Cutaneous protothecosis in kidney transplant recipient,

AnBrasDermatol.2020;95(2):210---213

Anais

Brasileiros

de

Dermatologia

CASE

REPORT

Cutaneous

protothecosis

in

kidney

transplant

recipient

夽,夽夽

Valeria

Romero

Godofredo

_,

_Milvia

_Maria

_Simões

_e

_Silva

_Enokihara

_,

Jane

Tomimori

_,

_Marilia

_Marufuji

_Ogawa

a_{DepartmentofDermatology,UniversidadeFederaldeSãoPaulo,SãoPaulo,SP,Brazil} b_{DepartmentofPathology,UniversidadeFederaldeSãoPaulo,SãoPaulo,SP,Brazil}

Received6June2019;accepted4August2019 Availableonline21January2020

KEYWORDS Harmfulalgal proliferation; Opportunistic infections; Skindiseases, infectious

Abstract Protothecosisisarareconditioncausedbytheaclorophylatedalgae ofthegenus

Prototheca.In humans, protothecosis, caused mainlyby P. wickerhamii, manifests itselfin threeforms:cutaneous,articularandsystemic.Itcanoccur inbothimmunocompetentand immunosuppressedindividuals,beingmuchmorecommoninthelatter.Wepresentanewcase ofprotothecosisinBrazilinakidneytransplantrecipient.

©2020SociedadeBrasileiradeDermatologia.PublishedbyElsevierEspa˜na,S.L.U.Thisisan openaccessarticleundertheCCBYlicense(http://creativecommons.org/licenses/by/4.0/).

Introduction

Protothecosis is an uncommon infection caused by the aclorophyllatedalgaeofthegenusPrototheca.Fivespecies are known, twoof which affect humans: P. zopfii and P. wickerhamii,thelatterbeingthemostcommon.

夽 _{Howtocitethisarticle:GodofredoVR,EnokiharaMMSS,}

Tomi-moriJ,OgawaMM.Cutaneousprotothecosis inkidneytransplant recipient.AnBrasDermatol.2020;95:210---3.

夽夽_{StudyconductedattheUniversidadeFederaldeSãoPaulo,São}

Paulo,SP,Brazil.

∗_{Correspondingauthor.}

E-mail:[email protected](V.R.Godofredo).

Thefirstcaseofhumaninfectionwasdescribedin1964 asacutaneous ulcerlocatedonthe footofa ricegrower in Sierra Leone.1 _{A littlemore than 200 cases have been}

reportedworldwide,with10inBrazil.2---4_Wereportanew

case of protothetosis that occurred in a renal transplant recipient(RTR)inBrazil.

Case

report

A 60-year-old male patient, a skin phototype IV, born in Caetité-BAandmovedtoSãoPaulo-SP35yearsago,reported a nodular lesion 6 months ago on the right leg (Fig. 1), withnohistoryofprevioustrauma.Regardinghispersonal history, thepatientwasRTR15 yearsago,due toarterial hypertension, andhad been treatedfor multiple previous squamouscellcarcinomas.Hehadalreadyusedcyclosporin https://doi.org/10.1016/j.abd.2019.08.022

0365-0596/©2020SociedadeBrasileiradeDermatologia.PublishedbyElsevierEspa˜na,S.L.U.ThisisanopenaccessarticleundertheCC BYlicense(http://creativecommons.org/licenses/by/4.0/).

Cutaneousprotothecosisinkidneytransplantrecipient 211

Figure1 Erythematousnoduleinthedistalthirdoftheright leg.

andazathioprine.Atthetimeoftheinfection,thepatient hadbeenusingprednisone5mg/dayandsirolimus1mg/day for5years.

Theinitialdiagnostichypothesiswassubcutaneous myco-sisandthepatientwasreferredforcompletelesionexcision. The material was sent for histopathological analysis and granulomatousinflammatoryprocesswasobservedwith sup-purationandsporangiagroupedwithinthecytoplasmofthe macrophages(Figs.2and3).Thesporangiawerestainedby PeriodAcid-Schiff(PAS)andGrocott,andpresentedamorula appearance(Figs.4 and5).Part oftheskin fragmentwas sent formycological examinationandfungal culture,with nogrowthofagents.

In the postoperative period, the surgical wound was allowed to heal by secondary intention and was initially performedwithcompressivecottondressing,thendressed dailywithtopicalmupirocinfor3weeks,andsilvernitrate 10% untilcomplete healing.The patientwastreatedwith fluconazole150mg/dayforaperiodof3months,until com-pletehealingofthelesion.

Discussion

The algaeof thegenus Protothecadonotpresent chloro-plasts,organellesthatcontainthechlorophyllpigment,so

Figure2 Presenceofagranulomatousinflammatoryprocess withsuppuration.Inthemiddle,thesporangia(Hematoxylin& eosin,x40).

Figure3 Presenceofsporangiagroupedwithinthecytoplasm ofmacrophages(Hematoxylin&eosin,x400).

Figure4 ThesporangiaappearstainedbyPAS(x400).

they do not have the capacity to perform photosynthe-sis. They need a heterotrophic source of nutrients, such asorganic carbon and nitrogen, and the skin is the most frequentlyaffectedorgan.5

212 GodofredoVRetal.

Figure5 Thesporangia appearstained inblackby Grocott (x400).

Prototheca spp. is widely distributed throughout the world. Algae are found in soil, in the decomposition of plants,inwater,andincertainfooditems.Theyalsoexist asasaprophyteorganisminthehumanskin,nailsand res-piratoryanddigestivetracts.1,6

Protothecaspp.resistschlorinetreatment,sewage treat-ment and intestinal digestion. This contributes to its persistenceinsewage, disseminationbydomestic animals andpermanenceintheenvironment.Itisalsoresistantto milk pasteurization, representing a problem for the con-sumptionofdairyproducts.6

Humanprotothecosisisrare,buttheincidenceishigher inimmunocompromisedpatients(localorsystemic corticos-teroids, immunobiologicals,7 _{hematologic malignancies or}

cancer,diabetesmellitus,AIDS,solidorganandbonemarrow transplantrecipients,alcoholismor autoimmunedisease). In the literature, only 219 cases of human protothecosis havebeendescribedworldwide,ofwhich11werereported inBrazil,1,4 _{includingthis one.Amongthecases ofhuman}

protothecosis, thereare only 15 reports of cases in solid organreceptors,4,7,8_{9 inrenaltransplantrecipientsand1}

inliver/kidneytransplantation.InBrazil,itisthefirstcase describedinarenaltransplantrecipient.

The pathogenesisof protothecosis is unknown.In most cases,thesourceoftheinfectionisexogenouscontactwith contaminatedsoilorwater,commonlyoccurringafter trau-maticinoculation.Theseinfectionswerealsodescribedas complicationsaftersurgery.

Inman,protothecosisiscausedmainlybyP.wickerhamii

andmanifestsitselfinthreeforms:cutaneous,articularand systemic,withanacuteor chronic course.The cutaneous formisthemostobserved.Lesionshaveaslowevolutionand variableappearance:plaques,papules,nodules,ulcerations andeczematouseruptions.Themostcommonpresentations arevesiculobullous lesion and ulceration.9 _{In the present}

case,thepatientpresentedanodularlesion,reminiscentof thephaeohyphomycosis, amycosis by dematiaceous fungi describedintherecipientsofsolidorgantransplantation.

In histopathological examination, there is a granulo-matousinflammatoryinfiltrate, consistingoflymphocytes, macrophages,giantcells and neutrophils.Instaining with PAS or Grocott, we can observe sporangia internally con-tainingsporangiospores,whichmaybeinsidemacrophages

orfreeintheexudate.Sporangiaaresurroundedbya cap-sule that can varyfrom7 to 30␮m; P.zopfii tends tobe larger (7---30␮m) than P. wickerhamii (3---15␮m).6 _A

fea-tureofP.wickerhamiiistoexhibitsporangiosporeswitha roundedcentralendospore,andthischaracteristichasbeen described as morula-like, daisy-like or raspberry-like.6 _In

thehistopathologicalexamination oftheourpatient, spo-rangiosporeswere betterevidenced withPAS and Grocott staining,soroutinescreeningwithspecialstainingfor nodu-larornodule-cysticlesionsintransplantrecipientsshouldbe included.

Thereis currentlynodefinitetreatment forPrototheca spp. due to the rarity of the disease. Amphotericin B appearstobeeffectiveincasesofdisseminatedinfection.5,8

Azole antifungals arealso used,although their efficacy is variable.5,10 _{Ourpatient hada good therapeutic response}

withsurgicaltreatmentandoralfluconazole,evolvingwith adequatehealingandtherewasnorelapseafter4yearsof follow-up.

Inconclusion,nodularornodule-cysticlesionsin trans-plantrecipientsshouldbebiopsiedtoscreenforinfectious agentsusingspecialstains(PAS,Grocott,Fite-Faraco). Cul-turingforfungiandmycobacteriaisalsorecommended.The lesion of protothecosis should be completely excised and healingleftbysecondaryintention.Complementingsurgical treatmentwithazolederivativesishighlyrecommended.

Financial

support

Nonedeclared.

Authors’

contributions

ValeriaRomeroGodofredo:Statisticalanalysis;approvalof the final version of themanuscript; conception and plan-ningofthestudy;elaborationandwritingofthemanuscript; obtaining,analysis,andinterpretationofthedata;effective participation in research orientation; intellectual partici-pation inthe propaedeuticand/or therapeuticconduct of thestudiedcases;criticalreviewoftheliterature;critical reviewofthemanuscript.

MilviaMariaSimõeseSilvaEnokihara:Intellectual partic-ipationinthepropaedeuticand/or therapeuticconductof thestudiedcases;criticalreviewofthemanuscript.

Jane Tomimori:Obtaining, analysis, and interpretation of thedata;intellectualparticipationin thepropaedeutic and/or therapeutic conduct of the studied cases; critical reviewoftheliterature;criticalreviewofthemanuscript.

Marilia Marufuji Ogawa: Approval of the final version of the manuscript;conception andplanning of the study; effectiveparticipationinresearchorientation;intellectual participationin thepropaedeuticand/or therapeutic con-ductofthestudiedcases;criticalreviewoftheliterature; criticalreviewofthemanuscript.

Conflicts

of

interest

Cutaneousprotothecosisinkidneytransplantrecipient 213

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