pathology of pyogenic liver abscess in children

Pathology of Pyogenic Liver Abscessin Children

FAUSTO E.L. PEREIRA,1* CARLOS MUSSO,2 AND JANE S. CASTELO2

1Department of Pathology, Nucleo de Doencas Infecciosas CBM-UFES, Av Marechal Campos 1468,29040-091 Vitoria, ES Brazil2Hospital Infantil N.S. da Gloria and Nucleo de Doencas Infecciosas CBM-UFES, Vitoria, ES Brazil

Received August 17, 1998; accepted January 4, 1999.

ABSTRACTLittle is known about preexisting lesions in livers ofchildren with pyogenic liver abscess (PLA). Study ofthese lesions may elucidate possible predisposing factorsfor the disease. In Vitoria, state of Espirito Santo, Brazil,PLA in children is frequently associated with helminthicinfections and eosinophilia. We hypothesize that nema-tode infection with larvae migrating through the liver is apredisposing factor for PLA, because the infection in-duces immunomodulation and likely trapping of bacte-ria in liver granulomas. In this report, we describeobservations of 22 cases of PLA in children studied atautopsy (16 cases) or in surgical biopsies (6 cases),including 17 boys and 5 girls ranging in age from 1 to 13years (mean 4.6 years, median 3.5 years). Multiple ab-scesses in both lobes were found in 13 cases and a singleabscess was found in the right lobe in 10 cases. All casesshowed histologically classical pyogenic inflammationwithout morphological evidence of amoebiasis. In sixcases there were granulomas similar to those caused bylarva migrans visceralis (from Toxocara or other nema-todes) in liver tissue not affected by the abscess. Nema-tode antigens in central areas of necrosis of granuloma inall six cases and fragments of a larva, possibly of Toxo-cara, were found on samples immunohistochemicallystained with polyclonal anti-Toxocara antibodies. Therewere numerous eosinophils in abscesses with Charcot-Leyden crystals. Eosinophils were found frequently inportal triads far from the abscess wall. In four cases, inwhich bile duct ascariasis was found, worms were notedin the bile ducts, and eggs were found in liver paren-chyma surrounding the abscess in two cases. Foreign-

body granulomas were found in one case in whichpenetrating trauma was the cause of abscess. In one casethere was one histiocytic granuloma whose origin wasnot determined. The observation of six cases of granu-loma similar to larva migrans visceralis (or produced byother nematode larva) in liver tissue not directly affectedby the abscess supports the hypothesis that helminthinfections with larva migrating through the liver are apredisposing factor for pyogenic hepatic abscess in chil-dren.

Key words: helminthiasis, larva migrans visceralis, liverabscess, toxocariasis

INTRODUCTIONPyogenic liver abscesses in children are rare indeveloped countries. The predisposing factors areimmunodeficiencies, alterations in innate defensemechanisms, appendicitis, cholecystitis, and, lessfrequently, skin and respiratory infections [1–4]. Indeveloping countries, reports of pyogenic liver ab-scess are uncommon, although some observationsindicate that they are more frequent than in devel-oped countries, even those countries where inva-sive amoebiasis is frequent [5–7]. In Vitoria (stateof Espirito Santo, Brazil) it has been reported thatpyogenic liver abscesses are frequent in childrenfrom poor socioeconomic conditions and are oftenassociated with peripheral eosinophilia and intesti-nal parasites [8,9]. These observations led us topropose that nematode infections, in which thelarvae migrate through tissues including the liver,*Corresponding author

Pediatric and Developmental Pathology 2, 537–543, 1999 Pediatric and Developmental Pathology

r1999 Society for Pediatric Pathology

would be a predisposing factor for pyogenic liverabscess in children. Immunomodulation inducedby helminthic infections [10,11] may reduce themicrobicidal activity of phagocytes, thus enhanc-ing the growth of bacteria trapped in granulomasinduced by nematode larvae in the liver.

There are few reports in the literature aboutthe pathology of pyogenic liver abscess in children,with regard to previous lesions in liver tissue notaffected by the abscess. Beaver [12] and Lee andBlock [13] proposed that lesions in liver tissuecould be areas of bacterial colonization. Theseauthors suggested that infection of focal areas ofnecrosis or scars of granulomatous hepatic lesionsis a predisposing factor for the development of liverabscess.

Considering the possibility that the presenceof preexisting granulomas induced by larva mi-grans visceralis (or other nematode larva) in theliver might represent a predisposing factor forpyogenic liver abscess, we studied the livers fromchildren with pyogenic liver abscesses in an at-tempt to demonstrate that such granulomas orother prexisting lesions could be associated withthe abscess. We report here the main pathologicfeatures observed in livers from 22 children withpyogenic liver abscess, studied at autopsy (16 cases)or in surgical biopsies (6 cases).

METHODSFrom December 1985 to January 1997, 22 cases ofPLA were studied at necropsy (16 cases) or insurgical specimens (6 cases in which a laparatomywas performed to drain the abscess) at the Pathol-ogy Unit at Children’s Hospital Nossa Senhora daGloria in Vitoria, Espirito Santo, Brazil. The dataregarding age, sex, origin of patients, bacterialetiology, peripherial eosinophilia, fecal examina-tion for parasites, and type of material studied arelisted in Table 1.

Fragments of liver parenchyma not involvedin the abscess and fragments of the abscess wallwere paraffin embedded and the sections stainedby routine methods. Nematode larvae or its anti-gens in granulomatous lesions were identifiedthrough a polyclonal anti-Toxocara serum in anindirect immunostaining procedure. The anti-Toxocara anti-serum was elicited in rabbits afteroral administration of infective Toxocara canis eggs

according to Smith et al. [14]. An avidin-biotinperoxidase kit from Sigma Chemical Co. (St. Louis,MO) was used to stain paraffin sections accordingthe manufacturer’s instructions. No previous ad-sorption with antigens of other nematode wasdone to the rabbit serum. For this reason, cross-reactivity with other nematode larvae was noteliminated [15].

Information regarding the number and local-ization of abscesses in surgical cases was obtainedby ultrasonography.

RESULTSData on the number and localization of abscesses,the presence of bile duct ascariasis or other associ-ated disease, presence of intestinal parasites, andpertinent microscopic observations for each caseare summarized in Table 2.

In all cases, the histological picture of theabscess was a typical purulent inflammation withfrequent bacterial colonies in the exudate. In caseswith multiple lesions, the abscesses were localizedalong the portal triads. Many eosinophils werefound in the exudative zone of abscesses in 11cases, especially in cases associated with bile ductascariasis or in other cases in which granulomassimilar to those induced by visceral larva migransor induced by other nematode larva were found.Charcot-Leyden crystals were found in the puru-lent exudate in two cases. Eosinophils infiltratingthe portal triads were found in 82% of cases (Table 2).

In six cases the liver tissue surrounding theabscess showed granulomas with macrophages inpalisade configuration with numerous eosinophilsencompassing amorphous eosinophilic material,resembling granulomas induced by visceral larvamigrans or other nematode larva (Figs. 1A and 2A).Sometimes the granulomas contained a large num-ber of eosinophils in tandem with macrophagesand infrequent giant cells. In these cases, theCharcot-Leyden crystals were frequently observed.

These granulomas are very similar to thoseformed around nematode larvae. All six cases hadnecrotic material stained by the polyclonal anti-Toxocara antibodies (Fig. 3A). In one case, therewas a granuloma presenting a circular structure,17.5 µm across, with an amorphous, thick wall anda 17 3 36 µm oval structure. These structures

538 F.E.L. PEREIRA ET AL.

resemble both cross- and oblique sections of anematode larva (Fig. 1A,B). These two structures,as well as the necrotic material, were stained bypolyclonal anti-Toxocara anti-serum (Fig. 3A–C).Because the polyclonal anti-Toxocara anti-serumused was not adsorbed with antigens of othernematodes to eliminate cross-reactivity, immuno-histochemical analysis enabled us to confirm thatthe structures observed were fragments of a nema-tode larva, not allowing identification of genera orspecies. The morphological and morphometricalcriteria presented by Nichols [16,17] however, sug-gest that the sections of larva observed here arefrom a Toxocara sp. (Fig. 1A,B). In the other fivecases, although the necrotic material observed insome granulomas was stained with polyclonal anti-Toxocara antibodies, remnants of larvae were notfound. Granulomas at different phases of cicatriza-tion were observed in all six cases.

Ascaris eggs were found in the pyogenic zonein two cases of bile duct ascariasis.

In a case of penetrating abdominal traumawith a wood picket, foreign-body granulomas withgiant cells engulfing material similar to vegetablefiber were found near the abscess wall (Fig. 2B).

A histiocytic granuloma, with foamy macro-phages and Langhans-type giant cells, was found inone case. It was not possible to identify the etiologyof this granuloma.

Lesions suggestive of Schistosoma mansoniinfection were not observed. No abscess showedany microscopic evidence of amebic necrosis.

Lesions suggestive of previous immunodefi-ciency disease were not found.

DISCUSSIONThe origin, age, and sex of patients, as well as thefrequency of bile duct ascariasis among the 21

Table 1. Profile of 22 cases of pyogenic liver abscess in children

Case Age (years) Sex Birthplace Eosinophils/ mm3 Culture Intestinal nematodea

N96 2 M Serrab 0 nd A

N240 5 F Cariacicab 1460 S. aureus A 1 S

N472 3 M A. Claudio 0 E. coli A

N583 1 M Serrab 904 S. aureus A

N587 4 M Vianab 1300 S. aureus Absent

N779 7 M Aimores 3190 S. aureus T

N818 10 F Vitoriab 1518 S. aureus Absent

N1036 12 M Serrab 1200 S. aureus Absent

N1401 2 M Cariacicab 936 S. aureus Absent

N1742 4 M Fundao 296 S. aureus Absent

N1920 1 F Vitoriab 174 nd A

N2029 2 F Cariacicab 0 S. aureus A 1 S

N2168 2 M T. de Freitas 118 S. aureus Absent

N2507 2 M A. Claudio 53 S. aureus A

N2656 2 F Guarapari nd nd A

N2664 5 M Colatina nd nd Absent

B1121 13 M S. Mateus 1690 nd nd

B1242 1 M Vitoriab 384 nd A

B1595 7 M Serrab 217 S. aureus nd

B3920 7 M Cariacicab 3744 nd A

B4432 2 M Aracruz 4379 nd A

B6268 7 M Cariacicab 2844 S. aureus A

A, Ascaris lumbricoides; B, biopsy; N, necropsy; nd, not done; S, Strongyloides stercoralis; T, Trichuris trichiura.aParasites observed in routine fecal examination or at autopsy.bSuburbs of metropolitan Vitoria.

PYOGENIC LIVER ABSCESSES 539

cases of pyogenic liver abscess in children studied,were similar to those observed in a series of casesreported in Vitoria [8,9]. As demonstrated by cul-ture results of abscess material, the main causativeorganism was Staphylococus aureus (13/14 cases),which was also found in prior reports from thesame hospital [8,9].

Macro- and microscopic observations showedtypical features of pyogenic abscess in all caseswith no morphological characteristics of amebicnecrosis. This concurs with prior reports of pyo-genic abscess in the southeastern region of Brazilwhere invasive amebiasis is uncommon [18].

Although the state of Espirito Santo has areasendemic for schistosomiasis, Schistosoma mansoni

infection was not diagnosed in this series. Thisobservation parallels our previous report demon-strating that schistosomiasis is not a significantpredisposing factor for pyogenic liver abscess inchildren in Vitoria [19]. As observed in previousreports [9,19], most of the cases studied here camefrom the urban periphery of metropolitan Vitoria(formed by the cities of Vitoria, the state capital,Cariacica, Serra, Vila Velha, and Viana), wheretransmission of schistosomiasis does not occur, butnematode infections are frequent.

The frequency of granulomas produced bynematode larvae observed among the 22 cases ofpyogenic liver abscess presented here (6/22 or28.6%) is very high, especially when the frequencies

Table 2. Number and localization of abscesses and associated pathological findings in 22 casesof pyogenic liver abscess in children

Case Abscesses Other findingsPortaleosinophilia

Lesions in surroundingliver tissue

N96 Several, RL/LL Bile duct ascariasis 1 Moderate steatosis; ascaris eggs in pyogenic area

N240 1, RL 111 Hydropic degeneration of hepatocytes

N472 Several, RL/LL Bile duct ascariasis 1 Severe diffuse steatosis

N583 Several, RL/LL Absent Diffuse hydropic degeneration of hepatocytes

N587 1, RL 1 Diffuse hydropic degeneration of hepatocytes

N779 1, RL 1 Granulomas similar to VLM; calcifications inabscess wall

N818 1, RL Chronic pyelonephritis 1 Hemosiderosis in abscess wall

N1036 1, RL 11 Diffuse hydropic degeneration and steatosis ofhepatocytes

N1401 1, RL 111 Hydropic degeneration of hepatocytes

N1742 Several, RL/LL 11 Granulomas similar to VLM

N1920 Several, RL/LL 111 Granulomas similar to VLM; focal steatosis

N2029 Several, RL/LL Bile duct ascariasis 11 Focal steatosis

N2158 Several, RL/LL 1 Granulomas similar to VLM

N2507 Several, RL/LL Absent Focal steatosis

N2656 Several, RL/LL 11 Diffuse hydropic degeneration of hepatocytes

N2664 1, RL Recent scar in abdominalwall

Absent Foreign body granulomas with foreign materialin giant cells

B1121 1, RL 111 Diffuse hydropic degeneration of hepatocytes

B1242 Several, RL/LL Bile duct ascariasis 11 Ascaris eggs in abscess wall

B1595 Several, RL/LL 111 Granulomas similar to VLM

B3920 Several, RL/LL 1 Unspecified histiocytic granuloma with Lang-hans-type giant cells

B4432 1, RL 111 Granulomas similar to VLM

B6268 Several, RL/LL Absent Diffuse hydropic degeneration and focal ste-atosis

LL, left lobe; RL, right lobe; VLM, visceral larva migrans; 1, mild; 11, moderate, 111, severe.


of similar granulomas observed in livers fromchildren necropsied at the same hospital are com-pared. Partial results in our laboratory demon-strate the presence of granulomas similar to thoseproduced by nematode larvae in 5 out of 92 chil-dren who died of diseases other than pyogenic liverabscess (C. Musso et al., unpublished data). Toxo-cara was probably the most frequent cause of thesegranulomas. Among 13 children with pyogenicliver abscess, 9 (69%) had a positive ELISA IgG testwith secretory–excretory antigens of second-stagelarvae of Toxocara canis. This frequency was signifi-cantly higher than that observed (28%) among 110patients without staphylococcal infection admittedat the same hospital [20]. Therefore, we suggest thepotential role of visceral larva migrans (from Toxo-cara or other nematodes) as a predisposing factorfor pyogenic liver abscess in children. It may beassumed that a visceral larva migrans granuloma(or granuloma induced by larvae of other hel-minth) would enhance the trapping of bacteria in

the liver. This hypothesis is reinforced by reportsdemonstrating an association between pyogenicliver abscess and acute schistosomiasis in children[21,22]. According to these reports, the necroticgranulomas induced by Schistosoma eggs duringan acute infection would predispose to the pres-ence of bacteria in the liver, facilitating abscessformation. Also, Jarry et al. [23], describing apyogenic liver abscess in a child with one femaleascaris in the jejunum, raised the hypothesis thatgranuloma induced by ascaris eggs or larvae in theliver, as described by Pelissier et al. [24], would be apredisposing factor for Staphylococcus growth inthe liver.

Immunomodulation induced by infection withhelminths may be another explanation for theincreased risk of pyogenic liver abscess in childrenwith larva migrans visceralis or other helminthia-ses. A dramatic induction of the Th2 lymphocytesubset occurs in helminthic infections, which iswell characterized in experimental models by the

Figure 1. A: Granuloma with morphology similar togranuloma induced by nematode larva. A central area ofnecrosis is surrounded by giant cells and macrophages.Eosinophils and lymphocytes are present in the periph-ery of the granuloma. Sections of two fragments of anematode larva (arrows) are observed within the ne-crotic area (H&E). B: High-magnification view of granu-loma showing cross-section of larva within necroticmaterial formed mainly by dead eosinophils (H&E).

Figure 2. A: Necrotic granuloma without remnants oflarva. There are some giant cells and a loose infiltrate ofmacrophages surrounding the necrotic area. Eosinophilsand lymphocytes are observed in the periphery ofthe granuloma (H&E). B: Foreign-body granuloma ob-served near the abscess wall in a case in which thepredisposing factor was a penetrating abdominal trauma(H&E).


induction of IL-4 and IL-5 and down-regulation ofinterferon g (IFN-g), resulting in eosinophilia andthe production of high levels of IgE [25,26]. Thisimmunomodulation would reduce the microbici-dal capacity of phagocytes, thus enhancing bacte-rial infections, as demonstrated in some animalmodels [27]. Another possibility is the action of theparasite as an adjuvant for IgE production againstbacterial antigens, thus inducing histamine releasein tissues with impairment of chemotactic andmicrobicidal activity of phagocytes, as occurs inJob’s syndrome [28–31]. The adjuvant effect ofparasite antigens for IgE production when a third-party antigen is administered at the time of ahelminthic infection has been well demonstrated[32–34]. The microbicidal activity of infected organ-isms has not yet been studied. In the only study ofleukocyte function during helminth infection inhumans, a reduced chemotaxis of neutrophils,which improved after treatment, was demon-

strated in vitro in one child with visceral larvamigrans [35].

Another possible explanation for the in-creased risk for pyogenic liver abscess in childrenbearing a nematode infection is the transportationof bacteria by larvae migrating through the liver.Supporting this hypothesis is the presence of en-teric bacteria in the digestive tract or adsorbed onthe surface of both Strongyloides larvae [36] andadult Schistosoma worms [37,38]. However, it seemsless likely in cases reported here, since most ofpyogenic liver abscesses were due to Staphylococusand not due to bacteria from enteric flora.

The hypothesis that helminth infection withmigrating larvae is a predisposing factor for pyo-genic liver abscess in children is supported by thefrequency of eosinophils in the abscess exudate (11cases) and in the portal triads (88% of cases), thehigh frequency of peripheral eosinophilia (57.1% ofcases with .600 eosinophils/mm3), and the highfrequency of intestinal parasites (65% of 20 cases)observed among the 22 cases presented here. Al-though eosinopenia is expected in pyogenic liverabscess because of the severity of the disease,eosinophilia is frequently observed in children withpyogenic liver abscess in Vitoria [9].

We conclude that the high frequency of granu-lomas similar to those of visceral larva migrans orproduced by larvae of other nematodes in childrenwith pyogenic liver abscess supports the hypothesisthat helminthic infection, mainly Toxocara, mayrepresent an important predisposing factor forliver abscess in children.

ACKNOWLEDGMENTS

We thank Steven Crowley and Abdallah Rebeiz forhelp in editing. Our research was supported byFACITEC (Science and Technology ResearchAgency from the municipality of Vitoria, ES, Bra-zil).

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pathology of pyogenic liver abscess in children

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