ABSTRACT
Background:
Malnutrition is a major public health problem in India, particularly in Chhattisgarh State with 18.9% under five children being wasted. Various factors like maternal nutrition, lack of sanitation and recurrent infection including parasitic have been documented risk factors. But the role of specific intestinal parasites and their contribution towards malnutrition are yet to be established.
Objectives:
To find the association of intestinal parasitic infection with severe acute malnutrition and to explore the association between intestinal parasitic infection with various cultural and demographic risk factors.
Material and Methods:
It was a community-based case control study done in Raipur, Chhattisgarh, India. A total of 190 patients were enrolled. 95 cases with severe acute malnutrition were selected from nutritional rehabilitation centers of Raipur District and control were children with normal nutritional status. Demographic data were collected with a structured questionnaire, and pooled stool samples were collected and examined in the Microbiology Laboratory of the Institute to see any associated parasitic infections.
Results:
The prevalence of parasitic infection was 8.4% among the cases and 2.1% among the controls. Giardiasis was the most common intestinal parasitic infection. Risk factors associated with parasitic infection were keeping long nails, eating food fallen on the ground and not maintaining hand hygiene. Illiterate mothers, not starting complementary feeds on time and poor socioeconomic status were the risk factors associated with SAM. No statistically significant association was found between severe acute malnutrition and parasitic infections in our study. Yet the number of children found infected with parasitic infection which were more in the cases group. However, parasitic infection as an independent risk factor for SAM could not be established.
Conclusion:
The study concluded that intestinal parasitic infection is not an associated risk factor for severe acute malnutrition. Ill-literate mother and practice of eating food fallen on the ground are risk factors for parasitic infection.
Keywords: Intestinal parasitic infection, risk factors for SAM, severe acute malnutrition (SAM)
Introduction
Nutrition is the cornerstone of physical, mental, social well-being and overall child development. Any compromise of nutrition makes a child vulnerable to various infections. The combination of undernutrition and infection leads to vicious cycle of worsening illness and deteriorating nutritional status. In the long run, it leads to stunting, impaired cognitive ability, reduced school performance and work performance.[1]
In the low-income countries of Asia and Africa, almost half of the under-5-children death is caused by malnutrition.[2] As per NFHS-5 data (2019–21), 32.1% children below five years are underweight; 35.5% are stunted; and 19.3% are wasted in India.[3] In Chhattisgarh, 31.3% of children under 5 years are underweight; 34.6% of children under 5 years are stunted; and 18.9% children are wasted.[4] Malnutrition stems from various factors starting from individual to social levels. Maternal nutritional status, inadequate food intake, lack of proper sanitation, social taboos, poverty, recurrent infections diarrhea, pneumonia, etc., are few to name.[5] The role of intestinal infection (bacterial, viral, helminthic or protozoal) with or without diarrhea has also been well-documented as a risk factor for malnutrition in developing countries. However, specific intestinal parasites and their contribution towards malnutrition are yet to be established.[6]
Intestinal parasitic infection (IPI) leads to loss of blood, malabsorption of nutrients, decline in food intake, diarrhea, vomiting, etc. These effects lead to or aggravate the disease per se.[7] In tropical countries with limited resources, hot and humid environment, sanitary and hygienic practices, living standards, drinking water and educational status tend to correlate with the chance of helminthic infection.[8]
Intestinal parasites include both multicellular helminths like Nematodes (roundworm), Cestodes (tapeworm), Trematodes (flatworms) and protozoan which are mostly unicellular and multiples inside human body. Common protozoal parasites are Giardia duodenalis, Cryptosporidium parvum and Entamoeba histolytica. Common helminthic infection on the other hand includes Ascaris lumbricoides, Trichuris trichiura, Strongyloides stercoralis and Hymenolepis nana.[9]
Studies done in various parts of India show different prevalence of parasitic infections. To quote a few, study done in Karnataka, India, showed the prevalence of parasitic infection to be 19.31% and E. histolytica was the most common infection.[10] Another study done in school going population in Andhra Pradesh showed 63.9% were infected with one or other intestinal parasites the mean age group being 8.8 years.[11] A study done among the school children in Durg, Chhattisgarh shows 78 children out of 250 (31.2%) being positive for one or more parasite.[12]
In order to reduce parasitic infections, globally periodic mass drug administration to population at high risk for parasitic infection can be considered. WHO also recommends empiric treatment of parasitic infections. This will lead to decrease in parasitic infections in the population and the associated morbidity.[13] In Raipur, no such study has ever been carried out. Hence, this study was conducted with a primary aim to evaluate the association of parasitic infection as a risk factor for severe acute malnutrition (SAM) among schoolgoing children in a Nutrition Rehabilitation Centre (NRC) in Raipur and to find the association of IPI with SAM. The secondary objectives of the study were to explore the association between IPI with various risk factors like age, gender, maternal education and other sanitary practices like open field defecation, hand washing, use of footwear, nail grooming, eating food fallen on the ground, etc. The results of this study would help in better understanding of the public health problem of malnutrition and measures to control the risk factors associated.
Material and Methods
The study was conducted between October 2020 and August 2022. It was a case control study conducted on children between 6 months and 5 years. The study protocol was duly approved by the Institute Ethics Committee, AIIMS, Raipur, vid letter number 1333/IEC-AIIMSRPR/2020. All children between 6 months and 5 years diagnosed to have severe acute malnutrition (SAM) as per WHO criteria and receiving treatment at the Kalibadi NRC of Raipur, CG, India, were the cases. Age- and sex-matched children with normal nutritional status or mild malnutrition (weight for height above -2SD) residing in the same geographical area were selected as controls. Children with secondary SAM and those, whose parents were not willing to participate were excluded.
The sample size was calculated using prior data which indicates that the probability of exposure among controls is 0.155 (15.5%) and the probability of exposure among cases is 0.328 (32.8%).[6] Using the PS software with the power of study being 80% and considering the level of significance (α =5%) P = 0.05, the sample size was calculated to be 95 each in the cases and control group.
Demographic data was collected by using a structured questionnaire designed for the study purpose. Socioeconomic status, father’s and mother’s educational level, mother’s age, initiation of breastfeeding, duration of exclusive breastfeeding and complementary feeding, sanitary practices, habits of eating foods fallen on ground and habit of keeping long fingernails and open field defecation were included.
Socioeconomic status for the household was assessed by Kuppuswamy classification. To check the association with the outcome variable, generated data were organized into low (scores <10), middle (11–15) and high (>16) categories. Education was categorized into literate and illiterate. Initiation of complementary feeding was categorized into two: at 6 months and below or above 6 months. Proper septic sanitation, open filed defecation, habits of washing hands after going to washroom with soap and water by mother or child, habits of taking foods fallen on the ground by the child were all categorized into present or not.
Stool sample collection: Mothers or caretakers were advised to collect fresh stool specimen of the child, amount being the size of distal phalanx in formalin containers for 3 days. Formalin helped in the preservation of ova, cyst, helminth, etc.
Three pooled samples of stool were collected from the caregivers once a week. These samples of each candidate were centrifuged together, and wet mount preparation was made. The wet mount preparation was processed in the Department of Microbiology, AIIMS Raipur.
The information of well-nourished and SAM children was blinded from the laboratory. The results of test along with various risk factors were entered into MS Excel separately for cases and controls. The total number of children with SAM and well-nourished and children with and without parasitic infection were calculated.
Results
In the study, a total of 190 children were enrolled, i.e. 95 each of cases and control. The average age of the participants in the cases group was 22.4 months and that among the controls was 23.65 months. Since it was a case control study with age- and sex-matched control, there were 48 males and 47 females in both the groups with male: female ratio being 1:1. Modified Kuppuswamy scale 2021 was used for the study. For the convenience, lower and upper lower has been grouped into low, lower middle as medium and upper middle and upper class as high. In cases, 70 children (73.7%) belonged to low socioeconomic group as compared to 28 (29.5%) in the control group. The distribution was statistically significant in relation to socioeconomic status. Apart from the socioeconomic status, maternal literacy status was also found to be a significant factor for malnutrition in the cases. Mothers of 59 children (62.1%) in the cases were illiterate, whereas only 14 (14.7%) mothers were illiterate in the control group. Fathers’ literacy status had no impact on malnutrition status. We did not find any significant difference in the proportion of babies who were breastfeed immediately after birth, but there was statistically significant difference in the percentage of children who were exclusively breastfeed beyond 6 months in the cases and control group. 88 (92.6%) of the children in malnutrition group were continued to be exclusively breastfed beyond 6 months as compared to 60 (63.2%) in the children with normal nutrition. Other factors which were significantly associated with malnutrition included hand hygiene after using toilet, eating food fallen on the ground and use of footwear by both mother and child. This is depicted in Table 1.
Table 1.
Risk factors for severe acute malnutrition (SAM)
| Factor | Category | Cases=95 | Control=95 | P |
|---|---|---|---|---|
| Socioeconomic status-Low | Low | 70 (73.7%) | 28 (29.5%) | <0.001 |
| Medium | 24 (25.3%) | 64 (67.4%) | ||
| Mothers education | Illiterate | 59 (62.1%) | 14 (14.7%) | <0.001 |
| Literate | 36 (37.9%) | 81 (85.3%) | ||
| Father`s education | Illiterate | 19 (20.0%) | 9 (9.5%) | =0.06 |
| Literate | 76 (80%) | 86 (90.5%) | ||
| Exclusive breastfeeding beyond 6 months | Yes | 88 (92.6%) | 60 (63.2%) | <0.001 |
| No | 7 (7.4%) | 35 (36.8%) | ||
| No | 79 (83.2%) | 15 (15.8%) | ||
| Use of footwear | Yes | 42 (44.2%) | 86 (90.5%) | <0.001 |
| No | 53 (55.8%) | 9 (9.5%) | ||
| Hand hygiene after using toilet | Yes | 34 (35.8%) | 79 (83.2%) | <0.001 |
| No | 61 (64.2%) | 16 (16.8%) | ||
| Eating food fallen on the ground | Yes | 66 (69.5%) | 20 (21.1%) | <0.001 |
| No | 29 (30.5%) | 75 (78.9%) |
In our study, only eight out of 95 individuals among the malnourished group had evidence of parasitic infection on stool routine microscopy. Among the controls, only two children had evidence of parasitic infection. Both these children had Giardia lamblia in the stool. Whereas in the cases four children had Giardia lamblia, two had Ancylostoma duodenale. Necator americanus and Entamoeba histolytica were seen in one case each. Although the cases had more parasitic infections than the control group, the difference was not significant statistically [Table 2].
Table 2.
Parasitic infections among cases and controls
| Stool Routine & Microscopy | Case | Control | ||
|---|---|---|---|---|
|
|
|
|||
| Count | % | Count | % | |
| Abnormal | 8 | 8.4% | 2 | 2.1% |
| Normal | 87 | 91.6% | 93 | 97.9% |
| Total | 95 | 100.0% | 95 | 100.0% |
P=0.06
We calculated the adjusted odds ratio (AOR) for the factors which were found to be significantly associated with SAM. Mother’s education, delayed initiation of complementary feeds, habit of eating or giving food fallen on the ground, no use of footwear and poor hand hygiene were significant risk factors for SAM. The AOR is mentioned in Table 3.
Table 3.
Statistically significant variables associated with SAM
| Characteristics | AOR | 95% C.I. | P | |
|---|---|---|---|---|
|
| ||||
| Lower | Upper | |||
| Mother’s Education | 11.711 | 2.978 | 46.054 | <0.001 |
| Initiation of Complementary feeding | 25.445 | 7.169 | 90.315 | <0.001 |
| Use of Footwear | 7.009 | 1.708 | 28.769 | 0.007 |
| Eating Foods Fallen on Ground | 9.278 | 2.670 | 32.247 | <0.001 |
| Washing Hands After Defecation | 6.230 | 1.725 | 22.500 | 0.005 |
| Constant | 0.017 | - | - | <0.001 |
Hosmer and Lemeshow Test P=0.949; Cox & Snell R Square=0.621 AOR: Adjusted Odds Ratio
Similarly, maternal education status (OR =4.03), practice of eating or giving food fallen on the ground (OR =12) were the only two factors which were linked with parasitic infections in the study population [Table 4].
Table 4.
Risk factors for parasitic infection
| Factors | Category | Parasitic infection | P | |
|---|---|---|---|---|
|
| ||||
| Present | Not present | |||
| Maternal education | Illiterate | 7 (9.6%) | 66 (90.4%) | 0.046 (OR=4.03) |
| Literate | 3 (2.6%) | 114 (97.4%) | ||
| Initiation of complementary feeding at 6 months | Yes | 2 (2.1%) | 94 (97.9%) | 0.06 |
| No | 8 (8.5%) | 86 (91.5%) | ||
| Exclusive breastfeeding beyond 6 months | Yes | 7 (4.7%) | 141 (95.3%) | 0.46 |
| No | 3 (7.1%) | 39 (92.9%) | ||
| Use of footwear | Yes | 6 (4.7%) | 122 (95.3%) | 0.73 |
| No | 4 (6.5%) | 58 (93.5%) | ||
| Practice of eating food fallen on the ground | Yes | 9 (10.5%) | 77 (89.5%) | 0.006 (OR=12) |
| No | 1 (1%) | 103 (99.0%) | ||
| Hand hygiene after using toilet | Yes | 3 (2.7%) | 110 (97.3%) | 0.09 |
| No | 7 (9.1%) | 70 (90.9%) | ||
OR: Odds ratio
Discussion
Undernutrition is a major public health problem and SAM refers to its severe form which is a nutritional emergency. In fact, combating undernutrition is the greatest global health challenges till date.[14]
There is no doubt that the global incidence of undernutrition is on decreasing trend. In India, as per NFHS 4 and 5 data the burden of wasting, stunting and severe wasting has shown drastic decrease. In Chhattisgarh, also severe wasting has decreased from 8.4% to 7.5%. As per the literature, SAM is associated with various risk factors like poor socio-economic status, maternal education, family size, etc. Helminthic infection is also identified as a risk factor of malnutrition in few studies.[13] Hence, this study was carried out to investigate this association in Raipur, Chhattisgarh.
The mean age of the cases was 22.54 ± 14.63 months and that of controls were 23.65 ± 15.54 months, 88.4% of the cases and 85.3% of the controls were in the age group of 6–36 months. Younger children were more acutely malnourished has been supported by studies done in Ethiopia (Kebede et al..).[15] and southern India (David et al.).[16] Kebede et al.[15] study was a retrospective hospital-based study and the mean age in their study was 27.4 (SD ±16.5) months, 62.6% children were in the age group of 6–24 months. Whereas David et al.[16] study was similar to our community-based case control study. In this study mean age of the children was 24 months and 39% children were in 12–23 months age group for both cases and controls. Children in the age group of 24–35 months accounted for 27.8% of cases and 22.6% of controls. These findings are in concordance with our study.
The gender of the participants did not emerge as a significant risk factor for malnutrition in our study and male: female ratio was 1:1. In our study, there were 48 males as against 47 females. However, in other studies significance of gender were noted. In 1997, Saito at el conducted a case control study in rural south India found female gender as the significant risk factor of severe malnutrition. In fact, female sex was found 3 times at risk of developing malnutrition than male children.[17]
The literacy status of the parent emerged as an important risk factor of malnutrition in this study. Mother’s education levels and malnutrition had a strong association, whereas father’s educational status was found unrelated to the nutritional status of the child. It concurs with the study done by Gupta at el. who found a strong relation found between nutritional status of the subjects and educational level of their mothers.[18] Similar study done by Bhat et al. also found that children with good nutritional status were those whose mothers were literate and had higher levels of knowledge regarding feeding practices and knowledge of weaning practices.[19]
Rizky et al. in their cross-sectional study with the aim to evaluate the prevalence of parasitic infection and the knowledge and risk factors associated with parasitic infection concluded that offsprings of the parents who had less knowledge about hygienic practices were more prone to develop parasitic infections.[20] Our study also corroborates this finding, and the odds of developing parasitic infection were 4.06 times in children whose mothers were illiterate as compared to those children whose mothers were literate.
Poverty is a basic determinant which influences malnutrition. Islam et al. in their case control study found that selected socioeconomic indicators such as poor family income have a significant association with undernutrition.[21] Galgamuwa et al.[22] in their community-based study from Sri Lanka also found that >70% subjects with undernutrition belonged to family with low income. Our study also revealed that SAM was more prevalent among the low socioeconomic status.
Pandey et al.[23] conducted a community-based cross-sectional unmatched case control study to find the risk factors for SAM among infants emphasizing context of breastfeeding and complementary feeding practices in central India and found that the odds of being severely malnourished increase with lack of exclusive breastfeeding and inappropriate complementary feeding or continuing exclusive breastfeeding beyond 6 months. Pravana et al.[24] conducted a case control study in Nepal to assess the various risk factors of malnutrition also emphasized that not initiating complementary feeding at the age of 6 months had 2.9 times more risk of developing undernutrition. Chanie et al.[25] found that not starting complementary feeding at 6 months was a risk factor for acute malnutrition. This may be because children above 6 months need additional food to meet nutritional requirements. Initiating adequate and timely complementary feeding is very important for achieving proper growth and development. These results concord with our study.
Not wearing footwear was identified as an important risk factor for developing parasitic infection in our study. Similar observations were made by Rahmi et al.[26] from Indonesia and Rizky et al.[20] from North Sumatra.
Dhaka et al.[27] in their cross-sectional study in rural districts of Haryana found that children who did not have the practice of washing hands regularly before taking food, habits of taking foods fallen on the ground, not maintaining proper nail hygiene had more association with helminthic infections. Our study also corroborates with this fact. Indeed, in our study odds of developing parasitic infection were 12 times more in children who had the habit of eating foods fallen on the ground (P = 0.006).
Lone et al. in their study in 2011, with an aim to ascertain the recent pattern and risk factors associated with parasitic infection cites that statistically significant risk factors associated with helminthic infections include open field defecation, untrimmed nails and improper hand hygiene after defecation.[28] In our study, the latter two factors were important risk factors for SAM and parasitic infection; however, we did not find open field defecation as a risk factor for parasitic infection among our population. No open field defecation and each of the household having septic tank can be attributed to Swachh Bharat Mission which improved the level of cleanliness through proper solid and liquid waste management.
Kabeta et al.[29] conducted a community-based cross-sectional study, in Zuria District, South Ethiopia, and found that half (51.3%) of children were infected with at least one type of intestinal parasite. Wasting, underweight and stunting were seen in children with parasitic infection as compared with nutritional normal children. A study done by Osman et al.[30] in Somali had a very high percentage of IPI 82.9% in children with malnutrition with 23.4% (43 of 184) had double parasitic infections. Similarly, Deka S et al.[31] in their tertiary care hospital-based study involving 123 under 5 children from North-Eastern India found a high prevalence of IPIs, i.e. 60.2% and 36.6%, in children with stunting and wasting, respectively. The prevalence of IPI was more in children with higher grade of malnutrition. This study also linked cryptosporidium species to wasting and ascaris and hookworms to stunting. The prevalence and malnutrition and parasitic infection was high in the study area. These results are in contradiction to our findings, where we did not find statistically significant association between parasitic infections and SAM. Our results match with Imam et al.[13] where the prevalence of parasitic infection was low, and no significant association was found between the parasitic infection and SAM. Our study findings suggest that a primary care. Physician may contribute to a significant extent to improve the nutritional status of under 5 children by educating mothers about the basic hygienic practices like hand washing, trimming of nails, use of footwear and avoid feeding food fallen on the ground.
Conclusion
In this case control study with 95 children in each group, prevalence of IPI was found to be 8.4% among cases and 2.1% among controls. Though more children in the cases group had parasitic infection, it was not statistically significant. Giardiasis was the most common parasitic infection found in the study. Mother’s education, poor socioeconomic status and younger age group were significant risk factors for SAM. Factors which increased the risk of parasitic infections included practice of keeping long fingernails, eating food fallen on the ground, unhygienic practices after using toilet and before meals.
Strengths of the study
Our study was a community-based case control study. Cases and controls were identified through WHO 2006 growth standards that increase the strength of the study. In our study, we analyzed the various risk factors of malnutrition and parasitic infection that can lead to various interventions which can improve health of child and prevent parasitic infection which includes initiation of complementary feeds at 6 months, regular trimming of fingernails, following recommended sanitary practices of hand washing after using toilet and before serving food, use of footwear and emphasis on maternal education.
Limitations of the study
Enrolling participants from multiple centers could have given a broader perspective. Due to intermittent excretion of intestinal parasites, follow-up stool samples could have given more accurate transmission rate. Other laboratory parameters like TLC and absolute eosinophilic count could have been included.
Ethics approval letter
Letter number 1333/IEC-AIIMSRPR/2020.
Conflicts of interest
There are no conflicts of interest.
Funding Statement
Nil.
References
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