Prevalence and epidemiological aspects of enteroparasittosis and its relationship with nutritional status in children living in the Beira Rio de Imperatriz neighborhood, MA in 2011

0
18
DOI: ESTE ARTIGO AINDA NÃO POSSUI DOI SOLICITAR AGORA!
PDF

ORIGINAL ARTICLE

PIRES, Renata de Cássia Coêlho [1], LUCENA, Adriana Dias [2], MANTESSO, Jhennyfer Barbosa de Oliveira [3], CORVELO, Tereza Cristina de Oliveira [4]

PIRES, Renata de Cássia Coêlho. Et al. Prevalence and epidemiological aspects of enteroparasittosis and its relationship with nutritional status in children living in the Beira Rio de Imperatriz neighborhood, MA in 2011. Revista Científica Multidisciplinar Núcleo do Conhecimento. Year 05, Ed. 07, Vol. 04, pp. 51-70. July 2020. ISSN: 2448-0959, Access link: https://www.nucleodoconhecimento.com.br/health/prevalence-and-epidemiological

SUMMARY

Intestinal parasitus is considered a public health problem, especially in developing regions, in children, they can trigger various consequences such as physical, mental and social retardation. Thus, this study investigated the prevalence and epidemiological aspects of enteroparasitosis and its relationship with anemia and nutritional status among children aged 1 to 10 years in a poor neighborhood of Imperatriz/MA/Brazil in 2011. Results of parasitological examination of feces, hemoglobin and seeric iron dosage, in addition to anthropometric measurements were analyzed. A prevalence of 60% was found for enteroparasittosis, represented by Ascaris lumbricoides (20%); Giardia lamblia (14%) and Endolimax nana (14%). As for gender and age group, no significant differences were identified in the prevalence of intestinal parasitoses. An association was observed between enteroparasitosis and anemia, either due to deficiency of sumoiron, hemoglobin or both of these estimators, and 80% (16/20) of children with anemia had intestinal parasitosis with predominance of A. lumbricoides. Nutritional assessment showed that 50.98% of the children had adequate nutritional status (eutrophic) and 34.31% presented alterations with low weight and nutritional risk and 57.14% of them were parasitized. In the socio-environmental aspects, the absence of public policies was recorded that corroborate the high prevalence of parasitasis. Thus, it can be verified that preventive measures are essential for the control of parasitasis, because in addition to the damage to health, they reflect the living conditions to which the community is exposed, such as poor basic sanitation and poor quality of life, especially for children.

Keywords: Children, intestinal parasitus, nutritional status.

INTRODUCTION

Enteroparasitosis is a relevant cause of health problems in developing countries, along with nutritional deviations. In Brazil, there is a tendency to increase the number of children with short stature and overweight, which may be associated with malnutrition1. Intestinal parasitosis is considered a public health problem, which despite all technological and medical advances, are still strongly incident nowadays, being able to trigger different consequences for their patients in healthy children, often do not lead to serious consequences, while in malnourished women they can harm not only weight gain but also height2.

In Brazil, the prevalence of intestinal parasites is high, varying between states and municipalities, such as São Paulo, where the prevalence of enteroparasites ranges from 11.5 to 21.3% among children aged 0 to 12 years3. On the other hand, the association between anemia and enteroparasitasis is a topic of increasing interest in the field of Public Health, especially in school-age children. Anemia usually results from simple or combined deficiency of nutrients such as iron, folic acid and vitamin B12. Other rarer types may be caused by pyridoxine, riboflavin and protein deficiency4.

In childhood, anemia along with parasitsis interferes with growth and development processes, behavioral and psychological changes, and decreased physical activity. Skin and mucosal alterations and impaired digestive and immune systems may also be observed5.

Among school-age children, the presence of some parasitos usually determines the appearance of anemia, especially iron deficiency. Hookworms (A. duodenale and N. americanus) are the helminths most associated with this pathology, but other species such as A. lumbricoides, T. trichiura and S. mansoni are also related to anemia. The intensity of the manifestation depends on age, nutritional status, parasitic load and association with other parasite species6.

Thus, in order to verify and monitor the current health conditions of children using primary care services of the Health Unit of the Beira Rio neighborhood in Imperatriz-Maranhão, an investigation was carried out regarding the presence of enteroparasitasis and their possible association with anemia and nutritional status in this infant sample.

MATERIALS AND METHODS

Series

The study consists of the analysis of 102 medical records of children aged 1 to 10 years attended at the Basic Health Unit of the Beira Rio neighborhood in Imperatriz, MA in 2011. The city of Imperatriz, MA is located in the west of the State of Maranhão, in microregion no. 38. It has limits with the municipalities of Cidelândia, São Francisco do Brejão, João Lisboa, Davinópolis, Governador Edison Lobão and the State of Tocantins. The municipality is 629.5 kilometers from the state capital. Its geographic coordinates are 5º 31′ 32′ south latitude; 47º 26′ 35′ longitude to W Gr., with an average altitude of 92 meters above sea level. Currently the city has 247,553 inhabitants7.

A standard form was used to collect information on anthropometry (weight and height), gender, age, school attendance, area of residence, presence of basic sanitation, garbage collection, occurrence of diarrhea and complications due to enteroparasitosis and the results of blood count tests; serum iron and parasite found in feces, in addition to recording negative cases to verify the prevalence of the described parasites.

PARASITOLOGICAL EXAMINATION OF FECES (EPF)

The parasitological diagnosis of feces was performed by direct method with morphological observation by light microscopy.

DIAGNOSTIC CRITERIA

Through the records of the Basic Health Unit, the diagnostic criteria were performed as follows:

a) Hemoglobin: determined by the quantitative evaluation of mean corpuscular hemoglobin (MCH) by absorbance by the cyanide hemoglobin method. Thus, according to WHO (World Health Organization) criteria for the determination of anemia, hemoglobin concentrations below 11g/dL are considered.

b) Seeric iron: analyzed using Merck’s colorimetric enzymatic method (in the Mega apparatus). Anemia was considered iron deficiency when serum iron concentration was lower than 45 mg/dL, in addition to blood stretch analysis in relation to the pattern of microcytic and hypochromic red blood cells.

c) For the classification of nutritional status, the anthropometric method was adopted, using the child’s card where the relationship between weight and age, weight and height is evaluated through the growth curve graph and then properly recorded in the family records of the child attended and follows the following standardization:

  • Variables: weight and age
  • Index: Weight and age (W A)
  • Reference: NCHS (National Center of Health Statistic – 1977)
  • Cutoff points: (p0, p1; p3; p10; p97).

These cutoff points (percentiles 0.1, 3, 10 and 97) for the Weight by Age indicator allow the following classification of child nutritional status according to the criteria of the Ministry of Health:

  • W/A below the 0.1 percentile: child with very low weight for age.
  • W/A greater than or equal to the 0.1 percentile and lower than the 3rd percentile: child with low weight for age.
  • W/A greater than or equal to percentile 3 and lower than 10th percentile: child at nutritional risk.
  • W/A greater than or equal to the 10th percentile and less than the 97th percentile: child with age-appropriate weight (eutrophic).
  • W/A greater than or equal to the 97th percentile: child at risk of overweight.

The classification of organic manifestations of the Food and Nutrition Surveillance System (FNSS) was adopted, which includes three groups:

  • Nutritional Adequacy (Eutrophy): Manifestation produced by the balance between consumption in relation to nutritional needs.
  • Nutritional Deficiency: Manifestations produced by quantitative and/or qualitative insufficiency of nutrient intake in relation to nutritional needs.
  • Nutritional disorder: Manifestations produced by excess and/or imbalance of nutrient intake in relation to nutritional needs.

ETHICAL ASPECTS

The study was submitted to analysis by the Research Ethics Committee of the Center for Tropical Medicine of the Federal University of Pará – FUPA and according to the criteria established in resolution 196/96 that deals with research with human beings.

DATA ANALYSIS

All variables described above were reported and compiled from the forms answered through medical records, where they were analyzed in databases of the BioEstat 5.0 program, and descriptive and analytical statistics were used. For the statistical analysis of the results, the chi-square and fisher’s exact tests were used. The accepted significance level was p < 0.05.

Results

We analyzed 102 medical records of children, aged 01 to 10 years, according to the data from the medical records analyzed 56.8% (58/102) represented the male sex and 43.2% (44/102) females. Table 01 shows the distribution of the results according to the gender and age group of the children surveyed.

Among the most common parasitosis found in the site surveyed, there was a predominance of protozoa (56%), represented by Entamoeba coli, Endolimax nana (nonpathogenic) and Giardia lamblia (pathogenic), which also presented in association, which generated 06 cases (06%) biparasitism in the children evaluated, however, there was a higher isolated index of helminties caused by Ascaris lumbricoides (20%). The specific distribution of these intestinal parasitus in the sample studied revealed 14% giardia lamblia and 4% of multiparasitim with 2% associated with Ascaris lumbricoides and Endolimax nana and 2% with Giardia lambria and Endolimax nana (Figure 1). In addition to these parasitic species, the following diners were identified: Entamoeba coli (6%), Endolimax nana (14%), and 02 cases had both species. The remaining 40% did not present any alteration of parasitological microscopy of feces.

In the distribution of intestinal parasitus regarding gender, prevalence rates of 60.34% (35/58) in males and 59.09% (26/44) in females were identified (Figure 01).

Figure 01 – Prevalence of intestinal parasitus according to gender classification.

Source: Field research, 2012.

This difference in prevalence between males and females was not statistically significant. (c2Yates = 0.006; p= 0.9395). Regarding age group, the following infection rates were verified: in the group < 4 years, 60.7% (17/28) were detected, among children aged ≥ 4 years and < 7 the rate was 59.45 (22/37) and among the age group ≥ 7 years up to 10 years of age the percentage of parasites was the same value as the previous group (Figure 02). There was no variation in the prevalence rate of enteroparasitasis between different age groups (c2 = 0.013; GL = 2; p= 0.9934).

Figure 02 – Prevalence of intestinal parasitus according to age group.

Source: Field research, 2012.

Regarding the relationship between seeric iron dosage and enteroparasitosis, the results show that 12 (11.76%) of the children presented alterations in serum iron levels, with values below expected, and of these 11 (91.66%) were parasitized, with 05 (45.45%) by Ascaris lumbricoides and 06 (54.56%) protozoa, including 27.27% with giardiasis. In the normality parameters, 78 (76.48%) children with normal serum iron levels and of these 40 (51.28%) were positive for intestinal parasitsis. In the statistical analysis of these data, it is verified that there is an association between the presence of intestinal parasitus and the deficiency of seeric iron as shown in table 02.

In the distribution of the population studied according to hemoglobin levels and their relationship with intestinal parasitosis, 11 (10.78%) children with low hemoglobin level (<11 g/dL), which inserts this percentage as patients with anemia, of these 07 (63.63%) were with some intestinal parasite. The association between the results of the parasitological examination of the feces and hemoglobin levels was not significant (Table 01).

Table 01 – Hemoglobin dosage levels related to the prevalence of enteroparasitosis in the population studied.

Hemoglobin Intestinal parasites Total (%)
Presence (%) Absence (%)
Deficiente (< 11 g/dl) 07 (63,63) 04 (36,37) 11 (10,78)
Normal (11-12 g/dl) 17 (60,71) 11 (39,29) 28 (27,45)
High (> 12 g/dl) 37 (58,73) 26 (41,27) 63 (61,77)
Total 61 (59,80) 41 (40,20) 102 (100)

(GWilliams test = 0.1040; GL = 2; p= 0.9493)

Source: Field research, 2012.

Table 02 refers to the distribution of the population studied according to the presence of anemia in relation to positive and negative PFS results, where values lower than the recommended hemoglobin and/or seric iron were characterized as anemia. These cases represented 19.62% (20/102) of the children studied, and 15% (3/20) had hemoglobin and iron deficiency, 40% (8/20) were deficient only in hemoglobin and 45% (9/20) were deficient only in summumoiron. Among children with anemia, either due to deficiency of suml iron, hemoglobin or both of these estimators, 80% (16/20) presented intestinal parasitosis with predominance of A. lumbricoides.

The comparative analysis of these data, considering presence x absence due to anemia and parasittosis demonstrated that the presence of anemia is dependent on intestinal parasitus (Exact bilateral Fisher Test = 0.0452). The assessment of the nutritional status of the studied population found that 18 children were underweight for age, and 17 children were at nutritional risk. Of these children, 57.14% (20/35) were parasitized, particularly with the predominance of G. lamblia and A. lumbricoides. Regarding eutrophy, 52 children were overweight and still 15 children were at risk of overweight. In these categories of eutrophic and overweight, the majority (61.19%) he also presented parasitosis (Table 5), and ascaridiasis was predominant on giardiasis. Thus, a dependency relationship between nutritional status and intestinal parasittosis was not evidenced in the sample studied.

Table 02 – Distribution of data according to the presence of anemia in relation to hemoglobin and serum iron levels.

Anemia Intestinal parasites Total
Presence (%) Absence (%)
Hb (<11)/Fe (<45) 02 (66,67) 01 (33,33) 03
Hb (<11)/Fe (>45) 05 (62,50) 03 (37,50) 08
Hb (>11)/Fe (<45) 09 (1,00) 09
Hb (>11)/Fe (>45) 45 (54,88) 37 (45,12) 82
Total 61 (59,81) 41 (40,19) 102

Source: Field research, 2012.

The Beira Rio neighborhood in Imperatriz (MA) was evaluated for the characteristics of basic sanitation that involved the identification of the main source of water supply and treatment, presence of sewage network, garbage collection and dispensing (Table 03). The data show that there is garbage collection in the studied community, as well as piped water, however, there is no sewage network and waste is dumped into aseptic waste. Regarding water treatment, 35.2% perform water treatment through filtration and 64.8% do not perform any type of treatment, the same being consumed directly from the taps. The place, despite having been considered with regular garbage collection, has the presence of garbage foci in wastelands and streets without proper pavement, with the presence of loose animals and poor sanitation, without weeding and streams with polluted water.

Table 03 – Distribution of data according to the basic sanitation at the site surveyed

Variable Yes (%) No (%) Total
Water treatment (35,2%) (64,8%) (100%)
Sewage network (0%) (100%) (100%)
Garbage collection (100%) (0%) (100%)
Piped water (100%) (0%) (100%)

Source: Field research, 2012.

Discussion

Intestinal parasitus is a worldwide distribution problem, but it is especially relevant in regions with low socio-economic level, because their transmission is related to environmental conditions and the quality of basic sanitation, conditions that are still very precarious in developing countries.

The research conducted in the Beira Rio neighborhood in Imperatriz (MA) showed a prevalence of 60% of intestinal parasitus, revealing the living conditions of this community. Other studies8, 9 among schoolchildren from different Brazilian regions reported similar prevalences, a picture that this disease is still strongly present in the Brazilian population.

In this study, it was found that more than half of each children’s gender had some type of parasite, therefore, this difference is not statistically significant. Likewise, the high frequency of enteroparasitosis observed among children of different age groups (<04; ≥04 and <07; ≥07 years) may be due to a deficit in self-care and neglect of hygiene habits and even to the fact that most of them (64.8%) make use of untreated and consumed water directly from the tap, which does not prevent the disposal of probable contamination by the supply network, such as protozoa that can resist the action of chlorine, when it is rarely used in water treatment10.

In some types of intestinal parasites, such as Giardia lamblia, as age advances the occurrence of this parasite decreases, because immunological factors are involved in this process, however, this characteristic can be used by other enteroparasitosis, because as the human being grows, his resilience, protection as well as hygiene and education levels also tend to improve11. Parasites can cause diseases in their host either by competition for nutrients or by immune response to invaders12.

In this study, the high prevalence of Ascaris lumbricoides (20%) can be compared to other findings13 that also detected high rates (51%) of this verminosis in children. This parasite is present in individuals living in conditions of large clusters, and its prevalence is higher in children. The habit of taking the hand to the mouth in several situations associated with other epidemiological factors of the disease causes this index to be increasingly high in this phase14.

Another justification for this prevalence of Ascaris lumbricoides can be attributed to the mode of transmission of this helminth, which infects people by fecal-oral route, common among children15. Thus, this evidence reinforces the reality of the disease in Brazil, where the frequency of these organisms may vary from region to region, because in addition to relying on the humid environment and vectors conducive to its cycle, it reveals the dismay with the community16. In general, the species A. lumbricoides affects 20 to 30% of the population of the Americas17.

As for protozoa, giardiasis was also prevalent (14%), although the results could have been more expressive, since the recording of the parasitological examination of feces adopted at the studied site came from only a single sample of feces, and this type of analysis when used for the detection of cysts, which are eliminated intermittently, can reduce by 30% to 50% the sensitivity of the result18 , which may have underestimated the frequency found for Giardia lamblia.

In this study, it should be highlighted that among the children identified with anemia, most of them had some type of parasite19. Since this significant association between parasitusis and anemia is explained by the result that iron is absorbed through the intestinal wall in the duodenum and jejunum and it is believed that this absorption may be impaired by the presence of Ascaris lumbricoides in this part of the intestine20. On the other hand, in ascaridíase, anemia is usually of secondary order, caused by hemorrhages, which can be produced by the larvae of this parasite in transit from capillaries to alveolos21.

The presence of anemia due to enteroparasitis is one resulting from various forms of blood loss, such as: malnutrition (Ascaris lumbricoids), hematophagous action (Ancylostoma sp.) and ulceration of intestinal mucous membranes (Entamoeba histolytica), and may evolve with worsening of the clinical picture, which is dependent on the parasitic load, age, nutritional and physiological status of the organism, as well as association with other pathogenic parasitic species. Although in this study ancylostoma sp. and Entamoeba histolytica have not been found in the children investigated22.

Anemic manifestations may also result from nutritional deficiencies, because among the immediate causes of anemia stand out etiological factors such as low intake of foods with iron sources, low absorption of iron ingested and losses of this micronutrient, as mentioned above, due to parasitic infections23.

Iron deficiency anemia is a nutritional problem of great magnitude in the world. Thus, relating these statements and taking into account the precarious socioeconomic conditions in which the investigated community lives, anemia can be caused by nutritional factors, such as low intake of iron-rich foods. Among the age groups, the prevalence of iron deficiency was higher among children (7/12; 58.33%) (1-4 years) compared to children in the school age group (> 6 years). This finding could be attributed to the benefit of children having access to iron supplementation in school meals. In childhood, particularly during school years, there is an increase in nutritional needs and anemia can have a negative effect on weight growth and height, besides interfering in learning23,24.

The analysis between enteroparasitasis and nutritional deficit did not show a positive correlation, due to the high frequency of eutrophic also parasitized (34%). Nutritional deficits can be aggravated by the presence of some parasitious species, such as Ascaris lumbricoides and Giardia lamblia.

In Brazil, poor children living in deprived regions tend to experience vicious cycles of malnutrition and repeated parasitic infections, often leading to morbidities. Thousands of children die each year in the world due to intestinal obstruction and other abdominal complications caused by intestinal parasites. In this study, children reported the occurrence of diarrhea, as well as the elimination of verits. Chronic diarrhea can lead to malnutrition by changes in the intestinal mucosa and infection of the gastrointestinal tract, not allowing a perfect absorption and thus affecting child development. Thus, intestinal parasitoses can cause protein losses, malnutrition, iron deficiency anemia and other alterations that easily lead to deficiency in physical and intellectual development24.

In general, parasitasis has a high prevalence in regions that do not have adequate social, economic and sanitary infrastructure25. These were the conditions found in the evaluated community, whose sanitation is deficient, with proximity between houses with polluted water sources, loose animals (dogs, cats, pigs and chickens), open streams and streets without pavement, revealing that this precarious and poorly preserved environment increases the risk of intestinal parasites, which meet the ideal conditions for maintaining their life cycles.

The present study observed that the parasite index of the protozoan class was higher in relation to helminths, including two nonpathogenic species (Entamoeba coli and endolimax nana), which serve as good indicators of these sanitary conditions, to which individuals are exposed. These nonpathogenic species present the same transmission routes of pathogenic species such as Entamoeba histolytica, E. dispar and Giardia duodenalis, reflecting the precarious environmental conditions to which this child population is exposed26.

Moreover, the fact that these intestinal parasitoses presented a homogeneous distribution in the child population, by sex and age group, demonstrates a comprehensive equality of the socio-environmental conditions existing in this community27. And this reinforces that promoting basic infrastructure and education is an effective tool to reduce the prevalence of these diseases.

Finally, taking into account the findings of this investigation, it is recommended that primary family health care programs be systematically and periodically reviewed on site, with efficient control strategies, through treatment with antiparasitics, nutritional supplementation and improvement in sanitation and personal hygiene conditions, aiming at a future opportunity, in terms of health and education for children in this community.

Conclusions

The prevalence of intestinal parasitoses reached 60% of children in the Beira Rio neighborhood, empress/MA, with a predominance of protozoa in the face of helminths, and a higher frequency for A. lumbricoids (20%) and among protozoa, Giardia lamblia (14%) was the most prevalent. Anemia was present in 19.6% of the children studied either due to deficiency of seeric iron and/or hemoglobin. A significant relationship of dependence between anemia and parasittosis was observed, with 80% of anemic patients presenting intestinal parasitasis. The highest proportion of the children studied presented eutrophic nutritional status, while approximately 34% of them were underweight and nutritional risk. The association between the state of malnutrition and the presence of intestinal parasitasis in the children studied did not reach statistical significance. The detection of high rates of altered health conditions due to anemia and malnutrition among the children studied are indicators of risks linked to the impairment of child development. Most children presented records of elimination of worm by mouth or anus and few were records for diarrhea, on the other hand no records of other clinical complications such as intestinal volvolence, liver problems or rectal bleeding were identified.

Low maternal education is significantly related to childhood intestinal parasittosis, which allows a reflection on the importance of educational actions for the prevention of studied morbidities such as intestinal parasitoses, anemia and nutritional status. Regarding epidemiological aspects, the investigated site presented precarious conditions of socio-environmental, economic and cultural development, constituting determinants of risks to human health. A change in the high prevalence rates related to intestinal parasitoses, anemia and nutritional status in infant populations depend on an improvement in the educational levels of populations and basic infrastructure conditions, such as housing, sanitation, good quality water and socioeconomic levels, particularly in the generation of employment and income and primarily expand access to health services for this community.

In the community studied, there is a need for more intense actions in the prevention of intestinal parasites, which can be represented by improvement in the sewage network, with safer water supply, use of filters or water boiling, regular garbage collection, infrastructure improvements and educational actions aimed at hygiene of adults and children, in addition to strengthening food care.

REFERENCES

  1. BATISTA FILHO, Malaquias; RISSIN, Anete. A transição nutricional no Brasil: tendências regionais e temporais. Cadernos de saúde pública, v. 19, p. S181-S191, 2003.
  2. SAWAYA, Ana Lydia. Desnutrição: consequências em longo prazo e efeitos da recuperação nutricional. Estudos avançados, v. 20, n. 58, p. 147-158, 2006.
  3. FERREIRA, Glauco Rogério; ANDRADE, Carlos Fernando Salgueirosa. Alguns aspectos socioeconômicos relacionados a parasitoses intestinais e avaliação de uma intervenção educativa em escolares de Estiva Gerbi, SP. Revista da sociedade brasileira de medicina tropical, v. 38, n. 5, p. 402-405, 2005.
  4. OLIVEIRA, Maria A; OSÓRIO, Mônica M. Consumo do leite de vaca e a anemia ferropriva na infância. Jornal de Pediatria, Rio de Janeiro, v. 81, n. 5, abr. 2005.
  5. NEUMAN, Nelson A. et al. Prevalência e fatores de risco para anemia no Sul do Brasil. Revista de Saúde Pública, v. 34, p. 56-63, 2000.
  6. MARINHO, Marcelo Silva et al. Prevalência de enteroparasitoses em escolares da rede pública de Seropédica, município do estado do Rio de Janeiro. Rev. bras. Anal. clín, v. 34, n. 4, p. 195-196, 2002.
  7. IBGE. Censo de 2010. Disponível em: https://cidades.ibge.gov.br/brasil/ma/imperatriz/panorama. Acesso em: 22 de Março de 2012.
  8. PEREIRA-CARDOSO, Franciano Dias et al. Prevalência de enteroparasitoses em escolares de 06 a 14 anos no município de Araguaína-Tocantins. Revista eletrônica de Farmácia, v. 7, n. 1, p. 11-11, 2010.
  9. BIASI, L. A. et al. Prevalência de enteroparasitoses em crianças de entidade assistencial de Erechim/RS. Revista Perspectiva, Erechim, v. 34, n. 125, p. 173-179, 2010.
  10. BORGES, Wanessa Ferreira; MARCIANO, Franciele Maia; OLIVEIRA, Heliana Batista de. Parasitos intestinais: elevada prevalência de Giardia lamblia em pacientes atendidos pelo serviço público de saúde da região sudeste de Goiás, Brasil. 2011.
  11. MI Machado. Teníase e Hymenolepiase. In: Cimerman S, Cimerman B. Medicina Tropical. Atheneu. São Paulo, 2003. p. 195-204.
  12. BEHRMAN, R.E.; KLIEGMAN, R.M.; ARVIN, A.M. Tratado de pediatria. 15 ed. Rio de janeiro: Guanabara Koogan, 1997.
  13. SOUZA, Autany Trindade de; FAUSTINO, Silvia Maria Mathes; RODRIGUES, Artemis Socorro do Nascimento. Determinação da anemia por deficiência de ferro em crianças de 03 a 04 anos associada à enteroparasitoses – Macapá-Amapá. Ciência Equatorial, Volume 1 – Número 1 – 1º Semestre 2011.
  14. SILVA, Elizângela Farias da; SILVA, Vinícius Bentivóglio Costa; FREITAS, Fagner Luiz da Costa. Parasitoses intestinais em crianças residentes na comunidade Ribeirinha São Francisco do Laranjal, Município de Coari, Estado do Amazonas, Brasil. Revista de Patologia Tropical. Vol. 41 (1): 97-101. jan.-mar. 2012.
  15. ORO, Débora; KOPROSKI, Greice Kelly; ORO, Neila Aparecida; SBARDELOTTO, Caroline; SEGER, Juliana. Prevalência de parasitas intestinais em crianças de Des­canso – Santa Catarina – Brasil. Unoesc & Ciência – ACBS, Joaçaba, v. 1, n. 2, p. 151-156, jul./dez. 2010.
  16. ALVES, JR, et al, 2003. Parasitoses. intestinais em região semi-árida do nordeste do Brasil: resultados preliminares distintos das prevalências esperadas. Caderno de Saúde Publica; 19(2): 667-670.
  17. ANDRADE, Elisabeth Campos de; LEITE, Isabel Cristina Gonçalves; VIEIRA, Marcel de Toledo; ABRAMO, Clarice; TIBIRIÇA, Sandra Helena Cerrato; SILVA, Priscila Lima. Prevalência de parasitoses intestinais em comunidade quilombola no Município de Bias Fortes, Estado de Minas Gerais, Brasil, 2008. Epidemiol. Serv. Saúde, Brasília, 20(3):337-344, jul-set 2011.
  18. TASHIMA, Nair Toshiko; SIMÕES, Maria Jacira Silva. Parasitas intestinais; prevalência e correlação com a idade e com os sintomas apresentados de uma população infantil de Presidente Prudente-SP. Rev. bras. anal. clin, v. 37, n. 1, p. 35-39, 2005.
  19. DE SOUZA QUEIROZ, Suzana; MARCO, A. de A. Anemia ferropriva na infância. Jornal de Pediatria, v. 76, n. Supl 3, p. S299, 2000.
  20. İŞLEK, İ. et al. Effects of ascaris infection on iron absorption in children. Annals of Tropical Medicine & Parasitology, v. 87, n. 5, p. 477-481, 1993.
  21. CANTOS, Geny Aparecida; DUTRA, Rosilene Linhares; KOERICH, João PK. Ocorrência de anemia ferropriva em pacientes com enteroparasitoses. Saúde Rev, v. 5, p. 43-8, 2004.
  22. ARAÚJO, B. S. et al. Associação das parasitoses intestinais com anemia e eosinofilia em escolares do povoado de Matilha dos Pretos, Feira de Santana, Bahia, Brasil. Sitientibus Série Ciências Biológicas, v. 9, n. 1, p. 3-7, 2009.
  23. BRITO, Luciara L. et al. Fatores de risco para anemia por deficiência de ferro em crianças e adolescentes parasitados por helmintos intestinais. Revista Panamericana de Salud Pública, v. 14, p. 422-431, 2003.
  24. VITALLE, Maria Sylvia de Souza; ROMERO, K.T.; MEDEIROS, E.L.G.R. Prevalência de anemia carencial ferropriva, parasitoses intestinais e estado nutricional em pacientes assistidos no centro de atendimento e apoio ao adolescente. Revista Brazilian Pediatric News, vol. 5, n.º 1, março, 2003.
  25. CARRILLO, Maria Ruth Gonçalves Gaede; LIMA, Angélica Alves; NICOLATO, Roney Luiz de Carvalho. Prevalência de enteroparasitoses em escolares do bairro Morro de Santana no município de Ouro Preto, MG. Rev. bras. anal. clin, v. 37, n. 3, p. 191-193, 2005.
  26. SEIXAS, Marieli Tavares Leite et al. Avaliação da frequência de parasitos intestinais e do estado nutricional em escolares de uma área periurbana de Salvador, Bahia, Brasil. Revista de Patologia Tropical/Journal of Tropical Pathology, v. 40, n. 4, p. 304-314, 2011.
  27. BRABOSA, Fábio de Castro; RIBEIRO, Maria Cecília Marques; MARÇAL JÚNIOR, Oswaldo. Comparação da prevalência de parasitoses intestinais em escolares da zona rural de Uberlândia (MG). Rev. patol. trop, v. 34, n. 2, p. 151-154, 2005.

[1] Nurse. Master in Pathology of Tropical Diseases. Professor of the Nursing course at the Federal University of Maranhão UFMA.

[2] Nurse. Master in Pathology of Tropical Diseases. Professor of the Nursing course at the Federal University of Maranhão UFMA.

[3] Nurse. Specialist in Women’s Health. Professor of the Nursing course at the Federal University of Maranhão UFMA.

[4] Guidance counselor. Full Professor, Institute of Biological Sciences, Federal University of Pará – UFPA (2016). He holds a bachelor’s degree in Biomedicine (UFPA/1976), a Master’s degree in Biological Sciences – Genetics (UFRJ/1983) and a Doctorate in Humanities – Ruprecht-Karls-Universität Heidelberg (1990).

Sent: March, 2020.

Approved: July, 2020.

DEIXE UMA RESPOSTA

Please enter your comment!
Please enter your name here