Obstetrics & Gynecology Track the topics, authors and articles important to you
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

Obstetrics & Gynecology 2001;97:701-706
© 2001 by The American College of Obstetricians and Gynecologists
This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by WEBB, J. C.
Right arrow Articles by SMITH, H. O.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by WEBB, J. C.
Right arrow Articles by SMITH, H. O.

ORIGINAL RESEARCH

Population-Based Study of Microinvasive Adenocarcinoma of the Uterine Cervix

JOEL C. WEBB, MD, CHARLES R. KEY, MD, PhD, CLIFFORD R. QUALLS, PhD and HARRIET O. SMITH, MD

From the Departments of Obstetrics and Gynecology, Pathology, and Mathematics and Statistics, University of New Mexico Health Sciences Center, Albuquerque, New Mexico.

Address reprint requests to: Harriet O. Smith, MD Division of Gynecologic Oncology Department of Obstetrics and Gynecology University of New Mexico Health Sciences Center 2211 Lomas Boulevard NE Albuquerque, NM 87131 E-mail: smith{at}salud.unm.edu


   Abstract
Top
Abstract
Materials and Methods
 Results
 Discussion
 References
 
Objective: To analyze lymph node status and survival rates of women with microinvasive cervical adenocarcinoma (International Federation of Gynecology and Obstetrics stages IA1 and IA2).

Methods: The Surveillance, Epidemiology, and End Results (SEER) Public-Use Database was used to identify cases of microinvasive cervical adenocarcinoma diagnosed between 1988 and 1997. Variables analyzed included stage, extent of surgery, lymph node status, radiation therapy, and age. Statistics included analysis of trends, analysis of variance, log-rank test, one-sided binomial confidence interval estimation, and power analysis.

Results: Among 301 reported cases, 131 had stage IA1 and170 IA2 disease. Simple hysterectomies were done in 54 women with IA1 and 64 with IA2 disease and radical hysterectomies were done in 50 and 83 women, respectively. Only one of 140 women who had lymphadenectomy had a single positive lymph node. There were four tumor-related deaths (one with IA1, and three with IA2 disease). There were no deaths among 96 women (47, IA1; 49, IA2) treated by simple hysterectomy alone. The mean follow-up was 46.5 months (range 1–119). The censored survival rate was 98.7% overall (99.2% IA1, 98.2% IA2). Power analysis estimated that 720 patients would be required in each group to detect a 2% difference in survival. Using one-sided 95% confidence interval estimations, the risk-adverse events rate for IA1 was no more than 3.57%, and 4.50% for IA2 disease.

Conclusion: Prognosis is excellent for microinvasive adenocarcinoma of the uterine cervix. In 96 cases (31.9%), simple hysterectomy alone proved adequate.

The treatment currently accepted for early invasive adenocarcinoma of the cervix is radical hysterectomy and bilateral pelvic lymphadenectomy or radiation therapy.1–3 In contrast, simple hysterectomy or cervical conization is considered adequate therapy for microinvasive (International Federation of Gynecology and Obstetrics [FIGO]) stage IA1 disease of squamous cell histology.1,3,4 Radical hysterectomy with pelvic lymphadenectomy is usually advocated for women with FIGO stage IA2 disease, although simple hysterectomy with or without pelvic lymphadenectomy has been reported in select cases.1,3–5 The rationale for the differences in treatment has been brought into question by recent studies suggesting that some women with microinvasive adenocarcinoma of the cervix can be treated adequately with simple abdominal or vaginal hysterectomy.6–13 Some reports also suggested that conization was sufficient.9,14 With less aggressive surgery, morbidity associated with radical surgery (increased blood loss and operative time, lymphocysts, lymphedema, prolonged hospitalization and recovery, urinary fistula, and bladder dysfunction) is decreased.15

A more aggressive surgical approach for early stage adenocarcinoma of the uterine cervix might be justified. Adequate histologic assessment of the extent of disease might be more difficult than with squamous cell tumors, and some authors reported a higher likelihood of residual disease after conization.8,9,13,16 Invasive adenocarcinoma may have a poorer prognosis than tumors with squamous cell histology.2,3,15,17–19 Given that the incidence of adenocarcinoma of the uterine cervix is increasing17,19,20 and that the disease is being diagnosed at earlier stages and in younger women,13 minimizing the morbidity associated with treatment of very early lesions is becoming increasingly important. Because this cancer is relatively uncommon, individually or collectively the number of reported cases of early stage adenocarcinoma specifically managed by simple hysterectomy is insufficient to evaluate the efficacy of that approach. Further limitations of retrospective hospital-based studies are disparities that exist with respect to expertise in pathologic interpretation and available treatment options.

The objective of this investigation was to evaluate differences in rates of survival and lymph node metastases in women with microinvasive adenocarcinoma (FIGO stage IA1 or IA2 cervical carcinoma) using population based data.


   Materials and Methods
Top
Abstract
 Materials and Methods
Results
 Discussion
 References
 
The Surveillance, Epidemiology, and End Results (SEER) Cancer Incidence Public-Use database includes all systematically recorded cases of histologically or cytologically confirmed invasive cancers between 1973 and 1997, the last year available in the current SEER database (August 1999 submission).21 The SEER program database is derived from population-based registries estimated to cover 9.6% of the United States population. Since 1988, the SEER database has included codes that distinguish early invasive cervical cancer cases that conform to modifications adopted by the 1995 FIGO staging criteria.4 Therefore, our search was restricted to cases registered between 1988 and 1997. The 1995 staging criteria conform to definitions for micro-invasive disease (stages IA1 and IA2) adopted by the Society of Gynecologic Oncologists in 1973, which often are used to guide therapy.

The SEER database allows for identification of specific cancer cases by a large number of variables, including age, primary site, histologic type, extent of disease, and type of primary and adjuvant treatments. The number of lymph nodes examined and their involvement can also be identified. Two staging codes were used to distinguish stage IA1 and IA2 disease, codes [11] and [12].22 The study group was limited to international classification of diseases (ICD) codes specific for malignant adenocarcinoma not otherwise specified [8140], papillary [8260], and villous [8262] morphologic variants.23 Site-specific surgery codes were used to determine the extent of surgical therapy, ie, no surgery [00]; incisional, needle, or aspiration biopsy [02]; local surgical excision, excisional biopsy, amputation of the cervix or cervical stump, laser surgery with pathology specimen, or conization [20]; simple hysterectomy with or without adenectomy [30,35,40]; and radical hysterectomy [50]. The [50] code included radical, modified radical, or extended hysterectomy without further distinction in the coding system.22 After determining whether lymph node sampling was done [site-specific surgery codes 00 versus 01–98], lymph node status (positive or negative), the number of nodes examined, and the location of positive nodes (regional or distant) were abstracted. Radiation therapy includes three codes that allow determination of radiation sequence with surgery, and treatment intent (none, refused, unknown, recommended, external beam, radioactive sources, and combination therapy). Women with no survival time (the date of last information was the same as the date of diagnosis) and cases not microscopically confirmed were excluded from the survival analysis. Causes of death by International Classification of Diseases (ICD-9-CM) codes also were determined.24

The SEER database includes a program that calculates age-adjusted and observed survival rates, but the survival program does not lend itself to multivariate analyses. Therefore, the "list" and "recode" options were used so patient-specific variables including age, year of diagnosis, treatment modalities, and survival (in months) could be included in the survival analysis. Statistically significant differences (P < .05) for age, radiation therapy, and survival, respectively, were determined using one-way analysis of variance, {chi}2, and log-rank tests (SAS/STAT Software; SAS Institute, Inc., Cary, NC). Trends were analyzed using the Joncheere-Terpstra test (StatXact-4 for Windows; CYTEL Software Corporation, Cambridge, MA). Adequacy of the sample size was evaluated using power analysis and univariable estimation procedures (one-sided 95% binomial confidence interval [CI] estimations).

To determine whether microinvasive adenocarcinoma has been analyzed using SEER or another population-based data set, and to compare our results with other published series, a systematic search was done using MEDLINE 1966–2000 (key words "cervical cancer," "adenocarcinoma," "simple hysterectomy," "radical hysterectomy," "early invasion," "epidemiology"). References from each relevant manuscript were reviewed.


   Results
Top
Abstract
 Materials and Methods
 Results
Discussion
 References
 
Between 1988 and 1997, 12,164 cases of histologically confirmed invasive cervical carcinomas were identified, 7270 of which were stage I disease. Of those, 301 cases of invasive adenocarcinoma (including papillary and villous) were recorded, accounting for 2.47% of all cases, and 4.10% of all stage I disease during the 10-year interval. Table 1Go gives the distribution of cases by type of surgery. There were 131 cases with stage IA1 and 170 with stage IA2 disease. In 50 cases, procedures [site-specific surgery codes] other than simple or radical hysterectomy included no surgery [00] (n = 1); incisional, needle, or aspiration biopsy of the primary site [02] (n = 7); local surgical excision, excisional biopsy, trachelectomy or amputation of the cervix or cervical stump, laser with pathology specimen, or conization [20] (n = 38); and hysterectomy, not otherwise specified [60] (n = 4). In 118 women (47.0%), including 54 with IA1 and 64 with IA2 disease, simple hysterectomy was done. Radical hysterectomy was done in 133 cases (53.0%), in 50 women with IA1 and 83 with IA2 disease. Site-specific surgery codes did not differentiate conization from other surgeries less radical than simple hysterectomy until 1993. Overall, the mean age of the 301 women was 43.7 ± 13.2 years. Using analysis of variance, there were no statistically significant differences in age by stage or type of surgery.


View this table:
[in this window]
[in a new window]
  		Table 1. Microinvasive Adenocarcinoma of the Cervix by Stage, Surgery, and Age
 
Lymphadenectomy was done in 140 women (46.5%); in 22, the number of nodes removed was not recorded. Among 118 for whom lymph node information exists, the mean (± standard deviation [SD]) number of lymph nodes removed was 19.5 ± 12.6, range 1–92. Among 118 cases treated by simple hysterectomy, no lymph node sampling was done in 96 (81.4%); in 22 cases, regional node sampling was done in conjunction with simple hysterectomy, and in 113, with radical hysterectomy (Table 2Go). Only one woman (39 years old) with IA2 disease diagnosed in 1991, who was treated by radical hysterectomy and no postoperative radiation therapy, had a positive regional lymph node (one of 11 nodes sampled).


View this table:
[in this window]
[in a new window]
  		Table 2. Lymphadenectomy by Stage and Type of Surgery
 
As depicted in Table 3Go, radiation therapy was given to 18 women (6.0%); it consisted of external beam (n = 7), intracavitary (n = 4), or both (n = 7). Only one woman received preoperative radiation therapy: she was 49 years old, had IA1 disease and underwent radical hysterectomy without lymphadenectomy after combination radiation therapy. She was alive without disease 50 months after diagnosis. The treatment fields prescribed could not be ascertained. One woman refused therapy, a 91-year-old with IA1 disease diagnosed by biopsy only [site-specific surgery code 02], who died of myocardial infarction 6 months after diagnosis. We could not determine whether radiation therapy was given to three women, including two in whom radiation therapy had been recommended. Trends analysis found that, with decreasing complexity of surgery (radical versus simple hysterectomy versus other), radiation therapy use (inclusive of intent to treat/unknown) was more likely (P = .003). By stage (IA1 versus IA2), there were no significant differences in the number of women who received radiation therapy (seven of 131 [5.3%] versus 11 of 170 [6.5%], P = .68). One hundred eight women did not receive radiation therapy (including unknown/recommended). Excluding women who had lymphadenectomy, 96 (31.9%) were treated by simple hysterectomy alone (47 with IA1 and 49 with IA2 disease).


View this table:
[in this window]
[in a new window]
  		Table 3. Radiation Therapy by Stage and Type of Surgery
 
Table 4Go provides analysis of survival, alive and censored by death from other causes, and from cervical cancer, by stage of disease and type of surgery. The mean follow up in months was 46.5 (range 1–119). There were no statistically significant differences in the observed survival rates by stage (P = .48, .95 for stage IA1 and IA2, respectively) or type of surgery (P = .75, .12). The interaction effect of stage and type of surgery also had no effect on survival (P = .87, .30). Overall survival, censored by other causes and uncensored, was 98.7% and 96.0%, respectively. Causes of death by ICD codes of the 12 deaths (4.0%) in this series included cervical cancer (four, 1.3%), cardiovascular disease (four, 1.3%), cirrhosis, diabetes mellitus, colon cancer, and breast cancer (one each). Although the mean age at diagnosis of the women who died (60.8 ± 17.4 years) was higher than that of survivors (43.0 ± 12.5 years, P = .005), there were no differences in the mean age at diagnosis of the women who died of cervical cancer (44.3 ± 10.2 years) compared with survivors (P = .82). To determine possible contributing factors, the four women who died of cervical cancer were analyzed separately. Three women with stage IA2 disease died, two after radical hysterectomy without postoperative radiation therapy, as described previously, one of whom had a single positive regional lymph node. Two women who had been treated by simple hysterectomy died; one with stage IA2 disease received adjuvant external beam radiation and the other, who had stage IA1 disease, had combination radiation therapy. Thus, the tumor-related death rate was one of 131 (0.76%) for stage IA1 and three of 170 (1.8%) for stage IA2 disease. By type of hysterectomy (IA1 plus IA2), the tumor-related death rate for simple hysterectomy (two of 118 [1.7%]) was essentially identical to that for radical hysterectomy (two of 133 [1.5%]). There were no deaths or recurrences among the 96 women (31.9%) treated by simple hysterectomy alone (no lymphadenectomy or radiation therapy, including recommended/unknown).


View this table:
[in this window]
[in a new window]
  		Table 4. Survival Analysis
 
We assumed simple hysterectomy without lymphadenectomy would be adequate therapy for stage IA1 microinvasive adenocarcinoma if the incidence of adverse events (pelvic node positivity or recurrence) were 1% or less. However, if the rate of positive lymph nodes or disease recurrence was 3% or more, then we would conclude that the risk was unacceptable. A power analysis determined the sample size necessary to detect a 2% difference, with approximately equal numbers of women in two groups, with 80% power and {alpha} = 0.05, was 720 in each group. Given the extremely low rates of recurrence or nodal metastases, no published series, including ours, had the power to determine whether there were differences in survival or risk of recurrence by stage (IA1 versus IA2).

In this series, one of 131 women with stage IA1 disease died of cervical cancer. A one-sided (95% binomial CI) estimation determined that the risk, given one adverse event in 131 consecutive cases, was no more than 3.57%. Given that this woman received combination radiation postoperatively, we also assumed that there were identifiable risk factors in the hysterectomy specimen that prompted further therapy and, among the nine women with IA1 disease who had postoperative radiation therapy (including recommended/ unknown) there were similar identifiable risk factors. Using those exclusion criteria, there were no adverse events (deaths, recurrences, or microscopically confirmed positive nodes) among 122 women with IA1 disease who did not receive radiation therapy. The estimation procedure, assuming 0 events in 122 consecutive cases, determined that the risk of an adverse event under those circumstances was no more than 2.43%, within the threshold of risk that we hypothesized was acceptable. In 170 women with stage IA2 disease, there were three tumor-related deaths. The estimation procedure, assuming three events in 170 consecutive cases, determined that the risk was no more than 4.50%, which is above our hypothetical criteria for conservative therapy. In this series, none of 96 women treated with simple hysterectomy and no other form of therapy had recurrent disease (mean follow-up 46.5 months, range 1–119). The estimation procedure determined the risk, given 0 events in 96 consecutive cases, was no more than 3%, also within our hypothesized threshold.


   Discussion
Top
Abstract
 Materials and Methods
 Results
 Discussion
References
 
There is no current consensus on a reproducible definition of microinvasive adenocarcinoma of the cervix.1,5–14,16–19,25 Although FIGO staging does not specifically exclude adenocarcinoma, those guidelines have been applied almost exclusively to tumors of squamous cell histology. The distinction between adenocarcinoma in situ and microinvasive disease, and the measured depth of invasion can be difficult to ascertain, resulting in questionable reproducibility between pathologists.8–10,16 Adenocarcinomas are of several different histologic and morphologic types, with differing behaviors and prognoses.2,9 Nevertheless, some investigators agree that microinvasive adenocarcinoma of the cervix can be defined reproducibly and that FIGO staging criteria can be applied.6–9

There are significant limitations to this retrospective analysis of the SEER population-based data. It was impossible to determine whether, in the simple hysterectomy group, diagnoses were made preoperatively or after review of hysterectomy specimens. If preoperative conization was done, status of the cone margins was not recorded, nor was presence or absence of lymphovascular space involvement. Although the number of nodes inspected and nodal groups involved could be determined, direct spread and sites of disease recurrence could not be abstracted specifically. The extent of hysterectomy (extended, modified radical, or radical hysterectomy) can influence survival, and all were specified by one SEER procedure code for radical hysterectomy. The type of surgeon who did the procedures, much less the extent of subspecialty training, could not be determined. The SEER database depends on input from nine to 11 tumor registries, depending on the time period analyzed, which greatly increases the potential for variability in reported data. Uniform review of all pathologic specimens by a gynecologic pathologist with expertise in defining microinvasive disease was not possible. Pathologic criteria used to guide radiation treatment planning also could not be determined. Perhaps the greatest limitation of the data is the fact that there were no universally accepted guidelines for staging early invasive adenocarcinoma of the cervix, and data entered into the SEER database were based upon staging guidelines that might have been intended for only squamous cell histology. Despite those limitations, we found that microinvasive adenocarcinoma of the uterine cervix, both stages IA1 and IA2, were associated with excellent disease-free censored survivals (99.2% and 98.2%, respectively).

Depth of invasion correlates with outcome for microinvasive cervical adenocarcinoma.6–9,11,18,25 In most reported series, microinvasion was defined as a depth of invasion less than 5 mm, although further stratification was also reported.6,14,18 Those series were relatively small, retrospective, and not population based. Some investigators suggested that increasing depth of invasion was associated with higher recurrence rates.11,18,25 The reported likelihood of disease spread or recurrence for IAl disease is minimal, but it is not zero.25,26 Although recurrent invasive adenocarcinoma rarely occurs after treatment of even adenocarcinoma in situ by simple hysterectomy, it has been reported.27

Tumor volume has been proposed as a more reliable indicator than depth of invasion alone, and this approach has been applied to early invasive cervical adenocarcinoma.6,10,12,28 Although tumor volume is best calculated by direct measurements in three dimensions, in specimens in which the third dimension of the tumor was not available, it was estimated by assuming that the missing dimension was 1.5 times the larger of the other two.28 When this formula is applied to the 1995 FIGO staging criteria, we calculated that tumor volumes for stage IA1 and IA2 disease should not exceed 220.5 mm3 and 367.5 mm3, respectively. If that is true, then all women in this series hypothetically had tumor volumes well below 500 mm3, the lowest suggested cutoff for conservative therapy. Even small tumors can recur, as shown by bilateral nodal metastases in a woman26 with an estimated tumor volume of only 40 mm3 and in our series by the death of a woman with IA1 disease.

Using MEDLINE (1966–2000) the largest series of microinvasive adenocarcinomas identified was a detailed summary of 436 cases (published and unpublished), and the number of cases from any one center ranged from one to 77.9 No population-based studies of microinvasive adenocarcinoma were found. Based on this search, our series of 301 women is the largest reported using any one database or institution, and includes more women treated by simple hysterectomy. In this series and others1,7,13,25–29 women were treated with simple hysterectomy without adverse consequences, which supports the hypothesis that, in properly selected cases, less radical surgery is sufficient. Regardless of the type of hysterectomy, deaths from cervical cancer for IA1 and IA2 disease were rare. Although 75% of all deaths related to cervical cancer were women with IA2 disease, in this series the sample size was insufficient to determine whether there were statistically significant differences in survival by stage (IA1 versus IA2). Using estimation procedures, the risk of a single adverse event for IA1 was no more than 3.57% and no more than 4.50% for IA2 disease. Because women with IA2 disease are at higher risk of positive lymph node status or recurrence, more aggressive therapy, including resection of the regional lymph nodes in addition to hysterectomy, might be warranted.


   Footnotes
 
PII S0029-7844(01)01330-8

Received November 8, 2000. Received in revised form December 14, 2000. Accepted January 25, 2001.


   References
Top
Abstract
 Materials and Methods
 Results
 Discussion
 References
 
1. Jones WB, Mercer GO, Lewis JL, Rubin SC, Hoskins WJ. Early invasive carcinoma of the cervix. Gynecol Oncol 1993;51:26–32.[Medline]

2. Chen RJ, Chang DY, Yen ML, Lee EF, Huang SC, Chow SN, et al. Prognostic factors of primary adenocarcinoma of the uterine cervix. Gynecol Oncol 1998;69:157–64.[Medline]

3. Photopulos GJ. Surgery or radiation for early cervical cancer. Clin Obstet Gynecol 1990;33:872–82.[Medline]

4. Creasman WT. New gynecologic cancer staging. Gynecol Oncol 1995;58:157–8.[Medline]

5. Creasman WT, Zaino RJ, Major FJ, DiSaia PJ, Hatch KD, Homesley HD. Early invasive carcinoma of the cervix (3 to 5 mm invasion): Risk factors and prognosis. Am J Obstet Gynecol 1998;178:62–5.[Medline]

6. Schorge JO, Lee KR, Flynn CE, Goodman A, Sheets EE. Stage IA1 cervical adenocarcinoma: Definition and treatment. Obstet Gynecol 1999;93:219–22.[Abstract/Free Full Text]

7. Nicklin JL, Perrin LC, Crandon AJ, Ward BG. Microinvasive adenocarcinoma of the cervix. Aust N Z J Obstet Gynaecol 1999;39:411–3.[Medline]

8. Kurian K, Al-Nafussi A. Relation of cervical glandular intraepithelial neoplasia to microinvasive and invasive adenocarcinoma of the uterine cervix: A study of 121 cases. J Clin Pathol 1999;52:112–7.[Abstract]

9. Ostor AG. Early invasive adenocarcinoma of the uterine cervix. Int J Gynecol Pathol 2000;19:29–38.[Medline]

10. Covens A, Kirby J, Shaw P, Chapman W, Franseen E. Prognostic factors for relapse and pelvic lymph node metastases in early stage I adenocarcinoma of the cervix. Gynecol Oncol 1999;74:423–7.[Medline]

11. Kaku T, Kamura T, Kunihiro S, Amada S, Kobayashi H, Shigematsu T, et al. Early adenocarcinoma of the uterine cervix. Gynecol Oncol 1997;65:281–5.[Medline]

12. Kaspar HG, Dinh TV, Doherty MG, Hannigan EV, Kumar D. Clinical implications of tumor volume measurement in stage I adenocarcinoma of the cervix. Obstet Gynecol 1993;81:296–300.[Abstract/Free Full Text]

13. Angel C, DuBeshter B, Lin JY. Clinical presentation and management of stage I cervical adenocarcinoma: A 25 year experience. Gynecol Oncol 1992;44:71–8.[Medline]

14. Schorge JO, Lee KR, Sheets EE. Prospective management of stage IA(1) cervical adenocarcinoma by conization alone to preserve fertility: A preliminary report. Gynecol Oncol 2000;78:217–20.[Medline]

15. Webb MJ. Radical hysterectomy. Baillieres Clin Obstet Gynaecol 1997;11:149–66.[Medline]

16. Fu YS, Berek JS, Hilborne LH. Diagnostic problems of in situ and invasive adenocarcinomas of the uterine cervix. Appl Pathol 1987;5:47–56.[Medline]

17. Brand E, Berek JS, Hacker NF. Controversies in the management of cervical adenocarcinoma. Obstet Gynecol 1988;71:261–9.[Abstract/Free Full Text]

18. Berek JS, Hacker NF, Fu Y, Sokale JR, Leuchter RC, Lagasse LD. Adenocarcinoma of the uterine cervix: Histologic variables associated with lymph node metastasis and survival. Obstet Gynecol 1985;65:46–51.[Abstract/Free Full Text]

19. McGonigle KF, Berek JS. Early-stage squamous cell and adenocarcinoma of the cervix. Curr Opin Obstet Gynecol 1992;4:109–19.[Medline]

20. Smith HO, Tiffany MF, Qualls CR, Key CR. The rising incidence of adenocarcinoma relative to squamous cell carcinoma of the uterine cervix in the U.S.—a 24 year population-based study. Gynecol Oncol 2000;78:97–105.[Medline]

21. Surveillance, Epidemiology, and End Results SEER* Stat 3.0, Bethesda, Md, U.S. Department of Health and Human Services, Public Health Service, National Institutes of Health, National Cancer Institute, Cancer Statistics Branch, 2000.

22. Cunningham J, Ries L, Hankey B, Seiffert J, Lyles B, Shambaugh E, et al. The SEER program code manual, revised edition. National Institutes of Health Publication 92-1999. Washington, DC: US Government Printing Office, 1992.

23. Percy C, Van Holten V, Muir C, eds. International classification of diseases for oncology (ICD-O), 2nd edition. Geneva: World Health Organization, 1990.

24. International Classification of Diseases, 9th Revision. Department of Health and Human Services Publication #92-1260.

25. Teshima S, Shimosato Y, Kishi K, Kasamatsu T, Kazuo O, Uei Y. Early stage adenocarcinoma of the uterine cervix. Cancer 1985;56: 167–72.[Medline]

26. Nagarsheth NP, Maxwell GL, Bentley RC, Rodriguez G. Bilateral pelvic lymph node metastases in a case of FIGO stage IA1 adenocarcinoma of the cervix. Gynecol Oncol 2000;77:467–70.[Medline]

27. Krivak TC, Retherford B, Voskuil S, Rose GS, Alagoz T. Recurrent invasive adenocarcinoma after hysterectomy for cervical adenocarcinoma in situ. Gynecol Oncol 2000;77:334–5.[Medline]

28. Burghardt E. Microinvasive carcinoma in gynecological pathology. Clin Obstet Gynecol 1984;11:239–57.

29. Andersen ES, Arffmann E. Adenocarcinoma in situ of the uterine cervix: A clinico-pathologic study of 36 cases. Gynecol Oncol 1989;35:1–7.[Medline]




This article has been cited by other articles:


Home page
 Obstet GynecolHome page
D. H. Moore
Cervical Cancer
Obstet. Gynecol., May 1, 2006; 107(5): 1152 - 1161.
[Abstract] [Full Text] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by WEBB, J. C.
Right arrow Articles by SMITH, H. O.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by WEBB, J. C.
Right arrow Articles by SMITH, H. O.

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS