Keywords:

Strongyloides stercoralis

– complicaciones – glomerulonefritis – Perú.

1. Instituto de Medicina Tropical Alexander von Humboldt (IMTAvH), Universidad Peruana Cayetano Heredia (UPCH), Lima, Perú.

2. Internal Medicine Residency Program, University of Texas Health Science, Houston, Texas, USA.

3. Instituto Especializado de Salud del Niño, Lima, Perú.

4. Laboratorio de Parasitología, Instituto de Medicina Tropical Alexander von Humboldt (IMTAvH), Universidad Peruana Cayetano Heredia

(UPCH), Lima, Perú.

Neotrop. helminthol., 1(1) , 2007

Strongyloidiasis, caused by

Strongyloides stercoralis

, is a serious Public Health problem in Peru. We report the case

of a two-year-old boy who was admitted at the Instituto Especializado de Salud del Niño in Lima with a diagnosis of

intestinal obstruction associated with fifteen days of diarrhea, fever and cough. The histopathological examination of

the necrotic tissue of colon showed intestinal neuronal dysplasia. During his hospitalization (12 days later) he pre-

sented hypereosinophilia (with 3,460 eosinophils/mm

), cough, fever and abnormal chest x-ray. Five days later, the

eosinophil count reached up to 34,286 cells/mm

. One day later,

S. stercoralis

larvae were found in a direct stool

smear. Serology tests for HTLV-1 and HIV were negative. Interestingly, our patient presented microscopic hematuria

and high blood pressure during the highest levels of eosinophils in blood, therefore acute glomerulonephritis was

suspected. Treatment with thiabendazole was readily started, and administered during seven days. After that, clini-

cal findings disappeared and larvae were no longer detected in stool examinations. The patient was asymptomatic

at discharged. This case presents strong evidence to be a hyperinfection of due to autoinfection triggered by the

surgery as a stress factor.

Resumen

Abstract

La strongyloidiosis, causada por

Strongyloides stercoralis

, es un serio problema de Salud Pública en el Perú. Re-

portamos a un niño de dos años de edad quien fue admitido en el Instituto Especializado de Salud del Niño en Lima

con el diagnóstico de obstrucción intestinal asociado a 15 días de diarrea, fiebre y tos seca. El examen histopatológi-

co del tejido necrótico del colon reveló displasia neuronal intestinal. Posteriormente, durante su hospitalización (12

días después) presentó hipereosinofilia (con 3,460 eosinófilos/mm

), tos, fiebre y una radiografía de tórax anormal,

5 días después el recuento de eosinófilos llegó hasta 34,286 células/mm

. Un día después se encontraron larvas

S. stercoralis

en el examen directo de heces. La serología para HTLV-1 y HIV 1 fueron negativos. Cabe men-

cionar que nuestro paciente presentó hematuria microscópica e hipertensión arterial durante los más altos niveles

de eosinófilos en sangre, por lo que se sospechó en una glomerulonefritis aguda. El tratamiento con tiabendazol se

inició rápidamente, y fue administrado durante siete días. Los hallazgos clínicos desaparecieron y no se encontraron

más larvas en los exámenes de heces. El paciente fue dado de alta asintomático. Este caso presenta fuertes indicios

de ser una hiperinfección por

S. stercoralis

debido a la autoinfección desencadenada por la cirugía la cual intervino

como factor estresante.

Palabras clave:

Strongyloides stercoralis

– complications – glomerulonephritis – Peru.

NOTA CIENTÍFICA / RESEARCH NOTES

STRONGYLOIDES STERCORALIS

ASSOCIATED WITH NEPHRITIC

SYNDROME IN A CHILD WITH INTESTINAL NEURONAL DYSPLASIA

STRONGYLOIDES STERCORALIS

ASOCIADO CON SINDROME NEFRÍTICO

EN UN NIÑO CON DISPLASIA INTESTINAL NEURONAL

Luis A Marcos1,2,4, Daniel Lozano3, Guillermo Calvo3, Lenin Romani1 & Angélica Terashima4

Forma de citar: Marcos, L A, Lozano, D, Calvo, G, Romani, L & Terashima A. 2007. Strongyloides stercoralis

associated

with nephritic syndrome in a child with intestinal neuronal dysplasia.

Neotropical Helminthology, vol. 1, no. 1,

pp. 37-42

Fecha de recepción: 12 de abril del 2006, fecha de aceptación: 22 de setiembre del 2006.

Neotrop. helminthol., 1(1) , 2007

Strongyloides stercoralis

and nephritic syndrome in a child. Marcos

et al.,

thorax, there were bilateral lung crackles and wheez-

ing. The abdomen was distended, diffusely tenderness

with peritoneal signs. No hepato- or splenomegaly were

present. No peripheral edema was noted. The bowel

sounds were hyperactive and a rectal examination re-

vealed mucus and blood in stools. Stool examination

(direct smear) showed from 7 to 15 red blood cells,

20 to 35 white blood cells per high power field and

Entamoeba

coli

cysts.

Chest X-ray did not show any alteration. The white blood

cell count was 22,600 cells/µL with 81% neutrophils,

hematocrit 34%, erythrocyte sedimentation rate (ESR)

35 mm/h, blood urea 34 mg/dL, creatinine 1.25 mg/dL,

serum potassium 1.82 mEq/dL. Other electrolytes were

normal. The potassium was adequately corrected and

the patient was hydrated, but abdominal distention and

peritoneal signs persisted. An abdominal X-ray showed

dilated intestinal loops. Therefore, the emergency team

decided to operate the patient with the diagnosis of in-

testinal obstruction.

The surgical findings were dilated intestinal loops and

narrowed descendent colon with signs of necrosis, so it

was resected. After the surgery, the patient was admitted

to The Intensive Unit Care (IUC) and was treated with

wide-spectrum antibiotics, some results of blood analy-

ses were: creatinine 0.79 mg/dL, serum potassium 3.23

mEq/dL and albumin 2.5 mg/dL. The histopathological

examination of colon showed neuronal intestinal dyspla-

sia. On September 29th, the patient had a functional

colostomy, improved favourably and coursed asymp-

tomatic. On October 6th, he presented with productive

cough and tachypnea.

The following day high fever (38,8 ºC) and crackles in

lower right thorax appeared. Chest X-ray revealed a pa-

renchymal infiltrated in the right parahiliar region. The

white blood cell count showed 17,300 cells/µL, 2%

bands, 38% neutrophils and 20% eosinophils. Therefore,

this was thought to account for nosocomial pneumo-

nia and the treatment was started with broad-spectrum

antibiotics. On October 10th, no clinical improvement

was reported. A control chest X-ray showed infiltrative

changes in the right lower lobe, parahiliar region and in-

terstitial diffuse patron was observed, similar to the first

chest X-ray.

The white blood cell count was 37,000 cells/µL, 1%

INTRODUCTION

Strongyloidiasis is an intestinal parasitic disease caused

Strongyloides stercoralis

, a soil-transmitted intestinal

nematode. It has been estimated to infect up to 100 mil-

lion people worldwide, mainly in tropical and subtropical

regions (Genta, 1989; Genta, 2001; Grove 1989). It

is one of the most important intestinal parasitic diseases

in humans because it can produce a life-threatening ill-

ness in immunocompromised hosts (HTLV-1 co-infec-

tion, neoplasm, AIDS, radiation, severe malnutrition or

chronic corticosteroids therapy) when larvae disseminate

to multiple organs causing the hyperinfection syndrome.

The complications in this stage are malabsorption,

paralytic ileus, meningitis, gastrointestinal hemorrhage,

gram-negative bacteremia, pneumonia and septic shock;

the fatality rate can reach up to 77% (Rodriguez & Calde-

ron, 1991; García-Godos

et al

., 1992; Ma-hmoud,

1996; Nonaka

et al.

, 1998; Thomas & Costello 1998;

Gotuzzo

et al.

, 1999; Chieffi

et al

., 2000; Adedayo

al.

, 2001)

In Peru, strongyloidiasis is a serious Public Health prob-

lem. There are many hyperendemic regions with preva-

lence rates up to 41% where children are mostly affected

(Rodríguez & Calderón, 1991; Marcos

et al.

, 2002).

The recommended treatment agents are ivermectin

and thiabendazole (Náquira

et al.

, 1989; Datry

et al.

1994).

We report a case of human strongyloidiasis with intes-

tinal neuronal dysplasia that developed clinical acute

glomerulonephritis and then it was resolved with antihel-

mintic treatment. We suggest the possibility of

Strongy-

loides

-associated glomerulonephritis.

A 2-year-old male was admitted to emergency room at

Instituto de Salud del Niño in Lima on September 25,

2002; transferred from Cusco with a 15-day history

of bloody diarrhea, fever and cough. He was born and

raised in a jungle region of Cusco and belonged to the

Shipibo tribe.

Examination findings at admission revealed a pale and ir-

ritable infant with significant dehydration. His body tem-

perature was 100 ºF (37.8 ºC), pulse 140/min, blood

pressure 90/60 mmHg, and respiratory rate 32/min. In

CASE REPORT

Neotrop. helminthol., 1(1) , 2007

bands, neutrophils 20% and eosinophils 50%, ESR 25

mm/h. On October 15th, cough was persistent and

physical examination was significant for diffuse roncus

predominantly in lower right lung. The patient was clini-

cally stable with low fever and cough. A control white

blood cell count showed 55,300 cells/µL with 62%

eosinophils. Stool examinations were repeated with di-

rect smear technique and the results were negatives. A

gastric aspirate was not obtained because the patient’s

father did not give consent.

Figure 1. Chest X-ray shows a persistent right para-

hiliar infiltrative during the highest eosino-

philia level.

On October 19th, the patient clinically had a stable evo-

lution. A stool examination (direct smear technique) re-

vealed larvae of

S. stercoralis

. Chest X-ray revealed a

persistent parenchymal infiltrated in the right parahiliar

region (Figure 1).

He received a 7-day course of thiabendazole 250mg

twice a day. HTLV-1 and HIV 1+2 ELISA’s were nega-

tives. On October 25th, a white blood cell count showed

25,600 cells/µL with 53% eosinophils. The previous

urine examinations did not have any abnormal finding.

However, the last urine examination showed between 8

and 10 red blood cells per high power field and also he-

moglobin. Moreover, fever, poor appetite and dyspnea

were reported.

On physical examination, his pulse was 160/min and

blood pressure 170/100 mmHg. Cardiology recom-

mended treating with captopril 1 mg/kg/doses to control

the hypertension. A nephritic syndrome was suggested.

A renal ultrasonography was performed but no altera-

tions were described. A doppler ultrasonography was

done showing normal renal arteries morphology. Anti-

streptolysin antibodies (ASO) were within normal values;

and cells of Lupus Erythematosus test (LE cells test) were

negatives.

On November 29th, a control of white blood cell count

reported 12,400 cell/µL and 29% eosinophils. On De-

cember 1st, both stool examinations (direct smear) and

gastric aspirate (after tutor’s consent) were negatives.

One week after beginning thiabendazole, a urinary test

was normal. Further blood analysis were made, blood

urea 30.7 mg/dL, creatinine 0.52 mg/dL, glucose 74.6

mg/dL, total proteins 7.3 mg/dL, albumin 3.7 mg/dL,

globulins 3.6 mg/dL, serum sodium 136 mEq/dL and

serum potassium 5.21 mEq/d.

On December 13th, eosinophilia decreased significantly

(13,400 white blood cell/µL with 10% eosinophils), ESR

26 mm/h and hematocrit 35%. His urine examination

by microscopy made on December 21st presented with

mild glucosuria but on physical examination, he appeared

well, and the vital signs were normal. Therefore, due to

his favourable clinical evolution the clinical team decided

to discharge for follow-up after a week. The day

following discharge, the patient with his father revisited

institute complaining of nausea, vomiting, oral intole-

rance and watery diarrhea.

A presumptive diagnosis of osmotic diarrhea with sig-

nificant dehydration was done and he was hospitalized

again. In the next days, he did not present vomiting and

diarrhea. Stool examinations done periodically with sed-

imentation cup technique and plate agar culture were

negative for

S. stercoralis

. His basal blood pressure was

90/50 mmHg however, he presented peaks of hyperten-

sion up to 130/80 mmHg in two opportunities.

He was treated with antihypertensive drugs. He not pre-

sented hypertension since the two first episodes. A Cap-

topril Renal Scan was carried out to rule out renal artery

stenosis versus renovascular hypertension but it did not

show any abnormality. Finally, we concluded that eosin-

ophilia caused by

S. stercoralis

infection or the parasite

by itself or immunological factors could be the causing

of glomerulonephritis since clinical findings disappear

after thiabendazole treatment. After two months, a uri-

nary test was made and it was normal. Blood pressure

Strongyloides stercoralis

and nephritic syndrome in a child. Marcos

et al.,

controls were normal until three months of follow-up.

We report a case of a child with neuronal dysplasia

operated because an intestinal obstruction syndrome,

who after the surgery developed a hyperinfection syn-

drome due to

S. stercoralis

infection associated with a

nephritic syndrome during the highest peak of eosino-

philia. Since antihelminthic treatment was started, im-

provement of renal impairment was observed and a de-

crease of eosinophils counts as well. Involvement of the

kidney, glomerulonephritis, has been described in asso-

ciation with

S. stercoralis

disseminated infection (Wong

et al.

, 1998; Mitsunaga

et al.

, 2003).

In fact, symptoms usually respond promptly, as in our

case, to appropriate antihelminthic therapy. However,

Strongyloides

-related glomerulonephritis has not been

demonstrated

in situ

yet.

The development of nephritic syndrome in our patient

could have been caused by many possible factors such as

previous bacterial infection, autoimmune disorder; high

eosinophils count in blood or

S. stercoralis

larvae

per

. However, a decrease of blood pressure was observed

after antihelmintic treatment, as well as absence of red

blood cells in urine, along with a decreasing of eosino-

phils in blood. Moreover, the following laboratorial tests

were negatives or within normal values: ASO, LE cells,

renal ultrasonographic doppler, captopril renal scan and

ESR. Thus, a possible cause of acute glomerulonephritis

in our patient could be

S. stercoralis

infection. Immuno-

logical disorders, eosinophils or the parasite itself can be

involved. A kidney biopsy could have been contributory

to our hypothesis, but this invasive method was not ne-

cessary in the patient, since the clinical picture improved

notoriously and the evolution was favorable.

During the hospitalization, a high suspicion of the infec-

tion by this nematode in the patient was the high number

of eosinophils observed in the blood smear. However,

a presumptive diagnosis of nosocomial pneumonia was

done initially two weeks after the surgery. Despite the

fact that he was started on antibiotics, there had neither

a clinical nor laboratory analysis improvement. By con-

trast, a significant increased of eosinophils count up to

34286 cell/µL appeared. These findings, a progressive

eosinophilia and pulmonary infiltrates, bring to mind a

spectrum of parasitic diseases, mainly in their migratory

stages, including differential diagnoses such as

Ascaris

lumbricoides

, hookworms,

S. stercoralis

hyperinfec-

tion, toxocariasis and

Paragonimus

spp. (MacLean

et al.

1999). However, the last is not endemic from the region

where the patient came from, and because of the hype-

reosinophilia (>1,500 cell/µL), the first option thought

was strongyloidiasis. In the following days, there were

larvae of

S. stercoralis

found in feces and the suspected

diagnosis was confirmed.

Two possible mechanisms are involved in this process.

First, the surgery as a stress condition could have been

the factor which triggered the mechanism of autoinfec-

tion. The time since larvae are carried to the lungs af-

ter enters systemic vessels are 2 weeks, and this was

the time which the surgery was performed. Therefore,

we think the surgery could be the triggering factor to

develop the autoinfection. Second, under some cir-

cumstances such as chronic constipation (eg. intestinal

neuronal dysplasia) larvae produced by the parasitic fe-

males could remain in the intestinal tract long enough to

develop into infective stages. Such larvae will penetrate

the tissues of the intestinal tract and develop as if they

had penetrated the skin. Both mechanisms may explain

the hyperinfection syndrome seen in the patient.

The importance of this parasitosis in Peru is noteworthy,

there had been reported high prevalence rates in several

regions mainly in the Amazonic Region (Gotuzzo

et al.

1999; Rodríguez and Calderón, 1991; Marcos

et al.

2002; Náquira

et al.

, 1989).

We have to mention that this parasitosis requires an

adequate parasitological sedimentation test to detect

larvae. In endemic areas, mostly in developing coun-

tries; a simple, economical and high sensitive parasi-

tological test should be routinely done. However, the

routine method in most of health centers is the direct

smear test, whose sensitive is low in comparison with

other sedimentation technique as Baermann’s Modi-

fied in Cup Technique described by Lumbreras (1963),

which is performed routinely in only a few health centers

in Peru (eg. IMTAvH). The stool examination controls of

our patient were made by this parasitological technique

and with cultures. However, the first stool examinations

done in the patient were carried out by direct smear,

even though larvae were found in the analysis. It is pro-

bably the heavy burden infection increased the likelihood

DISCUSSION

Neotrop. helminthol., 1(1) , 2007

to find them in feces by a direct smear.

The low level of suspicion for the diagnosis of strongy-

loidiasis can lead clinicians to delay the final diagnosis.

We need more studies to evaluate the role of

S. ster-

coralis

infection and renal impairment in humans. The

possibility of renal involvement should be carefully con-

sidered by physicians. This is the first case report of a

nephritic syndrome probably associated to

S. stercoralis

infection in a non-immunocompromised patient in Peru;

and despite its rarity in the clinical setting, it should be

considered in the differential diagnosis of patients with

glomerulonephritis, when associated with eosinophilia,

or in patients who come from endemic areas.

We thank Dr. Jessica N. Ricaldi, Institute of Tropical

Medicine Alexander von Humboldt, Lima, Peru, for her

assistance in the review of this manuscript.

Adedayo, AO, Grell, GA & Bellot, P. 2001.

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ACKNOWLEDGMENTS

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et al.,

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dence:

Luis A. Marcos

Instituto de Medicina Tropical Alexander von

Humboldt. Universidad Peruana Cayetano

Heredia

Av. Honorio Delgado 430, Urb. Ingeniería. San

Martín de Porres AP 4314, Lima 100.

Lima, Perú.

Correo electrónico/E-mail:

Luis.A.Marcos@uth.tmc.edu

Telefax: (511)-4823404

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