In the global village, clinicians should open their “clinical landscape” to a number of diseases they have little, if any, familiarity with. Moreover, some of them may present with uncommon, atypical presentations that may be mistaken for other disease

A Kawakami

Andrea Angheben

CS Chim

DG Colley

Dora Buonfrate

EC FAUST

EC Gonçalves

Elisa Vanino

F Bidegain

F Gobbi

Federico Gobbi

G Badir

GD Burchard

Giulia Martelli

H Pickering

J Zwang

JR Lambertucci

Laura Bortesi

Luciano Attard

LZ Goldani

M El Gazayerli

Maria Gobbo

N Zarrin-Khameh

P Grunstein

Pierluigi Viale

R Teixeira

T Osaki

TH Tang

Valentina Marchese

Xiao-Nong Zhou

Zeno Bisoffi

PLoS Neglected Tropical Diseases

PubMed

Crossref

Schistosoma mansoni Eggs in Spleen and Lungs, Mimicking Other Diseases

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Schistosoma mansoni Eggs in Spleen and Lungs, Mimicking Other Diseases.

Gobbi, Federico

Martelli, Giulia

ATTARD, LUCIANO

Buonfrate, Dora

Angheben, Andrea

Marchese, Valentina

Bortesi, Laura

Gobbo, Maria

VANINO, ELISA

VIALE, PIERLUIGI

Bisoffi, Zeno

Archivio istituzionale della ricerca - Alma Mater Studiorum Università di Bologna

SYMPOSIUMSchistosoma mansoni Eggs in Spleen andLungs, Mimicking Other DiseasesFederico Gobbi1*, Giulia Martelli2, Luciano Attard2, Dora Buonfrate1, Andrea Angheben1,Valentina Marchese1,3, Laura Bortesi4, Maria Gobbo1, Elisa Vanino2, Pierluigi Viale2,Zeno Bisoffi11 Center for Tropical Diseases, Ospedale Sacro-Cuore Don Calabria, Negrar, Verona, Italy, 2 InfectiousDiseases Unit, Department of Medical and Surgical Sciences, Ospedale S. Orsola-Malpighi, Alma MaterStudiorum University of Bologna, Bologna, Italy, 3 Acute and Chronic Viral Hepatitis Department, SecondaUniversità degli Studi di Napoli, Naples, Italy, 4 Department of Pathology, Ospedale Sacro-Cuore DonCalabria, Negrar, Verona, Italy* federico.gobbi@sacrocuore.itCase PresentationCase 1A 25-year-old migrant presented to the Unit of Infectious Diseases of Bologna in October2013. After leaving Senegal in 2009, he stayed in Libya for two years before reaching Italy byboat in 2011. In August 2013, he was involved in a road accident, reporting a fracture of thepelvis and a traumatic bowel perforation. A rectal resection with colostomy was carried out,and external osteosynthesis was done. After the surgical intervention, sepsis appeared: fever>38°C, tachypnea, WBC 28,000/μl, and procalcitonin 2.3 nanogr/ml (normal<0.5). Anabdominal CT scan showed portal vein thrombosis and multiple embolic infarctions involvingthe lungs, kidneys, and spleen. A carbapenemase-resistant Klebsiella pneumoniae (KPC) strainwas identified in the blood culture, in the rectal swabs, in the colostomy, and in the sputumspecimens; an intravenous antibiotic treatment with meropenem, colistin, tigecycline, andrifampin was promptly started. The patient’s conditions slightly improved, but a furtherabdominal CT scan revealed a fluid intrasplenic lesion (Fig 1A).Suspecting a massive splenic hematoma, a splenectomy was carried out on November 2013.An abundant purulent exudate was found in the spleen; the histologic examination revealedseveral Schistosoma mansoni eggs (Fig 1B). Serology for S.mansoni (enzyme immunoassay[EIA]) resulted positive (37 U/mL, negative<12), and S.mansoni eggs were detected in stoolspecimens too. The blood tests showed hypereosinophilia (2,510 eosinophils/μl) and raised IgE(7,110 IU/mL). The patient was treated with praziquantel (40 mg/kg/day, divided in two doses,for 3 d). After two weeks, eosinophils decreased, and no more S.mansoni eggs were found inthe stool; his condition promptly improved and antibiotic therapy was stopped. Six monthsafter the accident, he successfully underwent surgical restoration of intestinal continuity. Rectalswab test for KPC resulted negative.Case 2A 27-year-old migrant presented to the Center for Tropical Diseases (CTD), Negrar, Verona,in May 2014, complaining of abdominal pain for 2 mo. After leaving Mali in 2009, he stayed inLibya for five years before reaching Italy by boat in February 2014. The blood tests showed 690PLOS Neglected Tropical Diseases | DOI:10.1371/journal.pntd.0003860 July 23, 2015 1 / 6OPEN ACCESSCitation: Gobbi F, Martelli G, Attard L, Buonfrate D,Angheben A, Marchese V, et al. (2015) Schistosomamansoni Eggs in Spleen and Lungs, Mimicking OtherDiseases. PLoS Negl Trop Dis 9(7): e0003860.doi:10.1371/journal.pntd.0003860Editor: Xiao-Nong Zhou, National Institute ofParasitic Diseases, Chinese Center for DiseasesControl and Prevention, ChinaPublished: July 23, 2015Copyright: © 2015 Gobbi et al. This is an openaccess article distributed under the terms of theCreative Commons Attribution License, which permitsunrestricted use, distribution, and reproduction in anymedium, provided the original author and source arecredited.Funding: The authors received no specific fundingfor this work.Competing Interests: The authors have declaredthat no competing interests exist.eosinophils/μl, further increased up to 1,020/μl; C reactive protein and erythrocyte sedimenta-tion rate tested normal. The IgE was elevated (4,950 IU/mL). The quantiferon tuberculosis(TB) test was negative and so were anti-HIV and anti-HCV antibodies. A chronic hepatitis Binfection was diagnosed. Serology for S.mansoni (ELISA) resulted positive (Optical Density4.07, negative<0.9), and S.mansoni eggs were detected in stool specimens. The patient wastreated with praziquantel (40 mg/kg/day, divided in two doses, for 3 d). Abdominal echographyrevealed signs of cirrhosis and moderate splenomegaly. A liver biopsy demonstrated periportal“Symmer’s pipestem” fibrosis and the presence of S.mansoni eggs. Chest X-ray showed a smallFig 1. Case 1. a) Splenic lesion at CT scan. b) Schistosomamansoni egg in spleen tissue.doi:10.1371/journal.pntd.0003860.g001Fig 2. Case 2. a) Pulmonary nodule at CT scan. b) S. mansoni egg in lung tissue.doi:10.1371/journal.pntd.0003860.g002PLOS Neglected Tropical Diseases | DOI:10.1371/journal.pntd.0003860 July 23, 2015 2 / 6pulmonary nodule in the right lung. A pulmonary CT scan detected multiple nodules between7 and 13 mm of diameter (Fig 2A).A biopsy allowed us to remove the bigger nodule (13 mm diameter), located in the rightlung, close to the pleura. Histological examination of the nodule revealed several S.mansonieggs (Fig 2B) surrounded by histiocytes. Meanwhile, reverse transcription PCR (RT-PCR)resulted positive forMycobacterium tuberculosis on two sputum samples, and a specific treat-ment for tuberculosis was started.Case DiscussionUsually, eggs of S.mansoni are found in stool, the intestinal tract, and the liver, rarely in thecentral nervous system (CNS) [1]. Ectopic sites of S.mansoni are reported in the literature,but almost all of them were found by autopsy. Ectopic sites are defined as adult worms and/oreggs outside the portal-mesenteric system, that is, excluding the liver and intestine [2]. Gonçal-ves et al., in their series of 1,863 consecutive autopsies carried out in Belo Horizonte, Brazil,reported 313 cases (16.8%) of S.mansoni infection, with eggs found in almost all organs;ninety-three cases with schistosomiasis (29.7%) had eggs in the lungs, while one case (0,3%)had eggs in the spleen. Other organs involved were the pancreas (6.4%), brain (4.8%), lymphnodes (3.8%), testicles (3.2%), kidney (2.9%), oesophagus (1.0%), gall bladder (1.0%), heart(1.0%), stomach (0.3%), spinal cord (0.3%), ovary (0.3%), pleura (0.3%), prostate (0.3%), andeye (0.3%) [2]. According to the authors, ectopic locations probably derive from a high parasiteburden, causing portal hypertension and subsequent embolization of the parasite eggs throughthe collateral portal-systemic circulation [2]. This theory could explain a diffuse homogeneouspresence of S.mansoni eggs in the different organs, but not the finding of a mass as reported inour two cases. Faust in 1947 reported that adult worms, too, were occasionally discovered [3]: amale of S. haematobium in the circumflex branch of the coronary artery [4], and a pair of maleand female worms with degenerating eggs in a branch of the superior ophthalmic vein, causinga palpebral tumor [5]. Brumpt, in 1949, reported that females of S.mansoni can be found, andlay eggs, in different organs including the lungs [6].Faust analysed five possible explanations of ectopic lesions in schistosomiasis [3]: the firsttheory, that the metacercariae develop to adult worms near the sites of penetration into theskin, was considered not consistent with critical studies on the development of schistosomes inthe body of the definitive host; the second theory, a patent foramen ovale, implied a highlyimprobable combination of circumstances; the third theory, that the eggs may escape throughthe pulmonary capillaries and be deposited in distant arterioles, was discarded because of thecharacteristic disposition of eggs in nests or aggregates, and the tissue reaction around thevenules rather than arterioles. He considered more probable the fourth theory, that adultworms may travel against venous blood flow into collateral vessels and, on reaching the endvenules, deposit their eggs, and the fifth theory, that the vertebral venous system provides a nat-ural, valveless, intercommunicating channel from portal and caval veins to all parts of the body[3].A common feature of our two cases was the presence of comorbidities: in case 1, a sepsisdue to KPC and in case 2, a pulmonary TB. Interestingly, a case of pulmonary schistosomiasischaracterized by a lower lobe lung mass associated with pulmonary TB was recently reported[7]: the species involved was a S. japonicum, and the eggs were found at postmortem examina-tion [7].PLOS Neglected Tropical Diseases | DOI:10.1371/journal.pntd.0003860 July 23, 2015 3 / 6In the literature, an association between S.mansoni and bacteremia is reported: the bacteriamore frequently associated are Salmonella, Escherichia coli, and Salmonella aureus [8,9]. Sev-eral pathogenic mechanisms have been proposed to explain this association: from an enhancedbacterial adhesion to granulomata to an inhibition of Th1 immune response [8,10]. Schistoso-miasis is also reported to be a predisposing factor for pyogenic liver abscess [8,10,11]. In one ofthe case reports, the liver biopsy showed a great number of S.mansoni eggs in the hepatic tissue[11].Unnecessary surgical procedures for unrecognized parasitic diseases have been reportedboth for the lungs and the spleen. According to a case report fromMartinique reported in1988, an open chest lung biopsy was performed in a female patient on suspicion of Carring-ton’s disease, resulting in a case of pulmonary S.mansoni bilharziasis [12]. In the United States(2008) and in Japan (2007), two patients with pulmonary nodules were submitted, respectively,to a fine-needle aspiration biopsy and to a right middle and lower lobectomy; the histologicalexam revealed in both cases the presence of Paragonimus [13,14]. Concerning unnecessarysplenectomy, performed under suspicion of malignant lymphoproliferative disorders, severalexamples have been reported for different parasitic diseases. Three patients developed malariaafter surgery, with a final diagnosis of hyperreactive-malarial splenomegaly (HMS) [15,16]. Intwo cases, the true cause of splenomegaly was an unrecognized visceral leishmaniasis [17,18].In two more cases, histology of the spleen revealed multiple granulomata around Loa loamicrofilariae [19]. The description of the latter, published cases, was crucial to spare an unnec-essary splenectomy to a further patient seen at CTD, Negrar by some of us [20]. Besides a clini-cal suspicion of loiasis (hypereosinophilia, Calabar swelling), not confirmed by laboratoryidentification, the latter patient also presented multiple hypoechogenic lesions of the spleenthat completely disappeared (along with the eosinophilia and the other clinical signs) a fewweeks after presumptive treatment of L. loa infection with diethylcarbamazine DEC [20]. Asfor schistosome, to our knowledge, our case 1 is the first description of S.mansoni eggs in thespleen tissue of a living patient.We treated both patients with a three day course of praziquantel (40 mg/kg/day, divided intwo doses), which differs fromWHO recommendations (40mg–60mg/kg body weight as a sin-gle dose) [21]. In a meta-analysis carried out by Zwang and Olliaro [22], the cure rate of a sin-gle dose of praziquantel was 76.7% and, considering that our patients were not at risk forreinfection, we wanted to increase the odds of cure.ConclusionsIn the global village, clinicians should open their “clinical landscape” to a number of diseasesthey have little, if any, familiarity with. Moreover, some of them may present with uncommon,atypical presentations that may be mistaken for other diseases. With this possibility in mind,an accurate clinical and epidemiological history, along with appropriate laboratory exams, canhelp the clinician to make the appropriate decision while avoiding unnecessary invasive andpotentially dangerous procedures. In particular, the clinicians should consider schistosomiasisdue to S.mansoni in case of a patient coming from sub-Saharan Africa, the east coast of SouthAmerica between Venezuela and Brazil, the Caribbean, Egypt, and the Arabian peninsula.Ethics StatementThe two patients gave written informed consent for the publication of these case reports.PLOS Neglected Tropical Diseases | DOI:10.1371/journal.pntd.0003860 July 23, 2015 4 / 6Key Learning PointsReferences1. Colley DG, Bustinduy AL, Secor WE, King CH. Human schistosomiasis. Lancet. 2014; Jun 28; 383(9936):2253–64. doi: 10.1016/S0140-6736(13)61949-2 PMID: 246984832. Gonçalves EC, Fonseca AP, Pittella JE. Frequency of schistosomiasis mansoni, of its clinicopathologi-cal forms and of the ectopic locations of the parasite in autopsies in Belo Horizonte, Brazil. J Trop MedHyg. 1995; Oct; 98(5):289–95. PMID: 75632533. FAUST EC. An inquiry into the ectopic lesions in schistosomiasis. Am J Trop Med Hyg. 1948; Mar; 28(2):175–99. PMID: 188580204. El Gazayerli M. Unusual site of schistosome worm in the circumpflex branch of left coronary artery.Jour. Egyptina Med Assn. 1939; 22:34–37.5. Badir G. Schistosomiasis of the conjunctiva. Br J Ophthalmol. 1946; Apr; 30(4):215–21. PMID:181702096. Brumpt E. Précis de parasitologie. Vol I. Masson Editeurs. Paris, France; 1949; 687–90.7. Tang TH, Wong SS, LamW, CheukW, Lai CK, Wu TC. A 93-year-old man with a left lung mass andexudative pleural effusion. Schistosoma japonicum. Clin Infect Dis. 2014; Jan; 58(2):300–1. doi: 10.1093/cid/cit678 PMID: 243688138. Lambertucci JR, Rayes AA, Serufo JC, Nobre V. Pyogenic abscesses and parasitic diseases. Rev InstMed Trop Sao Paulo. 2001; Mar-Apr; 43(2):67–74. PMID: 113404789. Lambertucci JR, Rayes AA, Serufo JC, et al. Schistosomiasis and associated infections. Mem InstOswaldo Cruz. 1998; 93 Suppl 1:135–9. PMID: 992133510. Goldani LZ, dos Santos RP, Sugar AM. Pyogenic liver abscess in patients with schistosomiasis man-soni. Trans R Soc Trop Med Hyg. 2005; Dec; 99(12):932–6. PMID: 1615735611. Teixeira R, Pfeilsticker FJ, Santa Cecília et al. Schistosomiasis mansoni is associated with pyogenicliver abscesses in the state of Minas Gerais, Brazil. Mem Inst Oswaldo Cruz. 2001; 96 Suppl:143–6.PMID: 1158644012. Grunstein P, Broquie G, Gayet AM, Bazelly B, Fouret P. Pulmonary bilharziasis due to Schistosomamansoni simulating Carrington's disease. Rev Pneumol Clin. 1988; 44(3):146–50. PMID: 305756513. Zarrin-Khameh N, Citron DR, Stager CE, Laucirica R. Pulmonary paragonimiasis diagnosed by fine-needle aspiration biopsy. J Clin Microbiol. 2008; Jun; 46(6):2137–40. doi: 10.1128/JCM.02424-07PMID: 1838544414. Osaki T, Takama T, Nakagawa M, Oyama T. Pulmonary Paragonimus westermani with false-positivefluorodeoxyglucose positron emission tomography mimicking primary lung cancer. Gen Thorac Cardio-vasc Surg. 2007; Nov; 55(11):470–2. PMID: 1804985615. Bidegain F, Berry A, Alvarez M, et al. Acute Plasmodium falciparummalaria following splenectomy forsuspected lymphoma in 2 patients. Clin Infect Dis. 2005; Jun 1; 40(11):e97–100. PMID: 15889352• Ectopic eggs of S.mansoni can be found in different organs including the lungs andspleen.• Schistosomiasis should be considered in “the clinical landscape” in case of travellerscoming from endemic countries with hypereosinophilia, even if the presentation is nottypical.• Unnecessary surgical procedures for unrecognized parasitic diseases can be avoided byan accurate clinical and epidemiological history, along with appropriate laboratoryexams.• In the literature, an association between S.mansoni and bacteremia is reported: thebacteria more frequently associated are Salmonella, E. coli and S. aureus.PLOS Neglected Tropical Diseases | DOI:10.1371/journal.pntd.0003860 July 23, 2015 5 / 616. Chim CS, Wong SS, Lam CC, Chan KW. Concurrent hyperreactive malarial splenomegaly and quartanmalarial nephropathy—Plasmodiummalariae revisited. 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World Health Organization (2006) Preventive chemotherapy in human helminthiasis: coordinated useof anthelminthic drugs in control interventions: a manual for health professionals and programmeman-agers. 2006; Available: whqlibdoc.who.int/publications/2006/9241547103_eng.pdf.Accessed 2/1/2014.22. Zwang J, Olliaro PL. Clinical efficacy and tolerability of praziquantel for intestinal and urinary schistoso-miasis-a meta-analysis of comparative and non-comparative clinical trials. PLoS Negl Trop Dis. 2014Nov 20; 8(11):e3286. doi: 10.1371/journal.pntd.0003286 PMID: 25412105PLOS Neglected Tropical Diseases | DOI:10.1371/journal.pntd.0003860 July 23, 2015 6 / 6

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Schistosoma mansoni eggs in spleen and lungs, mimicking other diseases

Schistosoma mansoni Eggs in Spleen and Lungs, Mimicking Other Diseases

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