Original Article Prognostic and clinicopathologic significance of AEG-1/MTDH and E-cadherin expression in human gallbladder carcinoma

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1 Int J Clin Exp Pthol 2018;11(12): /ISSN: /IJCEP Originl Article Prognostic nd clinicopthologic significnce of AEG-1/MTDH nd E-cdherin expression in humn gllbldder crcinom Song-To Xu 1,3*, Yong-Cho M 2*, Ci-Hong Wng 4*, Yue Xu 5*, Guo-Jin Gu 6,7 Deprtments of 1 Clinicl, 2 Bsic Medicl Science, Luohe Medicl College, Luohe, Henn, PR Chin; 3 Innovtive Science nd Technologicl Tem of Tumor Occurrence nd Prevention in Henn Province, Luohe, Henn Province, PR Chin; Deprtments of 4 Medicl Imging, 5 Neurosurgery, 6 Pthology, Ticng Affilited Hospitl of Soochow University, Ticng, Jingsu, PR Chin; 7 Deprtment of Pthology, The First People s Hospitl of Ticng, Ticng, Jingsu, PR Chin. * Equl contributors. Received October 5, 2018; Accepted October 25, 2018; Epub December 1, 2018; Published December 15, 2018 Abstrct: Astrocyte elevted gene-1 (AEG-1) nd E-cdherin re ssocited with tumorigenesis nd progression. The im of this study is to investigte the expression of AEG-1 nd E-cdherin in humn gllbldder cncer (GBC) nd explore their clinicl nd pthologicl significnce. The expression of AEG-1 nd E-cdherin protein were detected in 71 cses of humn GBC nd 22 cses of tumor-djcent tissue by the immunohistochemicl method. Our results demonstrte tht the positive expression (high expression) rte of AEG-1 ws 62.0% in humn GBC which ws higher thn tht in tumor-djcent tissues (13.6%), P< The positive expression of AEG-1 protein ws correlted with tumor TNM clssifiction, histologic grde, nd lymph node metstsis (P=0.037, P=0.033 nd P=0.020, respectively). The positive expression rte of E-cdherin ws 40.8% in GBC, which ws lower thn tht in tumor-djcent tissues (77.3%), P= Negtive expression (Low expression) of E-Cdherin ws significntly relted with tumor TNM clssifiction, histologic grde nd lymphtic metstsis (P=0.028, P=0.003 nd P=0.040, respectively). The expression of AEG-1 ws negtively correlted with the expression of E-Cdherin (r=0.530, P<0.001). The log-rnk test sttisticl nlysis suggested tht ptients with positive expression of AEG-1 or negtive expression of E-Cdherin protein hd shorter overll survivl time. Cox multivrite nlysis showed tht tumor TNM clssifiction, histologic grde nd lymphtic metstsis, AEG-1 nd E-cdherin expression were independent fctors for prognosis of GBC (P=0.013, P=0.019, P=0.001, P=0.011 nd P=0.025 respectively). In conclusion, positive expression of AEG-1 nd negtive expression of E-Cdherin re mrkedly correlted with tumor TNM clssifiction, histologic grde nd lymphtic metstsis. The expression of AEG-1 ws negtively correlted with the expression of E-Cdherin. Cox multivrite nlysis showed tht tumor TNM clssifiction, histologic grde nd lymphtic metstsis, positive expression of AEG-1 nd negtive expression of E-Cdherin were risk fctors for prognosis of GBC. Detection of AEG-1 nd E-Cdherin my be helpful to evlute prognosis nd infiltrtive cpbility of gllbldder crcinom. Keywords: AEG-1, gllbldder crcinom, survivl, E-cdherin, prognosis Introduction Gllbldder crcinom is the most common mlignnt tumor of the biliry system. There were 145,203 new cses of GBC in the world, ccounting for 1.1% of ll cses of the new mlignnt tumors in 2008 [1]. GBC s erly symptoms re not obvious, nd it presents t dvnced stge. Therefore, ptients will miss the opportunity of rdicl resection, nd the 5 yer survivl rte is poor [2] mking erly dignosis importnt. At present, the dignosis of GBC minly relies on non-invsive uxiliry imging nd trumtic exmintion, such s lproscopy nd biopsy. However, there is still lck of idel tumor mrkers for the dignosis nd prognosis of GBC. Astrocyte elevted gene-1 (AEG-1) lso is nmed Metdherin (MTDH) or LYRIC, nd is locted on humn chromosome 8 (8 q22) [3, 4]. Mny studies hve found tht AEG-1 is highly

2 Tble 1. Expression of AEG-1 nd E-cdherin in gllbldder crcinom nd tumor-djcent tissue Relted Fctor Gllbldder crcinom tissue Tumor-djcent tissue Negtive (-) Positive (+) Negtive (-) Positive (+) P Vlue AEG-1 27 (38.0) 44 (62.0 ) 19 (86.4 ) 3 (13.6) <0.001 E-cdherin 42 (59.2) 29 (40.8 ) 5 (22.7) 17 (77.3) Tble 2. Anlysis of AEG-1 nd E-cdherin positive expression nd relted fctors Relted Fctor n AEG-1 expression E-cdherin expression P Vlue Negtive (-) Positive (+) Negtive (-) Positive (+) P Vlue Sex Mle (44.8) 16 (55.2) (69.0) 9 (31.0) Femle (33.3) 28 (66.7) 22 (52.4) 20 (47.6) Age (yer) (37.2) 27 (62.8) (36.1) 18 (63.9) < (42.9) 16 (57.1) 17 (60.7) 11 (39.3) Tumor size (cm) < (47.5) 21 (52.5) (55.0) 18 (45.0) (25.8 ) 23 (74.2) 20 (16.0) 11 (84.0) TNM clssifiction I-II (53.8) 12 (46.2) (42.3) 15 (57.7) III-IV (28.9) 32 (71.1) 31 (68.9) 14 (31.1) Histologic grde Well + moderte (46.0) 27 (54.0) (48.0) 26 (52.0) Poor 21 4 (19.0) 17 (81.0) 18 (85.7) 3 (14.3) Lymphtic metstsis No (46.2) 28 (53.8) (51.9) 25 (48.1) Yes 19 3 (15.8) 16 (84.2) 15 (78.9) 4 (21.1) expressed in cncer tissues such s bldder cncer, lung cncer nd humn Retinoblstom, which cn inhibit cell poptosis, nd promote tumor ngiogenesis, nd cell prolifertion, invsion [5-7]. E-cdherin is locted on 16q22.1 chromosome, nd is clcium-medited cell dhesion molecule tht medites cell-cell contcts nd mintins norml epithelil cell integrity [8, 9]. It is well-known tumor cell prolifertion nd metstsis suppressor protein, nd the down regultion or loss of its expression is treted s moleculr mrker of epithelil-mesenchyml trnsition (EMT) [10-12]. EMT is ssocited with cncer invsion nd tumor progression. It cn cuse cells to lose polrity nd cell-cell contct nd some tumor cells to detch nd metstsize [13, 14]. However, the role of AEG-1 nd E-cdherin in gllbldder crcinom hs rrely been reported. In this study, we explored the expression of AEG-1 nd E-cdherin in 71 cses of gllbldder crcinom by SP immunohistochemistry. The im is to find convenient tool for the dignosis nd prognosis of the GBC. Mterils nd methods Ptients nd tissue smples The study protocol ws pproved by the ethics committee of the Ticng Affilited Hospitl of Soochow University. 71 cses of GBC nd 22 cses of tumor-djcent tissues smples were collected nd ptients with pproprite informed consent from Mrch 2011 to Mrch The verge ge of the 71 ptients who underwent surgery therpy ws 64.8 rnging 6026 Int J Clin Exp Pthol 2018;11(12):

3 Figure 1. AEG-1 were positive expression in GBC tissues nd its cytoplsm ws stined brown (200 ) (A). AEG-1 hd negtive expression in GBC tissues nd its cells were not stined (200 ) (B). E-cdherin were positive expression in GBC tissues nd its cell membrne or cytoplsm ws stined yellow (200 ) (C). E-cdherin were not expressed in GBC (200 ) (D). from 45 to 82 yers old. TNM clssifiction system ws proposed by Americn Joint Committee on Cncer (AJCC) in 2010 [15]. GBC ptients in the experimentl group were shown in Tbles 1 nd 2. All sections were confirmed s GBC by pthologists. They were followed up for 3 to 72 months vi telephone. None of these ptients received pre-opertive chemotherpy or rdiotherpy. Immunohistochemistry Immunohistochemicl nlysis ws performed s previously [5, 16]. In brief, ll specimens were cut into 4 μm sections nd bked, followed by deprffinized nd rehydrted. The specimens were incubted 10 min by 3% H 2 O 2, then they were incubted in citric cid buffer solution nd boiled. The sections were incubted with rbbit nti-humn AEG-1 ntibody (1:100; Wuhn Boster Biologicl Technology, Ltd; Wuhn, Chin) or rbbit nti-humn E-Cdherin ntibody (1:100 Wuhn Boster Biologicl Technology, Ltd; Wuhn, Chin), overnight t 4 C. After wshing with phosphte buffer sline (PBS), the specimens received secondry ntibody (Wuhn Boster Biologicl Technology, Ltd; Wuhn, Chin). The specimens more thn or equl to 4, nd negtive (-, low expression) when score ws less thn 4 [5]. Sttisticl nlysis The GrphPd Prism version 5.0 nd SAS 9.3 softwre were used for sttisticl nlysis. Chisqure test ws crried out with ctegoricl vribles. The overll survivl rtes were conducted with the Kpln-Meier method. Multivrite nlysis ws used for the Cox proportionl hzrds model. P-vlues <0.05 ws considered significnt. Results were incubted with streptvidin-horserdish peroxidse, nd DAB (Wuhn Boster Biologicl Technology, Ltd; Wuhn, Chin) ws droped for visuliztion nd followed by hemtoxylin counter-stining. The norml non-immune serum ws replced by AEG-1 or E-cdherin ntibody s negtive controls. Evlution of AEG-1 nd E- cdherin stining The stining intensity score ws 0 (negtive), 1 (light yellow), 2 (yellow brown), nd 3 (brown). The rte of positive cells is 0 (0%), 1 (0-50%), 2 (51-100%). The proportionl score nd the intensity score were dded to give the totl score. The expression ws defined s positive (+, high expression) when score ws AEG-1 nd E-cdherin expression in GBC nd tumor-djcent tissue As shown in Figure 1, AEG-1 stining ws predominntly observed in the cytoplsm of tumor cells (Figure 1A). E-cdherin stining ws predominntly observed on the cell membrne or cytoplsm of tumor cells (Figure 1C). The expression level of AEG-1 in the tumor ws significntly incresed compred with tumor-djcent tissue (P<0.001; Tble 1). The expression level of E-cdherin in the tumor ws significnt Int J Clin Exp Pthol 2018;11(12):

4 Figure 2. Kpln-Meier survivl curves of GBC ptients bsed on AEG-1 expression (A) or E-cdherin expression (B). ly decresed compred with tumor-djcent tissue (P=0.003; Tble 1). AEG-1 nd E-cdherin expression were ssocited with clinicopthologic chrcteristics of GBC The prognostic vlues of vribles were further tested by Cox multivrite nlysis. This showed tht tumor TNM clssifiction, histologic grde, lymph node metstsis, AEG- 1, nd E-cdherin expression were independent fctors for prognosis of GBC (P=0.013, P=0.019, P=0.019, P=0.001, P=0.011 nd P=0.025 respectively), Tble 3. TNM clssifiction, histologic grde nd lymphtic metstsis, positive expression of AEG-1, negtive expression of E-cdherin were risk fctors for prognosis. Correltions between AEG-1 nd E-cdherin expression in GBC tissue AEG-1 nd E-cdherin protein expression nd clinicopthologic fetures of GBC were exmined, s shown in Tble 2. Positive expression (high expression) rte of AEG-1 ws 62.0% in GBC, which ws higher thn in tumor-djcent tissues (13.6%), P< Positive of AEG-1 protein ws correlted with tumor TNM clssifiction, histologic grde, nd lymph node metstsis (P=0.037, P=0.033 nd P=0.020, respectively). However, AEG-1 protein expression ws not ssocited with sex, ge nd tumor size. Negtive expression (low expression) of E-Cdherin ws significntly relted with tumor TNM clssifiction, histologic grde, nd lymph node metstsis (P=0.028, P=0.003 nd P=0.040, respectively). However, E-cdherin protein expression ws not ssocited with sex, ge, nd tumor size. AEG-1 nd E-cdherin expression correlte with survivl in ptients with GBC Correltions re shown in Figure 2. Kpln- Meier survivl curves of GBC ptients re bsed on AEG-1 nd E-cdherin expression. Ptients with positive expression of AEG-1 protein showed significntly worse survivl compred with those with negtive expression (P<0.001, log-rnk test) (Figure 2A). Ptients with negtive E-cdherin protein showed significntly worse survivl compred with those ptients who were positive (P=0.027, log-rnk test) (Figure 2B). In GBC tissues, the expression of AEG-1 protein ws negtively correlted with the expression of E-cdherin protein (r=-0.530, P<0.001), Tble 4. Discussion Studies hve shown tht AEG-1 ctivtes different pthwys tht promote the development of tumors. First, it ctivtes the PI3K/AKT signl pthwy to promote cell prolifertion. Kikuno found tht the prolifertion of prostte cncer cells incresed significntly fter silencing of AEG-1, AKT ws upregulted, nd FOXO3 nd p27 were upregulted [17]. AEG-1 cn ctivte the NF-κB (nucler fctor kpp B) signl pthwy, further inducing cell prolifertion, ngiogenesis, invsion, nd metstsis [18, 19]. In ddition, AEG-1 overexpression promotes EMT in lung cncer by ctivting Wnt/β-ctenin signling, cusing tumor cell detchment nd metstsis to distnt tissues [20]. In the study, the positive rte of AEG-1 protein in GBC cells ws significntly higher thn tht in the prcncerous tissue (P<0.05). The positive rte of AEG-1 ws reltively higher in ptients with lymph node metstsis nd it incresed with the increse of TNM clssifiction, nd histologic grde. This indictes tht AEG-1 plys role in the occurrence nd development of gllbldder cncer, nd cn be used for n uxiliry mrker. The study found tht ptients with AEG-1 positive expression hd shorter overll survivl time compred with those with neg Int J Clin Exp Pthol 2018;11(12):

5 Tble 3. COX nlyses of different clinicopthologic vribles nd AEG-1 nd E-cdherin expression sttus s predictors for overll survivl in in gllbldder crcinom tissues Vrible Hzrd Rtio tive expression of AEG-1 [21, 22]. Our follow-up results lso showed tht ptients with positive expression of AEG-1 hd poor prognosis. Cox multivrite nlysis lso suggested tht positive expression of AEG-1 ws n independent risk fctor for prognosis of GBC. This suggests tht the AEG-1 protein is good prognostic mrker. With the development of moleculr biology technology, mny scholrs found tht knockdown of AEG-1 could inhibit the tumor cell migrtion nd invsion [4, 23, 24]. These suggested tht it might be potentil gene therpeutic trget for tumor. Mny studies hve found tht E-cdherin is low expression (negtive expression) in cncer tissues, nd ptients with low expression of E-cdherin hd shorter overll survivl time compred with those ptients with overexpression (positive expression) of E-cdherin [25-27]. In the study, the positive rte of E-cdherin protein in gllbldder cncer cells ws significntly lower thn tht in the prcncerous tissue (P<0.05). The positive rte of E-cdherin ws reltively lower in the ptients with lymph 95% Hzrd Rtio Confidence Limits node metstsis, nd it decresed with the increse of TNM clssifiction, nd histologic differentition grde. It indictes tht the loss of E-cdherin plys role in gllbldder tumor development, nd cn be used for the uxiliry dignosis of gllbldder crcinom. Our followup results lso showed tht ptients with negtive expression of E-cdherin hd poor prognosis. Cox multivrite nlysis lso suggested tht negtive expression of E-cdherin ws risk fctor for prognosis of GBC. Our study lso found tht AEG-1 ws overexpressed, while the expression of E-cdherin protein in gllbldder crcinom ws low, nd they were negtively correlted. This indicted tht AEG-1 hs regultory effect for E-cdherin protein. It is similr toprevious studies tht AEG-1 overexpression induces EMT by ctivting Wnt/β-ctenin signling, leding to the down-regultion of E-cdherin [20]. However, the fctors nd mechnisms tht ffect the occurrence nd development of tumors re very complex. We studied AEG-1 nd E-cdherin expression by immunohistochemistry only, which is limittion of the present study. In future studies, we cn knock down the expression of AEG-1 nd study its role in the occurrence nd development of GBC s well s for E-cdherin. Conclusion p vlue Sex (Mle vs. Femle) Age ( 65 vs. <65) Tumor size (<2.5 vs. 2.5) TNM clssifiction (I-II vs. III-IV) Histologic grde (well moderte vs. poor) Lymphtic metstsis (no vs. yes) AEG-1 (positive vs. negtive) E-cdherin (positive vs. negtive) Tble 4. Correltions between AEG-1 nd E- cdherin expression in gllbldder crcinom tissues E-cdherin AEG-1 Contingency + - coefficien (r) < χ 2 P Positive expression of AEG-1 or lost expression of E-cdherin were n importnt biomrker for progression, metstsis, nd prognosis in GBC. Ptients with positive expression of AEG-1 or negtive expression of E-cdherin hd poor survivl. AEG-1 hs n djustment effect for E-cdherin protein. They were negtively correlted. Positive expression of AEG-1 or negtive expression of E-cdherin correltes with lymph node metstsis, TNM clssifiction, nd histologicl differentition grde. Further work is wrrnted on these trgets in gllbldder crcinom Int J Clin Exp Pthol 2018;11(12):

6 Acknowledgements This work is supported by () the 2015 bsic nd dvnced technology reserch project of Henn Province, P. R. C. (No ), nd (b) Fundmentl Reserch Progrm (Applied foundtionl Reserch on Medicl nd Helth) of Ticng, Jingsu, PR Chin. (no. TC2018JCYL17). Disclosure of conflict of interest None. Address correspondence to: Guo-Jin Gu, Deprtment of Pthology, Ticng Affilited Hospitl of Soochow University, 58 South Chngsheng Street, Ticng , Jingsu, PR Chin. Tel: ; Fx: ; E-mil: References [1] Ferly J, Shin HR, Bry F, Formn D, Mthers C nd Prkin DM. Estimtes of worldwide burden of cncer in 2008: GLOBOCAN Int J Cncer 2010; 127: [2] Stinton LM nd Shffer EA. Epidemiology of gllbldder disese: cholelithisis nd cncer. Gut Liver 2012; 6: [3] Lee SG, Kng DC, DeSlle R, Srkr D nd Fisher PB. AEG-1/MTDH/LYRIC, the beginning: initil cloning, structure, expression profile, nd regultion of expression. Adv Cncer Res 2013; 120: [4] Wng Y, Wng T, Sun Y, Sun W nd Wng X. Astrocyte elevted gene-1 promotes tumour growth nd invsion by inducing EMT in orl squmous cell crcinom. Sci Rep 2017; 7: [5] Xu S, Gu G, Ni Q, Li N, Yu K, Li X nd Liu C. The expression of AEG-1 nd Cyclin D1 in humn bldder urothelil crcinom nd their clinicopthologicl significnce. Int J Clin Exp Med 2015; 8: [6] M Z, Chen Y, Dong S, Xu X, Liu J, Song P, Yu C nd Di L. AEG-1 mrna expression in nonsmll cell lung cncer is ssocited with incresed tumor ngiogenesis. Pthol Res Prct 2017; 213: [7] Chng Y, Li B, Xu X, Shen L, Bi H, Go F, Zhng Z nd Jons JB. Lentivirus-medited knockdown of strocyte elevted Gene-1 inhibits growth nd induces poptosis through mpk pthwys in humn retinoblstom cells. PLoS One 2016; 11: e [8] Kowlski PJ, Rubin MA nd Kleer CG. E-cdherin expression in primry crcinoms of the brest nd its distnt metstses. Brest Cncer Res 2003; 5: R [9] Demn JJ, Vn Lrebeke NA, Bruyneel EA, Brcke ME, Vermeulen SJ, Vennekens KM nd Mreel MM. Removl of silic cid from the surfce of humn MCF-7 mmmry cncer cells bolishes E-cdherin-dependent cell-cell dhesion in n ggregtion ssy. In Vitro Cell Dev Biol Anim 1995; 31: [10] Zhng Z, Bu X, Chen H, Wng Q nd Sh W. Bmi-1 promotes the invsion nd migrtion of colon cncer stem cells through the downregultion of E-cdherin. Int J Mol Med 2016; 38: [11] Onder TT, Gupt PB, Mni SA, Yng J, Lnder ES nd Weinberg RA. Loss of E-cdherin promotes metstsis vi multiple downstrem trnscriptionl pthwys. Cncer Res 2008; 68: [12] Petrov YI, Schecterson L nd Gumbiner BM. Roles for E-cdherin cell surfce regultion in cncer. Mol Biol Cell 2016; 27: [13] Lympertou D, Ginnopoulou E, Koutrs AK nd Klofonos HP. The exposure of brest cncer cells to fulvestrnt nd tmoxifen modultes cell migrtion differently. Biomed Res Int 2013; 2013: [14] Thiery JP, Acloque H, Hung RY nd Nieto MA. Epithelil-mesenchyml trnsitions in development nd disese. Cell 2009; 139: [15] In: Edge SB, Byrd DR, Compton CC, Fritz AG, Greene FL nd Trotti A, editors. AJCC Cncer Stging Mnul. 7th edition. New York, NY: Springer; [16] Xu S, Wen W, Zhou J, Liu J, Gu G. Clinicopthologicl significnce of expression of CIP2A nd c-myc in humn gllbldder crcinom. Int J Clin Exp Pthol 2017; 10: [17] Kikuno N, Shiin H, Urkmi S, Kwmoto K, Hirt H, Tnk Y, Plce RF, Pookot D, Mjid S, Igw M nd Dhiy R. Knockdown of strocyte-elevted gene-1 inhibits prostte cncer progression through upregultion of FOXO3 ctivity. Oncogene 2007; 26: [18] Emdd L, Srkr D, Su ZZ, Rndolph A, Boukerche H, Vlerie K nd Fisher PB. Activtion of the nucler fctor kppb pthwy by strocyte elevted gene-1: implictions for tumor progression nd metstsis. Cncer Res 2006; 66: [19] Srkr D, Prk ES, Emdd L, Lee SG, Su ZZ nd Fisher PB. Moleculr bsis of nucler fctorkppb ctivtion by strocyte elevted gene- 1. Cncer Res 2008; 68: [20] He W, He S, Wng Z, Shen H, Fng W, Zhng Y, Qin W, Lin M, Yun J, Wng J, Hung W, Wng L nd Ke Z. Astrocyte elevted gene-1 (AEG-1) induces epithelil-mesenchyml trnsition in 6030 Int J Clin Exp Pthol 2018;11(12):

7 lung cncer through ctivting Wnt/betctenin signling. BMC Cncer 2015; 15: 107. [21] Wng Y, Jin X, Song H nd Meng F. AEG-1 s predictor of sensitivity to neodjuvnt chemotherpy in dvnced epithelil ovrin cncer. Onco Trgets Ther 2016; 9: [22] Chen CY, Chen YY, Chen JJW, Chen KY, Ho CC, Shih JY, Chng YL, Yu CJ nd Yng PC. Astrocyte-elevted gene-1 confers resistnce to pemetrexed in non-smll cell lung cncer by upregulting thymidylte synthse expression. Oncotrget 2017; 8: [23] Li H nd Zho J. let-7d suppresses prolifertion nd invsion nd promotes poptosis of meningiom by trgeting AEG-1. Onco Trgets Ther 2017; 10: [24] Wng J, Chen X nd Tong M. Knockdown of strocyte elevted gene-1 inhibited cell growth nd induced poptosis nd suppressed invsion in ovrin cncer cells. Gene 2017; 616: [25] Li P, Sun T, Yun Q, Pn G, Zhng J nd Sun D. The expressions of NEDD9 nd E-cdherin correlte with metstsis nd poor prognosis in triple-negtive brest cncer ptients. Onco Trgets Ther 2016; 9: [26] Schneider MR, Hiltwein F, Grill J, Blum H, Krebs S, Klnner A, Buerschs S, Bruns C, Longerich T, Horst D, Brndl L, de Toni E, Herbst A nd Kolligs FT. Evidence for role of E-cdherin in suppressing liver crcinogenesis in mice nd men. Crcinogenesis 2014; 35: [27] Yun JA, Kim SH, Hong HK, Yun SH, Kim HC, Chun HK, Cho YB nd Lee WY. Loss of E-Cdherin expression is ssocited with poor prognosis in stge III colorectl cncer. Oncology 2014; 86: Int J Clin Exp Pthol 2018;11(12):

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