Surgical and pathological outcomes of abdominal radical trachelectomy versus hysterectomy for early-stage cervical cancer.

ORIGINAL STUDY

Surgical and Pathological Outcomes of Abdominal Radical Trachelectomy Versus Hysterectomy for Early-Stage Cervical Cancer Dandan Zhang, MD,*þ Jin Li, MD,*þ Huijuan Ge, MD,Þþ Xingzhu Ju, MD,*þ Xiaojun Chen, MD,*þ Jia Tang, MD,*þ and Xiaohua Wu, MD, PhD*þ

Objectives: The aim of this study was to compare the surgical and pathological outcomes for patients with early-stage cervical cancer after abdominal radical trachelectomy (ART) and abdominal radical hysterectomy (ARH). Methods: A prospective database of ART and ARH procedures performed in a standardized manner by the same surgical group was analyzed. The 3-segment technique was used for the accurate analysis of parametrial lymph nodes (PMLNs), and parametrial measurements were recorded by the same pathologist. Standard statistical tests were used. Result: Between August 2012 and August 2013, ART was attempted in 39 patients (28.6%), and ARH was attempted in 90 patients (71.4%). The parametrium resection length was similar with ART and ARH (44.60 vs 45.48 mm, P = 0.432), as were additional surgical and pathological outcomes, including histology, lymph node positive rate, and operation time. The PMLNs were found in 28 patients (77.78%) in the ART group and in 86 (95.56%) in the ARH group (P 9 0.05). Solitary PMLN metastases were observed in 3 patients (10.71%) in the ART group and in 6 (6.98%) in the ARH group. Five (55.6%) of these 9 patients had tumors of 2 cm or greater. The ARH patients (36, 40.00%) were more likely to receive postoperative chemotherapy or radiation compared with ART patients (13, 33.33%; P = 0.017). At a median follow-up of 12 and 12.5 months (P = 0.063), respectively, there were no recurrences or deaths in the ART or ARH groups. Conclusions: Using standardized techniques, ART provides similar surgical and pathological outcomes as ARH. For the patients with tumors of 2 cm or greater, PMLNs should be examined carefully. Further prospective data are urgently needed. Key Words: Abdominal radical trachelectomy, Abdominal radical hysterectomy, Parametrium resection, Parametrial lymph nodes Received March 13, 2014, and in revised form April 18, 2014. Accepted for publication April 29, 2014. (Int J Gynecol Cancer 2014;24: 1312Y1318)

Departments of *Gynecologic Oncology and †Pathology, Shanghai Cancer Center, Fudan University, Shanghai, PR China; and ‡Department of Oncology, Shanghai Medical College, Fudan University, Shanghai, PR China. Address correspondence and reprint requests to Xiaohua Wu, MD, Department of Gynecologic Oncology, Cancer Hospital of Fudan University, 270 Dong-an Rd, Shanghai 200032, PR China. E-mail: [email protected]. The authors declare no conflicts of interest. Copyright * 2014 by IGCS and ESGO ISSN: 1048-891X DOI: 10.1097/IGC.0000000000000185

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cancer is the second most common cancer in C ervical women in developing countries. More than 500,000 new 1

invasive cervical cancer cases are estimated to be diagnosed worldwide every year. Cervical cancer affects women of all ages, including those in their childbearing years. Because of the widespread use of cervical carcinoma screening, many women will be diagnosed at a relatively young age and at an early stage.2 Women with cervical cancer who have delayed childbearing often have a strong desire for fertility-preserving surgery. Therefore, the strong demand for fertility-sparing surgery options for younger cervical carcinoma patients has posed new challenges in the management of this disease.

International Journal of Gynecological Cancer

& Volume 24, Number 7, September 2014

Copyright © 2014 by IGCS and ESGO. Unauthorized reproduction of this article is prohibited.



Abdominal radical hysterectomy (ARH) with bilateral pelvic lymphadenectomy is the traditionally recommended treatment of early cervical cancer. Patients must undergo removal of the uterus and cervix, radical resection of the parametrial tissue and the upper vagina, and a complete bilateral pelvic lymphadenectomy.3 Considering that cervical cancer rarely spreads superiorly to the uterus,4 abdominal radical trachelectomy (ART) is designed as one of the fertility-sparing procedures used in the treatment of early-stage cervical cancer.5 Vaginal radical trachelectomy (VRT) was first described by Daniel Dargent in 1994, and Smith et al published the first report of ART in 1997,6 after which, various investigators reported their experience.7Y10 The standard ARTproceduresaresimilartoARH,includingtheremovalofmost of the uterosacral and cardinal ligaments and upper vagina with complete resection of the uterine artery.11 However, considering thattheparametrialtissueisthesiteofdirectextensionorlymphatic spread, the significance of resection of the parametrial tissues has yet to be determined. The goal of this study was to compare the pathological and surgical outcomes of using ART or ARH in stage IB1 cervical cancer.

MATERIALS AND METHODS A prospectively maintained database of stage IB1 cervical cancer patients who were scheduled to undergo ART or ARH was analyzed. All of the procedures were performed in the Department of Gynecologic Oncology at Fudan University Shanghai Cancer Center from August 1, 2012, to August 31, 2013, by the same surgeon. Patients meeting the institutional eligibility criteria (18 years or older; FIGO International Federation of Gynecology and Obstetrics stage IB1 disease; tumor size of G4 cm; and no evidence of metastasis on preoperative pelvic magnetic resonance imaging, positron emission tomography, or computer tomography) were considered eligible to be included. Patients who had a strong desire to preserve fertility and no clinical evidence of impaired fertility underwent ART with bilateral pelvic lymphadenectomy. The remaining patients underwent conventional ARH without preservation of the uterus. This included

Outcomes of ART Versus ARH

patients who underwent ARH after finding metastatic lymph nodes or positive endocervical margin at the initial ART. Records were retrospectively reviewed for basic demographic information, cancer history, details of the surgery, and pathological findings. Patients who were treated with ART had to first undergo pelvic lymphadenectomy to ensure the absence of pelvic lymph node (PLN) metastasis by frozen sections.11 The cervical canal was then separated from the corpus uteri and opened through a longitudinal section at the 12-o’clock location. A frozen section was made 10 mm from the surgical margin to assure safety. If all of the tested frozen sections were benign and at least a 10-mm clear margin was obtained for the endocervical edge, the uterus was reconstructed to the upper vagina.12 If the frozen section of the surgical margin was involved with cancerous tissues, ARH was performed. After the ART or ARH surgery, the parametrial tissue from each specimen was spread over a cork mold and well extended. To reduce bias in the parametrial measurements and lymph node counts, the measurement was recorded from a single pathologist on the unfixed specimen’s gross parametriallengthandhistologiclengthinthefinalpathologicalreport. The uterosacral, vesicouterine, and vaginal lengths were also recorded (Fig. 1). These dimensions were recorded in millimeters. Moreover, the mean length from both parametria was reported. However, if the length of parametrium was not recorded, the data were excluded. Finally, all the samples were fixed in 10% of formaldehyde solution for 24 hours and embedded in paraffin. To count the parametrial lymph nodes (PMLNs), the lateral parametrium and uterosacral and vesicouterine ligaments were excised from the uterus before fixation. Starting from their insertion into the uterine body and cervix, the lateral parametria were divided visually into the proximal, middle, and distal segments, with 20 mm each for both the proximal and middle segments and the remaining portion as the distal segment (Fig. 2). The PMLNs were defined as lymph nodes distributed all over the parametrial tissue. Microscopic examination was used to document the presence of PMLN. The pathological diagnosis then involved PMLN

FIGURE 1. The length of ligament was fixed and measured. A, Ligaments in coronal plane for trachelectomy specimens. B, Ligaments in coronal plane for hysterectomy specimens. C, Ligaments in transverse section. * 2014 IGCS and ESGO


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FIGURE 2. Each side of the lateral parametrium was divided into 3 segments. counting in each area where serial cross-sections (3 Km) were made. Immunohistochemistry of the parametrium was not performed. Additional patient and clinicopathological characteristics were extracted from the electronic medical records, including the age, number of pregnancies, operative time, surgical blood loss, postoperative hospital stay, histology, FIGO stage, depth of stromal invasion (DSI), LVSI (Lymphovascular Space Invasion), parametrial involvement, PLN counting, lymph node metastasis, and adjuvant treatment. The maximal tumor diameter was measured clinically as the greater of the values from the digital examinations, and the maximum DSI was defined as the depth of invasion in the final surgical specimen. These measurements were then used to classify the DSI as superficial or deep. In instances where there was no gross residual tumor identified in the final surgical specimen, the DSI was determined from the preoperative cone biopsy. Patients with intermediate-risk and high-risk characteristics, as described by Sedlis et al,13 were counseled to undergo adjuvant therapy. Postoperative adjuvant treatment for patients who underwent ART were recommended based on the previously published protocol.12 Patients at risk for recurrence based on final pathology after ARH were recommended to undergo adjuvant radiation with concurrent platinum-based chemotherapy. All patients were followed up upon completion of surgery or adjuvant treatments. Median counts were analyzed using the Mann-Whitney U test. Dichotomous groupings were analyzed using the W2 and Fisher exact tests, as appropriate. Statistical significance was defined as P G 0.05. Statistical analyses were performed using SPSS (Statistical Product and Service Solutions) version 19.0.

RESULTS Between August 2012 and August 2013, a total of 36 patients underwent a laparotomy for a planned fertilitysparing ART and pelvic lymphadenectomy. Meanwhile, 90 radical hysterectomies were performed within the same period by the same surgeons at our institute. Two patients underwent immediate radical hysterectomy because of positive surgical margins or positive PLNs, which were identified from

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intraoperative frozen sections from ART patients. In the ART group, 25 patients (69.44%) were diagnosed with squamous cell carcinoma versus 64 (71.11%) in the ARH group and 8 (22.22%) versus 17 (18.89%) with adenocarcinoma in the respective groups (P = 0.258). Twenty of the patients (55.56%) in the radical trachelectomy group had tumor size of less than 2 cm compared with 30 (33.33%) in the radical hysterectomy group (P G 0.001). The radical trachelectomy group, as expected, was slightly younger than the radical hysterectomy group, with a median age of 32 years (range, 20Y41 years) compared with 50 years (range, 20Y71 years) (P G 0.001). Twenty-two ART patients (58.33%) had not already had children. The median OR operation time was 144 minutes (range, 95Y193 minutes) in the ART group versus 108 minutes (range, 78Y198 minutes) in the ARH group. This difference reflects the wait time for the analysis of numerous frozen sections that are commonly requested during ARTs. The median blood loss during ART was slightly more than during ARH (200 mL [range, 50Y350 mL] vs 150 mL [range, 50Y300 mL], respectively; P = 0.006). Only 1 ART patient received a 200-mL blood transfusion. There was no difference in the median length of the postoperative hospital stay between the 2 groups, which was 7 days (range, 13Y22 days) in the ART group compared with 8 days (range, 13Y29 days) in the ARH group. The operative and clinicopathological outcomes are listed in Table 1. The mean follow-up interval was similar in the ART and ARH groups (12 and 12.5 months, P = 0.063). Postoperative radiation or chemotherapy was given to 13 patients (36.11%) in the ART group and 47 (52.22%) in the ARH group (P = 0.026). Adjuvant chemotherapy was provided to all patients in the ART group except 1 woman who refused and was eventually administered radiation after ovarian transposition during reoperation. In the ART group, adjuvant therapy was prompted by DSI with and without LVSI in 3 patients and 1 patient, respectively; LVSI only in 3 patients; and positive lymph node(s) in 5 patients, including 3 with only positive parametrial nodes. Two adults were diagnosed with embryonal rhabdomyosarcoma and underwent adjuvant chemotherapy. In the ARH group, radiation with concurrent chemotherapy was administered for 36 patients (40.00%) for LVSI or/and DSI and for 10 patients (11.11%) with lymph node metastasis with or without DSI. In those patients with measured parametria, the median gross length in the ART group was 44.60 mm (Fig. 1A) compared with 45.48 mm in the ARH group (Fig. 1B) (P = 0.432). The median (SD) histologic length was 25.91 (4.61) mm in the ART group, compared with 26.26 (5.29) mm in the ARH group (P = 0.738). There was no difference in the medial vesicouterine ligament length (4.03 vs 4.03 mm, P = 0.996) or the medial uterosacral ligament length (13.55 vs 13.28 mm, P = 0.771) in the ART group versus the ARH group. The medial vaginal length for each position in the ART group was similar to that in the ARH group (P 9 0.05). Table 2 lists the pathological results of the trachelectomy and hysterectomy specimens with bilateral parametrial measurements performed by the same pathologists. Some patients (12/36, 33.33%) underwent conization in the ART group, which is the standard examination before fertility-sparing surgery, with * 2014 IGCS and ESGO





TABLE 1. Patient characteristics and surgical outcomes ART (n = 36), n (%)

ARH (n = 90) , n (%)

P

32 (20Y41) 1 (0Y2)

50 (20Y71) 1.5 (1Y3)

G0.001 G0.001 0.258

25 (69.44) 8 (22.22) 1 (2.78) 2 (5.56)

64 17 8 1

Median (range) age, years Median (range) nulliparous, n Histology Squamous cell carcinoma Adenocarcinoma Adenosquamous carcinoma other Tumor size, cm G2 92 and G4 Median (range) PLNs obtained Median (range) PMLNs obtained Median (range) operating time, minutes Median (range) estimated blood loss, mL Blood transfusion (n) Median (range) postoperation hospital stay, days Median (range) follow-up interval, months Postoperative radiation or chemoradiation (n)

(71.11) (18.89) (8.89) (1.11) G0.001

20 16 18 2 144 200

(55.56) (44.44) (7Y34) (0Y11) (95Y193) (50Y350) 1 7 (13Y22) 12 (8Y19) 13 (36.11)

the result of no grossly visible lesions. Despite this finding, the surgeon also decided to do a radical excision as normal in the ART patients without gross tumors. The median PLN count from 36 ART patients was 18 (range, 7Y34), which was less than that in the ARH group (24; range, 5Y54) specimens from a total of 90 patients (P G 0.001). The time restrictions of the frozen section analysis during the procedure led to limitations in PLN selection. The median PMLN count was 2 (range, 0Y11) versus 2 (range, 0Y17) in the ART and ARH groups, respectively (P = 0.18), and the mean (SD) maximal diameters were 2.54 (1.80) mm versus 3.53 (2.83) mm (P = 0.190) (Table 3).

30 60 24 2 108 150

(33.33) (66.67) (8Y54) (0Y17) (78Y198) (50Y300) 0 8 (13Y29) 12.5 (8Y20) 47 (52.22)

0.013 0.180 G0.001 0.006 0.670 0.063 0.026

Twenty-eight (28/36) of the parametrial specimens (77.78%) from the ART group included 86 parametrial nodes, whereas 86 (86/90) of the ARH specimens (95.56%) had 305 PMLNs detected. In the ART group, 13 patients (46.42%) elected PMLN in the bilateral parametria, and another 15 patients (53.57%) had unilateral PMLN. In the 86 patients who had PMLNs in the ARH group, 53 (61.63%) possessed bilateral parametrial nodes, and 33 (38.37%) had PMLN on a single side. Most of the PMLNs were localized to the proximal segment in both the ART and ARH groups (63/86 [73.26%] and 212/301 [69.51%]). Furthermore, in the ART group, 5 patients possessed positive lymph nodes in total. For

TABLE 2. Pathologic results of the trachelectomy and hysterectomy specimens with bilateral parametrial measurements by the pathologists ART, Mean (SD), mm Medial gross length Left Right Medial histologic length Medial vesicouterine ligaments length Medial uterosacral ligaments length Medial vaginal length 12 o’clock 3 o’clock 9 o’clock 6 o’clock

ARH, Mean (SD), mm

P

44.60 49.45 46.42 25.91 4.03 13.55

(17.09) (17.72) (23.11) (4.61) (4.27) (4.86)

45.48 (21.23) 42.87 (16.62) 45.14 (20.64) 26.26 (5.29) 4.03 (1.86) 13.28 (4.57)

0.432 0.057 0.767 0.738 0.996 0.771

17.55 22.21 22.18 24.52

(6.49) (5.34) (4.41) (6.50)

17.35 (5.94) 21.34 (4.70) 22.44 (5.09) 25.02 (6.44)

0.877 0.382 0.796 0.700

* 2014 IGCS and ESGO


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TABLE 3. Pathologic results of the trachelectomy and hysterectomy median lymph node count ART (n), Median (Range) Total lymph node PLN Left Right Common lilac lymph node Left Right PMLN Total Left Right Uterosacral Vesicouterine Size, mean (SD), mm Inner region, n (%) Medial region, n (%) Lateral region, n (%)

P

18 (7Y34)

24 (8Y54)

0.013

6 (2Y12) 5 (1Y13)

7 (2Y20) 8 (1Y17)

0.007 0.001

3 (1Y9) 3 (1Y10)

3 (1Y15) 3 (1Y12)

0.941 0.633

1 (0Y11) 1 (0Y4) 1 (0Y5) 0 (0Y2) 0 (0Y1) 2.54 (1.80) 63/86 (73.26) 16/86 (18.60) 6/86 (6.98)

2 (0Y17) 1 (0Y6) 1 (0Y6) 0 (0Y3) 0 (0Y2) 3.53 (2.83) 212/301 (69.51) 58/301 (19.27) 31/301 (10.30)

0.180 0.079 0.131 0.847 0.969 0.190

3 patients, the parametrial node was the only positive node, and the other 2 patients had positive PLNs defined in the final pathology. In the 12 lymph node-positive patients, 6 patients were merely parametrial positive, and the others manifested involvement of both the parametrial and PLNs. None of the patients with PLN involvement escaped PMLN invasion. Furthermore, all of the metastatic lymph nodes observed were found in the proximal segment.

DISCUSSION The management of early-stage cervical carcinoma in young women who desire future fertility remains a challenge to gynecological oncologists. Radical trachelectomy is increasingly being offered as a fertility-sparing alternative in selected women with stage IB1 cervical carcinoma. There has not been a trial to compare fertility-sparing ART with ARH in the pathological parameters of stage IB1 cervical cancer. In this study, we attempted to determine the safety of ART from the perspective of comparison of pathologic specimen with that of ARH. The strength of this study is that, to our knowledge, it represents the first comparison of the pathologist’s measurements of the specimens from ART and ARH. Moreover, both procedures were performed at the same institution, by the same surgeons, and with the same pathologist. In the ART and ARH groups, the similar size of the measurable specimens demonstrates no difference in the surgical removal of the parametrial tissue. Extending the resection of the parametria in radical hysterectomies and trachelectomies has been discussed intensively during the past 15 years. During the past decade, few investigators have reported histopathological information on the extent of parametrectomy in radical hysterectomy series. Einstein et al14 have compared the surgical

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ARH (n), Median (Range)

and pathological outcomes between the VRT and ART approaches for stage IB1 cervical cancer. In that series, the median measured parametrial length in the VRT group was less than that in the ART group (1.45 vs 3.97 cm, P G 0.0001), and parametrial nodes were detected in 8 of the ART specimens (57.3%) in contrast to no patients in the VRT group (P = 0.0002). The authors thought that parametrial removal in early cervical cancer remains important for several reasons, which are as follows: (1) to eliminate parametrial spread and indicate further therapy, (2) to prevent local recurrence, and (3) to obtain a clear margin on the cervical primary.14 The larger parametrial specimen yielded by the ART could have important clinical implications. Lintner et al15 followed up 45 patients with stage I cervical cancer measuring more than 2 cm in diameter, and the 5-year survival rate (93.5%) was equal to (or better than) the rates reported for patients treated by radical hysterectomy. Their survival data seem to support the hypothesis that ART is a safe treatment option for patients with invasive cervical cancer lesions of more than 2 cm. In addition, there were significantly more patients (55.56%) with tumor size of less than 2 cm in the radical trachelectomy group compared with that in the radical hysterectomy group (33.33%). Existing research demonstrates that a larger tumor size in cervical cancer is associated with parametrial involvement.16,17 Sufficient parametrial tissue was resected on our patients in this study, which confirmed that ART is equivalent to that of ARH. In this study, 13 ART patients (36.11%) received postoperative adjuvant therapy, which was less than the proportion of ARH cases (47 cases, 52.22%). There were no cases of recurrence during the follow-up period. In general, the significance of tumor size to the selection of patients eligible for fertility-sparing surgery remains a controversial issue. Plante et al18 demonstrated that * 2014 IGCS and ESGO




the risk for recurrence was significantly increased for lesions greater than 2 cm in VRT. Mathevet and colleagues19 reported the same observation. The 2013 NCCN (National Comprehensive Cancer Network) cervical cancer guidelines separated the treatment of stage I cervical cancer, but the approach is most validated in lesions less than 2 cm. Recently, Li et al12 reported that, of 55 patients who underwent ART with exophytic tumor size between 2 and 4 cm, 20 of these (36.4%) underwent adjuvant chemotherapy after ART because of unfavorable pathological findings. The rate of adjuvant therapy exceeds the previously reported rate of 9% to 32%.7,20 This difference may be correlated with wider parametrial resection, which was 5.4 cm on average.12 No evidence of recurrent disease during a follow-up period of 22.8 months was recorded. The ART has expanded the scope of fertilitysparing surgery to larger tumors. Lymph nodes can be found in the parametrial tissues; most are in the cardinal ligament and, less frequently, in the vesicouterine and uterosacral ligaments. In the study of Burghardt and Pickel,21 PLMNs were detected in greater than 90% of the patients and were detected in all the ligaments examined, including the lateral parametrium (52%) and the uterosacral ligament (9%), and the median number of removed PMLNs was 5 (range, 1Y25 lymph nodes). In our study, the 3-segment technique was used for the accurate analysis of PMLN. The PMLNs were detected in 28 (77.78%) of the 36 and 86 (95.56%) of the 90 patients in the ART and ARH groups, respectively, which is slightly lower than previously reported. Given that a median of 1 to 3 lymph nodes was found, the presence and number of PMLNs may be clinically useful, similar to reports concerning PLNs. The increased PLMN counting in ARH indicates that the PLMNs are not only located concomitantly with the uterine artery but are also evenly distributed in the parametrium tissue. When preserving the uterus, a portion of the broad ligament is spared from resection; it is possible that the findings of this study are reflective of lesser area removed in ART compared with ARH. Pathological parametrial involvement in early cervical cancer is uncommon; the incidence is only 6% to 31% in stage IB1 cervical carcinoma according to a series of reports.22,23 In our study, 3 patients undergoing ART had PMLN metastases only, indicating that the parametrium is the first site of extracervical involvement. These findings are consistent with those of Twombly,24 who reported that the lymph from the cervix is drained by 3 main trunks, with the lateral trunk serving as the main lymphatic drainage running through the lateral parametrium. As previously described by Girardi et al,25 we show that there are many lymph nodes in the middle and distal segments of the lateral parametrium and in the proximal, which can be potential metastatic sites. For all of the patients who were only PMLN positive, 5 (5/9, 55.6%) had tumors of 2 cm or greater, including 1 (1/3, 33.3%) from the ART group and 4 (4/6, 66.7%) from the ARH group. Metastases to the parametrial nodes are of adverse prognostic significance.25 The draining nodes located in the proximal parametrium may have escaped histologic detection, and those in the distal parametrium are not always removed during radical total hysterectomy.26 The ART as a fertility-preserving


operation for larger tumors should provide a wider excision of the parametrium for the removal of local lymph metastasis and dictate the necessity of postoperation adjuvant therapy, reducing the possibility of local recurrence. Stegeman et al27 have reported parametrial tumor involvement in 2 (1.94%) of 103 patients. The same group performed a meta-analysis of 696 patients, which showed a prevalence of parametrial tumor involvement of 0.63% in patients with tumors of 2 cm in diameter or less. Similar rates of 0.4% and 0.6%, respectively, have been reported by Wright et al23 and Covens et al.16 Solitary PMLN metastases were detected in 8.3% (3/36) of patients in the ART group, which is higher than previously reported. This higher number may be a result of the 3-segment technique, which involved inspection of all the parametrial tissues separated from the cervix and/or uteri. The solitary positive PMLN should be considered the sentinel node because it is the first lymph node reached by metastasizing cancer cells from the tumor. Positive parametrial nodes are distributed throughout the entire parametrium, and the frequency of positive nodes is linearly associated with tumor volume.25,28 The high proportion of parametrial involvement in the ARH group might be explained by the tumor size, which was larger than 2 cm in most of the patients (60/90, 66.67%). The patients with solitary positive parametrial nodes were evenly distributed in FIGO stage IB1 disease, which confirms that the parametrium is a major route for lymphatic spread. Therefore, the extent of parametrial resection is indispensable and should be carried out as a type III radical hysterectomy along the pelvic sidewall in the ART procedure, especially in cases involving larger tumors. For clinical practice, our study demonstrates that sentinel node identification should begin with PMLN using the 3-segment technique, which could be applied in frozen sections in the future. Attention should be paid to the possibility of positive PLMN without pelvic node metastasis. Parametrial sentinel nodes are difficult to detect on lymphoscintigraphy or blue dying because they are situated close to the point of tracer administration, and the afferent lymphatic channels are too short to distinguish colors in the vicinity of the cervix.

CONCLUSIONS We conclude that the data indicate that ART is appropriate for patients with early cervical cancer. Solitary PMLN metastasis is a high-risk factor for local recurrence, which has not been recognized before, and can provide evidence for postoperative therapy, especially for patients with tumors of 2 cm or greater. Our study further highlights the need for prospective studies to determine the role of ART in patients with stage IB1 (2Y4 cm) cervical carcinoma.

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16. Covens A, Rosen B, Murphy J, et al. How important is removal of the parametrium at surgery for carcinoma of the cervix? Gynecol Oncol. 2002;84:145Y149. 17. Gemer O, Eitan R, Gdalevich M, et al. Can parametrectomy be avoided in early cervical cancer? An algorithm for the identification of patients at low risk for parametrial involvement. Eur J Surg Oncol. 2013 Jan;39(1):76Y80. 18. Plante M, Renaud M-C, Franc¸ois H, et al. Vaginal radical trachelectomy: an oncologically safe fertility-preserving surgery. An updated series of 72 cases and review of the literature. Gynecol Oncol. 2004;94:614Y623. 19. Mathevet P, Laszlo de Kaszon E, Dargent D. Fertility preservation in early cervical cancer. Gynecol Obstet Fertil. 2003;31:706Y712. 20. Abu-Rustum NR, Neubauer N, Sonoda Y, et al. Surgical and pathologic outcomes of fertility-sparing radical abdominal trachelectomy for FIGO stage IB1 cervical cancer. Gynecol Oncol. 2008;111:261Y264. 21. Burghardt E, Pickel H. Local spread and lymph node involvement in cervical cancer. Obstet Gynecol. 1978;52:138Y145. 22. Kinney WK, Hodge DO, Egorshin EV, et al. Identification of a low-risk subset of patients with stage IB invasive squamous cancer of the cervix possibly suited to less radical surgical treatment. Gynecol Oncol. 1995;57:3Y6. 23. Wright JD, Grigsby PW, Brooks R, et al. Utility of parametrectomy for early stage cervical cancer treated with radical hysterectomy. Cancer. 2007;110:1281Y1286. 24. Twombly GH. The lymphatics of the female genital organs. Ann Surg. 1965;162:1045. 25. Girardi F, Lichtenegger W, Tamussino K, et al. The importance of parametrial lymph nodes in the treatment of cervical cancer. Gynecol Oncol. 1989;34:206Y211. 26. Landoni F, Maneo A, Cormio G, et al. Class II versus class III radical hysterectomy in stage IB-IIA cervical cancer: a prospective randomized study. Gynecol Oncol. 2001;80:3Y12. 27. Stegeman M, Louwen M, van der Velden J, et al. The incidence of parametrial tumor involvement in select patients with early cervix cancer is too low to justify parametrectomy. Gynecol Oncol. 2007;105:475Y480. 28. Winter R, Haas J, Reich O, et al. Parametrial spread of cervical cancer in patients with negative pelvic lymph nodes. Gynecol Oncol. 2002;84:252Y257.



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Nerve-sparing radical abdominal trachelectomy versus nerve-sparing radical hysterectomy in early-stage (FIGO IA2-IB) cervical cancer: a comparative study on feasibility and outcome.

Surgical outcomes of robotic radical hysterectomy using three robotic arms versus conventional multiport laparoscopy in patients with cervical cancer.

Early stage cervical cancer: aborted versus completed radical hysterectomy.

Radical trachelectomy for early stage cervical cancer: the Queensland experience.

Radical hysterectomy with adjuvant radiotherapy versus radical radiotherapy for FIGO stage IIB cervical cancer.

Reproductive outcomes after laparoscopic radical trachelectomy for early-stage cervical cancer.

Abdominal scar characteristics as a predictor of cervical stenosis after abdominal radical trachelectomy.

MRI findings before and after abdominal radical trachelectomy (ART) for cervical cancer: a prospective study and review of the literature.

Vaginal-assisted laparoscopic radical hysterectomy (VALRH) versus laparoscopic-assisted radical vaginal hysterectomy (LARVH) in the treatment of cervical cancer: surgical results and oncologic outcome.

Adjuvant chemotherapy versus concurrent chemoradiotherapy for high-risk cervical cancer after radical hysterectomy and systematic lymphadenectomy.

Abdominal radical trachelectomy: a Romanian series.

Widespread recurrence 7 years after radical abdominal trachelectomy for early cervical adenocarcinoma.

Radical Abdominal Trachelectomy for IB1 Cervical Cancer at 17 Weeks of Gestation: A Case Report and Literature Review.

Clinical observation of laparoscopic radical hysterectomy for cervical cancer.

Classical radical hysterectomy and nerve-sparing radical hysterectomy in the treatment of cervical cancer.

Impact of diabetes mellitus on oncological outcomes after radical hysterectomy for early stage cervical cancer.

Oncological outcomes of nerve-sparing radical hysterectomy for cervical cancer: a systematic review.

Menstrual pattern after abdominal radical trachelectomy.

A new method of surgical margin assuring for abdominal radical trachelectomy in frozen section.

[Is radical hysterectomy necessary in surgical procedure for early stage cervical cancer?].

Role of cervical cytology in surveillance after radical trachelectomy for cervical cancer.

Bladder function after radical hysterectomy for cervical cancer.

Laparoendoscopic single-site radical hysterectomy for early stage cervical cancer.