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Management of Low-Grade Appendiceal Mucinous Neoplasm with Extensive Peritoneal Spread Diagnosed during Pregnancy: Two Case Reports and Literature Review

Management of Low-Grade Appendiceal Mucinous Neoplasm with Extensive Peritoneal Spread Diagnosed... Hindawi Case Reports in Oncological Medicine Volume 2020, Article ID 8853704, 9 pages https://doi.org/10.1155/2020/8853704 Case Report Management of Low-Grade Appendiceal Mucinous Neoplasm with Extensive Peritoneal Spread Diagnosed during Pregnancy: Two Case Reports and Literature Review Ekaterina Baron , Vadim Gushchin , Mary Caitlin King , Andrei Nikiforchin , and Armando Sardi Department of Surgical Oncology, The Institute for Cancer Care at Mercy, Mercy Medical Center, 227 St. Paul Place, 4th Floor Weinberg, Baltimore, Maryland 21202-2001, USA Correspondence should be addressed to Armando Sardi; asardi@mdmercy.com Received 29 June 2020; Revised 30 September 2020; Accepted 3 October 2020; Published 15 October 2020 Academic Editor: Ossama W. Tawfik Copyright © 2020 Ekaterina Baron 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. Clinical decisions in patients with peritoneal dissemination of low-grade appendiceal mucinous neoplasms (LAMN) diagnosed during pregnancy are challenging. However, their slow progression and favorable prognosis allow deferring definitive treatment until after spontaneous delivery, a reasonable period of breastfeeding, and fertility preservation. Case Presentation. Two pregnant patients were incidentally diagnosed with LAMN and extensive peritoneal spread at 20 weeks gestation and at cesarean section. Treatment with cytoreductive surgery and hyperthermic intraperitoneal chemotherapy in both cases was delayed until spontaneous delivery at term and breastfeeding in the first patient and breastfeeding and fertility preservation in the second patient. Both patients remain disease-free for over 5 years, and their children are healthy. The literature review highlights the challenges that physicians face in treating pregnant patients with stage IV appendiceal tumors. Conclusion. Pregnancy management decisions in patients with peritoneal spread from mucinous appendiceal tumor should be based on understanding the tumor biology and prognosis. Definitive treatment in pregnant patients with favorable tumors, such as LAMN, may be delayed until spontaneous delivery without compromising maternal survival. 1. Introduction time, up to 20% of AMN present with peritoneal carcinoma- tosis (PC) [2], considered stage IV according to the American th Treating neoplasms diagnosed during pregnancy entails Joint Committee on Cancer (AJCC) 8 edition [3]. However, weighing the risks and benefits for both mother and fetus. excellent long-term outcomes can be achieved in AMN with This requires considering multiple factors, such as tumor cytoreductive surgery and hyperthermic intraperitoneal biology and prognosis, stage, gestational age at diagnosis, effi- chemotherapy (CRS/HIPEC) [4]. cacy, toxicity, invasiveness of required treatment, and patient Diagnosis of PC during pregnancy is often considered to preferences. Particularly, the management of stage IV tumors be a life-threatening condition where oncological concerns of with extensive dissemination during pregnancy poses addi- the mother outweigh fetal risks. In the few published cases of tional challenges because it demands rapid and complex PC from low-grade appendiceal tumors diagnosed during ethical decisions, which should be based on a deep under- pregnancy, all managed with early labor induction, early standing of tumor behavior and all available options. cesarean section, or pregnancy termination in favor of faster Appendiceal mucinous neoplasms (AMN) are a rare definitive treatment [5–8]. However, the favorable prognosis group of malignancies with high heterogeneity of histopath- and slow progression of LAMN, even with extensive PC, ologic subtypes and survival outcomes [1]. They range from allows performing CRS/HIPEC after spontaneous delivery, low-grade neoplasms with favorable prognosis to high- which minimizes fetal risks without compromising maternal grade tumors with significantly worse outcomes. At the same survival [9] We present two unique cases of LAMN with PC 2 Case Reports in Oncological Medicine MA MA (a) (b) Figure 1: (a) Abdominal and pelvic MRI (sagittal plane) without IV contrast shows a gravid uterus and a substantial amount of T2 hyperintense fluid. (b) Abdominal and pelvic MRI (coronal plane) without IV contrast demonstrates an enlarged perforated appendix with extraluminal mucin (arrow) and T2 hyperintense fluid collection in the pelvis. B: bladder; C: cervix; F: fetus; IV: intravenous; MA: mucinous ascites; MRI: magnetic resonance imaging; U: uterus. MA MA (a) (b) Figure 2: (a), (b) Abdominal and pelvic MRI without IV contrast ((a) coronal plane, (b) axial plane) shows a gravid uterus and significant amount of T2 hyperintense fluid, some of which is loculated with internal septations (arrows). B: bladder; F: fetus; IV: intravenous; MA: mucinous ascites; MRI: magnetic resonance imaging; P: placenta; U: uterus. diagnosed during pregnancy and managed with delayed progression as low and recommended to defer definitive CRS/HIPEC in the postpartum period accompanied by a treatment until the postpartum period. A healthy 2,950 g literature review. (6.6 lbs.) male was born by uncomplicated spontaneous vaginal delivery at 38 weeks gestation. Staging with computed tomogra- phy (CT) of the chest, abdomen, and pelvis revealed multiple 2. Case #1 bilateral subdiaphragmatic, omental, mesenteric, and liver cap- sule mucinous implants and no extraperitoneal metastases. A 31-year-old woman, gravida 2 para 1, with a history of asthma and anemia presented with a large intra-abdominal Tumor markers (CEA, CA 125, and CA 19-9) were normal. mass and ascites found incidentally on routine prenatal ultra- After 4 months of breastfeeding, the patient underwent CRS/HI- sound (US) at 20 weeks gestation. Prior to that, the patient PEC with 40 mg mitomycin-C heated to 41-42 Cfor 90 minutes had an uneventful pregnancy and skipped US during the first using the closed technique. The peritoneal cancer index (PCI) trimester prenatal screening. An ovarian primary tumor was (range 0-39) [10] was 37. The surgery lasted 708 minutes with suspected and abdominopelvic magnetic resonance imaging an estimated blood loss of 1,100 ml. Complete cytoreduction (MRI) without contrast was performed within one week. with residual small membranes on the small bowel (complete- MRI showed a disrupted appendiceal tip surrounded by soft ness of cytoreduction (CC) score 1) [4] was achieved. The post- tissues and fluid, as well as a substantial amount of abdomi- operative period was complicated by anemia requiring red blood nopelvic fluid with internal septations and debris, suggesting cell transfusion. The patient was discharged on postoperative an appendiceal mucinous neoplasm with PC (Figures 1(a), day (POD) 9 with deep vein thrombosis (DVT) prophylaxis 1(b), 2(a), 2(b)). Appendectomy, right salpingo-oophorec- (40 mg of enoxaparin daily). However, she was readmitted twice: tomy, omentectomy, and peritoneal biopsy were performed first with splenic and portal vein thrombosis (POD 15) and then at 21 weeks gestation and pathology confirmed LAMN with with rectal bleeding (POD 30) after subsequent increase in th cellular mucinous peritoneal implants (AJCC 8 anticoagulant dose. Regular follow-up included physical stage IVA). The patient was referred to a peritoneal surface malignancy examinations; imaging of the chest, abdomen, and pelvis; and center. Considering the favorable prognosis of LAMN even with tumor markers every 6 months. At 63 months of follow-up, extensive peritoneal spread, we assessed the risk of rapid tumor the patient remains disease-free and her child is healthy. Case Reports in Oncological Medicine 3 among peritoneal malignancy centers to treat patients with 3. Case #2 a peritoneal spread from AMN. In our center, we opted to A 31-year-old healthy woman, gravida 3 para 0, underwent delay CRS/HIPEC and allow the pregnancy to progress cesarean section at 40 weeks gestation due to premature rup- naturally. ture of membranes and protracted labor and delivered a The approach to delay definitive treatment in our cases healthy 3,561 g (7.9 lbs.) male newborn. The patient had a was based on the well-known favorable prognosis of LAMN history of lower back pain and mild anemia throughout the with extensive peritoneal spread treated with CRS/HIPEC. pregnancy and started experiencing diarrhea at 35 weeks. Two previously published cases of well-differentiated appen- The full prenatal screening, including US in each trimester, diceal adenocarcinoma with PC, which currently is consid- revealed only an echogenic intracardiac focus of the fetus. ered to be the same grade (G1) and prognostic stage (IVA) Otherwise, the pregnancy was uneventful. During cesarean as LAMN, managed their patients with early labor induction section, mucin originating from the appendix tip was found (35 weeks) and early cesarean section (33 weeks) followed by adherent to the uterus, right ovary, and fallopian tube. CRS/HIPEC in 2.5 weeks and 2 months, respectively [3, 5, 7]. Appendectomy and peritoneal biopsy were performed, and Moreover, Haase et al. proposed managing peritoneal surface th pathology showed LAMN with PC (AJCC 8 stage IVA). malignancies diagnosed during pregnancies with early induc- The chest, abdominal, and pelvic CT scan 3 weeks after tion and delaying treatment to 35 weeks if diagnosed in the nd delivery showed perihepatic and perisplenic capsular 2 trimester [5]. However, labor at 34-37 weeks of gestation implants. Tumor marker assessment showed elevated CEA refers to late preterm delivery and is associated with up to 8.8 ng/ml (N 0-5 ng/ml) and normal CA 125 and CA increased risk for numerous complications for the infant 19-9. Definitive treatment was delayed for breastfeeding and should be avoided when possible [11]. We believe that and oocyte retrieval for cryopreservation of 4 embryos. Three the histopathology and disease pathogenesis must be consid- months postdelivery, the patient underwent CRS/HIPEC ered carefully before inducing early delivery or termination. nd with 90-minute perfusion of 40 mg mitomycin-C heated to In case #1, the diagnosis was made in the 2 trimester (20 41-42 C. PCI was 27, and a complete cytoreduction was weeks) during routine prenatal screening. Previous studies achieved (CC-score 0) after 487 minutes of surgery. The demonstrate an excellent prognosis of LAMN patients with patient was discharged on POD 8 without major complica- 5-year overall survival up to 80-96% 9, 12]. This data suggests tions. She was readmitted several times over the last 5 years that the slow progression of LAMN allows for a natural with small bowel obstructions that resolved nonoperatively. progression of pregnancy and deferring CRS/HIPEC for a Three years after CRS/HIPEC, the patient had a second child reasonable period. Therefore, we opted to postpone CRS/HI- via surrogate maternity using a frozen embryo. The follow- PEC for 8 months in case #1 until spontaneous at term deliv- up was the same as the previous case. After 67 months, the ery with subsequent breastfeeding and for 4 months in case patient is disease-free and her children are doing well. #2 for breastfeeding and fertility preservation without compromising survival outcomes in either case as it is onco- logically safe. 4. Discussion Diagnosing and staging AMN might be challenging dur- ing pregnancy due to the limited availability of safe diagnostic The presented patients were diagnosed with a rare appendi- ceal tumor and PC at an advanced gestational age of preg- methods and nonspecific clinical presentation. Considering nancy: 20 weeks and 40 weeks during cesarean section. To patient and fetus risks, only tests that may influence clinical our knowledge, these are the first published cases of perito- management should be performed. Once peritoneal spread neal spread from LAMN diagnosed during pregnancy man- or local appendiceal tumor is suspected during prenatal pelvic aged with delayed CRS/HIPEC, which, for patient #1, US, additional imaging is required for staging and making allowed spontaneous delivery of a healthy baby at 38 weeks decisions regarding diagnostic surgery. Abdominopelvic MRI with 4 months of breastfeeding and, for patient #2, 3 months without contrast is a safe and informative alternative to CT of breastfeeding and cryopreservation of embryos that were during pregnancy for clarifying the diagnosis of peritoneal eventually used successfully. lesions [13, 14]. The MRI in case #1 demonstrated a disrupted Diagnosis of PC at any stage of pregnancy is dramatic appendiceal tip and signs of mucin distributed throughout the and associated with multiple challenges for both physician abdomen and pelvis (Figures 1 and 2). These findings shifted and patient. While there are numerous reports of appendi- our focus from initially suspected ovarian origin to appendi- ceal tumors diagnosed during pregnancy (Tables 1 and 2), ceal tumor and directed the diagnostic surgery. we found only 6 with PC: 4 diagnosed during pregnancy Defining histopathologic subtype and stage is crucial for and 2 of diagnosed during cesarean section. Of the four cases establishing treatment in patients with PC. We believe that diagnosed during pregnancy, one was managed with preterm diagnostic open or laparoscopic surgery for appendectomy, induction of labor at 35 weeks, two were managed with an peritoneal biopsy, and thorough revision of the abdomen early cesarean section at 30 and 33 weeks, and one was termi- and pelvis is reasonable and should be performed in all nated at 18 weeks [5–8]. The time of definitive treatment in patients with PC on imaging regardless of pregnancy stage. the two cases diagnosed at cesarean section is unknown as Laparoscopy has advantages in this case as it allows inspect- patients were referred to outside facilities [10, 11]. This may ing the majority of the abdominal cavity, including the upper demonstrate that pregnancy termination or early labor abdomen. However, the use of laparoscopy in pregnant induction with rushing CRS/HIPEC is a common strategy women is controversial. A meta-analysis of 11 retrospective 4 Case Reports in Oncological Medicine Table 1: Literature review of appendiceal tumors diagnosed during pregnancy. Time from Gestational Clinical Treatment during Pregnancy pregnancy Breast- # Author (year) Age Pathology PC Staging Treatment postpregnancy PCI CC score Complications Status Child age at dx presentation pregnancy outcome end to feeding treatment POD 15: portal 4 mos Routine Appy, Spontaneous MRI abd/pelv at 20 vein nd Present case 2 Tx +12 mos 5 yrs, 1 31 LAMN Yes prenatal omentectomy, vaginal delivery weeks; CT chest/abd/pelv CRS/HIPEC (Mit-C) 4 mos 37 CC-1 thrombosis Healthy #1 (20 weeks) milk NED screening RSO, peritoneal bx (38 weeks) after delivery POD 30: rectal donor bleeding Neutropenia, Well-differentiated Routine Early induce CRS/HIPEC (Mit- nd Haase et al. 2 Tx (17 Appy, RSO, prolonged ileus 5 yrs, 2 30 mucinous Yes prenatal vaginal delivery CT after delivery C) + EPIC (5-FU); 2.5 weeks 28 CC-1 - Healthy (2010) [5] weeks) omental bx (NGT, TPN), NED adenocarcinoma screening (35 weeks) adjuvant XELOX x8 cycles DVT Infiltrating Colonoscopy, CT CRS/HIPEC (5-FU nd Chiverto et al. mucinous 2 Tx Abdominal Terminated 10 mos, 3 36 Yes Dx lap, open appy chest/abd/pelv after + Oxaliplatin; adjuvant - 6 Complete - NA NA (18 weeks) pain x4 days with misoprostol (2012) [6] adenocarcinoma NED termination FOLFOX x6 Mos (T3N1M1a) Routine Laparoscopic R RDS Well-differentiated prenatal adnexectomy, prophylaxis; CRS/HIPEC (Mit-C No Canuto et al. mucinous 2 yrs, st 4 38 Yes 1 Tx screening (R peritoneal early C-section - + Cisplatin); adjuvant 2 mos - residual -- Healthy (2016) [7] adenocarcinoma NED ovarian washing/bx (16 (33 weeks, 5 FOLFOX x8 cycles tumor (pT4apN1) mass) weeks, 4 days) days) Moderately Abdominal rd Sebire et al. differentiated 3 Tx (29 pain, C-section (30 Abd US (29 weeks); fine- CRS; adjuvant 5- 0 days (at Residual 6 mos, 5 29 Yes None - -- Healthy (2000) [8] adenocarcinoma; weeks) vomiting, weeks) needle liver bx FU/Epirubicin/carboplatin C-section) tumor AWD liver metastasis UTI Acute Donnenfeld Perforated invasive Induced vaginal Chest X-ray, CT abd, rd Tx (31 appendicitis Urgent open appy, 6 et al. (1986) 25 grade 1 mucinous No delivery colonoscopy 3 days after R hemicolectomy 9 days NA NA None - 30 days Healthy weeks) with abscess drain [24] adenocarcinoma (33 weeks) delivery peritonitis Well-differentiated mucinous Spontaneous nd Morgan et al. 2 Tx (26 Acute Urgent open R 36 mos, 7 vaginal delivery - None NA NA NA None - 30 adenocarcinoma, No - (2004) [25] weeks) abdomen hemicolectomy NED negative peritoneal (at term) washings Non-perforated Terminated Zeteroğlu Symptoms nd mucinous 2 Tx with R hemicolectomy, 1 yr, 8 et al. (2003) 35 No of acute Urgent appy - 3 days NA NA None NA NA appendiceal (21 weeks) misoprostol omentectomy NED [26] appendicitis cyctadenocarcinoma (21 weeks) Perforated Symptoms nd Casey et al. appendiceal 2 Tx 9 36 No of acute Open appy - - None NA NA NA - - - - (2003) [27] mucious (21 weeks) appendicitis cystadenoma Spontaneous Kalu and US due to miscarriage US at 5 weeks (adnexal st Mucus adenoma 1 Tx 10 Croucher 42 No vaginal None (anembryonic mass); US in 3 Mos Laparotomy/appy 3 mos NA NA None NA - NA with mucocele (5 weeks) (2004) [28] bleeding pregnancy) (enlarging ovarian mass) (7 weeks) Symptoms Spontaneous nd Idris et al. 2 Tx (22 1 yr, 11 35 Mucocele No of acute Open appy vaginal delivery - None NA NA NA None - - (2015) [29] weeks) NED appendicitis (at term) Case Reports in Oncological Medicine 5 Table 1: Continued. Time from Gestational Clinical Treatment during Pregnancy pregnancy Breast- # Author (year) Age Pathology PC Staging Treatment postpregnancy PCI CC score Complications Status Child age at dx presentation pregnancy outcome end to feeding treatment Symptoms Spontaneous st Gilboa et al. 1 Tx of acute Appy miscarriage -- - NANA - - - NA 12 31 Carcinoid tumor No (2008) [30] (9 weeks) appendicitis (5 days post-op) Symptoms § rd Louzi et al. Well-differentiated 3 Tx (34 Vaginal delivery 23 mos, 13 36 of acute Urgent appy No - R hemicolectomy 2 weeks NA NA - - Healthy (2006) [31] carcinoid tumor weeks) (35 weeks) NED appendicitis Well-differentiated MRI abd at 29 weeks, carcinoid with Symptoms Spontaneous normal 24-hour urine 5- nd Piatek et al. 2 Tx (25 1 yr, 14 28 gangrenous No of acute Appy vaginal delivery HIAA; whole body None NA NA NA None - Healthy (2016) [32] weeks) NED appendicitis (KI-67: appendicitis (38 weeks) SPECT 3 Mos after <1%) delivery Symptoms Spontaneous st Berrios 1 Tx Negative liver scan 23 mos, 15 23 Carcinoid tumor No of acute Appy vaginal delivery None NA NA NA - - Healthy (1965) [33] (2 months) during pregnancy NED appendicitis (at term) Symptoms Bleeding luteum st Berrios 1 Tx (10 of ruptured 16 26 Carcinoid tumor No cyst, incidental - - None NA NA NA - - No FU - (1965) [33] weeks) ectopic appy pregnancy Pitiakoudis Symptoms Spontaneous rd Carcinoid tumor 3 Tx (32 17 et al. (2008) 24 No of acute Appy vagina delivery - - - NA NA None - - Healthy (0.5 cm) weeks) [34] appendicitis (39 weeks) Symptoms nd Korkontzelos Carcinoid tumor 2 Tx C-section (36 0 days (at 18 23 No of acute Urgent appy - R hemicolectomy NA NA - - - Healthy (2005) [35] (2.2 cm) (16 weeks) weeks) C-section) appendicitis Article in French. The cases reporting peritoneal spread at presentation are in italics. 5-FU: 5-fluorouracil; 5-HIAA: 5-hydroxyindoleacetic acid; Abd: abdomen; Appy: appendectomy; AWD: alive with disease; Bx: biopsy; CC: completeness of cytoreduction; CRS/HIPEC: cytoreductive surgery with hyperthermic intraperitoneal chemotherapy; C-section: cesarean section; CT: computed tomography; DVT: deep vein thrombosis; Dx: diagnosis/diagnostic; FOLFOX: folinic acid+5-fluorouracil+oxaliplatin; IVF: in vitro fertilization; LAMN: low-grade appendiceal mucinous neoplasm; Lap: laparoscopy; Mit-C: mitomycin C; mos: months; NA: not applicable; NED: no evidence of disease; NGT: nasogastric tube; PC: peritoneal carcinomatosis; PCI: peritoneal cancer index; Pelv: pelvis; R: right; RDS: respiratory distress syndrome; SPECT: single-photon emission computed tomography; TPN: total parenteral nutrition; Tx: trimester; US: ultrasound; UTI: urinary tract infection; XELOX: capecitabine+oxaliplatin; Yr (s): year (s). 6 Case Reports in Oncological Medicine Table 2: Literature review of appendiceal tumors diagnosed during cesarean section. Clinical Author Gestational findings HIPEC C-section Postpartum CC Breast- # Age Pathology PC C-section indication Staging PCI Complications Status Child (year) age at dx during referral surgery treatment score feeding pregnancy Present Premature rapture of CT chest/abd/pelv 3 CRS/HIPEC (Mit-C) Prolonged 6 yrs, 1 31 LAMN Yes 40 weeks Uneventful Yes Appy 27 CC-0 3 mos Healthy case #2 membranes weeks after C-section in 3 months ileus NED Manan Well-differentiated Appy, removal Large size of previous Unknown (referred to Postpartum tumor 2 et al. 41 mucinous Yes At term Uneventful Yes of all gelatinous babies with outside facility for - - None - - Healthy markers (2010)[36] cystadenocarcinoma material complicated delivery CRS/HIPEC) Lower Well-differentiated Unknown (referred to Abdu et al. abdominal R Failure of cervical 3 36 mucinous Yes 40 weeks Yes - outside facility for - - - - - Healthy (2009) [37] pain at 37 hemicolectomy dilation adenocarcinoma CRS/HIPEC) weeks Inubashiri et al. Cephalopelvic CT scan 1 month after 4 24 LAMN No 38 weeks Uneventful NA Appy None NA NA None - 6 days Healthy (2019) disproportion C-section [38] Yohannes Fetal hypoxia, et al. CT abd/pelv after C- nd 5 31 LAMN No 38 weeks Uneventful NA Appy dysfunctional 2 None NA NA - - LTFU Healthy (2019) section stage of labor [39] Gallo et al. Well-differentiated Postpartum barium Dysfunctional 5 yrs, 6 (2001) 29 mucinous No 38 weeks Uneventful NA Appy enema, abdominal R hemicolectomy NA NA - - Healthy spontaneous delivery NED [40] cystadenocarcinoma scan, chest X-ray Berrios Cephalopelvic 7 (1965) 21 Carcinoid tumor No At term Uneventful NA Appy - - NA NA - - - Healthy disproportion [33] Berrios et al. 8 30 Carcinoid tumor No 38 weeks - NA Appy - - - NA NA - - No FU - (1965) [33] Gökaslan et al. 5 mos, 9 30 Carcinoid tumor No - - NA Appy - None None NA NA - - Healthy (2001) NED [41] The cases reporting peritoneal spread at presentation are in italics. Abd: abdomen; Appy: appendectomy; CC: completeness of cytoreduction; CRS/HIPEC: cytoreductive surgery with hyperthermic intraperitoneal chemotherapy; C-section: cesarean section; CT: computed tomography; Dx: diagnosis; FU: follow-up; LAMN: low-grade appendiceal mucinous neoplasm; LTFU: lost to follow-up; Mit-C: mitomycin C; mos: months; NA: not applicable; NED: no evidence of disease; PC: peritoneal carcinomatosis; PCI: peritoneal cancer index; Pelv: pelvis; Yrs: years. Case Reports in Oncological Medicine 7 Acute abdomen syndrome Incidental finding on prenatal screening (pelvic US) Incidental finding during C-section Urgent appendectomy, abdomen revision, Appendectomy, abdomen revision, Clarifying abdominal US AND/OR MRI peritoneal biopsy peritoneal biopsy at C-section • US-guided ascites aspiration with cytology in 3rd trimester OR • Laparoscopic/open appendectomy, abdomen revision, peritoneal biopsy in Staging with chest, abdominal, pelvic imaging any trimester AMN confined to appendix Mucin outside appendix and/or peritoneal carcinomatosis Referral to CRS/HIPEC center Referral to CRS/HIPEC center Without With rupture rupture Low-grade High-grade Low-grade High-grade AMN AMN AMN AMN st nd rd 1 2 3 Negative resection Positive resection trimester trimester trimester margin margin Discuss with patient Discuss with patient Discuss with patient Discuss with patient Discuss with patient Discuss with patient Discuss with patient Consider early Consider labor induction or Consider delivery Consider delivery Consider delivery Consider delivery Consider termination labor induction delivery at term at term at term at term at term • Restaging with chest, abdominal, pelvic imaging AND Surveillance Cecectomy Right hemicolectomy • Consider fertility preservation AND • CRS/HIPEC Figure 3: Algorithm of appendiceal mucinous neoplasm management diagnosed during pregnancy. The algorithm here is consistent with that for the first two scenarios except pregnancy management. AMN: mucinous appendiceal neoplasm; CRS/HIPEC: cytoreductive surgery with hyperthermic intraperitoneal chemotherapy; C-section: cesarean section; MRI: magnetic resonance imaging; PC: peritoneal carcinomatosis; US: ultrasound. studies showed that laparoscopic appendectomy is associated signs of acute abdomen (n =13 cases), (2) symptomatic or with higher fetal loss in pregnant women compared to open asymptomatic PC diagnosed incidentally during prenatal surgery [15]. At the same time, the largest study of almost screening (n =5 cases), and (3) AMN with/without PC inci- 20,000 pregnant women reported a higher risk of adverse dentally found on cesarean section (n =9 cases) (Tables 1 obstetrical events including miscarriages, preterm labor, and 2). Each of these scenarios requires a different strategy and intrauterine death after open surgery [16]. In case #1, to determine the optimal treatment plan and make decisions open appendectomy and peritoneal biopsy were performed, regarding pregnancy preservation and timing of definitive rather than full abdominal cavity exploration, for further his- treatment (Figure 3). The treatment of tumor confined to topathology assessment since PC had been already confirmed the appendix usually requires only local resection varying with MRI. from appendectomy/cecectomy for low-grade neoplasms to Regardless of the approach, surgical specimens obtained right hemicolectomy in high-grade tumors. Pregnant from the diagnostic surgery require meticulous pathologic patients with ruptured appendiceal lesions and/or peritoneal assessment. Frozen sections should not be used to diagnose involvement require CRS/HIPEC and should be referred to a appendiceal tumors due to their complex pathology and specialized peritoneal surface malignancy center as soon as low concordance between frozen sections and final pathology possible. Considering the various prognoses of AMN histo- pathologic subtypes, successful treatment does not always [17]. Fine needle biopsy of appendiceal neoplasm should also be avoided due to potential peritoneal spread and inadequate require pregnancy termination or early labor induction. sampling [18]. Given the rarity and complexity of appendi- Therefore, decisions regarding pregnancy management and ceal neoplasm histopathology, we recommend the removal preservation ought to be made case by case at a specialized of the entire appendix and revision of slides at a specialized peritoneal surface malignancy center by a multidisciplinary team including a CRS/HIPEC surgeon and gynecologist. peritoneal surface malignancy center as it can drastically affect the management [19]. In both presented cases, pathol- Thrombotic complications after CRS/HIPEC performed ogy assessment of specimens, including the entire primary in the postpartum period might be a specific hazard. In case appendiceal tumor and peritoneal biopsy, confirmed LAMN #1, the patient developed a rare and threatening complication with peritoneal spread which directed our delayed treatment of the portal and splenic vein thromboses. This condition is uncommon in the absence of cirrhosis and other causes of approach. AMN management depends on histopathologic subtype, portal hypertension and usually represents a hypercoagula- prognosis, and stage at presentation. Based on previously tive state [20]. Of 788 CRS/HIPEC procedures at our center, published and our cases, appendiceal tumors during preg- only 3 (0.4%) patients developed this complication. Gener- nancy usually present as one of the three clinical scenarios: ally, pregnancy and the postpartum period are associated with an increased risk of venous thrombosis compared to (1) local tumor with/without appendix rupture with clinical 8 Case Reports in Oncological Medicine nancy,” World Journal of Surgical Oncology, vol. 7, no. 1, p. 48, the general population with the highest risk in the postpar- tum period [21, 22]. Additionally, major surgeries and malig- nancies also exacerbate this risk [23]. Thus, postpartum [6] Y. Chiverto, E. Cabezas, T. Pérez-Medina, and L. 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Management of Low-Grade Appendiceal Mucinous Neoplasm with Extensive Peritoneal Spread Diagnosed during Pregnancy: Two Case Reports and Literature Review

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Hindawi Case Reports in Oncological Medicine Volume 2020, Article ID 8853704, 9 pages https://doi.org/10.1155/2020/8853704 Case Report Management of Low-Grade Appendiceal Mucinous Neoplasm with Extensive Peritoneal Spread Diagnosed during Pregnancy: Two Case Reports and Literature Review Ekaterina Baron , Vadim Gushchin , Mary Caitlin King , Andrei Nikiforchin , and Armando Sardi Department of Surgical Oncology, The Institute for Cancer Care at Mercy, Mercy Medical Center, 227 St. Paul Place, 4th Floor Weinberg, Baltimore, Maryland 21202-2001, USA Correspondence should be addressed to Armando Sardi; asardi@mdmercy.com Received 29 June 2020; Revised 30 September 2020; Accepted 3 October 2020; Published 15 October 2020 Academic Editor: Ossama W. Tawfik Copyright © 2020 Ekaterina Baron 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. Clinical decisions in patients with peritoneal dissemination of low-grade appendiceal mucinous neoplasms (LAMN) diagnosed during pregnancy are challenging. However, their slow progression and favorable prognosis allow deferring definitive treatment until after spontaneous delivery, a reasonable period of breastfeeding, and fertility preservation. Case Presentation. Two pregnant patients were incidentally diagnosed with LAMN and extensive peritoneal spread at 20 weeks gestation and at cesarean section. Treatment with cytoreductive surgery and hyperthermic intraperitoneal chemotherapy in both cases was delayed until spontaneous delivery at term and breastfeeding in the first patient and breastfeeding and fertility preservation in the second patient. Both patients remain disease-free for over 5 years, and their children are healthy. The literature review highlights the challenges that physicians face in treating pregnant patients with stage IV appendiceal tumors. Conclusion. Pregnancy management decisions in patients with peritoneal spread from mucinous appendiceal tumor should be based on understanding the tumor biology and prognosis. Definitive treatment in pregnant patients with favorable tumors, such as LAMN, may be delayed until spontaneous delivery without compromising maternal survival. 1. Introduction time, up to 20% of AMN present with peritoneal carcinoma- tosis (PC) [2], considered stage IV according to the American th Treating neoplasms diagnosed during pregnancy entails Joint Committee on Cancer (AJCC) 8 edition [3]. However, weighing the risks and benefits for both mother and fetus. excellent long-term outcomes can be achieved in AMN with This requires considering multiple factors, such as tumor cytoreductive surgery and hyperthermic intraperitoneal biology and prognosis, stage, gestational age at diagnosis, effi- chemotherapy (CRS/HIPEC) [4]. cacy, toxicity, invasiveness of required treatment, and patient Diagnosis of PC during pregnancy is often considered to preferences. Particularly, the management of stage IV tumors be a life-threatening condition where oncological concerns of with extensive dissemination during pregnancy poses addi- the mother outweigh fetal risks. In the few published cases of tional challenges because it demands rapid and complex PC from low-grade appendiceal tumors diagnosed during ethical decisions, which should be based on a deep under- pregnancy, all managed with early labor induction, early standing of tumor behavior and all available options. cesarean section, or pregnancy termination in favor of faster Appendiceal mucinous neoplasms (AMN) are a rare definitive treatment [5–8]. However, the favorable prognosis group of malignancies with high heterogeneity of histopath- and slow progression of LAMN, even with extensive PC, ologic subtypes and survival outcomes [1]. They range from allows performing CRS/HIPEC after spontaneous delivery, low-grade neoplasms with favorable prognosis to high- which minimizes fetal risks without compromising maternal grade tumors with significantly worse outcomes. At the same survival [9] We present two unique cases of LAMN with PC 2 Case Reports in Oncological Medicine MA MA (a) (b) Figure 1: (a) Abdominal and pelvic MRI (sagittal plane) without IV contrast shows a gravid uterus and a substantial amount of T2 hyperintense fluid. (b) Abdominal and pelvic MRI (coronal plane) without IV contrast demonstrates an enlarged perforated appendix with extraluminal mucin (arrow) and T2 hyperintense fluid collection in the pelvis. B: bladder; C: cervix; F: fetus; IV: intravenous; MA: mucinous ascites; MRI: magnetic resonance imaging; U: uterus. MA MA (a) (b) Figure 2: (a), (b) Abdominal and pelvic MRI without IV contrast ((a) coronal plane, (b) axial plane) shows a gravid uterus and significant amount of T2 hyperintense fluid, some of which is loculated with internal septations (arrows). B: bladder; F: fetus; IV: intravenous; MA: mucinous ascites; MRI: magnetic resonance imaging; P: placenta; U: uterus. diagnosed during pregnancy and managed with delayed progression as low and recommended to defer definitive CRS/HIPEC in the postpartum period accompanied by a treatment until the postpartum period. A healthy 2,950 g literature review. (6.6 lbs.) male was born by uncomplicated spontaneous vaginal delivery at 38 weeks gestation. Staging with computed tomogra- phy (CT) of the chest, abdomen, and pelvis revealed multiple 2. Case #1 bilateral subdiaphragmatic, omental, mesenteric, and liver cap- sule mucinous implants and no extraperitoneal metastases. A 31-year-old woman, gravida 2 para 1, with a history of asthma and anemia presented with a large intra-abdominal Tumor markers (CEA, CA 125, and CA 19-9) were normal. mass and ascites found incidentally on routine prenatal ultra- After 4 months of breastfeeding, the patient underwent CRS/HI- sound (US) at 20 weeks gestation. Prior to that, the patient PEC with 40 mg mitomycin-C heated to 41-42 Cfor 90 minutes had an uneventful pregnancy and skipped US during the first using the closed technique. The peritoneal cancer index (PCI) trimester prenatal screening. An ovarian primary tumor was (range 0-39) [10] was 37. The surgery lasted 708 minutes with suspected and abdominopelvic magnetic resonance imaging an estimated blood loss of 1,100 ml. Complete cytoreduction (MRI) without contrast was performed within one week. with residual small membranes on the small bowel (complete- MRI showed a disrupted appendiceal tip surrounded by soft ness of cytoreduction (CC) score 1) [4] was achieved. The post- tissues and fluid, as well as a substantial amount of abdomi- operative period was complicated by anemia requiring red blood nopelvic fluid with internal septations and debris, suggesting cell transfusion. The patient was discharged on postoperative an appendiceal mucinous neoplasm with PC (Figures 1(a), day (POD) 9 with deep vein thrombosis (DVT) prophylaxis 1(b), 2(a), 2(b)). Appendectomy, right salpingo-oophorec- (40 mg of enoxaparin daily). However, she was readmitted twice: tomy, omentectomy, and peritoneal biopsy were performed first with splenic and portal vein thrombosis (POD 15) and then at 21 weeks gestation and pathology confirmed LAMN with with rectal bleeding (POD 30) after subsequent increase in th cellular mucinous peritoneal implants (AJCC 8 anticoagulant dose. Regular follow-up included physical stage IVA). The patient was referred to a peritoneal surface malignancy examinations; imaging of the chest, abdomen, and pelvis; and center. Considering the favorable prognosis of LAMN even with tumor markers every 6 months. At 63 months of follow-up, extensive peritoneal spread, we assessed the risk of rapid tumor the patient remains disease-free and her child is healthy. Case Reports in Oncological Medicine 3 among peritoneal malignancy centers to treat patients with 3. Case #2 a peritoneal spread from AMN. In our center, we opted to A 31-year-old healthy woman, gravida 3 para 0, underwent delay CRS/HIPEC and allow the pregnancy to progress cesarean section at 40 weeks gestation due to premature rup- naturally. ture of membranes and protracted labor and delivered a The approach to delay definitive treatment in our cases healthy 3,561 g (7.9 lbs.) male newborn. The patient had a was based on the well-known favorable prognosis of LAMN history of lower back pain and mild anemia throughout the with extensive peritoneal spread treated with CRS/HIPEC. pregnancy and started experiencing diarrhea at 35 weeks. Two previously published cases of well-differentiated appen- The full prenatal screening, including US in each trimester, diceal adenocarcinoma with PC, which currently is consid- revealed only an echogenic intracardiac focus of the fetus. ered to be the same grade (G1) and prognostic stage (IVA) Otherwise, the pregnancy was uneventful. During cesarean as LAMN, managed their patients with early labor induction section, mucin originating from the appendix tip was found (35 weeks) and early cesarean section (33 weeks) followed by adherent to the uterus, right ovary, and fallopian tube. CRS/HIPEC in 2.5 weeks and 2 months, respectively [3, 5, 7]. Appendectomy and peritoneal biopsy were performed, and Moreover, Haase et al. proposed managing peritoneal surface th pathology showed LAMN with PC (AJCC 8 stage IVA). malignancies diagnosed during pregnancies with early induc- The chest, abdominal, and pelvic CT scan 3 weeks after tion and delaying treatment to 35 weeks if diagnosed in the nd delivery showed perihepatic and perisplenic capsular 2 trimester [5]. However, labor at 34-37 weeks of gestation implants. Tumor marker assessment showed elevated CEA refers to late preterm delivery and is associated with up to 8.8 ng/ml (N 0-5 ng/ml) and normal CA 125 and CA increased risk for numerous complications for the infant 19-9. Definitive treatment was delayed for breastfeeding and should be avoided when possible [11]. We believe that and oocyte retrieval for cryopreservation of 4 embryos. Three the histopathology and disease pathogenesis must be consid- months postdelivery, the patient underwent CRS/HIPEC ered carefully before inducing early delivery or termination. nd with 90-minute perfusion of 40 mg mitomycin-C heated to In case #1, the diagnosis was made in the 2 trimester (20 41-42 C. PCI was 27, and a complete cytoreduction was weeks) during routine prenatal screening. Previous studies achieved (CC-score 0) after 487 minutes of surgery. The demonstrate an excellent prognosis of LAMN patients with patient was discharged on POD 8 without major complica- 5-year overall survival up to 80-96% 9, 12]. This data suggests tions. She was readmitted several times over the last 5 years that the slow progression of LAMN allows for a natural with small bowel obstructions that resolved nonoperatively. progression of pregnancy and deferring CRS/HIPEC for a Three years after CRS/HIPEC, the patient had a second child reasonable period. Therefore, we opted to postpone CRS/HI- via surrogate maternity using a frozen embryo. The follow- PEC for 8 months in case #1 until spontaneous at term deliv- up was the same as the previous case. After 67 months, the ery with subsequent breastfeeding and for 4 months in case patient is disease-free and her children are doing well. #2 for breastfeeding and fertility preservation without compromising survival outcomes in either case as it is onco- logically safe. 4. Discussion Diagnosing and staging AMN might be challenging dur- ing pregnancy due to the limited availability of safe diagnostic The presented patients were diagnosed with a rare appendi- ceal tumor and PC at an advanced gestational age of preg- methods and nonspecific clinical presentation. Considering nancy: 20 weeks and 40 weeks during cesarean section. To patient and fetus risks, only tests that may influence clinical our knowledge, these are the first published cases of perito- management should be performed. Once peritoneal spread neal spread from LAMN diagnosed during pregnancy man- or local appendiceal tumor is suspected during prenatal pelvic aged with delayed CRS/HIPEC, which, for patient #1, US, additional imaging is required for staging and making allowed spontaneous delivery of a healthy baby at 38 weeks decisions regarding diagnostic surgery. Abdominopelvic MRI with 4 months of breastfeeding and, for patient #2, 3 months without contrast is a safe and informative alternative to CT of breastfeeding and cryopreservation of embryos that were during pregnancy for clarifying the diagnosis of peritoneal eventually used successfully. lesions [13, 14]. The MRI in case #1 demonstrated a disrupted Diagnosis of PC at any stage of pregnancy is dramatic appendiceal tip and signs of mucin distributed throughout the and associated with multiple challenges for both physician abdomen and pelvis (Figures 1 and 2). These findings shifted and patient. While there are numerous reports of appendi- our focus from initially suspected ovarian origin to appendi- ceal tumors diagnosed during pregnancy (Tables 1 and 2), ceal tumor and directed the diagnostic surgery. we found only 6 with PC: 4 diagnosed during pregnancy Defining histopathologic subtype and stage is crucial for and 2 of diagnosed during cesarean section. Of the four cases establishing treatment in patients with PC. We believe that diagnosed during pregnancy, one was managed with preterm diagnostic open or laparoscopic surgery for appendectomy, induction of labor at 35 weeks, two were managed with an peritoneal biopsy, and thorough revision of the abdomen early cesarean section at 30 and 33 weeks, and one was termi- and pelvis is reasonable and should be performed in all nated at 18 weeks [5–8]. The time of definitive treatment in patients with PC on imaging regardless of pregnancy stage. the two cases diagnosed at cesarean section is unknown as Laparoscopy has advantages in this case as it allows inspect- patients were referred to outside facilities [10, 11]. This may ing the majority of the abdominal cavity, including the upper demonstrate that pregnancy termination or early labor abdomen. However, the use of laparoscopy in pregnant induction with rushing CRS/HIPEC is a common strategy women is controversial. A meta-analysis of 11 retrospective 4 Case Reports in Oncological Medicine Table 1: Literature review of appendiceal tumors diagnosed during pregnancy. Time from Gestational Clinical Treatment during Pregnancy pregnancy Breast- # Author (year) Age Pathology PC Staging Treatment postpregnancy PCI CC score Complications Status Child age at dx presentation pregnancy outcome end to feeding treatment POD 15: portal 4 mos Routine Appy, Spontaneous MRI abd/pelv at 20 vein nd Present case 2 Tx +12 mos 5 yrs, 1 31 LAMN Yes prenatal omentectomy, vaginal delivery weeks; CT chest/abd/pelv CRS/HIPEC (Mit-C) 4 mos 37 CC-1 thrombosis Healthy #1 (20 weeks) milk NED screening RSO, peritoneal bx (38 weeks) after delivery POD 30: rectal donor bleeding Neutropenia, Well-differentiated Routine Early induce CRS/HIPEC (Mit- nd Haase et al. 2 Tx (17 Appy, RSO, prolonged ileus 5 yrs, 2 30 mucinous Yes prenatal vaginal delivery CT after delivery C) + EPIC (5-FU); 2.5 weeks 28 CC-1 - Healthy (2010) [5] weeks) omental bx (NGT, TPN), NED adenocarcinoma screening (35 weeks) adjuvant XELOX x8 cycles DVT Infiltrating Colonoscopy, CT CRS/HIPEC (5-FU nd Chiverto et al. mucinous 2 Tx Abdominal Terminated 10 mos, 3 36 Yes Dx lap, open appy chest/abd/pelv after + Oxaliplatin; adjuvant - 6 Complete - NA NA (18 weeks) pain x4 days with misoprostol (2012) [6] adenocarcinoma NED termination FOLFOX x6 Mos (T3N1M1a) Routine Laparoscopic R RDS Well-differentiated prenatal adnexectomy, prophylaxis; CRS/HIPEC (Mit-C No Canuto et al. mucinous 2 yrs, st 4 38 Yes 1 Tx screening (R peritoneal early C-section - + Cisplatin); adjuvant 2 mos - residual -- Healthy (2016) [7] adenocarcinoma NED ovarian washing/bx (16 (33 weeks, 5 FOLFOX x8 cycles tumor (pT4apN1) mass) weeks, 4 days) days) Moderately Abdominal rd Sebire et al. differentiated 3 Tx (29 pain, C-section (30 Abd US (29 weeks); fine- CRS; adjuvant 5- 0 days (at Residual 6 mos, 5 29 Yes None - -- Healthy (2000) [8] adenocarcinoma; weeks) vomiting, weeks) needle liver bx FU/Epirubicin/carboplatin C-section) tumor AWD liver metastasis UTI Acute Donnenfeld Perforated invasive Induced vaginal Chest X-ray, CT abd, rd Tx (31 appendicitis Urgent open appy, 6 et al. (1986) 25 grade 1 mucinous No delivery colonoscopy 3 days after R hemicolectomy 9 days NA NA None - 30 days Healthy weeks) with abscess drain [24] adenocarcinoma (33 weeks) delivery peritonitis Well-differentiated mucinous Spontaneous nd Morgan et al. 2 Tx (26 Acute Urgent open R 36 mos, 7 vaginal delivery - None NA NA NA None - 30 adenocarcinoma, No - (2004) [25] weeks) abdomen hemicolectomy NED negative peritoneal (at term) washings Non-perforated Terminated Zeteroğlu Symptoms nd mucinous 2 Tx with R hemicolectomy, 1 yr, 8 et al. (2003) 35 No of acute Urgent appy - 3 days NA NA None NA NA appendiceal (21 weeks) misoprostol omentectomy NED [26] appendicitis cyctadenocarcinoma (21 weeks) Perforated Symptoms nd Casey et al. appendiceal 2 Tx 9 36 No of acute Open appy - - None NA NA NA - - - - (2003) [27] mucious (21 weeks) appendicitis cystadenoma Spontaneous Kalu and US due to miscarriage US at 5 weeks (adnexal st Mucus adenoma 1 Tx 10 Croucher 42 No vaginal None (anembryonic mass); US in 3 Mos Laparotomy/appy 3 mos NA NA None NA - NA with mucocele (5 weeks) (2004) [28] bleeding pregnancy) (enlarging ovarian mass) (7 weeks) Symptoms Spontaneous nd Idris et al. 2 Tx (22 1 yr, 11 35 Mucocele No of acute Open appy vaginal delivery - None NA NA NA None - - (2015) [29] weeks) NED appendicitis (at term) Case Reports in Oncological Medicine 5 Table 1: Continued. Time from Gestational Clinical Treatment during Pregnancy pregnancy Breast- # Author (year) Age Pathology PC Staging Treatment postpregnancy PCI CC score Complications Status Child age at dx presentation pregnancy outcome end to feeding treatment Symptoms Spontaneous st Gilboa et al. 1 Tx of acute Appy miscarriage -- - NANA - - - NA 12 31 Carcinoid tumor No (2008) [30] (9 weeks) appendicitis (5 days post-op) Symptoms § rd Louzi et al. Well-differentiated 3 Tx (34 Vaginal delivery 23 mos, 13 36 of acute Urgent appy No - R hemicolectomy 2 weeks NA NA - - Healthy (2006) [31] carcinoid tumor weeks) (35 weeks) NED appendicitis Well-differentiated MRI abd at 29 weeks, carcinoid with Symptoms Spontaneous normal 24-hour urine 5- nd Piatek et al. 2 Tx (25 1 yr, 14 28 gangrenous No of acute Appy vaginal delivery HIAA; whole body None NA NA NA None - Healthy (2016) [32] weeks) NED appendicitis (KI-67: appendicitis (38 weeks) SPECT 3 Mos after <1%) delivery Symptoms Spontaneous st Berrios 1 Tx Negative liver scan 23 mos, 15 23 Carcinoid tumor No of acute Appy vaginal delivery None NA NA NA - - Healthy (1965) [33] (2 months) during pregnancy NED appendicitis (at term) Symptoms Bleeding luteum st Berrios 1 Tx (10 of ruptured 16 26 Carcinoid tumor No cyst, incidental - - None NA NA NA - - No FU - (1965) [33] weeks) ectopic appy pregnancy Pitiakoudis Symptoms Spontaneous rd Carcinoid tumor 3 Tx (32 17 et al. (2008) 24 No of acute Appy vagina delivery - - - NA NA None - - Healthy (0.5 cm) weeks) [34] appendicitis (39 weeks) Symptoms nd Korkontzelos Carcinoid tumor 2 Tx C-section (36 0 days (at 18 23 No of acute Urgent appy - R hemicolectomy NA NA - - - Healthy (2005) [35] (2.2 cm) (16 weeks) weeks) C-section) appendicitis Article in French. The cases reporting peritoneal spread at presentation are in italics. 5-FU: 5-fluorouracil; 5-HIAA: 5-hydroxyindoleacetic acid; Abd: abdomen; Appy: appendectomy; AWD: alive with disease; Bx: biopsy; CC: completeness of cytoreduction; CRS/HIPEC: cytoreductive surgery with hyperthermic intraperitoneal chemotherapy; C-section: cesarean section; CT: computed tomography; DVT: deep vein thrombosis; Dx: diagnosis/diagnostic; FOLFOX: folinic acid+5-fluorouracil+oxaliplatin; IVF: in vitro fertilization; LAMN: low-grade appendiceal mucinous neoplasm; Lap: laparoscopy; Mit-C: mitomycin C; mos: months; NA: not applicable; NED: no evidence of disease; NGT: nasogastric tube; PC: peritoneal carcinomatosis; PCI: peritoneal cancer index; Pelv: pelvis; R: right; RDS: respiratory distress syndrome; SPECT: single-photon emission computed tomography; TPN: total parenteral nutrition; Tx: trimester; US: ultrasound; UTI: urinary tract infection; XELOX: capecitabine+oxaliplatin; Yr (s): year (s). 6 Case Reports in Oncological Medicine Table 2: Literature review of appendiceal tumors diagnosed during cesarean section. Clinical Author Gestational findings HIPEC C-section Postpartum CC Breast- # Age Pathology PC C-section indication Staging PCI Complications Status Child (year) age at dx during referral surgery treatment score feeding pregnancy Present Premature rapture of CT chest/abd/pelv 3 CRS/HIPEC (Mit-C) Prolonged 6 yrs, 1 31 LAMN Yes 40 weeks Uneventful Yes Appy 27 CC-0 3 mos Healthy case #2 membranes weeks after C-section in 3 months ileus NED Manan Well-differentiated Appy, removal Large size of previous Unknown (referred to Postpartum tumor 2 et al. 41 mucinous Yes At term Uneventful Yes of all gelatinous babies with outside facility for - - None - - Healthy markers (2010)[36] cystadenocarcinoma material complicated delivery CRS/HIPEC) Lower Well-differentiated Unknown (referred to Abdu et al. abdominal R Failure of cervical 3 36 mucinous Yes 40 weeks Yes - outside facility for - - - - - Healthy (2009) [37] pain at 37 hemicolectomy dilation adenocarcinoma CRS/HIPEC) weeks Inubashiri et al. Cephalopelvic CT scan 1 month after 4 24 LAMN No 38 weeks Uneventful NA Appy None NA NA None - 6 days Healthy (2019) disproportion C-section [38] Yohannes Fetal hypoxia, et al. CT abd/pelv after C- nd 5 31 LAMN No 38 weeks Uneventful NA Appy dysfunctional 2 None NA NA - - LTFU Healthy (2019) section stage of labor [39] Gallo et al. Well-differentiated Postpartum barium Dysfunctional 5 yrs, 6 (2001) 29 mucinous No 38 weeks Uneventful NA Appy enema, abdominal R hemicolectomy NA NA - - Healthy spontaneous delivery NED [40] cystadenocarcinoma scan, chest X-ray Berrios Cephalopelvic 7 (1965) 21 Carcinoid tumor No At term Uneventful NA Appy - - NA NA - - - Healthy disproportion [33] Berrios et al. 8 30 Carcinoid tumor No 38 weeks - NA Appy - - - NA NA - - No FU - (1965) [33] Gökaslan et al. 5 mos, 9 30 Carcinoid tumor No - - NA Appy - None None NA NA - - Healthy (2001) NED [41] The cases reporting peritoneal spread at presentation are in italics. Abd: abdomen; Appy: appendectomy; CC: completeness of cytoreduction; CRS/HIPEC: cytoreductive surgery with hyperthermic intraperitoneal chemotherapy; C-section: cesarean section; CT: computed tomography; Dx: diagnosis; FU: follow-up; LAMN: low-grade appendiceal mucinous neoplasm; LTFU: lost to follow-up; Mit-C: mitomycin C; mos: months; NA: not applicable; NED: no evidence of disease; PC: peritoneal carcinomatosis; PCI: peritoneal cancer index; Pelv: pelvis; Yrs: years. Case Reports in Oncological Medicine 7 Acute abdomen syndrome Incidental finding on prenatal screening (pelvic US) Incidental finding during C-section Urgent appendectomy, abdomen revision, Appendectomy, abdomen revision, Clarifying abdominal US AND/OR MRI peritoneal biopsy peritoneal biopsy at C-section • US-guided ascites aspiration with cytology in 3rd trimester OR • Laparoscopic/open appendectomy, abdomen revision, peritoneal biopsy in Staging with chest, abdominal, pelvic imaging any trimester AMN confined to appendix Mucin outside appendix and/or peritoneal carcinomatosis Referral to CRS/HIPEC center Referral to CRS/HIPEC center Without With rupture rupture Low-grade High-grade Low-grade High-grade AMN AMN AMN AMN st nd rd 1 2 3 Negative resection Positive resection trimester trimester trimester margin margin Discuss with patient Discuss with patient Discuss with patient Discuss with patient Discuss with patient Discuss with patient Discuss with patient Consider early Consider labor induction or Consider delivery Consider delivery Consider delivery Consider delivery Consider termination labor induction delivery at term at term at term at term at term • Restaging with chest, abdominal, pelvic imaging AND Surveillance Cecectomy Right hemicolectomy • Consider fertility preservation AND • CRS/HIPEC Figure 3: Algorithm of appendiceal mucinous neoplasm management diagnosed during pregnancy. The algorithm here is consistent with that for the first two scenarios except pregnancy management. AMN: mucinous appendiceal neoplasm; CRS/HIPEC: cytoreductive surgery with hyperthermic intraperitoneal chemotherapy; C-section: cesarean section; MRI: magnetic resonance imaging; PC: peritoneal carcinomatosis; US: ultrasound. studies showed that laparoscopic appendectomy is associated signs of acute abdomen (n =13 cases), (2) symptomatic or with higher fetal loss in pregnant women compared to open asymptomatic PC diagnosed incidentally during prenatal surgery [15]. At the same time, the largest study of almost screening (n =5 cases), and (3) AMN with/without PC inci- 20,000 pregnant women reported a higher risk of adverse dentally found on cesarean section (n =9 cases) (Tables 1 obstetrical events including miscarriages, preterm labor, and 2). Each of these scenarios requires a different strategy and intrauterine death after open surgery [16]. In case #1, to determine the optimal treatment plan and make decisions open appendectomy and peritoneal biopsy were performed, regarding pregnancy preservation and timing of definitive rather than full abdominal cavity exploration, for further his- treatment (Figure 3). The treatment of tumor confined to topathology assessment since PC had been already confirmed the appendix usually requires only local resection varying with MRI. from appendectomy/cecectomy for low-grade neoplasms to Regardless of the approach, surgical specimens obtained right hemicolectomy in high-grade tumors. Pregnant from the diagnostic surgery require meticulous pathologic patients with ruptured appendiceal lesions and/or peritoneal assessment. Frozen sections should not be used to diagnose involvement require CRS/HIPEC and should be referred to a appendiceal tumors due to their complex pathology and specialized peritoneal surface malignancy center as soon as low concordance between frozen sections and final pathology possible. Considering the various prognoses of AMN histo- pathologic subtypes, successful treatment does not always [17]. Fine needle biopsy of appendiceal neoplasm should also be avoided due to potential peritoneal spread and inadequate require pregnancy termination or early labor induction. sampling [18]. Given the rarity and complexity of appendi- Therefore, decisions regarding pregnancy management and ceal neoplasm histopathology, we recommend the removal preservation ought to be made case by case at a specialized of the entire appendix and revision of slides at a specialized peritoneal surface malignancy center by a multidisciplinary team including a CRS/HIPEC surgeon and gynecologist. peritoneal surface malignancy center as it can drastically affect the management [19]. In both presented cases, pathol- Thrombotic complications after CRS/HIPEC performed ogy assessment of specimens, including the entire primary in the postpartum period might be a specific hazard. In case appendiceal tumor and peritoneal biopsy, confirmed LAMN #1, the patient developed a rare and threatening complication with peritoneal spread which directed our delayed treatment of the portal and splenic vein thromboses. This condition is uncommon in the absence of cirrhosis and other causes of approach. AMN management depends on histopathologic subtype, portal hypertension and usually represents a hypercoagula- prognosis, and stage at presentation. Based on previously tive state [20]. Of 788 CRS/HIPEC procedures at our center, published and our cases, appendiceal tumors during preg- only 3 (0.4%) patients developed this complication. Gener- nancy usually present as one of the three clinical scenarios: ally, pregnancy and the postpartum period are associated with an increased risk of venous thrombosis compared to (1) local tumor with/without appendix rupture with clinical 8 Case Reports in Oncological Medicine nancy,” World Journal of Surgical Oncology, vol. 7, no. 1, p. 48, the general population with the highest risk in the postpar- tum period [21, 22]. Additionally, major surgeries and malig- nancies also exacerbate this risk [23]. Thus, postpartum [6] Y. Chiverto, E. Cabezas, T. Pérez-Medina, and L. 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Case Reports in Oncological MedicineHindawi Publishing Corporation

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