A case of pulmonary adenocarcinoma showing rapid progression of peritoneal dissemination after immune checkpoint inhibitor therapy
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1 Shinozki et l. BMC Cncer (2018) 18:620 CASE REPORT A cse of pulmonry denocrcinom showing rpid progression of peritonel dissemintion fter immune checkpoint inhiitor therpy Open Access Tro Shinozki 1, Eri Iwmi 1, Shinnosuke Ikemur 1, Ttsu Mtsuzki 1, Tkhiro Nkjim 1, Kzuhiko Hshimoto 2 nd Tkeshi Tershim 1* Astrct Bckground: Immune checkpoint inhiitors re stndrd tretments for non-smll cell lung cncer. Unique cses with prdoxicl ccelertion of the disese fter immunotherpy hve een reported. These hve een descried s cses of hyperprogressive disese. Cse presenttion: A 76-yer-old mn ws dignosed with pulmonry denocrcinom with pleurl dissemintion nd liver nd drenl metstses. Genomic nlysis reveled neither EGFR muttions nor ALK trnsloctions. Immunohistochemicl nlysis reveled progrmmed deth-lignd 1 tumor proportion score of 23%. Chemotherpy with cropltin, pclitxel, nd evcizum resulted in Grde 3 skin eruption nd disese progression. Pemrolizum ws initited s second-line tretment. However, peritonel dissemintion nd scites developed. The ptient died 2 weeks lter. The utopsy reveled widespred peritonel dissemintion nd n extensive hemorrhgic infrction. Conclusion: This ws rre cse of hyperprogressive disese with rpid progression of peritonel dissemintion fter pemrolizum tretment. Keywords: Adenocrcinom, Hyperprogressive disese, Immune checkpoint inhiitor, Lung cncer, Pemrolizum, Peritonel dissemintion Bckground Immune checkpoint inhiitors (ICIs) re currently stndrd tretments for non-smll cell lung cncer (NSCLC) [1, 2]. The unique dverse events tht cn rise fter tretment with ICIs, including pneumonitis, colitis, nd thyroiditis, re known s immune-relted dverse events [3]. Recently, unique cses with prdoxicl ccelertion of the disese fter immunotherpy hve een reported [4, 5]. These hve een descried s cses of hyperprogressive disese. In one study, hyperprogressive disese ws oserved in 9% of ptients treted with ICIs [4]. * Correspondence: tersim@tdc.c.jp 1 Deprtment of Respirtory Medicine, Tokyo Dentl College Ichikw Generl Hospitl, Sugno, Ichikw, Chi , Jpn Full list of uthor informtion is ville t the end of the rticle Herein, we report on cse of hyperprogressive disese fter tretment with pemrolizum, n ICI currently used in the tretment of NSCLC. The clinicl course in this cse ws highly unusul s it exhiited rpid progression of peritonel dissemintion shortly fter single dministrtion of pemrolizum. Moreover, this is one of the first reports to document hyperprogressive disese y utopsy. Cse presenttion A 76-yer-old mn with no history of smoking presented with n norml shdow on chest X-ry. He hd medicl history of hypertension, dyslipidemi, reflux esophgitis, nd enign prosttic hyperplsi. He hd mild dyspne on exertion. Physicl exmintion did not revel ny norml findings nd the results of the The Author(s) Open Access This rticle is distriuted under the terms of the Cretive Commons Attriution 4.0 Interntionl License ( which permits unrestricted use, distriution, nd reproduction in ny medium, provided you give pproprite credit to the originl uthor(s) nd the source, provide link to the Cretive Commons license, nd indicte if chnges were mde. The Cretive Commons Pulic Domin Dediction wiver ( pplies to the dt mde ville in this rticle, unless otherwise stted.
2 Shinozki et l. BMC Cncer (2018) 18:620 Pge 2 of 5 lortory tests were within norml limits. The ptient hd n Estern Coopertive Oncology Group performnce sttus (ECOG PS) score of 1. Chest X-ry reveled tumor in the left hilr region nd left pleurl effusion. This ws confirmed y enhnced computed tomogrphy (CT) scn, which showed 40 mm tumor in the left lower loe with left pleurl effusion. Enhnced CT scn of the domen reveled liver nd drenl metstses. Tissue specimens otined y ronchoscopy reveled well-differentited denocrcinom (Fig. 1). Genomic nlysis ws performed to identify whether there were ny driver muttions present. This reveled tht there were no sensitizing muttions in the epiderml growth fctor receptor (EGFR) gene, nor were there trnsloctions in the nplstic lymphom kinse (ALK) gene. Immunohistochemicl nlysis of progrmmed deth-lignd 1 (PD-L1) expression using the murine 22C-3 ntiody, expressed s the tumor proportion score (TPS), reveled TPS of 23% (Fig. 1). Furthermore, there were no increses in the serum levels of vrious tumor mrkers. First-line chemotherpy with cropltin (re under the curve, 6), pclitxel (200 mg/m 2 ), nd evcizum (15 mg/kg) ws initited for pulmonry denocrcinom ct3n1m1c (Stge IVB). However, skin eruption developed during the week following dministrtion nd spred to his whole ody. The size of the liver metstsis in the S4 region lso incresed from 1.0 to 1.3 cm nd new liver metstses were detected (Fig. 2). The ECOG PS score of the ptient ws 1. Since the ptient s skin eruption ws clssified s Grde 3 dverse event (Common Terminology Criteri for Adverse Events, version 4.0) nd the disese ws progressive, tretment ws switched to n ICI. Pemrolizum (200 mg/ody) ws dministered s second-line tretment. Following dministrtion, the ptient egn to experience grdul loss of ppetite nd dominl distension, followed y worsening of his generl condition. On Dy 13 fter pemrolizum dministrtion, n enhnced CT scn showed progression of the liver metstses (Fig. 3). There ws lso lrge mount of scites nd widespred peritonel dissemintion (Fig. 3, c). These were novel findings tht hd not een oserved prior to pemrolizum tretment. The ptient died suddenly due to rpid progression of respirtory filure on Dy 14 fter pemrolizum dministrtion. An utopsy reveled extensive Stge IV lung denocrcinom originting from the left lower loe with metstses in the lungs, left pleur, liver, drenl glnds, kidneys, pncres, stomch, smll intestine, colon, one mrrow, nd lymph nodes of the ilterl hilr nd pr-ortic lesions. Dissemintion to the peritoneum (Fig. 4), omentum, nd diphrgm ws lso documented y utopsy. Microscopic exmintion of the peritonel Fig. 1 Histopthologicl findings of tissue specimens otined under ronchoscopy. Hemtoxylin nd eosin stining showing well-differentited denocrcinom (200 mgnifiction). 22C-3 ntiody stining ginst progrmmed deth-lignd 1. Tumor proportion score, 23% Fig. 2 Enhnced computed tomogrphy (CT) imging. CT ws performed fter single course of cytotoxic chemotherpy. The size of the liver metstsis in the S4 region incresed from 1.0 to 1.3 cm (rrow)
3 Shinozki et l. BMC Cncer (2018) 18:620 Pge 3 of 5 Fig. 4 Mcroscopic exmintion of the utopsy specimens reveled widespred peritonel dissemintion (rrows) c Fig. 3 Enhnced computed tomogrphy (CT) imging. After single dministrtion of pemrolizum, the size of the liver metstsis incresed from 1.3 to 1.6 cm (rrow). nd c Widespred peritonel dissemintion (rrows) nd lrge mount of scites were visile fter pemrolizum tretment tissue confirmed the presence of well-differentited invsive denocrcinom (Fig. 5). Immunohistochemicl nlysis of the peritonel tissue reveled tht the PD-L1 TPS of the tumor cells ws 12% (Fig. 5), which is similr to the score for the tumor tissue otined y ronchoscopy. Overexpression of the MDM2 gene ws not detected y immunohistochemistry. In ddition to these findings, n extensive hemorrhgic infrction due to Fig. 5 Histopthologicl findings of peritonel utopsy specimens. Hemtoxylin nd eosin stining of the peritonel tissue reveled n invsive, well-differentited denocrcinom (100 mgnifiction). 22C-3 ntiody stining ginst progrmmed deth-lignd 1. Tumor proportion score, 12%
4 Shinozki et l. BMC Cncer (2018) 18:620 Pge 4 of 5 tumor emolism ws oserved in the right lung (Fig. 6, ). This ws recorded s the cuse of deth sed on the utopsy. Discussion nd conclusions To the est of our knowledge, this is the first cse of lung cncer with hyperprogressive disese showing rpid progression of peritonel dissemintion fter ICI tretment. Moreover, this is the first cse where hyperprogressive disese ws documented y utopsy. Hyperprogressive disese hs recently een descried in cses treted with immunotherpy [4, 5]. In current tretment strtegies for dvnced NSCLC, the ICI pemrolizum is recommended s first-line therpy in cses where the TPS is 50% nd s second-line therpy in cses where the TPS is 1 49% [1, 2]. It is criticl to determine whether the progression oserved in this cse ws hyperprogressive disese, pseudoprogression, or nturl progression, s is often oserved in the terminl stges of mlignnt diseses. ICIs re sometimes known to result in unique response ptterns, such s pseudoprogression [6]. However, the utopsy findings in Fig. 6 Histopthologicl findings of utopsy specimens from the right lung. Hemtoxylin nd eosin stining (100 mgnifiction). Verhoeff-Vn Gieson elstic stining. An extensive hemorrhgic infrction due to tumor emolism ws oserved (rrow) the present cse ruled out the possiility of pseudoprogression. Chmpit et l. proposed tht hyperprogressive disese should e defined s > 2.0-fold increse in tumor growth rte fter immunotherpy [4]. Kto et l. defined hyperprogressive disese s time-to-tretment filure of < 2 months, > 50.0% increse in tumor urden, nd > 2.0-fold increse in tumor growth rte [5]. In our cse, the scle mesurle region ws the liver metstses. The time elpsed etween the 1.0 to 1.3 cm nd 1.3 to 1.6 cm enlrgement of the trget lesion of the liver ws 51 nd 19 dys, respectively. The volume douling time efore nd fter pemrolizum tretment ws 45 nd 21 dys, respectively (volume douling time = [(T1 T0) log2]/[3log(d1/d0)],where D1 nd D0 re the dimeters t T1 nd T0, respectively) [7]. There ws > 2.0-fold increse in tumor growth rte since tumor growth rte is the inverse of the volume douling time (i.e., tumor growth rte = 1 / volume douling time) [8]. In previous study, the medin time from dignosis of Stge IV disese to peritonel metstsis ws 16.5 (rnge, ) months mong 410 ptients with metsttic NSCLC [9], which is notly longer thn the 2.3 months in this cse. Moreover, the time from pemrolizum dministrtion to peritonel metstsis ws just 0.4 months (13 dys). The novel ppernce of widespred peritonel dissemintion nd lrge mount of scites within 13 dys met the criteri of time-to-tretment filure of < 2 months nd suggested tht the clinicl course of our cse ws much more rpid thn the nturl terminl course. Finlly, utopsy findings reveled greter progression of the metstses thn CT scn imges tken 1 dy prior to the ptient s deth. Together, these indicte tht this ws cse of hyperprogressive disese. The clinicl course of our cse ws highly unique due to the presence of widespred peritonel dissemintion. Peritonel dissemintion is rre clinicl event in lung cncer ptients, with utopsy results indicting n incidence of % [10, 11]. It is even rrer tht peritonel dissemintion develops during the clinicl course. A 26-yer study of 1024 lung cncer ptients reported tht only 12 ptients (1.2%) developed cliniclly detectle peritonel dissemintion [12]. Another study found tht in 410 ptients with metsttic NSCLC, 33 ptients (8%) developed peritonel dissemintion nd tht this ws highly ssocited with pleurl dissemintion [9]. In our cse, it is possile tht pleurl dissemintion nd hyperprogressive disese contriuted to peritonel dissemintion. The mechnisms of hyperprogressive disese re not yet understood. Tumor profiles nd ptient chrcteristics re thought to e importnt fctors. The finding tht the PD-L1 TPS ws similr efore nd fter the
5 Shinozki et l. BMC Cncer (2018) 18:620 Pge 5 of 5 dministrtion of pemrolizum in our cse ws in greement with the finding tht hyperprogressive disese ws not ssocited with the PD-L1 sttus of tumors [4]. Kto et l. showed tht cncer ptients with MDM2 gene mplifiction or EGFR muttions hd incresed rtes of tumor growth fter tretment with ICIs [5]. However, in our cse, EGFR ws wild-type nd there ws no overexpression of the MDM2 gene. In terms of ptient chrcteristics, ge > 65 yers ws identified s the only ssocited fctor for hyperprogressive disese [4]. Although there my e other unknown risk fctors, it is likely tht old ge ws the primry risk fctor for progressive disese in our cse. Our report hs severl limittions. Firstly, there is the potentil tht the rpid progression seen in our ptient ws due to the nturl course or intrinsic cncer iology rther thn pemrolizum therpy. In fct, the disese ws chemoresistnt nd progressive prior to pemrolizum tretment. The widespred peritonel dissemintion, however, suggested ccelerted progression fter pemrolizum tretment. Secondly, the tumor growth rte is not stndrdized model for response nd the definition of hyperprogressive disese proposed y Chmpit et l. hs not een widely ccepted y the roder oncology community [13]. In our cse, the rpid growth of the tumor ws shown y shortening of the douling time of the trget lesion of the liver. The strength of our cse is the fct tht true progression ws documented y utopsy nd tht utopsy specimens will e useful for elucidting the mechnisms of hyperprogressive disese in the future. In this report, we descrie cse of pulmonry denocrcinom showing rpid progression of peritonel dissemintion soon fter single dministrtion of pemrolizum. It is likely tht old ge ws risk fctor for progressive disese fter ICI tretment. Clinicins should consider the possiility of hyperprogressive disese in smll suset of ptients fter ICI tretment. Further studies re needed to elucidte the risk fctors nd mechnisms of hyperprogressive disese following immunotherpy. Arevitions ALK: Anplstic lymphom kinse; CT: Computed tomogrphy; ECOG PS: Estern Coopertive Oncology Group performnce sttus; EGFR: Epiderml growth fctor receptor; ICI: Immune checkpoint inhiitor; NSCLC: Non-smll cell lung cncer; PD-L1: Progrmmed deth-lignd 1; TPS: Tumor proportion score Ethics pprovl nd consent to prticipte Not pplicle. Consent for puliction Written informed consent ws otined from the ptient s fmily for puliction of this cse report nd ny ccompnying imges. Competing interests The uthors declre tht they hve no competing interests. Pulisher s Note Springer Nture remins neutrl with regrd to jurisdictionl clims in pulished mps nd institutionl ffilitions. Author detils 1 Deprtment of Respirtory Medicine, Tokyo Dentl College Ichikw Generl Hospitl, Sugno, Ichikw, Chi , Jpn. 2 Deprtment of Pthology nd Lortory Medicine, Tokyo Dentl College Ichikw Generl Hospitl, Sugno, Ichikw, Chi , Jpn. Received: 28 Jnury 2018 Accepted: 23 My 2018 References 1. Herst RS, Bs P, Kim DW, Felip E, Pérez-Grci JL, Hn JY, et l. Pemrolizum versus docetxel for previously treted, PD-L1-positive, dvnced non-smll-cell lung cncer (KEYNOTE-010): rndomised controlled tril. Lncet. 2016;387: Reck M, Rodríguez-Areu D, Roinson AG, Hui R, Csőszi T, Fülöp A, et l. Pemrolizum versus chemotherpy for PD-L1-positive non-smll-cell lung Cncer. N Engl J Med. 2016;375: Michot JM, Bigenwld C, Chmpit S, Collins M, Cronnel F, Postel-Viny S, et l. Immune-relted dverse events with immune checkpoint lockde: comprehensive review. Eur J Cncer. 2016;54: Chmpit S, Dercle L, Ammri S, Mssrd C, Holleecque A, Postel-Viny S, et l. Hyperprogressive disese is new pttern of progression in Cncer ptients treted y nti-pd-1/pd-l1. Clin Cncer Res. 2017;23: Kto S, Goodmn A, Wlvlkr V, Brkusks DA, Shri A, Kurzrock R. Hyperprogressors fter immunotherpy: nlysis of genomic ltertions ssocited with ccelerted growth rte. Clin Cncer Res. 2017;23: Chiou VL, Burotto M. Pseudoprogression nd immune-relted response in solid tumors. J Clin Oncol. 2015;33: Schwrtz M. A iomthemticl pproch to clinicl tumor growth. Cncer. 1961;14: Mckintosh JA, Mrshll HM, Yng IA, Bowmn RV, Fong KM. A retrospective study of volume douling time in surgiclly resected non-smll cell lung cncer. Respirol. 2014;19: Ptil T, Aisner DL, Noonn SA, Bunn PA, Purcell WT, Crr LL, et l. Mlignnt pleurl disese is highly ssocited with susequent peritonel metstsis in ptients with stge IV non-smll cell lung cncer independent of oncogene sttus. Lung Cncer. 2016;96: Arms HL, Spiro R, Goldstein N. Metstses in crcinom; nlysis of 1000 utopsied cses. Cncer. 1950;3: McNeill PM, Wgmn LD, Neifeld JP. Smll owel metstses from primry crcinom of the lung. Cncer. 1987;59: Stoh H, Ishikw H, Ymshit YT, Kurishim K, Ohtsuk M, Sekizw K. Peritonel crcinomtosis in lung cncer ptients. Oncol Rep. 2001;8: Shron E. Cn n immune checkpoint inhiitor (sometimes) mke things worse? Clin Cncer Res. 2017;23: Avilility of dt nd mterils All dt generted or nlyzed during this study re included in this pulished rticle. Authors contriutions TS contriuted to tretment decisions, the collection of clinicl dt, dt nlysis, nd writing the mnuscript. EI, SI, TM, TN, nd TT contriuted to the interprettion of the clinicl dt nd chest imges. KH contriuted to the utopsies, pthologicl exmintions, nd immunohistochemicl nlysis. All uthors hve red nd pproved the finl mnuscript.
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