analysis of cancer-specific

survival for stage IA1 cervical cancer

Squamous cell carcinoma is indicated with a solid line, and adenocarcinoma is indicated with a
dashed line.
Spoozak. Microinvasive cervical adenocarcinoma. Am J Obstet Gynecol 2012.

American Journal of Obstetrics & Gynecology JANUARY 2012

Oncology

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TABLE 3

Cox proportional hazards model of factors associated with cancerspecific survival for women with stage IA1 and IA2 cervical cancer
Variable

Stage IA1

Stage IA2

Histology
.....................................................................................................................................................................................................................................
Squamous
Referent
Referent
.....................................................................................................................................................................................................................................
Adenocarcinoma
0.79
(0.212.94)
0.51 (0.181.47)
..............................................................................................................................................................................................................................................
Treatment
.....................................................................................................................................................................................................................................
Hysterectomy
Referent
Referent
.....................................................................................................................................................................................................................................
Conization
1.84
(0.665.17)
0.87 (0.332.26)
..............................................................................................................................................................................................................................................
Age.....................................................................................................................................................................................................................................
at diagnosis, y
40
Referent
Referent
.....................................................................................................................................................................................................................................
41-65
3.48
(0.9113.30)
1.30 (0.572.94)
.....................................................................................................................................................................................................................................
65
17.01
(4.1769.47)
1.78
(0.615.21)
..............................................................................................................................................................................................................................................
Race.....................................................................................................................................................................................................................................
White
Referent
Referent
.....................................................................................................................................................................................................................................
Black
0.45
(0.063.54)
1.09 (0.353.35)
.....................................................................................................................................................................................................................................
Other
0.65
(0.133.39)
0.98 (0.283.41)
..............................................................................................................................................................................................................................................
Year.....................................................................................................................................................................................................................................
of diagnosis
1988-1993
Referent
Referent
.....................................................................................................................................................................................................................................
1994-1999
0.83
(0.242.85)
0.74 (0.331.65)
.....................................................................................................................................................................................................................................
2000-2005
0.32
(0.071.46)
0.49 (0.161.49)
..............................................................................................................................................................................................................................................
SEER
registry
.....................................................................................................................................................................................................................................
West
Referent
Referent
.....................................................................................................................................................................................................................................
Central
1.01
(0.323.23)
0.59 (0.191.79)
.....................................................................................................................................................................................................................................
East
0.92
(0.292.92)
1.08
(0.462.51)
..............................................................................................................................................................................................................................................
Marital
status
.....................................................................................................................................................................................................................................
Married
Referent
Referent
.....................................................................................................................................................................................................................................
Single
1.72
(0.644.61)
1.81 (0.853.85)
..............................................................................................................................................................................................................................................
Tumor
grade
.....................................................................................................................................................................................................................................
1
Referent
Referent
.....................................................................................................................................................................................................................................
2.....................................................................................................................................................................................................................................
3.44 (0.3632.47)
0.56 (0.191.61)
3
6.26
(0.5966.35)
1.22 (0.393.24)
..............................................................................................................................................................................................................................................
Lymph
node
metastasis
.....................................................................................................................................................................................................................................
No
Referent
Referent
.....................................................................................................................................................................................................................................
Yes
93.63 (5.671546.63)
1.39 (0.1512.65)
..............................................................................................................................................................................................................................................
Radiation
.....................................................................................................................................................................................................................................
No
Referent
Referent
.....................................................................................................................................................................................................................................
Yes
0.68 (0.123.85)
3.86 (1.619.29)
..............................................................................................................................................................................................................................................

SEER, Surveillance, Epidemiology, and End Results.

Spoozak. Microinvasive cervical adenocarcinoma. Am J Obstet Gynecol 2012.

comes are similar for squamous cell carcinomas and adenocarcinomas. Second,
conservative fertility-preserving treatment
appears to be safe for women with stage
IA1 and IA2 adenocarcinomas.
Given the concern that adenocarcinomas are associated with an inferior prognosis, prior staging systems have not acknowledged microinvasive adenocarcinomas as an

entity. In contrast, most studies have suggested that women with minimally invasive adenocarcinomas have an excellent
prognosis.12-21,24
In a systematic review of published literature, Hou et al12 noted that the survival for stage IA1 adenocarcinomas was
99%, whereas survival for stage IA2 lesions was 98%. Although these findings

Research

are encouraging, a paucity of data has

been reported to compare the survival of
microinvasive squamous cell carcinomas and adenocarcinomas. Our analysis
confirmed that survival was excellent for
women with both stage IA1 and IA2 adenocarcinomas. Furthermore, we noted
that survival for women with adenocarcinomas and squamous cell carcinomas
was similar when matched by stage.
These findings provide strong support
for the revised FIGO staging system for
cervical cancer.10
A major concern for both prognosis
and treatment planning for women with
microinvasive adenocarcinomas is the
risk of nodal and parametrial metastases.12-16,18,21 In a review of more than
800 cases of stage IA1 and IA2 adenocarcinomas, the risk of nodal metastasis appeared to be approximately 1.3% for
women with stage IA1 tumors and 3.5%
for IA2 neoplasms. In this analysis only 1
patient with parametrial disease was
noted. Recurrence rates were reported at
1.6% for patients with stage IA1 cancers
and 2.8% for women with IA2 tumors.12
In our analysis we noted similarly low
rates of nodal metastasis, less than 1% for
both stage IA1 and IA2 adenocarcinomas. Interestingly, we found nodal disease in 3-3.8% of women with microinvasive squamous cell carcinomas. This
slightly higher rate of nodal spread in
women with squamous tumors may be a
result of selection bias in performing
lymphadenectomy only in women with
squamous cell carcinomas who appeared
to be at higher risk for recurrence. Similarly, physicians were more likely to perform lymphadenectomy in women with
adenocarcinomas, suggesting that physicians believe that nodal disease is more
likely in women with this histology.
Radical hysterectomy is considered
by many to be the treatment of choice
for microinvasive cervical adenocarcinoma.12,14,18,21 In addition to loss of
fertility, the procedure is associated
with substantial morbidity. The overall
excellent survival of women with stage
IA1 adenocarcinoma and the fact that
parametrial metastasis appears to be
exceedingly rare both provide a strong
rationale for less radical surgical therapy.12-16,18,21 For women with stage

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Oncology

IA1 squamous cell carcinoma, prior

studies have suggested that oncologic
outcomes are equivalent for conization
and hysterectomy.11
Among women with stage IA1 adenocarcinomas, conization has also been associated with favorable outcomes.12-15,18,21
An analysis of 52 patients with stage IA1
adenocarcinomas noted no recurrences after an average of 80 months of follow-up.13
In our report 5 year survival was nearly
equivalent for women with stage IA1 adenocarcinoma for conization and hysterectomy. Likewise, in our multivariable
model type of treatment had no impact on
survival.
Given the favorable outcomes for
women with stage IA1 adenocarcinomas,
histology alone should not be a contraindication to fertility-preserving conization.
We noted that women with squamous cell
tumors were more likely to undergo
conization than women with adenocarcinomas (26% vs 18%). Women with adenocarcinomas who are treated with
conization should have a clear margin of
excision and require close follow-up.12
For women with microinvasive cervical cancer, it is unclear whether there is a
difference in survival between stage IA1
and IA2 tumors.12-14,17 In a prior analysis of SEER data, Smith et al14 found no
differences in the frequency of positive
lymph nodes or death for stage IA1 and
IA2 tumors. In our analysis substage had
no appreciable effect on survival for
women with microinvasive cervical adenocarcinomas. For women with stage
IA2 cervical adenocarcinomas, survival
was similar for women for both conization and hysterectomy. Interestingly, we
noted that survival was inferior for
women with stage IA2 squamous cell
carcinoma who underwent conization
compared with those treated with hysterectomy. This finding clearly warrants
further study.
Although our study benefits from the
inclusion of a large number of subjects,
we recognize several important limitations. As with any analysis of tumor registry data, central pathology review was
not available. This is particularly important because measurement of the precise
depth of invasion for microinvasive cer80.e5

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FIGURE 2

Kaplan-Meier analysis of cancer-specific

survival for stage IA2 cervical cancer

Squamous cell carcinoma is indicated with a solid line, adenocarcinoma is indicated with a dashed
line.
Spoozak. Microinvasive cervical adenocarcinoma. Am J Obstet Gynecol 2012.

vical carcinomas, particularly adenocarcinomas, can be problematic.

SEER lacks data on some important
pathologic characteristics including
lymphovascular space invasion and margin status that would have provided additional insights into the patterns of care
and utilization of adjuvant radiotherapy
for women with microinvasive adenocarcinomas. SEER does not capture data

on patterns of recurrence or their treatment. This is particularly important for

patients with microinvasive adenocarcinomas to capture the rates of hysterectomy and recurrence after conization.
Finally, it is impossible to measure individual patient and physician preferences
that may have had an impact on treatment.
In conclusion, we noted that microinvasive cervical adenocarcinoma is asso-

TABLE 4

Five year survival stratified by histology, stage, and treatment

Stage

Squamous cell

Adenocarcinoma

5 year survival

5 year survival

Stage IA1

.....................................................................................................................................................................................................................................

Hysterectomy

1143

95.6% (93.896.9)

433

96.9% (94.098.4)

467

95.1% (91.997.0)

121

98.8% (91.599.8)

.....................................................................................................................................................................................................................................

Conization

..............................................................................................................................................................................................................................................

Stage IA2

.....................................................................................................................................................................................................................................

Hysterectomy

1072

96.3% (94.897.4)

373

98.2% (88.199.7)

317

90.2% (85.893.2)

61

97.8% (95.199.0)

.....................................................................................................................................................................................................................................

Conization

..............................................................................................................................................................................................................................................

The 95% confidence intervals are indicated in parentheses.

Spoozak. Microinvasive cervical adenocarcinoma. Am J Obstet Gynecol 2012.

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ciated with an excellent prognosis. For
women with stage IA1 and IA2 tumors,
histology has little effect on outcome;
survival is similar for adenocarcinomas
and squamous cell tumors. For the majority of women with microinvasive cervical cancer, conization appears to be a
safe alternative to hysterectomy.
f
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