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ORIGINAL ARTICLE  
Year : 2022  |  Volume : 65  |  Issue : 3  |  Page : 565-571
Mucinous appendiceal neoplasms and pseudomyxoma peritonei: Morphological and clinical findings, differential diagnosis, and prognosis


1 Department of Pathology, Kayseri City Training and Research Hospital, Kayseri, Turkey
2 Department of Radiation Oncology, Kayseri City Education and Research Hospital, Kayseri, Turkey
3 Department of General Surgery, Kayseri City Training and Research Hospital, Kayseri, Turkey
4 Department of Medical Oncology, Kayseri City Training and Research Hospital, Kayseri, Turkey

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Date of Submission15-Aug-2021
Date of Decision13-Jan-2022
Date of Acceptance23-Jan-2022
Date of Web Publication08-Jun-2022
 

   Abstract 


Background: Low-grade appendiceal mucinous neoplasms (LAMN) of the appendix have bland cytological features and well-differentiated morphology. Despite this, they may cause a pseudomyxoma peritonei (PMP) disease characterized by mucinous deposits in the peritoneal cavity and may exhibit malignant behavior. Aims and Objectives: In this study, we evaluated the clinical course and histopathological findings of LAMN. The rate of progression to PMP, factors affecting its development, and the clinical course of cases with PMP were investigated. Materials and Methods: Twelve thousand and forty-seven cases who underwent appendectomy were reviewed, and 71 mucinous lesions cases whose slides are in our archive were included in the study. Histopathological findings were re-evaluated. Morphological findings that guide the differential diagnosis, the clinical course of the patients, and factors affecting PMP development were determined. Results: The cases were divided into group 1 non-neoplastic (9.9%), group 2 benign (18.3%), group 3 LAMN (60.6), and group 4 malignant neoplasms (11.3%). Age, gender, appendix diameter, gross appearance, epithelial characteristics, and presence of microcalcification were significantly different between the patient groups. The presence of mucin in the ileocecal region was found to be significant in the development of PMP. It was observed that the additional procedure performed after the appendectomy did not prevent a recurrence. Conclusion: LAMNs are lesions with characteristic findings and different behaviors. The only method to distinguish from the lesions included in the differential diagnosis is to interpret the histopathological findings correctly. Additional operations after appendectomy do not contribute to preventing recurrence.

Keywords: Appendix, low-grade appendiceal mucinous neoplasm, mucinous lesions, prognosis, pseudomyxoma peritonei

How to cite this article:
Akay E, Arslan A, Eren SK, Özhan N, Karaman H. Mucinous appendiceal neoplasms and pseudomyxoma peritonei: Morphological and clinical findings, differential diagnosis, and prognosis. Indian J Pathol Microbiol 2022;65:565-71

How to cite this URL:
Akay E, Arslan A, Eren SK, Özhan N, Karaman H. Mucinous appendiceal neoplasms and pseudomyxoma peritonei: Morphological and clinical findings, differential diagnosis, and prognosis. Indian J Pathol Microbiol [serial online] 2022 [cited 2022 Aug 15];65:565-71. Available from: https://www.ijpmonline.org/text.asp?2022/65/3/565/351622





   Introduction Top


Low-grade appendiceal mucinous neoplasms (LAMN) of the appendix have bland cytological features and well-differentiated morphology. Despite this, they may cause a pseudomyxoma peritonei (PMP) disease characterized by mucinous deposits in the peritoneal cavity and may exhibit malignant behavior.[1],[2] Different terminologies have been used in the past for similar lesions of LAMN, such as mucocele, mucinous adenoma, mucinous cystadenoma, mucinous tumor with uncertain malignant potential, borderline mucinous tumor, low-grade mucinous adenocarcinoma, and low-grade mucinous neoplasm with high recurrence risk.[3],[4],[5] Different nomenclatures have caused uncertainty for clinicians in estimating the management and course of the disease. In terms of pathologists, the lack of standard criteria in diagnosing the disease resulted in high diagnostic discrepancies in consultations between different centers.[6],[7]

In 2016, the Peritoneal Surface Oncology Group International (PSOGI) consensus was realized. The aim was to agree on common terminology, distinguish between invasive and non-invasive mucinous neoplasms, and identify criteria that could identify those at risk of developing PMP[1]. Thus, the long-standing confusion of terminology in the naming and classification of mucinous neoplasms of the appendix has ended.

The most common cause of PMP is LAMN. Although it is low-grade, the fact that it causes PMP indicates that LAMNs still have unknown aspects.

The aims of this study are to evaluate the clinical course and histopathological findings of an appendiceal mucinous lesions in our center, to investigate the presence of findings other than the morphological findings determined in the PSOGI consensus, to examine the differential diagnosis of mucinous lesions, and to determine the progression rate to PMP, the factors affecting the development of PMP, and the clinical course of patients who develop PMP.


   Materials and Methods Top


Our study was approved by the Clinical Research Ethics Committee of Kayseri City Hospital (Protocol No. 2021/397). The pathology laboratory information system was reviewed between June 2009 and June 2019 in the Pathology Clinic of Kayseri City Training and Research Hospital. Using the keywords appendix and appendectomy, 12047 appendectomy materials were found. Patients diagnosed with an appendiceal mucinous lesion were selected. Seventy-one patients diagnosed with an appendiceal mucinous lesion were selected and their sample slides were re-evaluated. The type of initial surgical procedure, the gross appearance of the appendix, its diameter (mm), the follow-up period of the patients, the operation procedure if there is an additional operation afterward, and their survival were obtained. The appendiceal mucinous neoplasms were classified and staged according to WHO 2019, 5th edition.[2] The number of hematoxylin and eosin-stained slides reviewed ranged from 1–34 (mean 5.2). For each appendix, the following parameters were recorded: the dominant feature of the neoplastic epithelium (flat, undulating, villous) [Figure 1]a, [Figure 1]b, [Figure 1]c, muscularis mucosal loss (absent, focal loss, complete loss), fibrosis/hyalinization, microcalcification, dissection of the wall with mucin, infiltrative destructive pattern of invasion, extension (expansion, diverticulum-like, dissecting), rupture of the appendix, serosal mucin/presence of cells in mucin, surgical resection margin of the appendix, stage of tumor, and whether the entire appendix was sampled or not. The cellularity of mucin was determined in PMP cases. The location of the organ or region involved in PMP was recorded. The degree of cellular mucin was cytologically graded depending on the presence of low grade (grade 1), high grade (grade 2), and signet ring cells (grade 3).[2]
Figure 1: (a) A cross-section of a case of LAMN with a flat epithelium. The lamina propria under the epithelium has disappeared and is replaced by fibrous connective tissue (HE ×50). (b) LAMN covered by undulating epithelium, (HE ×25). (c) LAMN covered by villiform epithelium (HE ×50). (d) Hyperplastic polyp of appendix (HE ×50). (e) HE section of the serrated lesion. The lamina propria and muscularis mucosa are preserved. Dilatation at the bases of the crypts draws attention (HE ×25). (f) Complete loss of surface epithelium is a common artifact in LAMNs (HE ×25)

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Because two patients were consultation cases and two patients continued their treatment in another center, information about the follow-up status of four patients could not be obtained.

The conformity of the data to the normal distribution was evaluated with histogram, q-q graphs, and Shapiro-Wilk test. Pearson χ2 analysis was used to compare categorical data. Univariate and multivariate logistic regression analyses were applied to determine the risk factors of the PMP variable. P < 0.25 significant variables were included in the multiple models, and the Forward LR method was applied to determine the independent risk factors. Risk ratios are given with 95% confidence intervals. Data were evaluated with R 3.6.2 software (www.r-project.org). Significance level was accepted as P < 0.05.


   Results Top


The cases were 41 (57.7%) male and 30 (42.3%) female (M/F ratio: 1.37), and mean age was 49.69 ± 17.24 (median 50). Of the samples, 65 were appendectomy material, 4 were right hemicolectomy, and 2 were appendectomy material with a total abdominal hysterectomy and bilateral salpingo-oophorectomy (TAH-BSO). Complementary right hemicolectomy was performed in 6 of 65 appendectomy cases, and peritoneum was sampled simultaneously in 3 of them. Lymph node metastasis was not detected in 10 cases with lymph nodes for histological examination (pN0). The entire appendix was sampled in 45 (63.4%) cases.

The cases were grouped as group 1 non-neoplastic (9.9%), group 2 benign lesions (18.3%), group 3 LAMN (60.6), and group 4 malignant neoplasms (11.3%). The histopathological findings are given in [Table 1]a, and the clinical and prognostic findings are given in [Table 1]b.


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Group 1, non-neoplastic: Three had diverticulum [Figure 2]b, 3 had mucosal hyperplastic changes secondary to acute appendicitis, and 1 had retention cyst. Overall survival (OS) was 55.4 months (14–111 months). None of the patients in the non-neoplastic group had a peritoneal recurrence or mucinous neoplasia during the follow-up.
Figure 2: (a) Microcalcification foci are seen in the acellular mucin (HE ×100). (b) At low magnification, an apendicial diverticulum has a central lumen with surrounding mucosa (HE ×25). (c) A case of LAMN with growth in a diverticular pattern. There is fibrotic stroma under the epithelium. Lack of lymphoid tissue and loss of lamina propria in the diverticular patern of the LAMNs are characteristic findings (HE ×25). (d) Sections of mucinous adenocarcinoma, mucin lined with malignant epitehelial cells (arrow) (HE ×25). (e) In PMP, ovarian sections are observed on the right side, and mucin containing a small number of malignant cells is observed on the left side (HE ×25). (f) PMP composed of acellular mucin (HE ×100)

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Group 2, Benign lesions: Six cases were diagnosed as hyperplastic polyps, and 7 were diagnosed as serrated lesions [Figure 1]d, [Figure 1]e. Clinical follow-up of 1 patient could not be reached. Peritoneal recurrence or mucinous neoplasia was not observed in any of the other 11 cases during follow-up.

Group 3, LAMN: Forty-one cases were diagnosed as LAMN. Fourteen (32.6%) of the pT4 cases were pT4a, and 1 of them was pT4b (2.3%). There was 1 (2.3%) case with the epithelium of LAMN at the resection margin and 1 (2.3%) case had villous architecture in the epithelium without dysplasia. The patient who had a positive surgical margin did not have any further surgical intervention and there was no sign of recurrence in the 17th month of follow-up. The patient who had with villous architecture at the resection margin, faced a recurrence 8 months after the operation. The appendix diameter of this case was 30 mm, the stage was pT4a, and there was a macroscopic rupture of the appendix. Villous architecture at the proximal surgical margin of the case, free acellular mucin in the ileocecal serosa (ileocecal mucin), and acellular mucin in the biopsy taken over the omentum were observed (pM1a). Although the patient underwent right hemicolectomy after an appendectomy, recurrence developed. The patient is in the 18th month of follow-up. In 1 of the LAMN cases, invasion of neighboring organs was present at the first presentation (pT4b, M1a). The patient is alive, and his OS is 83 months.

There were no high-grade appendiceal mucinous neoplasms in our series.

Group 4, Malignant: There were 8 appendiceal carcinomas in the malignant group, of which 6 were adenocarcinoma NOS (including 3 cases mucinous adenocarcinoma, 2 cases nonmucinous adenocarcinoma, and 1 case signet ring cell carcinoma) and 2 were appendiceal goblet cell adenocarcinoma. Two patients (25%) with pT4a had mucinous adenocarcinoma and, 6 (75%) cases were pT3, their overall survival was respectively 53 and 17 months, and they were followed up without recurrence. In the follow-up of the case with signet ring cell carcinoma, liver metastasis was observed, and the patient died due to the disease in the 41st month. One patient died of non-disease reason at 56th month. In [Table 1]b, the follow-up and events of all groups are summarized.

There was a statistically low but significant difference between the groups in terms of gender due to the fact that all patients in the non-neoplastic group were male (P = 0.048). It was determined that the age difference between the groups was statistically significant (P = 0.002), and the difference was due to the age of the patients in group 4 being higher than those in groups 1 and 3 (P = 0.001 and P = 0.023, respectively). The median value of tumor diameter was 11 (4–60) mm, and there was statistical significance between the groups. It was observed that the difference was due to the tumor diameters of the patients in groups 3 and 2 (P = 0.002). There was a statistically significant difference between the groups because none of the cases in Groups 1 and 2 had microcalcifications, but Groups 3 and 4 had microcalcifications (P = 0.013). There was a statistically significant difference between the epithelial features and the groups (P < 0.001). It was determined that the difference was due to the fact that the flat and undulating epithelial variants in group 3 were more than in the other groups.

In 3 cases with PMP, the diagnosis was LAMN. The rate of PMP development in our LAMN cases was 6.97%. The mean follow-up period of our PMP cases is 52.3 months, and they are alive. Recurrence was not observed in two cases with negative proximal surgical margins. In contrast, recurrence was observed in the case with villous architecture at the surgical margin despite right hemicolectomy after appendectomy. The diameter of the appendix was larger in this case compared to the others. The clinical-pathological findings of the cases developing PMP are given in [Table 2]a.


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In [Table 2]b, the factors that affected the PMP variable were evaluated with single and multiple binary logistic regression analyses. According to the results of single binary logistic regression analysis, the risk effects of recurrence and the presence of mucin in the ileocecal region on the PMP variable were found to be statistically significant (P = 0.047 and P = 0.020, respectively). The risk ratios for these variables were found to be 25 and 20, respectively. According to the multiple binary logistic regression analysis results, when the recurrence and ileocecal musin variables were evaluated as risk effects on the PMP variable, only the ileocecal musin variable remained in the model. This variable's risk ratio and confidence interval was found to be 0.05 (0.01–0.62).


   Discussion Top


Most of the appendiceal neoplasms are detected incidentally.[8] Mucinous lesions are encountered in approximately 0.3% of appendectomies.[9] The rate of mucinous lesions in our series was 0.48%.

Mucinous neoplasms of the appendix are grouped under three main headings: polyps, mucinous neoplasms, and adenocarcinomas.[1] Polypoid lesions of the appendix are hyperplastic polyps and serrated lesions. Luminal mucin in some serrated lesions and sometimes serrated architecture in LAMNs can make it difficult to distinguish between the two lesions. Preservation of the appendix's mucosal architecture, dilatation at the bases of crypt, eosinophilic cytoplasm of cells, and prominence of goblet cells favor serrated lesions.[6] It is recommended to be classified as LAMN in cases with serrated lesion and LAMN findings together if the lesion sits on a fibrotic wall and diverticulum-like protrusions.[3]

LAMNs are common in 6th-decade women in the literature.[9],[10] In our study, the F/M ratio was 1.1, and the mean age was 48.6 years in our LAMN cases. Our average age is younger than the literature. The average age of our male patients is 41.4 years, and the average age of our female patients is 55.4 years. The F/M ratios in large series are approximately 2.[5],[10],[11] In the studies, the number of female cases is higher than in our study.[5],[9],[10],[11] From this, it can be concluded that LAMN occurs at a younger age in male cases than in females.

The findings of LAMNs were loss of muscularis mucosae, submucosal fibrosis, undulating or flattened epithelial growth, “pushing” or diverticulum-like growth into the wall, dissecting acellular mucin, rupture of appendix and mucin, and/or neoplastic cells outside the appendix.[1] In our study, loss of muscularis mucosa was observed in all of our cases diagnosed with LAMN and 50% of our malignant cases. There was no loss of muscularis mucosa in the benign and non-neoplastic groups (P < 0.001). Submucosal fibrosis was detected in 72.1% of our LAMN cases and 25% of malignant cases (P < 0.001). The finding that was not among the morphological findings but found statistically significant among our groups was the presence of microcalcification (P = 0.013) [Table 1]a. In our series, calcification accompanying mucin in the lumen or the wall was detected in 16 cases (15 LAMN, 1 mucinous adenocarcinoma). In our study, the rate of microcalcification in LAMNs was 35% [Figure 2]a. Similarly, in the study of Carr et al.,[12] no microcalcification was found in the benign group. We think that microcalcification and other findings will help in the diagnosis and differential diagnosis of LAMN.

Surface epithelial loss is common in mucinous lesions of the appendix [Figure 1]f. This artifact, which we encountered in most of our LAMN cases showing dilatation with mucin increase, is very severe in 18.6% of cases. The only way to overcome this situation is to sample the entire tissue in mucinous neoplasms.[5],[10],[11],[13],[14]

High-grade appendiceal mucinour neoplasms (HAMNs) are neoplasms characterized by high-grade mucinous epithelial proliferation with/without extracellular mucin and pushing tumor margins.[1],[2] There were no HAMNs in our series.

Mucin in the appendix wall can also occur in non-neoplastic conditions such as diverticulum. The distinction between LAMN, which grows in a diverticulum-like pattern, and a ruptured appendicial diverticulum, has been studied, and despite the flattening of the epithelium, the preservation of the mucosal architecture and non-neoplastic epithelium are helpful findings favoring the diverticulum.[15],[16],[17],[18] It has been reported that 42% of LAMNs are associated with diverticulum.[15] In our series, this rate is 20.9%. In ruptured diverticulum cases, mucin outflow from the appendix is not a risk factor for PMP; thus, the distinction is very important in patient follow-up.[16]

It has been suggested that the progression of LAMNs in a diverticulum-like pattern plays a role in PMP formation [Figure 2]c.[15],[17] In our study, PMP did not develop in any of our 20.9% LAMN cases that showed growth in a diverticulum-like pattern. Although diverticulum in LAMNs causes perforation and allows mucin to escape out of the appendix and into the periappendicular region, we support the view that unless the tumor has a biological capacity, it will not cause PMP development.[10]

Mucinous adenocarcinomas, which are included in the differential diagnosis of LAMN, constitute 40% of all appendiceal adenocarcinomas.[9] This rate was 37.5% in our breakdown of cases in group 4. The most important criterion in distinguishing between mucinous adenocarcinoma and LAMN is the absence of destructive infiltrative invasion in LAMN. Findings such as the presence of desmoplasia, small abortive infiltrative glands, tumor budding, and cellular mucin pools [Figure 2]d are in favor of adenocarcinoma.[1],[2]

PMP has colon, pancreatic, ovarian, and urachal cancers in its etiology, but the most common cause is mucinous neoplasms of the appendix.[3],[10],[19] They show slow growth, and metastasis capacity is quite low unless it is high grade.[19],[20]

In LAMN-associated PMP, 5-year survival is 63%–91%, and 10-year survival is 45%–68% (10,19). In our series, PMP developed in 6.97% of our LAMN cases. The follow-up period of the cases was 52.3 (18-56-83) months, and 3 of them were alive too.

Among the factors affecting PMP development, many variables such as the stage of the tumor, the cellularity of the mucin, mucin in the surrounding organs other than the appendix, and the condition of the surgical margins have been investigated. The development of PMP in pT4a tumors is between 5% and 75%.[5],[13],[19] In our study, PMP developed in 14.3% of our 14 pT4a cases. In our cases, the mucin was acellular, and recurrence occurred in one of them. It has been suggested that in cases with recurrence despite being acellular, there may be an incomplete evaluation due to the incomplete sampling of the appendix.[5],[13] In our series, the appendix of the case was fully sampled in 45 cases. As in the appendix, 190 PMP cases were examined in a study on the sampling procedure of tissues belonging to PMP cases, and the presence of epithelial cells in the mucin was detected when the sampling numbers of those with acellular mucin in the first samples were increased.[21] It is clear that there must be mucin-producing cells somewhere in these lesions. As the authors stated, it seems that the density of the cells will become important, not the presence.[10],[21]

Our other LAMN case stage that developed PMP was pTis, mucin cellular, and low epithelial grade [Table 2]a [Figure 2]e, [Figure 2]f. Thus, our case shows that LAMNs, even with pTis, can cause PMP.

The mean follow-up period of our 8 cases with pT3 was 39 (16–69) months, and PMP did not develop. It has been suggested that the pT3 stage behaves like pTis, and its existence is controversial.[11] In our study, we observed that PMP developed even in the case of pTis. pT3 cases also have this risk. However, after more data, it can be predicted that the pT3 stage can also be included in pTis, similar to the fact that pT1 and pT2 stages are not used in LAMNs.

An important point in the prognosis is the condition of the proximal surgical margin. In the literature on this subject, no significant difference was observed in the follow-up of patients with acellular mucin who underwent and did not undergo cecal resection; therefore, additional resection was not recommended.[22] It has been reported that resection margin positivity is not among the factors determining recurrence.[23] The procedure applied in each center is different. In our center, 3 of our LAMN cases underwent right hemicolectomy with an additional operation after appendectomy. Despite right hemicolectomy, PMP developed in one case [Table 2a].

It has been reported that CRS-HIPEC can be applied in the treatment of PMP if there is a response to the treatment with cytoreductive surgery and hyperthermic intraperitoneal chemotherapy (CRS-HIPEC) in Grade 1 and systemic chemotherapy in Grade 2 and 3.[24] Cytoreductive surgery was performed in our grade 1 case.

In summary, LAMNs are rare lesions with distinctive findings and different behaviors. The only method for other lesions that cause difficulties in the differential diagnosis is the correct interpretation of histopathological findings. We suggest that in the presence of microcalcification, in addition to the determined morphological criteria, more careful examination is required before the lesion can be diagnosed as benign.

With the consensus in naming and classification, clinicians contributed to the interpretation of the disease. In this way, a more consistent approach will be displayed in patient management. Due to the limited data on pTis and pT3 tumors, the behavior of tumors with these stages, whether the pT3 stage is included in the pTis category, and the factors that affect the formation of PMP need to be clarified. Additional operations after appendectomy do not contribute to preventing recurrence. In conclusion, the behavior of LAMNs and the causes of PMP remain a mystery, and the cases need to be contributed to the literature.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
   References Top

1.
Carr NJ, Cecil TD, Mohamed F, Leslie HS, Sugarbaker PH, González-Moreno S, et al. A Consensus for classification and pathologic reporting of pseudomyxoma peritonei and associated appendiceal neoplasia: The results of the Peritoneal Surface Oncology Group International (PSOGI) modified Delphi process. Am J Surg Pathol 2016;40:14-26.  Back to cited text no. 1
    
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Nagtegaal ID, Klimstra DS, Washington MK. Tumours of the appendix. In: Lokuhetty D, White V A, Watanabe R, Cree I A, editors. WHO Classification of Tumours Digestive System. 5th ed. Lyon: International Agency for Research on Cancer; 2019. p. 135-51.  Back to cited text no. 2
    
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Carr NJ, Bibeau F, Bradley RF, Dartigues P, Feakins RM, Geisinger KR, et al. The histopathological classification, diagnosis and differential diagnosis of mucinous appendiceal neoplasms, appendiceal adenocarcinomas and pseudomyxoma peritonei. Histopathology 2017;71:847-58.  Back to cited text no. 3
    
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Misdraji J. Mucinous epithelial neoplasms of the appendix and pseudomyxoma peritonei. Mod Pathol 2015;28:67-79.  Back to cited text no. 4
    
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Pai RK, Beck AH, Norton JA, Longacre TA. Apendiceal mucinous neoplasms: Clinicopathologic study of 116 cases with analysis of factors predicting recurrence. Am J Surg Pathol 2009;33:1425-39.  Back to cited text no. 5
    
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Arnold CA, Graham RP, Jain D, Kakar S, Lam-Himlin DM, Naini BV, et al. Knowledge gaps in the appendix: A multi-institutional study from seven academic centers. Mod Pathol 2019;32:988-96.  Back to cited text no. 6
    
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Valasek MA, Thung I, Gollapalle E, Hodkoff AA, Kelly KJ, Baumgartner JM, et al. Overinterpretation is common in pathological diagnosis of appendix cancer during patient referral for oncologic care. PLoS One 2017;12:e0179216.  Back to cited text no. 7
    
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Gundogar O, Kimiloglu E, Komut N, Cin M, Bektas S, Gonullu D, et al. Evaluation of appendiceal mucinous neoplasms with a new classification system and literature review. Turk J Gastroenterol 2018;29:533–42.  Back to cited text no. 8
    
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Paşaoğlu E, Dursun N. The current approach to appendiceal mucinous neoplasms and pseudomyxoma peritonei. J Curr Pathol 2018;2:46-56.  Back to cited text no. 9
    
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Ballentine SJ, Carr J, Bekhor EY, Sarpel U, Polydorides AD. Updated staging and patient outcomes in low-grade appendiceal mucinous neoplasms. Mod Pathol 2021;34:104–15.  Back to cited text no. 10
    
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Bell PD, Huber AR, Drage MG, Barron SL, Findeis-Hosey JJ, Gonzalez RS. Clinicopathologic features of low-grade appendiceal mucinous neoplasm: A single-institution experience of 117 cases. Am J Surg Pathol 2020;44:1549-55.  Back to cited text no. 11
    
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Carr NJ, McCarthy WF, Sobin LH. Epithelial noncarcinoid tumors and tumor-like lesions of the appendix. A clinicopathologic study of 184 patients with a multivariate analysis of prognostic factors. Cancer 1995;75:757-68.  Back to cited text no. 12
    
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Yantiss RK, Shia J, Klimstra DS, Hahn HP, Odze RD, Misdraji J. Prognostic significance of localized extra-appendiceal mucin deposition in appendiceal mucinous neoplasms. Am J Surg Pathol 2009;33:248-55.  Back to cited text no. 13
    
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Umetsu SE, Shafizadeh N, Kakar S. Grading and staging mucinous neoplasms of the appendix: A case series and review of the literature. Hum Pathol 2017;69:81-9.  Back to cited text no. 14
    
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Lamps LW, Gray GF, Dilday BR, Washington MK. The coexistence of low grade mucinous neoplasms of the appendix and apendiceal diverticula: A possible role in the pathogenesis of pseudomyxoma peritonei. Mod Pathol 2000;13:495-501.  Back to cited text no. 15
    
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Hsu M, Young RH, Misdraji J. Ruptured appendiceal diverticula mimicking low-grade appendiceal mucinous neoplasms. Am J Surg Pathol 2009;33:1515-21.  Back to cited text no. 16
    
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Pasaoglu E, Leblebici C, Okcu O, Boyaci C, Dursun N, Yardimci HA, et al. The relationship between diverticula and low-grade mucinous neoplasm of the appendix. Does the diverticulum play a role in the development of periappendicular mucin deposition or pseudomyxoma peritonei? Pol J Pathol 2016;67:376-83.  Back to cited text no. 17
    
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Hissong E, Goncharuk T, Song W, Yantiss RK. Post-inflammatory mucosal hyperplasia and appendiceal diverticula simulate features of low-grade appendiceal mucinous neoplasms. Mod Pathol 2020;33:953-61.  Back to cited text no. 18
    
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Davison JM, Choudry HA, Pingpank JF, Ahrendt SA, Holtzman MP, Zureikat AH, et al. Clinicopathologic and molecular analysis of disseminated appendiceal mucinous neoplasms: Identification of factors predicting survival and proposed criteria for a three-tiered assessment of tumor grade. Mod Pathol 2014;27:1521-39.  Back to cited text no. 19
    
20.
Bradley RF, Stewart JHt, Russell GB, Levine EA, Geisinger KR. Pseudomyxoma peritonei of appendiceal origin: A clinicopathologic analysis of 101 patients uniformly treated at a single institution, with literature review. Am J Surg Pathol 2006;30:551-9.  Back to cited text no. 20
    
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Al-Azzawi M, Misdraji J, van Velthuysen MF, Shia J, Taggart MW, Yantiss RK, et al. Acellular mucin in pseudomyxoma peritonei of appendiceal origin: What is adequate sampling for histopathology? J Clin Pathol 2020;73:220–2.  Back to cited text no. 21
    
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Arnason T, Kamionek M, Yang M, Yantiss RK, Misdraji J. Significance of proximal margin involvement in low grade appendiceal mucinous neoplasms. Arch Pathol Lab Med 2015;139:518-21.  Back to cited text no. 22
    
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Foster JM, Gupta PK, Carreau JH, Grotz TE, Blas JV, Gatalica Z, et al. Right hemicolectomy is not routinely indicated in pseudomyxoma peritonei. Am Surg 2012;78:171-7.  Back to cited text no. 23
    
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Bijelic L, Kumar AS, Stuart OA, Sugarbaker PH. Systemic chemotherapy prior to cytoreductive surgery and HIPEC for carcinomatosis from appendix cancer: Impact on perioperative outcomes and short-term survival. Gastroenterol Res Pract 2012;2012:163284.  Back to cited text no. 24
    

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Correspondence Address:
Ebru Akay
Kayseri City Training and Research Hospital, Pathology, 38100 Kocasinan/Kayseri
Turkey
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/ijpm.ijpm_827_21

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