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Memórias do Instituto Oswaldo Cruz
Fundação Oswaldo Cruz, Fiocruz
ISSN: 1678-8060 EISSN: 1678-8060
Vol. 97, Num. 1, 2002, pp. 119-121
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Mem Inst Oswaldo Cruz, Rio de
Janeiro, Vol. 97(1) 2002, pp. 119-121
Frequency of Strongyloides stercoralis
Infection in Alcoholics
Luiz Carlos Marques de Oliveira/+,
Camila Toffoli Ribeiro, Daniel de Melo Mendes, Tatiana Cunha Oliveira, Julia
Maria Costa-Cruz*
Ambulatório de Alcoolismo, Departamento
de Clínica Médica, Faculdade de Medicina *Laboratório de
Parasitologia, Departamento de Imunologia, Microbiologia e Parasitologia, Instituto
de Ciências Biomédicas, Universidade Federal de Uberlândia,
Avenida Pará 1720, Campus Umuarama, 38400-902 Uberlândia, MG, Brasil
+Corresponding author. Fax: +55-34-3218.2349. E-mail: oliveiralcm@ufu.br
Received 25 April 2001
Accepted 16 August 2001
Code Number: oc02022
Several studies have shown that chronic alcoholics
have increased susceptibility to infections due to higher exposure to infectious
agents as well as breakdown in their immune defenses. As Strongyloides
stercoralis infection is usually more
relevant in immunocompromised patients, the aim of this study was to evaluate
the frequency of S. stercoralis
infection in alcoholics. Thus, coproparasitological examination was carried
out in 145 subjects, from which 45 were chronic alcoholics (mean age of 45.7
± 11.0 years), 10 were nonalcoholic cirrhotic patients (mean age of 50.2
± 13.1 years), and 90 were asymptomatic nonalcoholic subjects (mean age
of 46.7 ± 10.1 years), which served as controls. From the alcoholics,
9 had hepatic cirrhosis, 9 had chronic pancreatitis and 27 had neither cirrhosis
nor pancreatitis. For the diagnosis of strongyloidiasis, the Baermann-Moraes
and Lutz methods were used in three fecal samples from each subject. Samples
were collected at alternated days, and three slides of each sample were analyzed
for each method, thus totalizing 2,610 slides examined. The frequency of strongyloidiasis
in the total alcoholic group (33.3%) and in the subgroups of alcoholics, i.e.,
patients with hepatic cirrhosis (44.4%), with chronic pancreatitis (33.3%),
and those with no cirrhosis or pancreatitis (29.6%) was statistically higher
than that found in the control group (5.5%). None of the individuals with nonalcoholic
hepatic cirrhosis had S. stercoralis
infection. Our results showed that the chronic alcoholism itself is an important
factor that predisposes to strongyloidiasis.
Key words: Strongyloides stercoralis -
alcoholism - hepatic cirrhosis - chronic pancreatitis
Strongyloides stercoralis is widely spread
throughout the world, especially in tropical and subtropical regions. This worm
has a complex parasitic life cycle and many patients chronically infected with
S. stercoralis are asymptomatic, and thus, S. stercoralis infection
can persist for decades. However, in some situations, hyperinfection or disseminated
infection has been found usually associated with host immunosupression (Grove
1996).
Infections are more frequent and severe among
alcoholics probably due to dulled mental function, breakdown of local protective
barriers, aspiration, exposure to pathogens and malnutrition (MacGregor 1986),
in addition to alterations of host immune defense mechanisms caused by alcoholism
(MacGregor 1986, Jerrells 1991, Cook 1998). Despite the fact that alcoholism
is a condition observed in patients with S. stercoralis hyperinfection
(Grove 1996), no controlled study was found in the available literature showing
that strongyloidiasis is more frequent in alcoholic than nonalcoholic patients.
As we have often found patients infected with
S. stercoralis in our ambulatory for alcoholism treatment, the present
study was proposed to investigate the frequency of this infection in these alcoholic
patients.
PATIENTS AND METHODS
A total of 145 subjects were evaluated in this
study, from which 45 were alcoholics (mean age of 45.7 ± 11.0 years),
10 had nonalcoholic hepatic cirrhosis (mean age of 50.2 ± 13.1 years),
and 90 were asymptomatic nonalcoholic subjects (mean age of 46.7 ± 10.1
years), which served as controls. From the alcoholics, 9 had hepatic cirrhosis,
9 had chronic pancreatitis, and 27 had no debilitating disease. All subjects
had similar background and current socio-economic conditions. None of them had
used corticosteroids or any other immunosupressor drug. Informed consent was
obtained from all individuals.
Three fecal samples from each subject were collected
at alternated days in plastic recipients without conservatives and stored at
4°C. Parasitological diagnosis was carried out within the first 24 h after the
feces have been collected, by the Baermann-Moraes (Baermann 1917, Moraes 1948)
method, using approximately 10 g of feces of each samples. Furthermore, 10%
formalin solution was added to remaining samples for further analysis by the
Lutz (1919) method. Three slides were prepared for the Baermann-Moraes analysis
and three for the Lutz analysis for each of the 435 samples. Thus, a total of
2,610 slides were examined. Fisher's exact test was used for statistical analyses.
RESULTS
The frequency of S. stercoralis infection
in the alcoholic group (33.3%) was higher (p < 0.001) than that found in
the control group (5.5%). When analyzing the subgroups of alcoholic patients,
the frequency of this infection in patients with hepatic cirrhosis (44.4%),
chronic pancreatitis (33.3%), and those with no such diseases (29.6%) also were
statistically higher as compared to the control group, but with no significant
difference among the subgroups. In addition, the frequency of strongyloidiasis
in patients with alcoholic hepatic cirrhosis (44.4%) was higher (p < 0.05)
than that of the patients with nonalcoholic hepatic cirrhosis (0%). This latter
group was not included in the control group (Table).
No protozoan infection or any other helminthiasis was found in the group of
alcoholic patients, and out of the four alcoholic patients who had diarrhea
none had a positive stool examination for S. stercoralis. In the control
group, other than five cases of S. stercoralis infection, one (1.1%)
case of Giardia lamblia and one (1.1%) case of hookworm infection were
found.
DISCUSSION
Our results showed that the frequency of S.
stercoralis infection among alcoholics was higher (p < 0.001) than that
in the control group (33.3% versus 5.5%); such frequency, in the alcoholic group,
was higher than that found in a study carried out in Costa Rica (5.7%), in which
a single sample of feces was examined (Avendaño et al. 1999), whereas
in our study, three samples from each patient were examined. The frequency of
strongyloidiasis in alcoholic cirrhotic patients (44.4%) in this study was similar
to that found in cirrhotics patients from another region of the State of Minas
Gerais (40.2%), which was predominant in alcoholic cirrhosis (Gaburri et al.
1997).
When an individual is infected with S. stercoralis
there are three possible outcomes that are probably dependent on host immune
system: eradication of infection, chronic infection and hyperinfection or disseminated
infection (Grove 1996). Thus, at least two hypotheses could be proposed to explain
the high prevalence of S. stercoralis infection in alcoholics: (1) higher
predisposition to infection and/or (2) breakdown of immune defenses to eliminate
the parasites, and consequently, greater amount of parasite shed in the feces,
thus facilitating the diagnosis.
The first hypothesis can occur, at least in some
alcoholic patients, due to poor hygiene conditions, either as a result of higher
heteroinfection by walking barefoot in contaminated sites or by autoinfection,
in this latter case, rhabditiform larvae present in the perianal region from
infected individuals transform in infective filariform larvae and then penetrate
(Grove 1996). This infection way also occurs in patients that evacuate in their
clothes or due to deficient hygiene following the evacuation (Costa-Cruz 2000).
Concerning the second hypothesis, immunodeficiency
would be related to impairment in the ability of the host immune system to eliminate
the parasite, which could occur at level of the intestinal mucosa, the cell-mediated
and/or humoral immunity, or the complement system.
The defense system at level of intestinal mucosa
is related to mast cells, which can act either directly on the parasites or
indirectly through their ability to attract and modulate eosinophils; the activation
of mast cells can represent an important effector mechanism to contain the initial
infection and to protect the host from a disseminated infection (Barrett et
al. 1988, Nawa et al. 1994). The findings of reduced number of macrophages in
the duodenal mucosa in alcoholics suggest that in these individuals there is
a weakening of this part of the nonspecific immune system (Maier et al. 1999).
In patients with alcoholic cirrhosis a reduced IgA secretion into the intestinal
lumen was also observed, which could be partially responsible for the high incidence
of intestinal infection observed in severe cirrhosis (Pelletier et al. 1982).
In the cell-mediated immune response to helminths,
there is a predominant Th2 profile from T helper cells with secretion of cytokines
such as IL-3, IL-4, IL-5, IL-6, IL-10 and IL-13; IL-3 and IL-4 stimulate basophils
and mast cells, IL-4 and IL-13 stimulate B cells to produce IgE antibodies,
IL-5 promotes attraction and activation of eosinophils and induction of IgA,
and IL-6 promotes stimulation of granulocytes, T and B cells (Finkelman et al.
1999, Roitt et al. 1999, Costa-Cruz 2000). Clinical evidence on the impairment
of the cell-mediated immunity includes a higher frequency of tuberculosis and
head and neck cancers in alcoholics than in non-alcoholics (MacGregor 1986).
The chronic use of ethanol can result in a loss of lymphoid cells from the peripheral
blood, spleen, and thymus associated with a loss of lymphocyte function, especially
T-cell-dependent immune responses, resulting in an increased incidence of infections,
which would be primarily opportunistic infections (Jerrells 1991). In alcoholics
the number of circulating T lymphocytes is reduced as is the ability of their
lymphocytes to undergo blast transformation in response to mitogenic stimulation
(Glassman et al. 1985, MacGregor 1986). Alcohol has been shown to affect production
of some cytokines, and changes in their balance have profound effects on the
function of the immune cells; experimentally, it has been reported that alcohol
exposure shifted the Th1/Th2 balance toward Th2 excess (Cook 1998). The acute
and chronic effects of alcohol also prevent the normal delivery of polymorphonuclear
cells to sites of bacterial invasion, thus contributing significantly to increase
the frequency and the severity of bacterial infections in alcoholics, regardless
of concomitant alcoholic liver disease (MacGregor 1986). Several effects on
immunity of alcoholics can disappear with the abstinence (Lundy et al. 1975,
Maier et al. 1999).
The most of individuals infected by S. stercoralis
produces specific IgG, IgM, IgA and IgE antibodies, with characteristic increasing
of IgE and IgG4 responses in this helminthiasis; IgA, IgE and IgG4 antibodies
seem play an important role in the control of the levels of infection by S.
stercoralis (Costa-Cruz 2000). The effector IgA-mediated immune mechanism
modulates the larval output by decreasing the worm fecundity and egg viability,
whereas IgE regulates the autoinfection and IgG4 blocks the IgE-mediated responses,
thus having a central role for the establishment and persistence of asymptomatic
chronic strongyloidiasis (Atkins et al. 1999). Chronic alcoholics often have
greatly increased serum immunoglobulin levels. Typically, IgA is elevated both
in alcoholics with and without alcoholic liver disease, IgG is elevated in alcoholic
liver disease, and IgM is only elevated in alcoholic liver disease with active
disease, such as alcoholic hepatitis (Cook 1998). The changes in the humoral
arm of the immune system of patients who chronically ingested alcohol are detectable
before overt clinical or biochemical signs of liver damage (Drew et al. 1984).
Although the increase of immunoglobulins antibody is usually associated with
the development of specific immunity, alcoholic patients with greatly elevated
immunoglobulin levels are often immunodeficient (Cook 1998).
Deposition of complement components C1q, C3,
C4, C8 and properdin can be found on the larval surface (Messias et al. 1994).
S. stercoralis filariform larvae and its antigenic preparations activate
the complement system by both classical and alternative pathways, and promotes
the adhesion of peripheral blood mononuclear and polymorphonuclear cells on
the larval surface and these cells can contain enzymes that are lethal to S.
stercoralis. Thus, the complement system in association with the effector
cells plays an important role in the nonspecific immune defense of the host
against S. stercoralis infection, suggesting the complement system as
a first line of host defense (Messias et al. 1994). Regarding the action of
the alcohol on the complement system, the data are too conflicting to allow
generalization, although serum bactericidal activity may be impaired transiently
by acute intoxication, and patients with cirrhosis of the liver tend to have
reduced serum complement activity (MacGregor 1986).
Our results showed that the chronic alcoholism
itself is an important factor that predisposes to strongyloidiasis, which can
be resulting of higher predisposition to infection or due to countless immunodeficiencies
described in alcoholics.
ACKNOWLEDGEMENTS
To Maria das Graças Marçal for
technical assistance.
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© 2002
Instituto Oswaldo Cruz - Fiocruz
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