High prevalence of Strongyloides stercoralis infection among the elderly in Brazil.

Little is known about the frequency of intestinal parasites in the elderly due to a lack of attention given to the occurrence of these infections among older adults. This study compares the frequency of Strongyloides stercoralis and other enteroparasites between elderly living in nursing homes (n = 100) and those noninstitutionalized (n = 100) from Uberlândia, state of Minas Gerais, southeastern Brazil, associated with data of epidemiological and socio-demographic conditions. Through coproparasitological examination of both groups, enteroparasites were detected in 15 of 200 individuals examined (7.5%; CI: 5.1- 9.9). S. stercoralis was the most frequent parasite 10/200 (5%; CI: 4.2-5.8), being significantly higher in males and in individuals with autonomy for daily living activities. There were no statistical differences in the prevalence of parasites between the two groups compared. In conclusion, S. stercoralis infection was highly prevalent in elderly patients and it does not depend on whether the individual was institutionalized or not.

INTRODUCTION

The aging of the human population constitutes a great challenge for the modern society7 11 13 17. It became necessary to accomplish epidemiological studies to know the profile of the elderly population, and also the needs and demands for social and health services that guarantee good health and improvement of their life quality9 14 43.

Age-related malnutrition, morphological and physiological alterations and immunity dysfunction can enhance susceptibility for cancer, chronic degenerative and autoimmune diseases, increasing illness and death rates in elderly people8,15,18.34.

According to the World Health Organization, protozoal and helminthic intestinal infections are believed to affect 3.5 billion people worldwide, causing illness in 450 million35. Helminth infections are highly prevalent in tropical and subtropical areas, where the low socioeconomic level and the precarious hygienic-sanitary conditions are favorable for the transmission and maintenance of these pathogens45. Among the parasitic nematodes, Strongyloides stercoralis is the most aggressive parasite, since it may cause hyperinfection and dissemination of strongyloidiasis through auto-infection20 23 27. Thus, chronic intestinal parasitism in elderly patients may result in a serious health problem27 29 32.

According to the prevalence, the infection by Strongyloides is classified as: sporadic (< 1%), endemic (1-5%) and hyperendemic (> 5%)28 and its heterogeneous worldwide distribution makes the strongyloidiasis an important current subject. For instance, in healthcare of the Valencian community (Spain), in a total of 493 cases of strongyloidiasis diagnosed, 94% were found in patients in the 51-91 years age group2. Little is known about the frequency of intestinal parasites in the elderly in Brazil or in the rest of the world due to a lack of studies on the occurrence of some neglected infections among older individuals.

Thus, the aim of this study was to compare the frequency of S. stercoralis and other enteroparasites among older adults living in nursing homes and non-institutionalized older individuals, associated with data of epidemiological and socio-demographic conditions.

MATERIALS AND METHODS

This study was approved by the Research Ethics Committee of the Federal University of Uberlândia and was evaluated from August 2002 to August 2003.

Group 1 consisted of 100 (42 men and 58 women) asymptomatic older people (≥ 60 years old), picked randomly from among the 139 individuals living in nursing homes, from four philanthropic institutions in Uberlândia, state of Minas Gerais, southeastern region of Brazil.

Group 2 consisted of 100 (41 men and 59 women) randomly selected asymptomatic non-institutionalized elderly (≥ 60 years old) from the Centro Educacional de Assistência Integrada (CEAI) that renders service in health, education, culture, leisure and social welfare fields. A questionnaire was used to evaluate the epidemiological and sociodemographic data of the elderly people.

Both groups were submitted to an individual stool examination of three fecal samples. Fecal samples were collected in plastic vials without preservatives with intervals of one to four days, and processed by three coprological methods: the Baermann3, HOFFMANN et al. 21 and RITCHIE30 and by the Safranin/Methylene Blue staining technique4. Six hundred samples were collected. There being four slides for each sample and for each method. A total of 9,600 slides were analyzed under light microscope (Olympus, CH-2, Japan) at ×100, ×400 and ×1000 by two investigators. Positive cases for parasites were referred to the nearest health unit in order to receive specific treatment.

Statistical analysis was performed with a relative test of the difference between two proportions (Z) using Statistics for Windows - Release 4.5 statistical software (Statsoft Inc. 1993) to determine the association between Groups 1 and 2. A 95% confidence interval (CI) was stipulated. Results were considered significant when p < 0.05.

RESULTS

Table 1 characterizes both groups according to epidemiological and socio-demographic aspects. In Group 1 the ages ranged from 60 to 98 years old and in Group 2 from 60 to 96 years old. In both groups, women were predominant (58% in Group 1 and 59% in Group 2).

Table 1

Distribution of epidemiological and socio-demographic parameters in institutionalized (Group 1) and non-institutionalized (Group 2) elderly from Uberlândia, Brazil

Parameter of elderly	Group 1 (n = 100)	Group 2 (n = 100)	Significance level
Age (years)	76.2 ± 10.0 SD	72.9 ± 7.3 SD
Gender
Males	42	41	N.S.
Females	58	59	N.S.
Marital status
Single	51	11	p = 0.0001
Married	7	55	p = 0.0001
Widow/er	27	30	N.S.
Divorced	12	4	p = 0.0383
NI	3	0	N.S.
Education
Illiterate	36	13	p = 0.0002
Elementary	29	84	p = 0.0001
High school	2	3	N.S.
NI	33	0	p = 0.0001
ADL
Independent	38	98	p = 0.0001
Partially dependent	23	1	p = 0.0001
Dependent	39	1	p = 0.0001
Alcoholic
Yes	6	5	N.S.
No	94	95	N.S.
Income
No income	19	1	p = 0.0001
Salary	0.81 ± 0.4 SD	2.1 ± 1.4 SD	N.S.

NI = not informed; ADL: activities of daily living; N.S. = no statistically significant difference. Salary = 85.5 dollars monthly income.

Parasites were detected in 15 of 200 elderly individuals examined (7.5% CI: 5.1-9.9). Fecal consistence of all the samples collected was not diarrheic. The age group distribution of enteroparasite infected elderly respectively for Groups 1 and 2 was 60-69 y [3/28 (9.3%) and 0/35]; 70-79 y [0/32 and 5/47 (10.6%)] and ≥ 80 y [5/40 (12.5%) and 2/18 (11.1%)]. A possible tendency for progressive increase of the parasitism was observed among the age groups, though a statistically significant difference was not seen.

Table 2 presents the frequency of the parasites in both groups; S. stercoralis was the most frequent parasite 10/200 (5% CI 4.2-5.8). All infected subjects presented asymptomatic strongyloidiasis. The proportion of infected men in relation to women was 4:1 in both groups. A case of co-infection was observed in Group 1. From the 10 S. stercoralis positive cases eight (80%) were male subjects with autonomy for activities of daily living (ADL) (p < 0.05). Three of the ten infected elderly (30%) had a past history of alcoholism, two (20%) being from subjects of Group 1, one of them shedding filariform larvae (L3) in the feces, as well as the individual of Group 2.

Table 2

Frequency of enteroparasites in institutionalized of Group 1(n = 100) and non-institutionalized Group 2 (n = 100) elderly from Uberlândia, Southeastern Brazil

Enteroparasites	Group 1 Positives	Group 2 Positives	Significance level p < 0.05
Strongyloides stercoralis only	4	5	N.S.
S. stercoralis + Giardia lamblia	1	0	N.S.
Giardia lamblia	0	2	N.S.
Hookworms	2	0	N.S.
Balantidium coli	1	0	N.S.
Negatives	92	93	N.S.
Total	100	100

N.S.: No statistically significant difference.

DISCUSSION

The frequency (7.5%) of enteroparasites found in this study reveals clinical and epidemiological importance. The control of enteroparasite infection is still a challenge in developing countries due to susceptibility of the host, favorable conditions of the environment, low socioeconomic level and precarious hygienic sanitary conditions16 45. SIRIVICHAYAKUL et al. 39 have found that the prevalence of infection is much higher in institutionalized mentally handicapped than in non-institutionalized people, since collective living conditions are risk factors for high prevalence of parasitism at the institutions. However, the parasite prevalence detected in the present study cannot be compared to the other studies due to the lack of studies among institutionalized individuals.

In spite of the fact that there were differences between the two groups regarding the socio-demographic parameters, these did not influence the results, due to the fact that the prevalence of enteroparasites was similar in both groups. In the population studied a slight increase frequency among women can be explained by a higher female life expectancy than that of men. The marital status, bachelors or widowers, associated with the lack of financial resources and loss of autonomy for ADL, may play an important role in the institutionalization process31. In Brazil, the idea that the care of the elderly is the responsibility of the family still flourishes. However, social policies are needed to aid and support those elderly without financial resources in order to avoid institutionalization9 12.

In the present study, S. stercoralis was the most frequent enteroparasite among the infected individuals, 80% of them being men, all having presented asymptomatic strongyloidiasis. These findings were in accordance with other studies2 16 33. The asymptomatic infection which occurs in most of the patients chronically infected may persist for several decades26 37. However, in some cases the infection may be followed by symptoms such as diarrhea, abdominal pain, nausea, malabsorption, weight loss and anemia1 23. Some reports have described a significant association between human T cell lymphotropic virus type-1 (HTLV-1) and S. stercoralis hyperinfection20 40 41. Case reports of hyperinfection syndrome or disseminated infection in immunocompromised elderly showed high mortality indexes associated with the use of immunosuppressive therapy as well as protein-caloric malnutrition and the aging process32 42. Chronic alcoholism is another factor referred to as a predisposition to strongyloidiasis, and the frequency of infection by S. stercoralis in alcoholic patient varies from 33.3% to 44%1 42. In this study, among the individuals that had a past history of alcoholism, two were shedding (L3) larvae in feces, suggesting cases of hyperinfection. The findings suggest that strongyloidiasis remains a serious public health problem in older individuals. As demonstrated by three fecal samples, the prevalence of strongyloidiasis is probably underestimated in literature because the diagnosis is difficult and false negative results become frequent due to a scarcity or absence of worms at the moment of the examination in asymptomatic patients, because it is imperative that multiple stool samples be examined in order to make a correct diagnosis38.

Hookworm infections have heterogeneous global distribution and high prevalence in the developing countries in tropical and subtropical areas6 10 45. CHANGHUA et al. 10 observed that the prevalence of hookworm infection increased with age. The frequency of hookworm infection (2%) found in this study was lower than that reported by different researchers in epidemiological studies carried out in provinces of China. The high prevalence of hookworm infections in elderly Chinese patients has been attributed to the constant soil polluted with human feces that is used for fertilizing vegetables6 10, which does not occur in Brazil.

The highly significant association between hookworm and S. stercoralis (OR > 6), and the series of self-reported morbidity markers associated with these two helminth species are particularly noteworthy. The S. stercoralis age-prevalence curve showed an almost parallel shape to the hookworm age-prevalence curve, reaching an infection rate of approximately 20% in older adults5. In the present study, infection by S. stercoralis and hookworm in institutionalized elderly was also detected; however, the probable source of infection was not due to institutionalization. They had no contact with the ground in any of the four institutions neither did they have contact with the external environment of the institutions; therefore it is possible that the elderly were infected prior to institutionalization.

The frequency (1%) of Giardia lamblia was found lower than that observed by other authors, being all asymptomatic individuals19 22. Nevertheless, G. lamblia may cause acute diarrhea, besides other symptoms such as, abdominal pain, nausea, vomiting, malabsorption, fever, appetite and weight loss22.

Balantidium coli is the only known pathogenic ciliated protozoa that can produce disease in humans. The infection may be subclinical in humans, as it is mostly in pigs, or may develop as a fulminant infection with bloody and mucus-containing diarrhea; this can lead to perforation of the colon. Occasionally, the parasite is able to invade organs and cause ulcerations in the mucosa and submucosa membranes, thrombosis in the affected vessels and even pulmonary colonization36 44. In the present study, a case of asymptomatic balantidiasis was detected; possibly a chronic infection, since the infected individual was an 87 year old woman, who had been living in the institution for more than two years.

Balantidiasis is a zoonotic disease and is acquired by humans via the fecal-oral route from the normal host, the pig, where it is asymptomatic. Water is the vehicle for most cases of balantidiasis. Human-to-human transmission may also occur. The major factors leading to human balantidiasis include (i) close contact between pigs and humans, (ii) a lack of appropriate waste disposal in swine and human excrement contaminate drinking water sources (e.g., wells and streams) and food, and (iii) subtropical and/or tropical climatic conditions (e.g., warmth and humidity) favoring survival of cysts. In institutional populations (mental hospitals, prisons, and orphanages), where pigs are an unlikely source of infection, outbreaks are the result of asymptomatic carriers and the difficulties involved in maintaining hygienic control36. In our study, the only elderly that presented B. coli in the feces were institutionalized and probably acquired the protozoan prior to the admission to the institution considering that the local hygienic conditions were strictly controlled and the elderly had no contact with the external environment.

Studies have suggested that elderly individuals have an increased risk for occurrence of severe cryptosporidiosis. Cryptosporidium is a cause of acute infectious diarrhea in elderly, the disease being characterized by a shorter incubation period, probably due to a greater inherent host susceptibility to parasite infection24 25. This fact was not observed in this study and no case of cryptosporidiosis was detected in the elderly by using Safranin/Methylene-Blue staining technique4.

In conclusion, S. stercoralis infection was highly prevalent in the studied population and it does not depend on whether the individual was institutionalized or not. Therefore, early diagnosis through specific methods is relevant in asymptomatic elderly in order to prevent the risk of hyperinfection or disseminated infection, thus avoiding high mortality rates.