International Journal of Infectious Diseases 17 (2013) e925–e927

Case Report

Histopathological findings of an uncommon co-infection: Echinococcusvogeli, HIV, hepatitis C virus, and hepatitis B virus

Fernanda Barbosa de Almeida a, Christiane Leal Correa b, Nilton Ghiotti de Siqueira c,Nellysie Virgınia F.M. dos S. Castro de Carvalho c, Rosangela Rodrigues-Silva a,*,Arnaldo Feitosa B. de Andrade d, Jose Roberto Machado-Silva d

a Laboratory of Helminth Parasites of Vertebrates, Oswaldo Cruz Institute, Rio de Janeiro, Brazilb Laboratory of Experimental Pathology, Gama Filho University, Rio de Janeiro, Brazilc Acre State Hospital Foundation and Federal University of Acre, Acre, Brazild Department of Microbiology, Immunology and Parasitology, Faculty of Medical Sciences, State University of Rio de Janeiro, Rio de Janeiro, Brazil

A R T I C L E I N F O

Article history:

Received 4 July 2012

Received in revised form 7 March 2013

Accepted 9 April 2013

Corresponding Editor: Andy Hoepelman,

Utrecht, the Netherlands

Keywords:

Co-infection

Polycystic echinococcosis

HIV

HCV

HBV

S U M M A R Y

Our work represents the first case report of polycystic echinococcosis co-infection with HIV, hepatitis C

virus (HCV), and hepatitis B virus (HBV). Structural liver alterations were found to be related to parasitic

structures and necroinflammatory foci (karyopyknosis, karyorrhexis, and karyolysis), consistent with

Echinococcus vogeli. Visceral adipose tissue and intrahepatic triglyceride droplets (macrovesicular and

microvesicular steatosis) indicated abnormal fat anabolism, which probably resulted from both viral-

induced hepatopathy and drug-related toxicity. In summary, our results suggest that the observed liver

abnormalities reflected the coincident exposure to hepatotropic viruses and parasites causing polycystic

echinococcosis and were not indicative of opportunistic relationships among these pathogens.

� 2013 International Society for Infectious Diseases. Published by Elsevier Ltd. All rights reserved.

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1. Introduction

Polycystic echinococcosis (PE) is the designation for infectionwith the larval phase of Echinococcus vogeli. PE is an emergingzoonosis of public health concern, as it leads to significant humanmorbidity in the humid, tropical forest areas of South and CentralAmerica.1 In the last four decades, a total of 178 cases have beenreported, in which the liver and mesentery were most oftenaffected.2

Hepatitis C virus (HCV) and hepatitis B virus (HBV) havebecome increasingly common among people living with HIVworldwide, and they strongly increase the risk of liver injury in thispopulation.3 Relatively little is known about how a concomitantparasitic co-infection may impact host tissues, especially if theyshare the same target organ. To our knowledge, this paper reportsthe first occurrence of co-infection of polycystic echinococcosisand HIV, HCV, and HBV viral infections.

* Corresponding author. Tel.: +55 21 2562 1485.

E-mail address: rsilva@ioc.fiocruz.br (R. Rodrigues-Silva).

1201-9712/$36.00 – see front matter � 2013 International Society for Infectious Disea

http://dx.doi.org/10.1016/j.ijid.2013.04.002

2. Case report

Written informed consent was obtained from the patient. A 45-year-old woman was admitted to a tertiary teaching hospital withright-sided abdominal discomfort and pain of 20 years duration.She had lived in Tarauaca, a rural area within the state of Acre, inthe northern region of Brazil. Physical examination revealed anabdominal mass. A computed tomography (CT) scan showed livercysts (Figure 1A). A presumptive diagnosis of polycystic echino-coccosis was made, and albendazole (600 mg/day) for 60 days wasprescribed. Her past medical history was significant for HIV, HCV,and HBV virus co-infection. The patient was placed on a regimen ofhighly active antiretroviral therapy (HAART) using tenofovir (TDF,300 mg once daily) in combination with lamivudine (3TC, 150 mgtwice daily) and lopinavir/ritonavir (LPV/r, 400/100 mg twicedaily).

On exploratory laparotomy, clusters of cystic masses(Figure 1B) in segment VI, on the vena cava, and on the diaphragmwere excised. The patient’s postoperative course was uneventful.No recurrence was observed on CT scan at the 11-month follow-up.Histological examination of two hepatic and two mesenteric cystswas carried out under light microscopy. Hematoxylin and eosin

ses. Published by Elsevier Ltd. All rights reserved.

Figure 1. Co-infection with Echinococcus vogeli, HIV, HCV, and HBV. (A) Liver computed tomography image showing two dissimilar cystic lesions (arrows). (B) Intraoperative

findings showing liver cystic lesions (arrows). (C) Representative image of liver polycystic echinococcosis, consisting of invaginated and evaginated protoscoleces

(arrowhead), a germinal layer (arrow), a laminated layer (&), and an adventitial layer (*), H&E stain (40�). The insert shows protoscoleces and free hooklets (1000�). (D)

Histopathology showing hepatic parenchymal necrosis with karyopyknosis (small arrow), karyorrhexis (arrow), and karyolysis (arrowhead), H&E (400�). The insert shows an

area of necrotic tissue with mixed inflammatory infiltrate (1000�). (E) Photomicrograph showing both microvesicular (arrowhead) and macrovesicular steatosis (arrow) and

a mixed inflammatory infiltrate consisting of both mononuclear (*) and polymorphonuclear cells (small arrow), H&E (400�). The insert shows fatty liver parenchyma

(1000�). (F) Mesenteric sections showing a hydatid cyst with fat accumulation (arrow) in the laminated layer (*), H&E (100�).

F.B. de Almeida et al. / International Journal of Infectious Diseases 17 (2013) e925–e927e926

(H&E)-stained sections revealed parasitic structures composed of ahost-origin layer (adventitia), an outer laminated layer, an innergerminative layer, brood capsules, invaginated or evaginatedprotoscoleces with different densities of calcareous corpuscles andfree hooklets (41.2 � 2.3 � 13.0 � 0.9 mm (large hooks) and32.4 � 3.1 � 10.6 � 1.3 mm (small hooks)), consistent with polycysticechinococcosis (Figure 1C). The liver parenchyma around the chronic

cysts showed prominent areas of calcification with collagen-richfibrous tissue and a short-origin layer. Young liver cysts had threecharacteristic layers and exhibited polymorphonuclear inflammatorycell infiltration, hyperemia, angiogenesis in the adventitial layer, anda thicker arteriole wall.

Histological evidence of viral hepatitis, hepatocellular degen-eration (karyopyknosis, karyorrhexis, and karyolysis), and

F.B. de Almeida et al. / International Journal of Infectious Diseases 17 (2013) e925–e927 e927

mononuclear cells within the necrotic foci were noted (Figure 1D).H&E staining evidenced discrete leukocyte infiltration andmacrovesicular and microvesicular steatosis within the hepato-cytes (Figure 1E).

Mesenteric cysts were characterized by the absence of anadventitial layer, by a thin germinal layer, and by an amorphousprotein material distributed along the thick laminated layer.Collagen and fibroblasts were observed. There was a small amountof leukocyte infiltrate, including macrophages, lymphocytes,eosinophils, and neutrophils, but protoscoleces were not found.The most striking pathological finding was a large amount ofadipose tissue permeating various regions of the laminated layer ofthe mesenteric cysts (Figure 1F).

3. Discussion

Because human behavior plays a pivotal role in the epidemiol-ogy of infectious diseases, it is predictable that individuals mayexperience combined infections.3 Shared mechanisms of trans-mission lead to high co-infection rates with both HCV and HBVamong those with HIV infection. Interestingly, PE is typically arural and occupational disease; however it has been associatedwith HIV, HCV, and HBV co-infections. This corroborates theepidemiological tendency of these three viruses to spread fromurban to rural areas,4 impacting the poorest and most vulnerablepopulations.

Given that the four infections share the same target organ, a keyquestion is how they are related. HIV causes a systemic viralinfection that destroys both innate and adaptive immune cells,allowing the onset of other infections in a weakened host.5 Despitethe potentially severe complications of co-infection with HIV and aparasite, HIV infection appears to have no impact on theprogression of PE, as determined by comparison with individualswith only PE.1,2 Polymorphonuclear inflammatory cell infiltrate,hyperemia, angiogenesis, and prominent areas of calcification with

collagen-rich fibrous tissue were observed in our patient. DuringHIV infection, other infectious agents are often opportunistic;5 inthe present case, the parasite infection was not opportunisticbecause PE had persisted for two decades.

Some histological sections showed liver steatosis and abnormallocalization of fat. Although HAART has a positive influence on thequality of life and longevity in HIV-infected patients, adverse drugreactions involving the liver have been widely reported.6 Increas-ing evidence indicates that both HIV infection and HAART areassociated with abnormal fat anabolism, including the formationof intrahepatic triglyceride droplets (macrovesicular and micro-vesicular steatosis) and lipodystrophy, which leads to visceraladipose tissue.6 In summary, our results suggest that polycysticechinococcosis does not behave as an opportunistic infection, andthe liver abnormalities reflected the coincident exposure tohepatotropic viruses (resulting in indications of abnormal fatanabolism such as lipodystrophy), to virus-induced factors, and toantiretroviral therapy.

Ethical approval: This work was approved by the IPEC-FIOCRUZinstitutional review board.

Conflict of interest: No conflict of interest to declare.

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