ABSTRACT.
School-age children bear the highest burden of fascioliasis in endemic countries. Few studies have addressed Fasciola in preschool children. We performed a secondary data analysis using two Fasciola databases from Cusco, Peru, comparing preschoolers with elementary school children. We included 2,630 children, 50% were female, the median age was 8.4 years (interquartile range [IQR] 6.1–10.5), and 15% (396/2,630) were < 5 years of age. Children < 5 years were less likely to be infected with Fasciola hepatica (P = 0.008) and Hymenolepis nana (P < 0.001) and more likely to have anemia (P < 0.001) and a lower median height for age Z (HAZ) score (P = 0.002). Fascioliasis was less common in younger children, but this group may be at higher risk for chronic complications caused by fascioliasis.
Fascioliasis in South America is a foodborne zoonosis caused by Fasciola hepatica. Infections in the highlands of Bolivia, Ecuador, and Peru account for almost half of all fascioliasis cases worldwide.1 In these endemic countries, school-age children bear the highest burden of the disease.2,3 Among 3,000 children studied in the Cusco region of Peru, older children were more likely to be infected than younger children.4
Children less than 5 years of age are usually not reached by school-based fascioliasis control programs and are underrepresented in Fasciola studies. Ve et al., reported a case series of 4 children under 4 years with fascioliasis in Vietnam. In their review of the literature, the authors only found 38 reports of infected children less than 4 years old.5 Younger children may be more vulnerable to fascioliasis complications such as anemia and weight loss, which have a large impact during this critical developmental stage.3 Thus, further characterization of fascioliasis in this population is urgently needed. The aim of this study was to compare the prevalence and risk factors for fascioliasis in children under 5 years old to older children.
We performed secondary data analysis pooling the databases from two Fasciola studies in the Cusco region of Peru.4 We selected children 3–12 years old with stool microscopy results for helminth infections and complete blood counts. Children were enrolled in three districts (Anta, Zurite, and Ancahuasi) from the Anta province and one district (Huancarani) from the Paucartambo province in the Cusco region of Peru. Information on age, sex, location of the household, education of the parents, height for age Z (HAZ) score, complete blood counts, and stool microscopy using the Kato–Katz and Lumbreras rapid sedimentation for gastrointestinal helminths were used for the analysis. The diagnosis of chronic Fasciola infection was defined as the presence of the parasite eggs in at least one stool sample. The 2007 WHO growth standards and criteria were used to define stunting.6 Hemoglobin values were adjusted for chronic high-altitude exposure using the CDC formula and anemia was defined according to WHO age- and sex-adjusted cutoffs.7 The Statistical Package for the Social Sciences version 25.0 software (SPSS, Inc., Chicago, IL) was used for the statistical analysis; two tail P values < 0.05 were considered statistically significant. Under 5 and 5- to 12-year-old groups were compared using the χ2 and the Mann–Whitney U tests for categorical and continuous variables. Both studies were reviewed by the Institutional Ethics Committee of Universidad Peruana Cayetano Heredia (#60574) and the University of Texas Medical Branch (#12-099 and #13-080).
The combined databases had 3,270 complete records including 2,630 records from children 3 to 12 years old. Half (1,318/2,630, 50.1%) were female, the median age was 8.4 (interquartile range [IQR] 6.1–10.5) years, and 15.1% (396/2,630) were under 5 years of age (Table 1). The median years of education of the mothers was 6 years (IQR 3–10). One in four children (672/2,630, 25.6%) had at least one helminth infection and 3.7% (98/2,630) had two or more helminths. The most common helminth infections were Hymenolepis nana (389/2,630, 14.8%) followed by Ascaris lumbricoides (156/2,630, 5.9%) and F. hepatica (148/2,630, 5.6%). Strongyloides stercoralis (45/2,630, 1.7%), Trichuris trichiura (26/2,630, 1%), and hookworm (17/2,630, 0.6%) were less common. The median HAZ score was −1.34 (IQR –0.76 to −1.97) and 23.6% (615/2,605) of the children met criteria for stunting. The mean altitude-corrected hemoglobin was 12.4 g/dL (±1.1) and 13.3% (345/2,586) of the children had anemia.
Table 1.
Demographics and characteristics of children < 5 years old and > 5 years old
| Characteristic | N (%) | ||||
|---|---|---|---|---|---|
| Total | < 5 years | 5–12 years | P * | ||
| Sex | Female | 1,318 (50.1) | 194 (49%) | 1,124 (50.3) | 0.672 |
| Male | 1,312 (49.9) | 202 (51) | 1,110 (49.7) | ||
| District | Anta | 1,255 (47.7) | 184 (46.5) | 1,071 (47.9) | 0.069 |
| Ancahuasi | 806 (30.6) | 108 (27.3) | 698 (31.3) | ||
| Zurite | 297 (11.3) | 51 (12.8) | 246 (11) | ||
| Huancarani | 272 (10.3) | 53 (13.4) | 219 (9.8) | ||
| Prior anemia treatment | Yes | 242 (9.7) | 51 (13.9) | 191 (9) | 0.004 |
| No | 2,241 (90.3) | 315 (86.1) | 1,924 (91) | ||
| Prior malnutrition treatment | Yes | 145 (5.8) | 43 (11.7) | 102 (4.8) | < 0.001 |
| No | 2,336 (94.2) | 325 (88.3) | 2,011 (95.2) | ||
| Prior parasite treatment | Yes | 460 (18.6) | 87 (23.6) | 373 (17.7) | 0.007 |
| No | 2,015 (81.4) | 281 (76.4) | 1,734 (82.3) | ||
| Anemia | Yes | 345 (13.3) | 96 (25.1) | 249 (11.3) | < 0.001 |
| No | 2,241 (86.7) | 287 (74.9) | 1,954 (88.7) | ||
| Stunting | Yes | 615 (23.6) | 109 (27.7) | 506 (22.9) | 0.037 |
| No | 1,990 (75.7) | 284 (72.3) | 1,706 (77.1) | 1 | |
| Characteristic | Mean (±SD) | ||||
| Total | < 5 years | 5–12 years | P † | ||
| Altitude corrected hemoglobin (g/dL) | 12.4 (±1.06) | 11.6 (±1.0) | 12.5 (±1.0) | < 0.001 | |
| Platelets × 103 | 355.4 (±75.8) | 379.2 (±78.9) | 351.2 (±74.5) | < 0.001 | |
| Total white cell count × 103 | 7.4 (±2.6) | 8.1 (±4.6) | 7.2 (±2.1) | < 0.001 | |
| Height for age Z score | −1.34 (±0.9) | −1.49 (±1.1) | −1.32 (±0.95) | 0.002 | |
| Years of school of the mother | 6.45 (±3.7) | 7.9 (±3.7) | 6.19 (±3.7) | < 0.001 | |
| Years of school of the father | 7.87 (±3.4) | 8.7 (±3.4) | 7.72 (±3.4) | < 0.001 | |
χ2 test.
Student’s t-test.
The mothers of children under 5 had higher median years of education than the mothers of the older children (9 years [IQR 5–11] versus 6 years [IQR 3–10], P < 0.001) (Table 1). Children under 5 were less likely to be infected with F. hepatica ([11/396] versus [137/2,234], odds ratio [OR] = 0.43 [95% CI 0.23–0.81], P = 0.008) and H. nana ([28/396] versus [361/2,234], OR = 0.39 [95%CI 0.26–0.58], P < 0.001). No other significant differences in the prevalence of helminth infections were found between age groups. The median-corrected hemoglobin of children under 5 was lower than that of older children (11.6 g/dL [IQR 11.05–12.25] versus 12.5 g/dL [IQR 11.8–13.1], P < 0.001). Children under 5 were more likely than older children to have anemia ([96/383] versus [249/2,203], OR = 2.62 [95% CI 2.01–3.42], P < 0.001). The median HAZ score was lower in children under 5 years old (−1.52 [IQR −0.9 to −2.07] versus −1.32 [IQR −0.74 to −1.94], P = 0.002).
Among children under 5, children from Huancarani were more likely to be infected with Fasciola than children from other districts (4/53 versus 7/343, OR = 3.91 [95% CI 1.1–13.87], P = 0.046) (Table 2). In addition, the mothers of children with Fasciola infection had fewer years of education (6 years [IQR 2–9] versus 9 years [IQR 6–11], P = 0.042). There were no differences by sex (P = 0.372), anemia prevalence (P = 0.478), or other intestinal helminth infections between children with Fasciola and those not infected. Similarly, the median-corrected hemoglobin values (P = 0.127) and HAZ scores (P = 0.195) were not significantly different between children with fascioliasis and those without infection.
Table 2.
Characteristics of children < 5 years old with and without fascioliasis
| Characteristic | N (%) | ||||
|---|---|---|---|---|---|
| Total | Fasciola (+) | Fasciola (−) | P * | ||
| Sex | Female | 194 (49) | 7 (63.6) | 187 (48.7) | 0.324 |
| Male | 202 (51) | 4 (36.4) | 198 (51.4) | ||
| District | Anta | 184 (46.5) | 6 (54.5) | 178 (46.2) | 0.59 |
| Ancahuasi | 108 (27.3) | 1 (9.1) | 107 (27.8) | ||
| Zurite | 51 (12.9) | 0 (0) | 51 (13.2) | ||
| Huancarani | 53 (13.4) | 4 (36.4) | 49 (12.7) | ||
| Prior anemia treatment | Yes | 51 (13.9) | 2 (18.2) | 49 (13.7) | 0.654 |
| No | 317 (86.1) | 9 (81.8) | 308 (86.3) | ||
| Prior malnutrition treatment | Yes | 43 (11.7) | 6 (54.5) | 37 (10.4) | < 0.001 |
| No | 325 (88.3) | 5 (45.5) | 320 (89.6) | ||
| Prior parasite treatment | Yes | 87 (23.6) | 2 (18.2) | 85 (23.8) | 1 |
| No | 281 (76.4) | 9 (81.8) | 272 (76.2) | ||
| Anemia | Yes | 96 (27.7) | 4 (36.4) | 92 (24.7) | 0.478 |
| No | 287 (74.9) | 7 (63.6) | 280 (75.3) | ||
| Stunting | Yes | 109 (27.7) | 5 (45.5) | 104 (27.2) | 0.183 |
| No | 284 (72.3) | 6 (54.5) | 278 (72.8) | ||
| Characteristic | Mean (±SD) | ||||
| Total | Fasciola (+) | Fasciola (−) | P † | ||
| Age (years) | 4.1 (±0.5) | 3.8 (±0.7) | 4.1 (±0.5) | 0.088 | |
| Altitude corrected hemoglobin (g/dL) | 11.6 (±1.0) | 11.1 (±0.8) | 11.6 (±1) | 0.111 | |
| Platelets × 103 | 379.2 (±78.9) | 323.2 (±90) | 380.9 (±78.1) | 0.017 | |
| Total white cell count × 103 | 8.1 (±4.6) | 7.3 (±1.9) | 8.1 (±4.6) | 0.606 | |
| Absolute eosinophil count | 313 (±554) | 530 (±389) | 306 (±557) | 0.188 | |
| Height for age Z score | −1.49 (±1.1) | −1.63 (±1) | −1.48 (±1.11) | 0.655 | |
| Weight for age Z score | −0.51 (±0.85) | −0.70 (±0.65) | −0.51 (±0.86) | 0.457 | |
| Years of school of the mother | 7.9 (±3.7) | 5.6 (±3.6) | 8.0 (±3.7) | 0.038 | |
| Years of school of the father | 8.7 (±3.4) | 6.5 (±3.1) | 8.8 (±3.4) | 0.033 | |
χ2 test.
Student’s t-test.
Children under 5 years had a higher prevalence of anemia and stunting than older children. During the first 5 years of life, neural plasticity is fundamental for cognitive development and disruptions of these processes can have long-term consequences.8 Local health authorities in Peru have established programs focused on decreasing anemia and malnutrition among children under 5 years that include water, sanitation, and hygiene education (WASH), iron and other dietary supplementation, and deworming.9 Programs focused on WASH to improve nutritional status in children under 5 years have shown inconsistent effectiveness.10,11 In addition, high coverage and compliance with nutritional supplementation have been difficult to attain especially in rural areas of Peru.9
In our study, one in every four children had a helminth infection. The most common helminths were H. nana, A. lumbricoides, and F. hepatica. The first two parasites are associated with fecal oral transmission and suggest significant contamination of the environment with human feces. The prevalence of Ascaris and hookworm infection was low, which may reflect ongoing school-based deworming. However, current deworming programs do not address the most common parasites found here such as F. hepatica and H. nana. Although transmission of F. hepatica is not fecal-oral, the lack of access to safe water may be associated with increased risk and the contamination of the environment with Fasciola eggs may help maintain the life cycle of the parasite in the community.5,12 We found a significantly lower prevalence of Fasciola infection in children < 5 years old in endemic areas of Cusco. This observation is similar to other studies on fascioliasis with a peak prevalence in school age children.2,13 Fasciola infection in children under 5 years was associated with living in Huancarani and less years of education of the parents, likely from precarious hygiene practices.14
There are some limitations to our study. The number of children under 5 years included in this study was low and may have limited the power to detect differences between the Fasciola infected and uninfected groups. We pooled data collected from studies performed at different time points with potential differences in local interventions to prevent malnutrition and parasite infections. Larger studies, adequately powered, specifically involving children under 5 years, are needed to confirm our findings.
In summary, our results demonstrate that children under 5 years old had a higher prevalence of malnutrition and anemia, but a lower prevalence of Fasciola and Hymenolepis infections. Given the vulnerability of children during the first years of life, these parasite infections and the socioeconomic factors that increase the risk of impaired development must be addressed by local authorities. Further research about the determinants and impact of fascioliasis in preschool children and the safety of triclabendazole treatment in this age group are needed.
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