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Hindawi Case Reports in Oncological Medicine Volume 2019, Article ID 1610653, 8 pages https://doi.org/10.1155/2019/1610653 Case Report Leiomyosarcoma of the Rectum as a Radiation-Induced Second Malignancy after Cervical Cancer Treatment: Case Report with Review of the Literature 1 1 2 1 Dmytro E. Makhmudov , Olena O. Kolesnik, Natalia N. Lagoda, and Maryna O. Volk Oncocoloproctology Department, National Cancer Institute, Lomonosova str. 33/43, Kyiv 03022, Ukraine Department of Pathomorphology, National Cancer Institute, Lomonosova str. 33/43, Kyiv 03022, Ukraine Correspondence should be addressed to Dmytro E. Makhmudov; dmahmudoﬀ@gmail.com Received 13 August 2019; Accepted 14 November 2019; Published 10 December 2019 Academic Editor: Peter F. Lenehan Copyright © 2019 Dmytro E. Makhmudov et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Background. Incidence of cervical cancer among women of reproductive age still remains signiﬁcantly high. In regard to prognostic features and risk factors, the standard treatment for most types of cervical cancer represents a combination of surgical treatment and radiation therapy, such as external beam radiation therapy and brachytherapy. Despite signiﬁcant advances of long-term oncological outcomes, radiation-induced secondary malignancies among cervical cancer survivors are still an issue. Current case report describes an incredibly rare case of radiation-induced leiomyosarcoma of the rectum, which occurred 32 years after cervical cancer treatment. Case Presentation. A 62-year-old female had a past medical history of FIGO stage IIB cervical cancer (squamous cell carcinoma pT2bN0M0). In 1987, she underwent radical hysterectomy with bilateral iliac lymph node dissection, followed by adjuvant radiation therapy—70 Gy external beam pelvic irradiation followed by 30.5 Gy of brachytherapy. Thirty-two years later, she presented with signs of rectal bleeding. Regarding past medical history, radiologic, endoscopic, and pathologic data, the patient was initially diagnosed with a malignant nonepithelial lower rectal tumor of the unknown origin and staged as mrT3a mrN0 cM0. Total mesorectal excision with complete mesocolic excision and central vascular ligation (CME/CVL) carried by an open approach was carried out. In an attempt to identify the tissue of origin, an immunohistochemistry assay had been performed. Tumor cells showed a high rate of mitotic activity with a 45% rate of Ki-67 expression, positive reaction for desmin, and SMA in all samples. Negative reaction for CD117 and S100 was observed. As a conclusion, the immunophenotype was identiﬁed as a grade 3 leiomyosarcoma (ISD-code 8890/3). Conclusions. We suggest that up to date, radical surgery with curative intent, as it was performed in our study, is the most evidence-based treatment option for patients with radiation-induced sarcomas of the rectum. 1. Background their scattered features, prognostic factors and optimal treatment strategy for primary colorectal sarcomas remain indeterminate. However, pooled data from a majority of Primary colorectal sarcomas are an extremely rare group of malignant mesenchymal tumors. They represent up to 0.1% recently published case series suggest that primary colorec- tal sarcomas are characterized by both rapid progression of all primary diagnosed colorectal malignancies . Leio- and very poor oncological outcomes with a median of sur- myosarcomas appear to be the most common histological subtype of primary colorectal sarcomas with incidence up vival ranging from 30 to 53 months and a local recurrence rate of up to 85% [3–6]. Overall ﬁve-year survival rate of to 90%. More rare of their subtypes are liposarcomas, patients with primary colorectal sarcomas is signiﬁcantly ﬁbrous histiocytomas, and desmoplastic small cell tumors lower comparing to those with colorectal cancer—43% . Regarding the small number of documented cases and 2 Case Reports in Oncological Medicine (a) (b) (c) Figure 1: Radiologic data from a high-resolution pelvic MRI. Tumor of the lower rectum (1) situated on the anterior wall was observed on sagittal (a) and axial T2-weighted scans (b) with signs of mesorectal invasion (blue arrowheads) ranging up to 3 mm and no radiologic features of lymph node metastases (3). Vaginal stump and rectovaginal sept (2) had a signiﬁcantly low intensity MR signal due to their ﬁbrotic transformation. On a series of diﬀusion-weighted images (c), a signiﬁcant delay of diﬀusion together with intense signaling on high b-factors was observed at the level of a tumor (blue arrowheads). and 52%, respectively . Tumor grade of primary colorec- identiﬁed. No radiological signs of either mesorectal fascia tal sarcomas is the most important prognostic factor for involvement or extramural vascular invasion (mrCRM and overall ﬁve-year survival—38% for high grade and 61% for mrEMVI ) had been observed (see Figures 1(a) and 1(b)). Vis- low grade . Besides, inappropriate staging algorithm and ible mesorectal lymph nodes had homogenous MR signal, wide use of local excision as a surgical option for primary smooth external margins, and a regular size, thus showing no treatment results in high rates of R1 and R2 resections with radiologic signs of lymph node involvement (mrN ). It was a local recurrence rate of 12.7%. Nevertheless, a number of noticeable that the stump of the vagina and rectovaginal sept authors suggest that curative surgery should be the main had prominent signs of ﬁbrosis regarding a highly intensive treatment option because data regarding chemotherapy MR signal on T2-weighted images. Malignant tumor features and radiation therapy is either lacking or it is controversial were also observed on a series of diﬀusion-weighted images [9, 10]. Colorectal sarcomas as a radiation-induced second (see Figure 1(c)). malignancy after cervical cancer treatment, on contrary to A CT scan with intravenous enhancement showed no primary ones, are an exceptionally rare entity. Up to date, signs of neither distant metastases neither thoracic or intra- only ﬁve cases had been described in the literature [11–15]. abdominal lymphadenopathy. Upper GI endoscopy and lab- In our current paper, we provide data on the sixth case of oratory data of standard blood, serum, and urine counts similar malignancy. revealed no signs of pathology. 2. Case Presentation 3. Surgical Treatment A 62-year-old female had a past medical history of FIGO stage IIB cervical cancer (squamous cell carcinoma Regarding past medical history, radiologic, endoscopic, and pT2bN0M0). In 1987, she underwent radical hysterectomy pathologic data, the patient was initially diagnosed with a with bilateral iliac lymph node dissection, followed by malignant nonepithelial lower rectal tumor of the unknown adjuvant radiation therapy—70 Gy external beam pelvic origin and staged as mrT3a mrN0 cM0. Being aware of pri- irradiation followed by 30.5 Gy of brachytherapy. Thirty- mary colorectal sarcomas, their recurrence and progression two years later, she presented with signs of rectal bleeding. patterns and a threatening rate of R1 and R2 resections, an Digital rectal examination revealed a solid exophytic institutional multidisciplinary board suggested curative sur- tumor on 5 cm above the anal verge. During rigid procto- gery as a primary treatment option. Total mesorectal excision sigmoidoscopy, a 3 cm anterior wall rectal tumor with (TME) with complete mesocolic excision and central vascu- irregular margins and swollen mucosa was observed. Addi- lar ligation (CME/CVL) carried by an open approach was tional ﬂexible colonoscopy showed no signs of synchronous selected as proper extent of surgery. Standardized surgical colorectal neoplasms. Snare biopsy result showed an undif- technique in this case included complete left ﬂexure mobili- ferentiated malignant nonepithelial tumor of unidentiﬁed zation, ligation of the inferior mesenteric artery at its origin histological origin. An attempt of immunohistochemistry near the aorta and inferior mesenteric vein just below the assay was undertaken unsuccessfully due to an insuﬃcient pancreatic tail with consecutive total mesorectal excision up amount of tissue. to the level of the pelvic diaphragm (see Figure 2). Accurate Consecutively, a pelvic MRI with a 1.5 Tl Philips Intera TME procedure had been exacerbated by severe ﬁbrotic machine had been performed for local staging. MERCURY changes of surrounding pelvic tissues due to postoperative protocol for high resolution imaging was applied. changes after iliac lymphadenectomy for cervical cancer On a series of sagittal and axial MR scans, a lower rectal and radiation-induced ﬁbrosis as well. Regarding the signiﬁ- tumor was observed on 4 cm above the anorectal junction with cant ﬁbrotic transformation of the anterior rectal wall with maximal extent of 30 mm in the greatest dimension. Mesorec- adjacent tissues, an intraoperative decision was made to tal inﬁltration with maximal depth of 3 mm (mrT ) was also avoid reconstruction aware of an estimated high risk of 3b Case Reports in Oncological Medicine 3 4. Pathologic Findings Macroscopically, the tumor was represented an exophytic homogenous lesion 45 × 25 mm with irregular margins and ulcerated surface covered with clots of ﬁbrin. The tumor originated from the muscular layer of the rectum with con- comitant mucosal invasion. Twelve regional lymph nodes were additionally examined. Initial histological appearance revealed a mixture of chaotic cellular and ﬁbrotic vegeta- tions. Among them, a subgroup of heterogeneous polykar- yocytes with signiﬁcant nuclear polymorphism (so called “monster cells”) was identiﬁed (see Figure 5). Those and other morphological features corresponded to a malignant low-grade mesenchymal tumor. All examined lymph nodes had no signs of metastases. In an attempt to identify the tissue of origin for a current tumor, an immunohistochemistry assay had been carried out. A panel of Ki-67, CD117, S100, smooth muscle actin (SMA), and desmin was used to conduct a diﬀerential diag- nosis between leiomyosarcoma and gastrointestinal stromal tumor. Tumor cells showed a high rate of mitotic activity with a 45% rate of Ki-67 expression (see Figure 6). There was a positive reaction for desmin and SMA in all samples (see Figures 7 and 8). On contrary, all samples had negative Figure 2: Resected gross specimen. 1: stump of the inferior reaction for CD117 and S100 (see Figures 9 and 10). As a mesenteric artery, 2: stump of the inferior mesenteric vein, 3: conclusion, the observed immunophenotype was identiﬁed preserved peritoneal window, 4: level of the peritoneal reﬂection, as a grade 3 leiomyosarcoma (ISD-code 8890/3). and 5: mesorectum. anastomotic leakage. Closure of the pelvic peritoneum was 5. Discussion avoided as well. On postoperative day 5, the patient developed such clin- In the current paper, we present the sixth case of radiation- ical signs as nausea, vomiting, and loss of ﬂatus and stool. induced leiomyosarcoma of the rectum which developed 32 Computed tomography of the chest, abdomen, and pelvis years after completion of cervical cancer treatment. revealed multiple “levels” of gas and liquid throughout the Throughout the last decades, signiﬁcant success was small intestine with a breakdown of peroral contrast at the achieved in the treatment of patients with pelvic malignan- level of distal ileal loop, which was situated at the cavity of cies, especially those who require either adjuvant or neoadju- minor pelvis, adherent to the stumps of both the rectum vant radiation therapy. As a consequence of overall survival and the vagina (see Figure 3). At that level, a noticeable defor- improvement, the problem of metachronous secondary mation of the intestinal loop with diﬀerence of luminal diam- malignancies among those patients who were exposed to eters was observed. On contrary, the lumen of a large radiation had arisen. According to the data of the National intestine was collapsed. Cancer Institute of USA, over 40% of all patients diagnosed By taking in regard both clinical and radiologic ﬁnd- with primary malignancy will have to undergo radiation ings, the patient was diagnosed with postoperative ileus therapy . Most of primary malignancies which require and an immediate reoperation had been carried out. Dur- radiation therapy as a treatment standard are breast, pros- ing abdominal examination, dilated intestinal loops with tate, cervical, rectal, and urinary bladder cancer. Among block of passage at the level of the pelvic diaphragm were long-term cancer survivors exposed to radiation, 16% are identiﬁed (see Figure 4). An adherent bowel wall was ﬁxed at risk of developing a secondary malignancy. Recent data between vaginal and rectal stumps as it was previously from a SEER database suggests that 6–9.9% of all patients described on a series of CT scans. By the end of abdomi- who underwent radiation therapy for prostate cancer are at nal and pelvic exploration, no additional pathological ﬁnd- a 34% risk of developing secondary lung, rectal, or urinary ings were observed. After detachment of adhesions, the bladder cancer. Majority of those patients develop secondary strangulated bowel was delivered back in the abdominal malignancies mostly after 10 years from treatment discon- cavity. Closure of the pelvis was performed with mobilized tinuation [17, 18]. body of the urinary bladder and remnant ﬂaps of pelvic Cervical cancer remains one of the leading cause of peritoneum. Postoperative period was uneventful within cancer-related morbidity and mortality among females . 30 days. The patient was safely discharged on postopera- It is known that only surgical treatment can be appropriate tive day 14 after initial surgery. At one year of follow- only in a relatively small subgroup of patients, particularly up, the patient is alive and has no radiological signs of among those who were initially diagnosed with FIGO stage neither local nor distant recurrence. IA1 (T1a1 by TNM) or less, i.e., with a depth of stromal 4 Case Reports in Oncological Medicine (a) (b) th Figure 3: Patient’s CT scans on the 6 postoperative day. Multiple intestinal “levels” of gas and ﬂuid throughout the abdominal cavity were observed ((a), red arrowheads). Part of the distal intestinal loop with diﬀerence in lumen diameters was situated at the level of the pelvic ﬂoor ((b), yellow arrowheads) and was adherent to both rectal and vaginal stumps. Figure 6: Poorly diﬀerentiated malignant mesenchymal tumor. Immunohistochemistry assay with Ki-67 antibodies. Figure 4: Intraoperative photo during reoperation. Dilated intestinal loops up to the level of distal ileum (1) are observed. The loop of a strangulated bowel (2) was adherent to the stump of the rectum and vagina deep inside the pelvic cavity. Figure 7: Poorly diﬀerentiated malignant mesenchymal tumor. Immunohistochemistry assay with desmin antibodies. Positive reaction in tumor cells observed. invasion up to 3 mm and lateral spread up to 7 mm . Recent NCCN guidelines suggest adjuvant radiation therapy for FIGO stage IA1 patients with a number of adverse risk features found at pathological examination, such as positive lymph nodes, parametrium invasion, or positive resection margins . A standard approach for cervical cancer radia- tion therapy includes combination of external beam radia- Figure 5: Poorly diﬀerentiated malignant mesenchymal tumor. tion therapy and brachytherapy. Overall radiation dosage Multiple sites of cellular and nuclear polymorphism are observed. depends on the range of primary tumor spread—in cases of Hematoxylin-eosin staining, ×100. tumors below 40 mm in maximum dimension, the overall dosage consists of 80 Gy and ≥85 Gy if above 40 mm. Case Reports in Oncological Medicine 5 Figure 8: Poorly diﬀerentiated malignant mesenchymal tumor. Figure 10: Poorly diﬀerentiated malignant mesenchymal tumor. Immunohistochemistry assay with SMA antibodies. Positive Immunohistochemistry assay with S100 antibodies. Negative reaction in tumor cells observed. reaction in tumor cells observed. secondary malignancy development was the age under 30 years at primary diagnosis of cervical cancer. Urinary bladder (4.5), vagina (2.7), stomach (2.1), and hematopoietic tissue (2.5) had the highest relative risk for secondary malignancy. It was noticeable that the rectum had the lowest relative risk among other pelvic organs (1.8). Other data from a study of Samerdokiene et al. suggest that secondary radiation- induced malignancies occur in 5.3% of cervical patients after a combination of external beam and brachytherapy. Among them, rectal malignancies consisted only 8.6% . A popu- lation study of 37,757 patients based on a data from SEER database demonstrated a 2.6-fold increase in a number of secondary malignancies among those cervical cancer patients Figure 9: Poorly diﬀerentiated malignant mesenchymal tumor. who underwent pelvic radiation therapy comparing to sur- Immunohistochemistry assay with CD117 antibodies. Negative gery alone . Nevertheless, the authors acknowledged that reaction in tumor cells observed. metachronous bronchopulmonary, esophageal, and oropha- ryngeal cancer were mostly caused by continuous smoking In cases of cervical cancer, the radiation ﬁeld includes and vaginal, vulval, and anal canal cancer—by HPV infection parametrium, sacrouterine ligaments, 3 cm of upper third rather than by previous radiation exposure. Similar retro- of the vagina below the tumor, and presacral, obturator, spective population-based data concerning a consistent pat- external, and internal iliac lymph nodes. By taking in regard tern of an increased secondary malignancy rate among all the anatomical relations of the cervix, it becomes clear that cervical cancer survivors was obtained from the Netherlands the most critical radiation sites are represented by the vagina, and Taiwan [25, 26]. Even though all secondary colon, rectal, the rectum, and the urinary bladder. In comparison, bony and anal malignancies in those studies were united in one pelvis structures receive signiﬁcantly lesser radiation dosages. subgroup, their relative risk ratio still remained one of the A successful combination of curative surgery and highly lowest. A study by Ohno et al., based on a pooled data from precise modalities of radiation therapy in either adjuvant or 2167 patients after a combination of external beam and neoadjuvant regimens had given a unique opportunity to brachytherapy for cervical cancer, reports a 9.7% rate of sec- improve cervical cancer patient’s overall and disease-free sur- ondary radiation-induced malignancies with 19% of them vival rates like never before. Hence, by dropping out of a can- related to adjacent irradiated organs . Soft tissue and cer recurrence group, those patients consequently enter bone sarcomas (22.0), leukemias (3.1), and urinary bladder another one—a risk group of developing a secondary malig- cancer (2.2) had the greatest relative risk rates. On the other nancy. The ﬁrst population-based study which highlighted hand, rectal cancer, hepatocellular carcinoma, and gastric a relevance between previous exposure to pelvic irradiation cancer (1.0, 1.2 and, respectively) possessed the lowest rela- and a risk of developing a second malignancy was presented tive risk rates. Lim et al. came up with a data of 72,805 inva- by Boice et al., in 1984 . The study included more than sive cervical cancer patients after pelvic irradiation within a 95,000 patients after pelvic radiation therapy for cervical study period of 7.34 years . A 3.68% rate (2678 cases) cancer within a 30-year study period. This population was of secondary radiation-induced malignancies with similar compared with more than 99,000 patients who underwent relative risk patterns—vagina (9.36), soft tissues and bones only curative surgery. Throughout the study period, 3324 (2.7), vulva (2.58), and anus and anal canal (2.42)—was (3.5%) secondary radiation-induced malignancies had been observed. It is noticeable that among the 35 sites of secondary observed, of which 1622 (1.7%) were located at the organs malignancy occurrence, rectal cancer had the lowest relative covered by the irradiation ﬁeld. The main risk factor of risk of 0.74. Correlation between previously treated cervical 6 Case Reports in Oncological Medicine Table 1: Pooled data of all identiﬁed case reports of radiation-induced leiomyosarcoma of the rectum after pelvic radiation therapy for cervical cancer. Time to diagnosis Year of Patient’s age Overall irradiation Radiation Selected treatment Authors of a secondary publication at diagnosis dosage (Gy) modality strategy malignancy (years) 40 Gy Intra-abdominal Drumea et al.  1993 62 70 17 1 2 resection of the rectum EBRT +30 Gy BT Caporale et al.  2003 N/A N/A N/A N/A N/A Intra-abdominal Basu et al.  2012 79 N/A N/A 26 resection of the rectum Sigmostomy+ Garcia-Ortega 50 Gy 2018 58 85 8 chemotherapy+pelvic et al.  EBRT+35 Gy BT exenteration+vulvectomy Jayakumar et al.  2015 58 N/A N/A 15 Local excision 70 Gy EBRT+ Current case report 2019 62 100.5 32 ТМЕ+CME/CVL 30.5 Gy BT 1 2 EBRT: external beam radiation therapy. BT: brachytherapy. cancer secondary colorectal cancer had been recently only in 12% of radiation-induced sarcomas. However, there highlighted in a paper of Rodriguez et al. . After 35 years was absolutely no data regarding a radiation-induced leio- of follow-up, an estimated risk of colon cancer was 2.5% in a myosarcoma after previous pelvic radiation therapy with surgery alone group and 6.5% in a radiation therapy group. intra-abdominal or either intrapelvic localization. For rectal cancer, the diﬀerence was more signiﬁcant—0.8% Remarkably, but up to date, there were only 5 published and 3.7%, respectively. Regression analysis survival model case reports of a radiation-induced leiomyosarcoma of the demonstrated a signiﬁcant increase of relative risk for colon rectum in a patient after previous radiation therapy for cervi- cancer development after 8 years and rectal cancer—after cal cancer (see Table 1). On the contrary, one of the largest recent studies by Thiels et al. evaluates a series of 433 primary 15 years of follow-up. The authors suggest that 8 years should be a cutoﬀ edge for colorectal cancer screening among cervi- colorectal sarcomas discovered within a 14-year observation cal cancer survivors. period . Among the 29.3% of patients with the rectum as First studies about the inﬂuence of ionizing radiation on a primary tumor site, only 57.5% had leiomyosarcomas. the development of malignancies were provided after a Although radiation-induced leiomyosarcomas of the rectum appear to be an extremely rare type of secondary nuclear attack in Japan at 1945. Three main issues had been discovered then: tissues with higher proliferative index (i.e., malignancies, there is an emerging data suggesting an intrin- epithelial and hematopoietic) are mostly aﬀected; very small sically diﬀerent sequence of molecular events responsible for number of radiation-induced sarcomas and a ratio of 8%/1 their development and occurrence comparing to primary Gray, which is a distribution of those who shall develop a sarcomas . Gonin-Laurent et al. recognize a mutation of ТР53 and RB1 genes as a key molecular event in the develop- malignancy among one hundred people exposed to an irradi- ation dosage of 1 Gy . Mechanisms and conditions for ment of radiation-induced sarcomas. Consecutive mutation radiation sarcoma development were ﬁrstly described by of a TP53 gene was identiﬁed in 58% of radiation-induced Cahan et al. in 1948 . It was noticed that the occurrence sarcomas and was related to deletion of other oncogenes in of pathologically conﬁrmed secondary sarcomas is related 52% [34, 35]. It was also mentioned that mutation of a TP53 gene led to inactivation of RB1, which showed no signs to an irradiation ﬁeld previously exposed to a dosage of at least 50 Gy. However, the only uncertainty was timing of of genetic alterations . Hyperexpression of р53 is recog- occurrence which could range from months to decades. nized as a speciﬁc pathogenic route for radiation-induced Despite meeting all of Cahan’s criteria, radiation-induced sarcoma development as well. Taubert et al. identiﬁed a р53 sarcomas in cervical cancer patients after pelvic radiation mutation in 9 out of 11 radiation-induced sarcoma cases . Finally, a study of Nakanishi et al. revealed a р53 muta- therapy are a very rare entity. Among all primary diagnosed soft tissue sarcomas, a range of 0.03% to 5.5% could be con- tion pattern in a series of 14 secondary radiation-induced soft sidered as radiation induced [32, 33]. tissue sarcomas in patients who previously underwent pelvic According to the largest published series of Cha et al., radiation therapy for cervical cancer . Real-time poly- only 125 (2.5%) out of 4884 primary soft tissue sarcomas sat- merase chain reaction detected polymorphism of р53 gene with an 88% rate of mutations in exons 5, 7, 8, 12, and 18. isﬁed Cahan’s criteria and were considered as radiation induced . Vast majority of those patients previously However, concomitant changes in the primary structure of underwent radiation therapy for breast cancer (29%), lym- a p53 protein were observed only in 31%. The authors con- phomas (16%), and prostate cancer (14%) with thoracic cav- clude that such a biological mislead might be a reason for a ity, thoracic wall, extremities, head and neck as a tumor site. long latency period between radiation exposure and clinical manifestation of secondary soft tissue sarcomas. Pathological features of leiomyosarcomas were identiﬁed Case Reports in Oncological Medicine 7  C. D. Randleman, B. G. Wolﬀ, R. R. Dozois, R. J. Spencer, L. H. 6. Conclusions Weiland, and D. M. Ilstrup, “Leiomyosarcoma of the rectum Among all radiation-induced malignancies aﬀecting long- and anus,” International Journal of Colorectal Disease, vol. 4, term cervical cancer survivors, soft tissue sarcomas occur no. 2, pp. 91–96, 1989. quite frequently. However, radiation-induced leiomyosar-  B. D. Minsky, A. M. Cohen, S. I. Hajdu, and D. 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