Indian J Med Res 154, August 2021, pp 284-292 Quick Response Code:

DOI: 10.4103/ijmr.IJMR_4240_20

Review Article

Surgery for cervical cancer: consensus & controversies

Pabashi Poddar & Amita Maheshwari

Division of Gynecologic Oncology, Tata Memorial Centre, Homi Bhabha National Institute, Mumbai,
Maharashtra, India

Received October 15, 2020

Surgery plays an important role in the management of early-stage cervical cancer. Type III radical
hysterectomy with bilateral pelvic lymph node dissection using open route is the standard surgical
procedure. There is level I evidence against the use of laparoscopic/robotic approach for radical
hysterectomy for cervical cancer. Emerging data support the use of sentinel lymph node biopsy and
nerve sparing radical hysterectomy in carefully selected patients with early-stage disease. In locally
advanced cervical cancer patients, the use of neoadjuvant chemotherapy (NACT) followed by radical
surgery yields inferior disease-free survival compared to definitive concurrent chemoradiation therapy.
Therefore, definitive concurrent chemoradiation is the standard treatment for locally advanced disease.
Fertility preserving surgery is feasible in highly selected young patients. Role of less-radical surgical
procedures in patients’ with low-stage disease with good prognostic factors is under evaluation.

Key words E
 arly-stage cervical cancer - fertility preservation - minimal invasive surgery - neoadjuvant chemotherapy - ovarian
preservation - radical surgery

Cervical cancer continues to be a major health short and long-term complications2. In order to reduce
challenge globally. Although there has been a gradual surgery-related complications without compromising
decline in the incidence of cervical cancer in India, it disease-free and overall survivals (OS), a variety of
still ranks the second most common cancer amongst modifications in the standard surgical approach have
Indian women1. Due to lack of organized screening been tried. A critical evaluation of important nuances
programmes in the country, majority of patients with in cervical cancer surgery is presented in this review.
cervical cancer present with advanced disease and
Role of minimal invasive surgery in cervical cancer
are treated with radical radiotherapy with or without
concurrent chemotherapy. For patients presenting Until recently, minimally invasive surgery
with early-stage disease, radical surgery is the (MIS), both laparoscopic and robotic approaches,
preferred treatment. Conventionally, type III open has been widely used by gynaecologic oncologists
radical hysterectomy with bilateral pelvic lymph node for cervical cancer surgery and was referred by many
dissection has been the standard surgical procedure for international scientific bodies as the standard of care3.
operable cervical cancer. This surgical approach leads to However, these recommendations were based on small
an excellent survival, but at the cost of treatment related observational studies and their meta-analyses showed

© 2022 Indian Journal of Medical Research, published by Wolters Kluwer - Medknow for Director-General, Indian Council of Medical Research
284
 PODDAR & MAHESHWARI: CERVICAL CANCER SURGERY 285

less intra-operative blood loss, fewer post-operative The LACC trial also refuted previously held
complications and faster recovery with equivalent belief that MIS approach was associated with fewer
survivals using MIS compared with open surgery in perioperative complications and better quality of life
patients with early cervical cancer4-6. In 2015, Wang et al4 compared with open route in patients undergoing radical
presented a systematic review of 12 non-randomized hysterectomy8,9. There was no significant difference in
studies comparing laparoscopic radical hysterectomy rates of intra-operative complications, serious adverse
(754 patients) with open radical hysterectomy (785 events or long-term morbidities between the two
patients) and found no significant difference in the arms8. In addition, no differences in mean FACT-Cx
five-year OS between the two approaches. Cao et al5 in (Functional Assessment of Cancer Therapy – Cervix)
a meta-analysis of 22 studies involving 2292 patients total scores were identified between the MIS and open
concluded that laparoscopic approach was safe and groups at six weeks or three months after surgery9.
had lower operative complications than open route. In Along with LACC trial, a cohort study was
a multicentre, retrospective study, Sert et al6 compared conducted on National Cancer Database which
robot-assisted radical hysterectomy with historical included 2461 women who had undergone either
cohort of patients who underwent open surgery and a MIS or open radical hysterectomy for Stage IA2
found no significant differences in survival between to IB1 cervical cancer from 2010 to 201310. Results
the two groups and better perioperative outcomes with of this retrospective study revealed that, at a median
robotic surgery. follow up of 45 months, the four-year mortality was
In 2018, results of Laparoscopic Approach to significantly higher in women who underwent surgery
Cervical Cancer (LACC) trial were reported7. The using minimally invasive route compared to those who
LACC was the first phase III randomized control trial underwent open surgery; 9.1 per cent among women
(RCT) that compared minimally invasive (laparoscopic who underwent MIS and 5.3 per cent among those
or robotic) radical hysterectomy with open radical who underwent open surgery (HR, 1.65; 95% CI, 1.22
hysterectomy in women with early-stage cervical to 2.22; P=0.002). The widespread use of minimally
cancer. The study was designed to test non-inferiority invasive route for cervical cancer surgery in the United
of MIS compared with open route, and the primary end States coincided with a 0.8 per cent (95% CI, 0.3-1.4)
point was disease-free survival (DFS) at 4.5 yr. The per year decline in the four-year relative survival rate
quality standard of surgery was evaluated by an expert after 200610.
committee before a surgeon was allowed to participate Since the publication of LACC trial, many
in the trial. In the MIS group, majority of women were observational studies comparing survival outcomes
treated by conventional laparoscopy (84%), whereas of MIS and open radical hysterectomy have been
16 per cent women underwent robot-assisted surgery. conducted by researchers. A recently published
The original sample size was 740 patients. However, systematic review and meta-analysis of 15 such
the trial was stopped prematurely by data and safety studies involving 9499 patients that compared survival
monitoring committee (DSMC) in November 2017 outcomes after MIS (laparoscopic or robot-assisted)
after an interim analysis revealed a significantly lower and open radical hysterectomy in patients with early-
DFS and OS in MIS group. At the time of termination, stage cervical cancer concluded that MIS radical
631 (85%) patients were enrolled into the study. The hysterectomy was associated with an increased risk of
rate of DFS at 4.5 yr was significantly inferior with recurrence and death compared with open surgery11.
MIS compared with open route; 86.0 per cent versus The pooled hazard of recurrence or death was 71 per
96.5 per cent [hazard ratio (HR), 3.74; 95% confidence cent higher (HR, 1.71; 95% CI, 1.36-2.15; P<0.001)
interval (CI), 1.63-8.58]. The study also showed a and the hazard of death was 56 per cent higher
worse OS with MIS compared to open surgery; three- (HR, 1.56; 95% CI, 1.16-2.11; P=0.004) with MIS
year OS 93.8 per cent versus 99.0 per cent (HR, compared with open surgery11. In contrast a large,
6.00; 95% CI, 1.77-20.30), respectively. MIS radical retrospective, multi-institutional study from Germany
hysterectomy was associated with higher rates of by Köhler et al12 revealed overall and recurrence-free
all-cause mortality (HR, 6.00; 95% CI, 1.77-20.3), survivals with vaginally assisted laparoscopic radical
disease-specific mortality (HR, 6.56; 95% CI, 1.48- hysterectomy that were comparable to the open surgery
29.0), and loco-regional recurrence (HR, 4.26; 95% CI, arm of the LACC trial. However, patients included in
1.44-12.6) compared to open surgery7. this study had more favourable features (i.e., smaller
286 INDIAN J MED RES, AUGUST 2021

tumours, less frequent lymph node involvement and PLND without compromising the detection of lymph
less need for adjuvant therapy) compared to LACC node metastasis, sentinel lymph node biopsy (SLNB)
trial population. Therefore, comparison of this study has been extensively studied in patients with early
with LACC trial is not appropriate. cervical cancer with encouraging results. SLNB may
serve as a relatively simple and effective method to
In view of level I evidence against the use of MIS in
know lymph node status in these patients. Sentinel
cervical cancer, many international guidelines including
lymph node technique may also increase identification
National Comprehensive Cancer Network (NCCN) and
of nodal metastasis due to the detection of lymph nodes
European Society of Gynecologic Oncology (ESGO)
at unusual locations and by identification of micro-
revised their previous recommendations and now state
metastases and isolated tumour cells19,20.
that the standard approach for radical hysterectomy is
open abdominal surgery13,14. In September 2019, the The AGO Study Group conducted a large,
Society for Gynecologic Oncology (SGO) released prospective, multicentre study across Germany and
an update declaring ‘the preponderance of the Austria on SLN detection using either radio-labelled
contemporary published literature suggests poorer technetium, patent blue or both21. They found SLN
survival outcomes for women undergoing radical detection rate of 88.6 per cent and the overall sensitivity
hysterectomy for cervical cancer with minimally of 77.4 per cent. Although the overall sensitivity of
invasive compared with open radical hysterectomy’15. SLNB was low, but it was higher in tumours ≤20 mm
(90.9%), with bilateral detection (87.2%), or when the
Many hypotheses have been postulated to explain
combination of technetium and patent blue was used.
poor survival with MIS in cervical cancer. These
Salvo et al19 conducted a retrospective analysis of 188
include the use of intrauterine manipulator, CO2 gas
patients with early cervical cancer who underwent
for pneumo-insufflation and intracorporeal colpotomy,
SLN mapping using blue dye, technetium-99m sulphur
leading to tumour spillage in the peritoneal cavity
colloid (Tc-99), and/or indocyanine green (ICG)
during MIS12. An additional consideration may be
followed by complete pelvic lymphadenectomy and
the quality of surgery and extent of surgical resection
showed a sensitivity of 96.4 per cent and negative
in MIS compared with open radical hysterectomy.
predictive value (NPV) of 99.3 per cent. The false-
Currently, ongoing robot-assisted approach to cervical
negative rate was 3.6 per cent. In 2011, results of
cancer trial is expected to address some of these issues16.
SENTICOL study were published, wherein 139
However, until more data on oncological safety of MIS
cervical cancer patients with Stage IA1–IB1 tumours
are available, open route continues to be the standard
underwent SLN biopsy followed by complete pelvic
of care in patients with early cervical cancer.
lymphadenectomy20. The authors reported a high
Sentinel lymph node biopsy (SLNB) in cervical sensitivity of 92 per cent and a NPV of 98 per cent of
cancer SLNB technique.
Lymph node metastasis is the single most important Use of ICG dye in place of methylene blue has
prognostic factor in patients with clinically early-stage improved overall and bilateral sentinel lymph nodes
cervical cancer. Lymph node status is also crucial for detection rates22. SLNB has been included in the NCCN
planning adjuvant treatment. Therefore, pelvic lymph guidelines for stage IB1 disease (<2 cm tumour)23.
node dissection (PLND) is an essential component of Adherence to the SLN mapping algorithm is important.
radical surgery for cervical cancer. The incidence of A side-specific complete nodal dissection must be done
lymph node involvement in clinically early cervical in case of failure of SLN detection and all suspicious
cancer is estimated to be only 10-20 per cent17. Though or grossly enlarged nodes must be removed regardless
PLND helps to identify lymph node metastasis, the of SLN mapping. Adequate and quality pathological
procedure may be associated with intra- and post- evaluation along with ultra-staging of sentinel lymph
operative complications. PLND-related intra-operative node is a prerequisite for SLNB because any undetected
complications include neurovascular and ureteral metastasis may adversely affect patient’s prognosis.
injuries, increased blood loss and blood transfusion and
Neoadjuvant chemotherapy (NACT) prior to
increased surgical time. In the post-operative period,
surgery
there is potential risk of infection, venous thrombo-
embolism, lymphoedema and lymphocyst formation18. Theoretically neoadjuvant chemotherapy (NACT)
In order to reduce complications associated with prior to surgery in locally advanced cervical cancer has
 PODDAR & MAHESHWARI: CERVICAL CANCER SURGERY 287

the potential to improve local control by increasing to cardinal, uterosacral and vesicouterine ligaments,
operability rates and offer a better systemic control by pelvic autonomic nerves are at risk of injury during
taking care of micro-metastasis. Earlier studies showed a conventional radical surgery for cervical cancer.
improvement in DFS and OS with NACT-surgery Damage may occur to the hypogastric nerve
compared to radiation alone in patients with locally (sympathetic nerve), the pelvic splanchnic nerve
advanced cervical cancer24,25. However, these studies (parasympa­thetic nerve), and the vesical branch of the
were conducted in pre-concurrent chemoradiation era pelvic plexus (both sympathetic and parasympathetic
and therefore their control arm was sub-optimal as per nerves) at various steps in a radical hysterectomy.
the current standard. The results of two well conducted The concept of nerve-sparing hysterectomy was
RCTs that compared NACT-surgery with concurrent described and popularized by Japanese gynaecologists
chemoradiation have been reported. The Indian study who took great efforts to modify the classical radical
was a single-centre, phase III, randomized trial which hysterectomy so as to preserve pelvic autonomic
recruited 633 patients with squamous cervical cancer nerves while maintaining the oncological outcome
(SCC) in stages IB2, IIA and IIB (FIGO 2009). Patients (the so-called Tokyo method)29. Data from various
were randomized between three cycles of NACT observational studies have demonstrated that NSRH
(paclitaxel + carboplatin; three weekly) followed minimizes surgery-related pelvic dysfunction, with
by radical hysterectomy (experimental arm) versus similar oncological outcomes as conventional radical
standard concurrent chemoradiation (control arm)26. hysterectomy. A meta-analysis by Lee et al30 including
The study revealed a poorer DFS in NACT-surgery 1796 patients from 23 studies revealed a lower
group compared with chemoradiation group; five-year incidence of urinary, colorectal, sexual dysfunction
DFS 69.3 per cent versus 76.7 per cent (HR, 1.38; and similar DFS and OS with NSRH compared with
95% CI, 1.02-1.87; P=0.038). The overall survival conventional radical hysterectomy. A retrospective
was similar between the two arms; five-year OS 75.4 cohort study on 406 patients from China demonstrated
and 74.7 per cent, respectively. In NACT arm, radical that NSRH for cervical cancer patients had better urinary
surgery was feasible in 72.15 per cent of patients and outcomes than conventional radical hysterectomy
32.2 per cent of patients required adjuvant treatment without compromising survival31. Although NSRH has
(radiation or chemoradiation) after surgery. Therefore, a shown a positive impact on the quality of life of the
considerable fraction of patients in NACT-surgery arm patients, the technique has not been standardized and
required multimodality treatment. The study concluded oncological safety has not been proven in randomized
that chemoradiation was superior to NACT-surgery in studies32,33. Therefore, further studies are required to
locally advanced cervical cancers. The second trial by establish the role of NSRH.
EORTC group was a multicentre, multinational phase
III RCT which included 620 patients with stages IB2, Fertility sparing surgery
IIA and IIB (FIGO 2014) cervical cancer27. There was The standard surgery for cervical cancer leads to
no difference in OS (72 vs. 76%, P=0.332) between the permanent loss of fertility. The innovative concept
two arms. Results on the quality of life and long-term of radical trachelectomy for fertility preservation
toxicity are yet to be reported. A meta-analysis of the in a young patient with early-cervical cancer was
above studies also showed superiority of concurrent conceived and popularized by Dargent et al34 in the
chemoradiation over NACT-surgery for DFS and severe early 70s. Since then, the procedure has undergone
acute toxicity and no difference in OS in patients with several modifications. Dargent procedure involved the
locally advanced cervical cancer28. In view of level I resection of the cervix, the upper part of the vagina
evidence, NACT surgery cannot be recommended in and the medial part of the parametria through a vaginal
patients with locally advanced cervical cancer and approach while preserving the uterine corpus combined
concurrent chemoradiation remains the standard of with laparoscopic PLND. With the introduction of
care. abdominal trachelectomy using either MIS or an open
Nerve sparing radical hysterectomy (NSRH) route, the vaginal procedure has become less common.
Intra-operative injury to autonomic nerve during Both oncological and fertility outcomes should
a radical hysterectomy is the cause for postoperative be kept in mind while considering fertility sparing
pelvic dysfunction including bladder, sexual and treatment and a detailed pre-operative counselling must
colorectal dysfunctions. Due to their close proximity be done. The proper selection of patients for fertility-
288 INDIAN J MED RES, AUGUST 2021

sparing surgery is important. Pre-treatment fertility followed by fertility sparing surgery (CoNteSSa) and
potential, cervical tumour size and location, histological Neoadjuvant chemotherapy and conservative surgery
subtype, depth of stromal invasion, lymph vascular in cervical cancer to preserve fertility (NeoCon-F) are
space invasion (LVSI) and nodal status are important two combined prospective phase II studies evaluating
factors in deciding for fertility-sparing surgery35. the feasibility of NACT in such cases45. These studies
Aggressive histologic types such as neuroendocrine aim to examine the safety and efficacy of NACT and
carcinoma and clear cell carcinoma are not suitable fertility-preserving surgery by simple trachelectomy/
for fertility-sparing surgery36. The presence of lymph conization in women with node negative FIGO 2018
nodal metastasis is an absolute contraindication for stage IB2 cervical cancer.
trachelectomy. Intrauterine infection and premature rupture
Fertility-preserving surgical procedure can be of membranes are two most important antepartum
further tailored based on the disease stage. In women complications after radical trachelectomy. Obstetric
with stage 1A1 disease without LVSI, radical cone outcome is better with a less radical approach. A recent
with negative margins can be done as the risk of lymph meta-analysis by Nezhat et al46 found mean clinical
node metastasis is <1 per cent in these patients37. In pregnancy rate after vaginal radical trachelectomy at
women with FIGO stage IA2 or stage 1A1 with LVSI, 67.5 per cent and mean live birth rate at 67.9 per cent.
the risk of pelvic lymph node metastasis is around A low cancer recurrence rate at 3.2 per cent at a median
5-8 per cent38. Therefore, radical trachelectomy with follow up of 39.7 months was also noted.
PLND is recommended, although some centres also Ovarian preservation
utilize radical cone or simple trachelectomy along with
PLND. For women with stage 1B1 disease, radical The median age for cervical cancer is mid
trachelectomy (abdominal or vaginal) combined with 40s; therefore, preservation of ovarian function is
pelvic lymphadenectomy is the procedure of choice. an important quality of life consideration in these
Currently, three studies are ongoing to evaluate the role patients. The incidence of ovarian metastasis is low
of cone biopsy or simple trachelectomy compared to in early-stage cervical cancer and therefore, ovarian
radical trachelectomy in women undergoing fertility- preservation is safe in carefully selected patients. Risk
preserving surgeries39-41. factors for ovarian metastasis in early-stage cervical
cancer include histopathological subtype, LVSI45;
An abdominal radical trachelectomy (ART) age, FIGO stage, depth of stromal involvement47,48
allows a more extensive paracervical and paravaginal and parametrial invasion49. Ovarian preservation
dissection compared with vaginal approach. Einstein is controversial in adenocarcinoma due to a higher
et al42 showed a 50 per cent wider parametrial resection risk of ovarian metastasis compared with squamous
in ART compared with vaginal radical trachelectomy. carcinoma50. However, Cheng et al49 in a meta-analysis
However, ART is also associated with increased risk of of cervical adenocarcinoma did not find any significant
adhesions and increased frequency of ligation of uterine difference in survival with or without ovarian
artery which may potentially impair subsequent fertility. preservation. Striking a balance between oncological
A few cases of uterine necrosis, septic complications safety and benefits of ovarian preservation is crucial in
and higher rates of premature delivery have also been a young patient with early cervical cancer and must be
reported43. Stage 1B2 tumours (>2 cm) are associated discussed with the patient before treatment. Preserved
with a higher rate of lymph node metastasis and local ovaries may be left in situ or transposed outside pelvis
recurrence and conventionally not considered for in case adjuvant radiation is anticipated.
fertility-preserving surgery. NACT preceding fertility-
sparing surgery has been introduced as a treatment Less- or non-radical surgery
option to preserve fertility in cervical cancer patients Parametrectomy is responsible for the majority
with tumours more than 2 cm. However, only limited of complications related to radical hysterectomy for
data are available on oncological outcomes and safety cervical cancer. In patients with low-risk disease, i.e.,
of such procedures44. NACT reduces the tumour volume tumour size ≤2 cm, superficial stromal involvement,
and the risk of microscopic disease thus increases absence of LVSI and negative lymph nodes, the risk of
feasibility of fertility-sparing surgery. A combination parametrial involvement is <1 per cent49-52. Considering
of paclitaxel and cisplatin doublet is used commonly. the rarity of parametrial involvement in patients with
Cervical cancer treated with neoadjuvant chemotherapy low-risk cervical cancer, many researchers have
 PODDAR & MAHESHWARI: CERVICAL CANCER SURGERY 289

questioned the need for removal of parametrial tissue and sexual function and the incidence and severity of
and extensive dissection of adjacent vital structures in lymphoedema after non-radical surgery. The study
the pelvis and have proposed non-radical procedures includes women with stage IA2–IB1 disease and
such as a simple hysterectomy or conization. Landoni favourable pathologic characteristics (squamous cell
et al53 in a small prospective randomized trial of 125 carcinoma of any grade or grade 1-2 adenocarcinoma,
patients compared class I (extrafascial hysterectomy) tumour size ≤2 cm, stromal invasion <10 mm and no
to class III (radical hysterectomy) hysterectomy in LVSI)40. The MD Anderson Cancer Center, USA is
patients with stages IBI and IIA cervical cancer with ≤4 conducting a prospective, international, multicentre
cm tumour diameter. This study showed no significant cohort study ConCerv (NCT01048853) with the aim
difference in adjuvant treatment, recurrence and overall to assess the oncologic safety and feasibility of simple
survival rates between the two arms but a higher hysterectomy or cone biopsy for early-stage (IA2–IB1
surgical morbidity after Class III radical hysterectomy <2 cm) low-risk (negative LVSI, negative margins on
(84 vs. 45%). Reade et al54 analyzed 341 patients with cone specimen) cervical cancer41.
early-stage cervical cancer who were treated with
either simple hysterectomy or simple trachelectomy Until results of these ongoing studies become
and showed crude recurrence rate 6.3 per cent and available, non-radical surgery cannot be considered a
disease-related mortality rate 1.5 per cent, comparable standard procedure and should not be practiced outside
outcomes were achieved by radical procedures. a clinical trial setting.

These and other small studies raised the possibility Conclusion

that non-radical surgical procedures may be considered Surgery plays an important role in the management
in carefully selected low-risk cervical cancer patients. of early-stage cervical cancer. A careful selection of
The criteria for low-risk are not well defined but patients is the key to successful outcomes. Conventional
generally include stage IB 1 (tumour size ≤2 cm), type III open radical hysterectomy with bilateral pelvic
without deep stromal invasion, no LVSI and negative lymph node dissection continues to be the standard
pelvic lymph nodes51,52. A preoperative magnetic procedure. Recent evidence is compelling against
resonance imaging is useful to determine tumour size, the use of minimally invasive route and open route
depth of cervical stromal invasion and parametrial and is recommended for radical hysterectomy. There is
vaginal spread. emerging evidence in favour of SLNB, but each centre
Currently, one randomized trial (the SHAPE must standardize the procedure before implementing
trial: NCT01658930) and two prospective cohort it in routine practice. Fertility preservation is possible
studies (GOG278: NCT01649089 and ConCerv: in highly selected patients. Ovaries can be preserved
NCT01048853) are ongoing to assess oncologic in a young patient undergoing radical hysterectomy.
safety, treatment-related morbidity, quality of life and The role of less-radical surgery in patients with early-
cost-effectiveness of non-radical surgery for low-risk cervical cancer with good prognostic features is still
early-stage cervical cancer39-41. The SHAPE (simple investigational and must not be offered outside a trial.
hysterectomy and pelvic node dissection in early Financial support & sponsorship: None.
cervix cancer) trial is a phase III randomized trial
comparing simple hysterectomy and pelvic LND to Conflicts of Interest: None.
radical hysterectomy and pelvic LND (or cone biopsy
to radical trachelectomy) in women with stage IA2– References
IB1cervical cancer with favourable features (squamous
1. Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA,
or adenocarcinoma or adenosquamous histology, Jemal A. Global cancer statistics 2018: GLOBOCAN
tumour size ≤2 cm, stromal invasion <50 per cent estimates of incidence and mortality worldwide for 36 cancers
and negative lymph nodes on imaging39. The primary in 185 countries. CA Cancer J Clin 2018; 68 : 394-424.
end point of the study is pelvic relapse-free survival 2. Ware RA, van Nagell JR. Radical hysterectomy with pelvic
in two groups. Treatment-related morbidity, quality of lymphadenectomy: Indications, technique, and complications.
life and cost-effectiveness will also be evaluated. The Obstet Gynecol Int 2010; 2010 : 1-9.
GOG 278 is a prospective study evaluating the impact 3. Cibula D, Pötter R, Planchamp F, Avall-Lundqvist E,
of non-radical surgery (extrafascial hysterectomy or Fischerova D, Haie Meder C, et al. The European Society of
cervical conization and pelvic LND) on bladder, bowel Gynaecological Oncology/European Society for Radiotherapy
290 INDIAN J MED RES, AUGUST 2021

and Oncology/European Society of Pathology guidelines for on-the-surgical-approach-for-radical-hysterectomy-in-the-

the management of patients with cervical cancer. Int J Gynecol treatment-of-women-with-cervical-cancer/, accessed on
Cancer 2018; 28 : 641-55. August 10, 2021.
4. Wang YZ, Deng L, Xu HC, Zhang Y, Liang ZQ. Laparoscopy 16. Falconer H, Palsdottir K, Stalberg K, Dahm-Kähler P,
versus laparotomy for the management of early stage cervical Ottander U, Lundin ES, et al. Robot-assisted approach to
cancer. BMC Cancer 2015; 15 : 928. cervical cancer (RACC): An international multi-center,
5. Cao T, Feng Y, Huang Q, Wan T, Liu J. Prognostic and safety open-label randomized controlled trial. Int J Gynecol
roles in laparoscopic versus abdominal radical hysterectomy Cancer 2019; 29 : 1072-6.
in cervical cancer: A meta-analysis. J Laparoendosc Adv Surg 17. Zhou J, Ran J, He ZY, Quan S, Chen QH, Wu SG, et al.
Tech 2015; 25 : 990-8. Tailoring pelvic lymphadenectomy for patients with stage
6. Sert BM, Boggess JF, Ahmad S, Jackson AL, IA2, IB1, and IIA1 uterine cervical cancer. J Cancer 2015; 6 :
Stavitzski NM, Dahl AA, et al. Robot-assisted versus open 377-81.
radical hysterectomy: A multi-institutional experience for 18. Achouri A, Huchon C, Bats AS, Bensaid C, Nos C,
early-stage cervical cancer. Eur J Surg Oncol 2016; 42 : 513-22. Lécuru F. Complications of lymphadenectomy for gynecologic
7. Ramirez PT, Frumovitz M, Pareja R, Lopez A, Vieira M, cancer. Eur J Surg Oncol 2013; 39 : 81-6.
Ribeiro R, et al. Minimally Invasive versus Abdominal 19. Salvo G, Ramirez PT, Levenback CF, Munsell MF,
Radical Hysterectomy for Cervical Cancer. N Engl J Med Euscher ED, Soliman PT, et al. Sensitivity and negative
2018; 379 : 1895-904. predictive value for sentinel lymph node biopsy in women with
8. Obermair A, Asher R, Pareja R, Frumovitz M, Lopez A, early-stage cervical cancer. Gynecol Oncol 2017; 145 : 96-101.
Moretti-Marques R, et al. Incidence of adverse events in 20. Lécuru F, Mathevet P, Querleu D, Leblanc E, Morice P,
minimally invasive vs. open radical hysterectomy in early Daraï E, et al. Bilateral negative sentinel nodes accurately
cervical cancer: Results of a randomized controlled trial. Am predict absence of lymph node metastasis in early cervical
J Obstet Gynecol 2020; 222 : 249.e1-10. cancer: Results of the SENTICOL study. J Clin Oncol 2011;
9. Frumovitz M, Obermair A, Coleman RL, Pareja R, Lopez A, 29 : 1686-91.
Ribero R, et al. Quality of life in patients with cervical cancer 21. Altgassen C, Hertel H, Brandstädt A, Köhler C, Dürst M,
after open versus minimally invasive radical hysterectomy Schneider A. Multicenter validation study of the sentinel
(LACC): A secondary outcome of a multicentre, randomised, lymph node concept in cervical cancer: AGO study group.
open-label, phase 3, non-inferiority trial. Lancet Oncol 2020; J Clin Oncol 2008; 26 : 2943-51.
21 : 851-60. 22. Buda A, Bussi B, Di Martino G, Di Lorenzo P, Palazzi S,
10. Melamed A, Margul DJ, Chen L, Keating NL, Grassi T, et al. Sentinel lymph node mapping with near-
Del Carmen MG, Yang J, et al. Survival after minimally infrared fluorescent imaging using indocyanine green:
invasive radical hysterectomy for early-stage cervical cancer. A new tool for laparoscopic platform in patients with
N Engl J Med 2018; 379 : 1905-14. endometrial and cervical cancer. J Minim Invasive Gynecol
11. Nitecki R, Ramirez PT, Frumovitz M, Krause KJ, 2016; 23 : 265-9.
Tergas AI, Wright JD, et al. Survival after minimally invasive 23. Abu Rustum NR, Yashar M, Bradley K, Campos SM,
vs open radical hysterectomy for early-stage cervical cancer: Chon HS, Chu C. et al. NCCN guidelines insights: Cervical
A systematic review and meta-analysis. JAMA Oncol cancer, version 1.2020. J Natl Compr Canc Netw 2020; 18 :
2020; 6 : 1019-27. 660-6.
12. Köhler C, Hertel H, Herrmann J, Marnitz S, Mallmann P, 24. Wen H, Wu X, Li Z, Wang H, Zang R, Sun M, et al. A
Favero G, et al. Laparoscopic radical hysterectomy with prospective randomized controlled study on multiple
transvaginal closure of vaginal cuff-a multicenter analysis. Int neoadjuvant treatments for patients with stage IB2 to IIA
J Gynecol Cancer 2019; 29 : 845-50. cervical cancer. Int J Gynecol Cancer 2012; 22 : 296-302.
13. Pennington KP, Urban RR, Gray HJ. Revisiting minimally 25. Sardi JE, Giaroli A, Sananes C, Ferreira M, Soderini A,
invasive surgery in the management of early-stage cervical Bermudez A, et al. Long-term follow-up of the first randomized
cancer. J Natl Compr Cancer Netw 2019; 17 : 86-90. trial using neoadjuvant chemotherapy in stage Ib squamous
14. European Society of Gynaecological Oncology. Laparoscopic carcinoma of the cervix: The final results. Gynecol Oncol
radical hysterectomy: An ESGO statement Available 1997; 67 : 61-9.
from: https://www.esgo.org/explore/council/laparoscopic- 26. Gupta S, Maheshwari A, Parab P, Mahantshetty U,
radical-hysterectomy-an-esgo-statement/, accessed on Hawaldar R, Sastri S, et al. Neoadjuvant chemotherapy
August 10, 2021. followed by radical surgery versus concomitant chemotherapy
15. The Society of Gynaecologic Oncology. SGO member and radiotherapy in patients with stage IB2, IIA, or IIB
update: Emerging data on the surgical approach for radical squamous cervical cancer: A randomized controlled trial.
hysterectomy in the treatment of women with cervical J Clin Oncol 2018; 36 : 1548-55.
cancer. Available from: https://www.sgo.org/clinical- 27. Kenter G, Greggi S, Vergote I, Katsaros D, Kobierski J,
practice/guidelines/sgo -member- update-emerging-data- Massuger L, et al. Results from neoadjuvant
 PODDAR & MAHESHWARI: CERVICAL CANCER SURGERY 291

chemotherapy followed by surgery compared to http://clinicaltrials.gov/ct2/show/NCT01658930, accessed on

chemoradiation for stage Ib2-IIb cervical cancer, EORTC October10, 2020.
55994. J Clin Oncol 2019; 37 : 5503. 40. National Institute of Health, U.S. National Library of
28. Marchetti C, Fagotti A, Tombolini V, Scambia G, De Felice F. Medicine. Studying the physical function and quality of life
Survival and toxicity in neoadjuvant chemotherapy plus before and after surgery in patients with stage I cervical cancer,
surgery versus definitive chemoradiotherapy for cervical ClinicaltTials.gov Identifier: NCT01649089. Available from:
cancer: A systematic review and meta-analysis. Cancer Treat https://clinicaltrials.gov/ct2/show/NCT01649089 accessed on
Rev 2020; 83 : 101945. October 10, 2020.
29. Kato T, Murakami G, Yabuki Y. A new perspective on nerve- 41. Schmeler KM, Pareja R, Lopez Blanco A, Humberto
sparing radical hysterectomy: Nerve topography and over- Fregnani J, Lopes A, Perrotta M, et al. ConCerv: a prospective
preservation of the cardinal ligament. Jpn J Clin Oncol 2003; trial of conservative surgery for low-risk early stage cervical
33 : 589-91. cancer. Int J Gynecol Cancer 2019; 29 : A14-5.
30. Lee SH, Bae JW, Han M, Cho YJ, Park JW, Oh SR, 42. Einstein MH, Park KJ, Sonoda Y, Carter J, Chi DS, Barakat RR,
et al. Efficacy of nerve-sparing radical hysterectomy vs. et al. Radical vaginal versus abdominal trachelectomy for
Conventional radical hysterectomy in early-stage cervical stage IB1 cervical cancer: A comparison of surgical and
cancer: A systematic review and meta-analysis. Mol Clin pathologic outcomes. Gynecol Oncol 2009; 112 : 73-7.
Oncol 2020; 12 : 160-8.
43. Bernardini M, Barrett J, Seaward G, Covens A. Pregnancy
31. Li L, Ma S, Tan X, Zhong S, Wu M. Surgical, urinary, and outcomes in patients after radical trachelectomy. Am J Obstet
survival outcomes of nerve-sparing versus traditional radical Gynecol 2003; 189 : 1378-82.
hysterectomy: A retrospective cohort study in China. Am J
44. Feng Y, Cao T, Wang Y, Huang H, Xie Y, Liu J. Neoadjuvant
Clin Oncol Cancer Clin Trials 2019; 42 : 783-8.
chemotherapy followed by conization to spare fertility in
32. Maas CP, Trimbos JB, Deruiter MC, Van De Velde CJ, cases of locally advanced cervical cancer: A case report and
Kenter GG. Nerve sparing radical hysterectomy: Latest review of the literature. Mol Clin Oncol 2016; 5 : 411-6.
developments and historical perspective. Crit Rev Oncol/
45. Plante M, Van Trommel N, Lheureux S, Oza AM, Wang L,
Hematol 2003; 48 : 271-9.
Sikorska K, et al. FIGO 2018 stage IB2 (2-4 cm) cervical
33. Kim HS, Kim K, Ryoo SB, Seo JH, Kim SY, Park JW, et cancer treated with neo-adjuvant chemotherapy followed
al. Conventional versus nerve-sparing radical surgery for by fertility sparing surgery (CONTESSA); neo-adjuvant
cervical cancer: A meta-analysis. J Gynecol Oncol 2015; 26 : chemotherapy and conservative surgery in cervical cancer
100-10. to preserve fertility (NEOCON-F). A PMHC, DGOG,
34. Dargent D, Martin X, Sacchetoni A, Mathevet P. Laparoscopic GCIG/CCRN and multicenter study. Int J Gynecol
vaginal radical trachelectomy: a treatment to preserve the Cancer 2019; 29 : 969-75.
fertility of cervical carcinoma patients. Cancer 2000; 88 : 46. Nezhat C, Roman RA, Rambhatla A, Nezhat F. Reproductive
1877-82. and oncologic outcomes after fertility-sparing surgery for
35. Schmeler KM, Frumovitz M, Ramirez PT. Conservative early stage cervical cancer: A systematic review. Fertil Steril
management of early stage cervical cancer: Is there a role for 2020; 113 : 685-703.
less radical surgery? Gynecol Oncol 2011; 120 : 321-5. 47. Yamamoto R, Okamoto K, Yukiharu T, Kaneuchi M,
36. Tempfer CB, Tischoff I, Dogan A, Hilal Z, Schultheis B, Negishi H, Sakuragi N, et al. A study of risk factors for
Kern P, et al. Neuroendocrine carcinoma of the cervix: A ovarian metastases in stage Ib-IIIb cervical carcinoma and
systematic review of the literature. BMC Cancer 2018; 4 ; 18. analysis of ovarian function after a transposition. Gynecol
Oncol 2001; 82 : 312-6.
37. Ramirez PT, Pareja R, Rendón GJ, Millan C, Frumovitz M,
Schmeler KM. Management of low-risk early-stage cervical 48. Landoni F, Zanagnolo V, Lovato-Diaz L, Maneo A, Rossi R,
cancer: Should conization, simple trachelectomy, or simple Gadducci A, et al. Ovarian metastases in early-stage cervical
hysterectomy replace radical surgery as the new standard of cancer (IA2-IIA): A multicenter retrospective study of 1965
care? Gynecol Oncol 2014; 132 : 254-9. patients (a cooperative task force study). Int J Gynecol Cancer
2007; 17 : 623-8.
38. Wenzel HH, Kol KG, Nijman HW, Lemmens VE,
Van der Aa MA, Ebisch RM, et al. Cervical cancer with ≤5 49. Cheng H, Huo L, Zong L, Kong Y, Yang J, Xiang Y.
mm depth of invasion and >7 mm horizontal spread – Is Oncological outcomes and safety of ovarian preservation for
lymph node assessment only required in patients with LVSI? early stage adenocarcinoma of cervix: A systematic review
Gynecol Oncol 2020; 158 : 282-6. and meta-analysis. Front Oncol 2019; 9 : 777.
39. National Institute of Health, U.S. National Library of 50. Sutton GP, Bundy BN, Delgado G, Sevin BU, Creasman WT,
Medicine. Radical versus simple hysterectomy and pelvic Major FJ, et al. Ovarian metastases in stage IB carcinoma of
node dissection with low-risk early stage cervical cancer, the cervix: A gynecologic oncology group study. Am J Obstet
ClinicaltTials.gov Identifier: NCT01658930. Available from: Gynecol 1992; 166 : 50-3.
292 INDIAN J MED RES, AUGUST 2021

51. Kim MK, Kim JW, Kim MA, Kim HS, Chung HH, Park NH, et 53. Landoni F, Maneo A, Zapardiel I, Zanagnolo V, Mangioni C.
al. Feasibility of less radical surgery for superficially invasive Class I versus class III radical hysterectomy in stage IB1-IIA
carcinoma of the cervix. Gynecol Oncol 2010; 119 : 187-91. cervical cancer. A prospective randomized study. Eur J Surg
52. Kodama J, Kusumoto T, Nakamura K, Seki N, Hongo A, Oncol 2012; 38 : 203-9.
Hiramatsu Y. Factors associated with parametrial involvement 54. Reade CJ, Eiriksson LR, Covens A. Surgery for early stage
in stage IB1 cervical cancer and identification of patients suitable cervical cancer: How radical should it be. Gynecol Oncol
for less radical surgery. Gynecol Oncol 2011; 122 : 491-4. 2013; 131 : 222-30.

For correspondence: Dr Amita Maheshwari, Division of Gynecologic Oncology, Tata Memorial Hospital, Homi Bhabha National Institute,
Dr. Ernest Borges Road, Parel, Mumbai 400 012, Maharashtra, India
e-mail:maheshwariamita@yahoo.com