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Strongyloides Duodenitis: Case Report
and Review of Literature
Bobby Kakati, MD; Shyam Dang, MD; Muhannad Heif, MD; Kari Caradine, MD; William McKnight, MD;
Farshad Aduli, MD
Strongyloides stercoralis affects 30 to 100 million people
worldwide and is a common cause of abdominal pain and
diarrhea. Strongyloidiasis is a chronic and limited disease;
however, in immunocompromised patients, hyperinfection syndrome can occur. Diagnosing strongyloidiasis early
is important, as almost all deaths due to helminths in the
United States are due to S stercoralis hyperinfection. Patients
infected with human immunodeficiency virus (HIV) do not
appear to be at an increased risk for S stercoralis hyperinfection. We report a case of an HIV-infected Hispanic woman
presenting with dyspepsia, emesis, abdominal pain, and
diarrhea diagnosed with S stercoralis on an esophagogastroduodenoscopy biopsy of the duodenum. The diagnostic
workup had been inconclusive and deciding to biopsy the
small bowel based on the nonerythematous boggy appearance of the duodenal folds was the key step in making the
correct diagnosis. Early diagnosis and treatment thwarted
the developing hyperinfection syndrome and likely prevented further morbidity and probably saved her life.
Keywords: HIV/AIDS n infection n Latinos
J Natl Med Assoc. 2011;103:60-63
Author Affiliations: Department of Internal Medicine (Drs Kakati and Dang),
Division of Gastroenterology and Hepatology (Drs Heif, McKnight, and
Aduli), and Department of Pathology (Dr Caradine), University of Arkansas
for Medical Sciences, Little Rock, Arkansas.
Correspondence: Bobby Kakati, MD, Department of Internal Medicine,
Division of Gastroenterology and Hepatology, Department of Pathology,
University of Arkansas for Medical Sciences, 4301 W Markham St, Little
Rock, AR 72205 ([email protected]).
Introduction
S
trongyloidiasis is a parasitosis caused by the intestinal nematode Strongyloides. It is a common cause of
abdominal pain and diarrhea worldwide, especially
in certain tropical and subtropical regions of the world
where it is endemic. It is usually a chronic and limited disease that remains undiagnosed in many patients. However,
in some immunosuppressed individuals, the infection
becomes overwhelming and causes high rates of mortality.
We report here a case of strongyloides duodenitis in
a patient with AIDS, presenting as abdominal pain and
60 JOURNAL OF THE NATIONAL MEDICAL ASSOCIATION
intractable nausea and emesis. Through this case report,
we intend to emphasize the importance of maintaining a
low threshold for endoscopy when investigating the etiology of gastrointestinal symptoms in immunocompromised patients. Patients with AIDS on antiretroviral
therapy frequently have dyspeptic symptoms that may
be nonspecific. Unless a high index of suspicion and low
threshold for endoscopy is maintained, strongyloidiasis,
a readily treatable disease, may be missed.
Case Report
A 41-year-old Hispanic woman with AIDS, CD4
count of 31, QHIV of 123 000, and on highly active antiretroviral therapy (HAART) consisting of tenofovir plus
lamivudine plus efavirenz presented to the emergency
department with a 4-day history of fever, chills, dyspepsia, significantly worsening abdominal pain, diarrhea,
nausea, and emesis. For 2 months she had intermittent
self-resolving 2- to 3-day episodes of dyspepsia, nausea,
vomiting, and diarrhea. She never had jaundice, hemetemsis, melena, hematochezia, or tenesmus.
At the time of presentation to us, she described her
subjective fever and chills as getting progressively worse
over the past 4 days. Her diarrhea had mucus and trace
blood, but there was no evidence of blood in her vomitus. Her abdominal pain was described as epigastric,
sharp, nonradiating, worse after eating, and not relieved
by defecation.
She was diagnosed with human immunodeficiency
virus at age 21 and started HAART 10 years ago.
Although she has been noncompliant with her HAART
secondary to financial reasons, she had never been ill
like this before. The patient was born in Mexico and had
been living in Batesville, Arkansas, for the previous 22
years. She did not report any recent travel outside the
United States, any sick contacts, recent antibiotic use, or
any new medications.
On general physical examination, the patient was
found to have pallor and was in moderate abdominal discomfort. Vital signs were stable. No oral or pharyngeal
thrush was noticed. No nuchal rigidity was elicited. The
respiratory and cardiovascular examinations were unremarkable. Her abdomen was soft but markedly tender in
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Strongyloides Duodenitis
epigastrium. No free fluid or organomegaly was appreciated. No peritoneal signs could be elicited. Her digital
rectal exam was unremarkable.
On routine labs, the patient was found to be anemic
with borderline microcytosis. Her white blood cell count
was normal, but a differential count suggested marked
eosinophilia (27%). Her urine analysis did not show any
evidence of a urinary tract infection. Amylase and lipase
were within normal limits. Transaminases were slightly
elevated. An acute abdominal series was obtained and
showed no evidence of obstruction or perforation.
Magnetic resonance imaging of the abdomen suggested
normal-appearing liver parenchyma with no evidence of
cholecystitis, cholelithiasis, or pancreatitis. Sputum cultures, blood cultures, and routine stool studies (eg, stool
cultures, ova and parasite examination, clostridium difficile toxin) without concentration methods were negative. The patient later underwent esophagogastroduodenoscopy (EGD), which did not show any significant
lesions other than mild bogginess in the duodenum
(Figure 1). However, multiple biopsies revealed sections
of the duodenum showing numerous strongyloides
organisms (Figure 2) deep in the crypts of the duodenal
mucosa with associated active duodenitis (Figure 3). As
the patient weighed 48 kg, she was started on an oral
course of ivermectin 9 mg daily until her symptoms of
fever, abdominal pain, nausea, vomiting, and diarrhea
resolved. The patient received ivermectin for a total of
14 days. On postdischarge follow-up with house staff,
infectious disease physicians, and the patient’s private
infectious disease physician, the patient reported no
reoccurrence in symptoms.
Discussion
Strongyloidiasis is caused by 2 species of the intestinal nematode Strongyloides. Strongyloides stercoralis is
the more common human pathogen, as it is dispersed
globally. Strongyloides fuelleborni is found sporadically
Figure 1. Esophagogastroduodenoscopy picture
showing nonerythematous boggy appearance
of duodenal folds
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in Africa and Papua New Guinea. S stercoralis affects
anywhere from 30 million to 100 million people in 70
countries across the world and is prevalent in Africa,
Asia, Southeast Asia, Central America and South
America, and parts of the eastern United States. In the
United States, endemic areas include Kentucky, West
Virginia, eastern Tennessee, and Maryland.1-3
S stercoralis is unique by its ability to replicate in the
human host with a lifecycle encompassing both free-living and parasitic stages. In the free-living cycle, the
rhabditiform larvae pass in the feces and can become the
filariform directly or after a free-living phase of male
and female adults.4 Humans acquire strongyloidiasis
during the parasitic cycle, when the filariform larvae
contaminate warm, humid soil and penetrate intact
human skin (usually the feet when people walk barefoot), travel through the bloodstream to the lungs,
migrate up the respiratory tract, are swallowed, and thus
reach the small intestine. There, the larvae mature into
adults that penetrate the mucosa of the small bowel. The
adult female worms reproduce by parthenogenesis, as
adult males do not exist. Eggs hatch and rhabditiform
larvae pass with the feces into the soil. Rhabditiform larvae can develop directly into filariform larvae without
leaving the host. This maturation results in autoinfection
and continuation of parasitism.4-7 Autoinfection can
result in continual infection for years—up to 64 years in
1 report.8
The clinical syndromes of S stercoralis extend from
acute strongyloidiasis to hyperinfection. In acute strongyloidiasis, a local reaction occurs instantly at the area
of larval entry and may last for a few weeks. Pulmonary
symptoms (eg, cough, tracheal irritation) occur during
the first few days, with gastrointestinal symptoms (eg,
diarrhea, anorexia, abdominal pain) starting 2 weeks
after infection. Larvae are noticeable in the feces after 3
to 4 weeks. Chronic strongyloidiasis is often asymptomatic.7 However, chronic gastrointestinal symptoms (eg,
Figure 2. Duodenal mucosa showing numerous
S. stercoralis
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Strongyloides Duodenitis
vomiting, diarrhea, constipation), pruritus ani, urticaria,
and asthma have also been reported.9,10
The ongoing autoinfection maintained in chronic
strongyloidiasis is contained by the host’s immune system. An abrogation of host immunity results in hyperinfection syndrome, which is an amplification of the normal
lifecycle and results in an increase in the total worm burden. This happens without the extension of the organism
outside of the usual migration pattern of the gastrointestinal and respiratory tract.5,11 Disseminated infection occurs
when the larvae migrate to organs other than the gastrointestinal and respiratory tracts, without necessarily implying a greater severity of disease.5,11,12 It has been reported
that hyperinfection and disseminated infection occur in
less than 3% of all cases of S stercoralis infection.13
Diagnosing strongyloidiasis early is important, as
almost all deaths due to helminths in the United States
are because of S stercoralis hyperinfection.14 Definitive
diagnosis of strongyloidiasis is usually made by detecting larvae in the stool. However, in most cases, the intestinal worm load is low, and larval output is minimal and
irregular. A single stool examination is unable to detect
larvae in up to 70% of cases. Repeat stool examinations
have been shown to improve diagnostic sensitivity.
Examining 3 vs 7 serial stool samples increases diagnostic sensitivity15,16 from 50% up to 99%.
As it is necessary to examine multiple stool samples
to detect S stercoralis larvae, it is important to understand that not identifying larvae in the stool does not
imply an absence of infection. The larvae can be identified in bronchoalveolar lavage fluid and bronchial washings and brushings.17,18 Upper and lower endoscopy can
also establish the diagnosis of strongyloidiasis, as larvae
may be seen on biopsies of the affected mucosa.19
Many immunodiagnostic assays have been used over
the years, including indirect immunofluorescence analysis of fixed larvae and gelatin particle agglutination.
Since there is no gold standard for diagnosing S
Figure 3. Duodenal mucosa showing single S
stercoralis (high power)
62 JOURNAL OF THE NATIONAL MEDICAL ASSOCIATION
stercoralis infection, there are conflicting reports on the
diagnostic efficiency of these serological studies. It is
believed and shown in population-based studies that
stool examination generally underestimates the prevalence of S stercoralis infection, whereas serological studies overestimate it.15 The major role of serological tests is
that these tests offer a screening method that, if positive,
can justify a further investigation for the parasite.
While prompt diagnosis is important, clinicians must
have a high suspicion of S stercoralis infection when
clinical signs and symptoms are present, as strongyloidiasis is difficult to diagnose and delaying therapy can
have fatal consequences. In uncomplicated strongyloidiasis, thiabendazole 25 mg/kg twice a day for 3 days (2
days in the United States) was first-line therapy for many
years, but this protocol produced undesirable side
effects, especially nausea and dizziness, and had a high
relapse rate.2,20 Ivermectin 200 µg/kg once a day for 2
days is better tolerated and has a higher cure rate than
thiabendazole.20 Ivermectin is the drug of choice in the
World Health Organization’s list of necessary drugs for
the treatment of S stercoralis.15 In disseminated disease,
hyperinfection syndrome, and the immunocompromised
patients, ivermectin is given daily until symptoms cease
and stool samples are negative for S stercoralis larvae
for at least 2 weeks (1 autoinfection cycle.) There is no
generally agreed-upon regimen, as data are limited.
Some experts recommend combining ivermectin with
albendazole, but evidence is limited.20
Generally, healthy individuals are asymptomatic
when chronically infected. Immunosuppression is the
greatest threat for hyperinfection. The risk factors for
hyperinfection are: (1) immunosuppressive therapy
(especially steroids), (2) human T-lymphotropic virus-1
(HTLV-1) infection, (3) solid-organ transplantation, (4)
hematologic malignancy, (5) hypogammaglobulinemia,
(6) chronic alcohol consumption, (7) uremia, (8) severe
malnutrition, and (9) diabetes mellitus.5,6,7,11,12 Patients
infected with HIV do not look to be at an increased risk
for S stercoralis hyperinfection. Although in the 1980s S
stercoralis hyperinfection was considered an opportunistic AIDS-defining illness, there are fewer than 30
published cases in the literature of hyperinfection occurring in HIV-infected patients. Furthermore, many of
these patients had a history of receiving steroids.7 In
HIV-infected patients, endoscopic duodenal findings of
strongyloidiasis are even rarer. Among the 18 published
reports of endoscopic duodenal findings in S stercoralis
infection, only 1 patient was HIV infected.19,21 We report
the second known case in the literature of S stercoralis
diagnosed on EGD biopsy of the duodenum in a HIVinfected patient.
It appears our patient was a chronic carrier of S stercoralis, with intermittent episodes of dyspepsia, abdominal pain, and diarrhea in the past years. Only in the 4
days prior to hospital admission did she
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Strongyloides Duodenitis
develop unremitting dyspepsia, severe abdominal pain,
worsening diarrhea, fever, and chills. It is unclear what
could have precipitated the developing hyperinfection
syndrome in this patient; however, it is apparent that
increased numbers of larvae are strongly associated with
the progression to hyperinfection.21
It is thought that impaired cellular immunity can disrupt the equilibrium of chronic strongyloidiasis toward
hyperinfection. Steroids and HTLV-1 are the most common risk factors cited in hyperinfection. Both of these
conditions negatively impact that part of the immune
system that controls many helminthic infections, the socalled Th2 response.7 The vital role of Th2 cytokines in
keeping S stercoralis infection in check has also been
shown in animal models as well.22 AIDS does not exclusively inhibit Th2 immunity. It is probable that compared with other immunocompromised states, the
greater Th2 response seen in AIDS could account for the
relatively fewer reported cases of S stercoralis hyperinfection than one would predict.23
Although S stercoralis hyperinfection is rare in HIVinfected patients, it is clear the infection is more common in HIV-infected patients vs healthy individuals.
Hyperinfection syndrome typically results in high mortality.20 Prompt diagnosis and therapy are the main determinants of outcome of the patient. Also, HIV-infected
patients who are able to produce increased peripheral
eosinophilia during hyperinfection, as our patient did,
seem to have a better prognosis.12,20
In our patient, the diagnostic workup had been inconclusive. Deciding to biopsy the small bowel based on the
nonerythematous boggy appearance of the duodenal
folds was the key step in making the correct diagnosis.
In the literature, endoscopic findings of the duodenum in
strongyloidiasis include normal mucosa, edema, erythema, erosion, swollen folds, granule, ulcer, polyp,
hemorrhage, megaduodenum, deformity, and stenosis.21
In the 1 HIV-infected patient, the duodenum was
described as mucosal hyperemia with a speckled white
appearance. As there is no pathognomonic finding in the
duodenum, it is important to maintain a low threshold to
biopsy a relatively unimpressive appearing bowel on
endoscopy, especially in immunocompromised patients.
Our patient ultimately received therapy 7 days since the
onset of symptoms. Timely diagnosis and providing
therapy without delay most likely saved this patient’s
life, as the case fatality rate of hyperinfection syndrome
in patients with diminished cellular immunity6,24 is
between 50% and 86%.
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