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Obstetrics & Gynecology 2002;100:781-787
© 2002 by The American College of Obstetricians and Gynecologists
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ORIGINAL RESEARCH

Assessment of Cervical Cancer Radioresponse by Serum Squamous Cell Carcinoma Antigen and Magnetic Resonance Imaging

Kiyoshi Ohara, MD, Yumiko Oishi Tanaka, MD, Hajime Tsunoda, MD, Masato Nishida, MD, Shinji Sugahara, MD and Yuji Itai, MD

From the Departments of Radiology and Gynecology, Institute of Clinical Medicine, University of Tsukuba, Tsukuba City, Japan.

Address reprint requests to: Kiyoshi Ohara, MD, University of Tsukuba, Institute of Clinical Medicine, 1-1-1 Tennodai, Tsukuba City 305-8575, Japan; E-mail: ki-ohara{at}md.tsukuba.ac.jp.


   ABSTRACT
TOP
ABSTRACT
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
OBJECTIVE: To investigate the possibility of objective clinical assessment of the radioresponse of cervical cancer via determination of serum squamous cell carcinoma antigen levels and magnetic resonance imaging (MRI)-based estimation of tumor shrinkage.

METHODS: The cases of 60 patients undergoing definitive radiotherapy for cervical squamous cell carcinoma (stage I–II: n = 20; stage III–IV: n = 40) were reviewed. Measurements of serum squamous cell carcinoma antigen levels (n = 60), estimated tumor volume on preradiotherapy MRIs (n = 60), and evaluated tumor shrinkage on postradiotherapy MRIs available (n = 30) were taken. The relation between postradiotherapy squamous cell carcinoma antigen level 2 months after the start of radiotherapy and disease recurrence was investigated. Regression analysis of tumor volume measured on MRIs was used to estimate the extent of tumor shrinkage 2 months after the start of radiotherapy.

RESULTS: Preradiotherapy squamous cell carcinoma antigen levels correlated significantly with preradiotherapy tumor volumes. Recurrence was identified in 27 patients as distant (n = 19), distant and local (n = 1), local (n = 5), or regional (n = 2). Of 51 patients with elevated preradiotherapy squamous cell carcinoma antigen levels, 33 achieved normalized levels after radiotherapy. Squamous cell carcinoma antigen normalization was associated with a higher recurrence-free survival rate at 2 years (74.3%) than that associated with nonnormalization of squamous cell carcinoma antigen (5.6%, P < .001). The extent of shrinkage ranged from 61% to 100%, and there was no local recurrence.

CONCLUSION: Postradiotherapy squamous cell carcinoma antigen status is a useful indicator of clinical outcome, particularly about tumor recurrence. It is not, however, useful for assessing response to radiotherapy. Magnetic resonance imaging is useful for obtaining an objective assessment of radioresponse.

The response of tumors to radiotherapy or chemotherapy is one of the most significant clinical predictors of cancer control. Tumor response is usually assessed morphologically by the extent of tumor shrinkage after treatment.1,2 The extent of shrinkage can be determined objectively by measuring tumors either directly or indirectly via magnetic resonance imaging (MRI) or computed tomography (CT) imaging techniques. For difficult-to-measure tumors, serum tumor-associated antigens can be used as biochemical measures of response to treatment. Serum prostate-specific antigen, for example, is a powerful indicator of the radioresponse of localized prostate cancer.3 In radiotherapy of cervical cancer, however, tumor response has been assessed only subjectively by pelvic examination. This is because physical examination is convenient for estimating the size, color, consistency, and extent of pericervical tumor infiltration, this form of response assessment by experts is considered a good predictor of the likelihood of local disease control, and CT scanning fails to differentiate the tumor mass from normal cervical tissue. Objective measures are needed, however, particularly at the time radiotherapy ceases, when the necessity for adjunctive treatment must be determined. Determination of serum levels of squamous cell carcinoma antigen, a tumor-associated antigen, has been used recently to monitor patients with cervical cancer.4 Squamous cell carcinoma antigen levels are useful clinical measures of estimating tumor burden before and after treatment.5 Magnetic resonance imaging is used in pretreatment staging because it clearly delineates the cervical tumor mass.6 Thus, we performed a retrospective analysis of squamous cell carcinoma antigen levels and MRI-based estimates of tumor shrinkage to determine whether these measures can be used at the time of cessation of radiotherapy as objective indicators of the radioresponse of cervical cancer.


   MATERIALS AND METHODS
TOP
ABSTRACT
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
The study included 60 patients who were selected from 116 consecutive patients with cervical squamous cell carcinoma treated primarily by radiotherapy between January 1990 and December 1998. Inclusion criteria comprised 1) pelvis-confined disease of clinical stage I–IVA of the International Federation of Gynecology and Obstetrics Staging System; 2) definitive radiotherapy, consisting of both external and intracavitary treatment; 3) serial determination of serum squamous cell carcinoma antigen levels before, during, and for 3 months or more after radiotherapy; and 4) preradiotherapy MRI study of the pelvis. Exclusion criteria were 1) postoperative recurrent disease, 2) discontinuation of radiotherapy, 3) treatment with neoadjuvant chemotherapy that could alter patterns of recurrence and of tumor response to radiotherapy, 4) incomplete determination of serum squamous cell carcinoma antigen levels, and 5) tumors difficult to identify or to measure on MRIs. Postradiotherapy MRI was performed arbitrarily for 30 of the 60 patients, and their MRIs were used to morphologically assess response to treatment.

External radiotherapy was performed with 10 MV x-rays through anteroposteriorly opposed, whole pelvic portals with a fraction size of 2.0 or 1.8 Gy at five fractions per week to a total dose of 50.0 or 50.4 Gy. Five elderly patients with stage IB or IIB disease were treated through small pelvic portals instead of whole pelvic portals. A midline shielding was placed when intracavitary radiotherapy was started. For patients with persistent parametrial induration or pelvic lymphadenopathy detected by pretreatment CT scanning, boost irradiation was given at doses up to 64.0 Gy in total (n = 22). For patients with paraaortic lymphadenopathy detected by CT scanning, paraaortic radiotherapy was given at total doses ranging from 40.0 to 50.4 Gy concurrent with (n = 1) or after (n = 5) pelvic radiotherapy. Intracavitary radiotherapy was performed with a high dose–rate remote afterloading system with cobalt-60 sources before September 1993 and with an iridium-192 source thereafter. A set of intrauterine tandem and vaginal ovoid applicators was usually used. The prescribed dose to reference point A was 6.0 Gy per insertion, and 3–6 weekly insertions were performed according to the tumor size. Typically, stage IIIB patients with medium-sized tumors were treated with 30 Gy of whole pelvic irradiation followed by four insertions of intracavitary radiotherapy concurrent with centrally shielded pelvic irradiation of 20–30 Gy, with the overall treatment time of 7 weeks. The overall pelvic radiotherapy treatment time ranged from 29 to 66 days (median 49 days), and for 48 (80%) of the patients it ranged from 40 to 60 days.

Serum squamous cell carcinoma antigen levels (normal <=1.5 ng/mL) were determined serially: prior to radiotherapy, once or twice per month during radiotherapy, and once per month after radiotherapy. Changes in serum squamous cell carcinoma antigen levels were analyzed in each patient over 3 months after the radiotherapy by plotting squamous cell carcinoma antigen levels on a semilogarithmic scale nomogram. The day that preradiotherapy squamous cell carcinoma antigen level was determined was considered day 0. We used a semi-logarithmic scale because radiation-induced cell death is exponential. Postradiotherapy squamous cell carcinoma antigen status was determined 2 months after the start of radiotherapy, typically near the time of cessation of radiotherapy.

A tumor was identified as a hyperintense lesion on T2-weighted MRIs. Tumor volume was estimated according to the following equation on the assumption that the tumor mass was ellipsoid in shape:


(1)

where V is the tumor volume, L is the maximum craniocaudal length, T is the maximum dorsoventral thickness, and W is the maximum lateral width. Preradiotherapy MRIs were obtained within 2 weeks before radiotherapy was begun. Postradiotherapy MRIs were obtained immediately before or immediately after the cessation of radiotherapy, which was between 24 and 65 days (median 42 days) after the start of radiotherapy. Because the postradiotherapy MRIs were not obtained at the same time in all cases, regression analysis was used to estimate the extent of shrinkage at 2 months after the start of radiotherapy. The resulting data were compared with the squamous cell carcinoma antigen response data obtained 2 months after the start of radiotherapy. Preradiotherapy and postradiotherapy tumor volumes for each patient (n = 30) were plotted on a semilogarithmic scale nomogram, with day 0 being the day that preradiotherapy tumor volume was determined. The semilogarithmic scale was used under the assumption that the tumors shrank exponentially over time (which was confirmed by our analysis of squamous cell carcinoma antigen levels). A tumor that showed shrinkage of 100% was regarded as 0.1 mm3 in volume for the purpose of exponential regression analysis. The rate of tumor shrinkage, defined as the slope of the tumor shrinkage curve, was determined by an exponential regression equation as follows:


(2)

where VD is the expected postradiotherapy tumor volume D number of days after radiotherapy initiation, V0 is the preradiotherapy tumor volume, and B is the rate of tumor shrinkage (day-1). The extent of shrinkage was calculated by substituting 60 for D in Equation 2.

During the clinical follow-up examinations, when a patient showed a continued rise in serum squamous cell carcinoma antigen levels without evidence of local recurrence, possible sites of recurrence were checked systemically. The initial site of recurrence was categorized as local (including disease persistence), regional (pelvic lymph node), or distant (outside the treated area).

Recurrence-free survival time and survival time were calculated by the Kaplan–Meier method, beginning at the start of radiotherapy. StatView 4.5 (Abacus Concepts Inc., Berkeley, CA) was used for all statistical analyses. The unpaired t test was used to analyze differences in preradiotherapy squamous cell carcinoma antigen levels and in preradiotherapy tumor volumes between patients grouped by clinical stage. The relation between preradiotherapy squamous cell carcinoma antigen levels and preradiotherapy tumor volumes was determined by regression analysis. Patterns of squamous cell carcinoma antigen level changes were determined. Postradiotherapy squamous cell carcinoma antigen status, that is, normalized or not normalized, was investigated in relation to the recurrence-free survival rate. Fisher exact test was used to analyze differences in postradiotherapy squamous cell carcinoma antigen status between patients grouped by clinical stage. The relation between the rate of tumor shrinkage and preradiotherapy tumor volume was determined by regression analysis. The extent of shrinkage was analyzed in relation to local disease control. The log-rank test was used to analyze differences in recurrence-free survival rates between patients grouped according to postradiotherapy squamous cell carcinoma antigen status. The Mann–Whitney U test was used for comparisons between unmatched pair groups. P values of less than .05 were considered statistically significant.


   RESULTS
TOP
ABSTRACT
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Patient characteristics are shown on Table 1Go. Preradiotherapy squamous cell carcinoma antigen levels ranged from <1.0 to 322.0 ng/mL (Table 1Go); levels were normal in nine patients (15.0%). Preradiotherapy squamous cell carcinoma antigen levels tended to be higher as disease stages increased. The differences were significant between patients with stage II disease and those with stage III disease, between patients with stage II disease and those with stage IV disease, and also between patients with stage III disease and those with stage IV disease. Preradiotherapy tumor volume ranged from 3.0 to 502.6 cm3. Preradiotherapy tumor volume also tended to be greater with stage increases in disease but did not differ statistically between groups. There was a significant positive correlation between preradiotherapy squamous cell carcinoma antigen levels and preradiotherapy tumor volumes (n = 60, r = .612, P < .001; Figure 1Go).


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  		Table 1. Tumor Volume and Squamous Cell Carcinoma (SCC) Antigen Level by Cancer Stage
 


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  		Figure 1. Correlation between preradiotherapy (preRT) tumor volumes estimated on magnetic resonance images and preRT serum squamous cell carcinoma (SCC) antigen levels.

Ohara. Cervical Cancer Radioresponse. Obstet Gynecol 2002.

 
As of the most recent follow-up examination prior to December 2000, 27 patients were living with no evidence of disease (range 4–98 months, median 49 months), 12 were living with disease (range 9–53 months, median 26 months), 15 had died of disease (range 3–35 months, median 18 months), and six had died of either intercurrent disease or old age without evidence of recurrence (range 4–72 months, median 20 months). Fifteen of the 60 patients were lost to follow up: two within 1 year (one without disease, one with disease), six between 1 and 2 years (three without disease, three with disease), and seven after 2 years (all without disease). The sites of initial recurrence were identified for all 27 patients showing recurrence; sites were distant only (n = 19), distant and local (n = 1), local only (n = 5), and regional only (n = 2).

Of 51 patients with elevated preradiotherapy squamous cell carcinoma antigen levels, 33 (64.7%) achieved a normal squamous cell carcinoma antigen status within 2 months of the start of radiotherapy (Table 1Go). Of the remaining 18 patients who failed to achieve normal squamous cell carcinoma antigen status within the first 2 months, four did so within another month; and two of these four underwent sequential paraaortic lymphnode irradiation. Patients with early-stage disease achieved squamous cell carcinoma antigen normalization at a higher rate than did those with advanced-stage disease, but the difference was not statistically significant (P = .099). The preradiotherapy squamous cell carcinoma antigen levels were significantly higher in the 18 patients in whom squamous cell carcinoma antigen was not normalized (range 2.7–322.0 ng/mL, median 27.2 ng/ mL) than in the 33 patients in whom squamous cell carcinoma antigen was normalized (range 1.7–176.0 ng/ mL, median 7.5 ng/mL; P = .003). Changes in squamous cell carcinoma antigen levels were biphasic, particularly in patients who achieved antigen normalization (Figure 2Go). The initial increase or plateau in the squamous cell carcinoma antigen level was observed 2–3 weeks after the start of radiotherapy and was followed by an exponential decline in the squamous cell carcinoma antigen level. The initial phase was identified in 30 (73.2%) of 41 patients for whom squamous cell carcinoma antigen levels 2–3 weeks after the start of radiotherapy were available.



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  		Figure 2. Changes of serum squamous cell carcinoma (SCC) antigen levels after the start of radiotherapy (RT) for 33 patients who achieved squamous cell carcinoma antigen normalization (<1.5 ng/mL) 2 months after RT (left) and for 18 patients who did not achieve it (right). Serum squamous cell carcinoma level changes are characterized in general by a biphasic pattern: a transient increase followed by an exponential decrease.

Ohara. Cervical Cancer Radioresponse. Obstet Gynecol 2002.

 
Of the 33 patients who achieved normal antigen levels, eight (24.2%) showed recurrence between 3.5 and 10.5 months (median 6.5 months) after the start of radiotherapy, with the recurrence sites being distant (n = 4), distant and local (n = 1), local (n = 2), and regional (n = 1). Of the 18 antigen-nonnormalized patients, 17 (94.4%) showed recurrence between 1 and 22 months (median 3 months) after the start of radiotherapy with the recurrence sites being distant (n = 14), local (n = 2), and regional (n = 1). The remaining patient showed antigen normalization 13 months after the start of radiotherapy and, at the most recent follow-up, had survived 5 years without evidence of disease. The cumulative recurrence-free rate was significantly higher in antigen-normalized patients than in antigen-nonnormalized patients (74.3% versus 5.6% at 2 years, P < .001; Figure 3Go).



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  		Figure 3. Recurrence-free survival rate according to post-radiotherapy status of serum squamous cell carcinoma (SCC) antigen.

Ohara. Cervical Cancer Radioresponse. Obstet Gynecol 2002.

 
In the 30 patients for whom postradiotherapy images were available, the preradiotherapy tumor volume ranged from 5.2 to 502.6 cm3 (median 46.4 cm3), and the postradiotherapy tumor volume ranged from 0.1 to 71.5 cm3 (median 1.3 cm3). These 30 patients included two patients for whom local disease was controlled at last examination but who were lost to follow-up within 2 years (12 and 15 months). The observed shrinkage ranged from 49.5% to 100% (median 96.0%); seven tumors disappeared completely, 13 shrank by 91% to 99%, and ten shrank by 90% or less. The rate of tumor shrinkage ranged from 0.007 to 0.058 day-1 (median 0.034 day-1). The rate correlated inversely with the preradiotherapy tumor volume (r = -.451, P = .012), indicating that small tumors responded more quickly to radiotherapy than large tumors.

The extent of shrinkage 2 months after the start of radiotherapy ranged from 61.4% to 100% (median, 99.3%); 11 tumors (36.7%) disappeared completely, whereas six tumors showed 90% or less shrinkage (Figure 4Go). Of the 30 patients noted above, 16 showed recurrence: distant (n = 12), local and distant (n = 1), local (n = 2), and regional (n = 1). Local disease control was achieved for 1 year or more in 25 patients (>2 years in 19 patients) and for less than 1 year in two patients. One patient who showed 94.7% tumor shrinkage but not normalization of squamous cell carcinoma antigen levels after radiotherapy suffered a local recurrence. Two other patients who had a local recurrence did achieve squamous cell carcinoma antigen normalization; one had 61.4% postradiotherapy shrinkage, and the other had 100% postradiotherapy shrinkage.



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  		Figure 4. The extent of tumor shrinkage 2 months after the start of radiotherapy (RT) in relation to the preRT tumor volume. Twenty-five patients achieved local control for 1 year or more after the start of RT (open circles), two achieved local control for less than 1 year (triangles), and the remaining three had local failure within 1 year (solid circles).

Ohara. Cervical Cancer Radioresponse. Obstet Gynecol 2002.

 

   DISCUSSION
TOP
ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Pretreatment serum squamous cell carcinoma antigen levels are significant indicators of prognosis in patients being treated for cervical squamous cell carcinoma.7–9 It is difficult with radiotherapy to achieve local control of large tumors, which are also, in contrast to small tumors, associated with a high risk of metastasis. We have shown a significant correlation between pretreatment serum squamous cell carcinoma antigen levels and pretreatment tumor volumes estimated on MRIs; however, the correlation was only moderate. This likely was owing to the following factors: heterogeneity in squamous cell carcinoma antigen concentrations and distribution among the histomorphologic cell types,10 our assumption in volume calculation that tumors are ellipsoid, and our disregard of the influence of metastatic lymph nodes on tumor cell burden. Therefore, serum squamous cell carcinoma antigen levels as indicators of tumor cell burden are more reliable for intrapatient comparisons than for interpatient comparisons.

Nonnormalization of the squamous cell carcinoma antigen level after radiotherapy was associated highly with recurrence, mainly with distant metastasis in patients with advanced stage III or stage IV disease. Hong et al9 also found that nonnormalization of the squamous cell carcinoma antigen level 3 months after the start of radiotherapy was a significant predictor of reduced survival time due to distant metastasis, even in patients with early stage I or II disease. Therefore, the tumors that will likely respond completely to radiotherapy without metastasizing are distinguishable by the postradiotherapy squamous cell carcinoma antigen normalization, although a few false negatives may occur.11,12 Ngan et al12 reported that three of 56 patients (5.4%) in whom antigen was normalized had histologic residual disease confirmed by biopsy, whereas three of five patients (60%) in whom antigen was not normalized had histologic residual disease.

Biochemical response may predict local control earlier than morphologic response does. Hong et al9 observed that squamous cell carcinoma antigen–normalized patients had a good prognosis regardless of palpable residual induration 2–3 months after radiotherapy. Among 214 antigen-normalized patients, those with residual induration and those without induration showed similar local recurrence rates: 13% (3/24) and 6% (11/190), respectively. This similarity implies that residual induration immediately after radiotherapy is not a strong predictor of local failure. This is supported by our MRI-based analysis of tumor shrinkage and by the findings of Flueckiger et al.13 Large tumors tend to shrink more slowly than small tumors, and therefore, large tumors take a relatively long time to disappear after sterilization. Magnetic resonance imaging is superior to physical examination in the differential assessment of residual tumors and coexisting radiation fibrosis associated with palpable induration. Therefore, squamous cell carcinoma antigen status will be of use in predicting, at the time of radiotherapy cessation, whether the residual tumor will become sterile.

The relation between an MRI-identified residual tumor and the presence of residual cancer cells was studied by Hatano et al in biopsy specimens.14 They observed that 14 of 42 patients showed an MRI-identified residual tumor 1 month after the cessation of radiotherapy, and that six of these 14 tumors were histologically positive. Among the respective six patients, the presence of residual cancer was confirmed in salvage surgery specimens from three patients and by recurrence in two patients; residual cancer was unconfirmed for the remaining patient because of ongoing intracavitary radiotherapy. Thus, MRI-based examination for residual tumor immediately after the cessation of radiotherapy fails to accurately predict the presence of residual cancer cells. A study of the relation between the presence of residual cancer cells and postradiotherapy squamous cell carcinoma antigen status is needed.

In summary, in definitive radiotherapy for patients with locally advanced cervical squamous cell carcinoma, determination of serum squamous cell carcinoma antigen status is useful for predicting systemic disease recurrence associated with nonnormalization of squamous cell carcinoma antigen rather than for assessing radioresponse quantitatively. Magnetic resonance imaging is useful for quantitative assessment of tumor shrinkage, and the majority of tumors eventually disappears or nearly disappears on MRIs obtained after radiotherapy. Because disease recurrence is associated even with tumors that disappear completely, however, methods that can precisely assess radioresponse, regardless of the tumor status on MRIs or whether a tumor persisting at the end of radiotherapy is later sterilized, are needed.


   Footnotes
 
MN is currently affiliated with the Department of Gynecology, Kasumigaura National Hospital, Tsuchiura City, Japan.

PII S0029-7844(02)02204-4

Received September 13, 2001. Received in revised form January 15, 2002. Accepted February 14, 2002.


   REFERENCES
TOP
ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
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8. Duk JM, Groenier KH, de Bruijin HWA, Hollema H, ten Hoor KA, van der Zee AGJ, et al. Pretreatment serum squamous cell carcinoma antigen: A newly identified prognostic factor in early-stage cervical carcinoma. J Clin Oncol 1996;14:111–8.[Abstract]

9. Hong JH, Tsai CS, Chang JT, Wang CC, Lai CH, Lee SP, et al. The prognostic significance of pre- and posttreatment SCC levels in patients with squamous cell carcinoma of the cervix treated by radiotherapy. Int J Radiat Oncol Biol Phys 1998;41:823–30.[Medline]

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11. Rose PG, Baker S, Founier L, Nelson BE, Hunter RE. Serum squamous cell carcinoma antigen levels in invasive cervical cancer: Prediction of response and recurrence. Am J Obstet Gynecol 1993;168:942–6.[Medline]

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13. Flueckiger F, Ebner F, Poschauko H, Tamussino K, Einspieler R, Ranner G. Cervical cancer: Serial MR imaging before and after primary radiation: A 2-year follow-up study. Radiology 1992;184:89–93.[Abstract/Free Full Text]

14. Hatano K, Sekiya Y, Araki H, Sakai M, Togawa T, Narita Y, et al. Evaluation of the therapeutic effect of radiotherapy on cervical cancer using magnetic resonance imaging.Int J Radiat Oncol Biol Phys 1999;45:639–44.[Medline]





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