Impact of intestinal helminthes infections on stunting, wasting, normal biochemical and hematological values on school children in Gondar town, Ethiopia.

Abstract

Background

According to food and agriculture (FAO) estimates, around 1.02 billion people are undernourished worldwide [1]. In spite of some progress in achievements of the nutrition related Millennium Development Goals like reducing maternal mortality, problems associated with children malnutrition and hunger have not been showing significant improvement [2, 3]. In 2016, approximately 5.6 million children under age five died in the world with the highest proportion in Africa [4]. According to world food program report in 2012 [5], of 66 million primary school-age children  attended classes hungry in developing world, 23 million or 34.8% were found in Africa. Globally, an estimated 165 million (26%) stunted, 101 million (16%) underweight and 52 million (11%) wasted children of under-five years of age were reported in 2011 [3]. According to the 2015 Millennium development goal (MDG) report, more than 30% of the global under nutrition for under 5 years children was found in Sub-Saharan Africa (SSA) [3, 6]. In Africa, 58 million stunted, 13.9 million wasted, 10.3 million overweight and 220 million calorie deficient under five children were also been reported [3]. The severity of children mortality, delayed mental development, poor school performance, reduced intellectual capacity and reduced immunity for diseases are related with severity of stunting and wasting [7]. The percentage of stunting and wasting reflect the cumulative effects of malnutrition and parasites infections [7. 8]. Helminth parasites infections are the major factors in causing malnutrition [9, 10].

Globally in 2010, 819 million Ascaris, 438.9 million Hook worm and 464.6 million Trichuristrichiura infections were reported in Asia (70%), in Sub-Sharan Africa (16 %) and other part of the world (22%) including the 1.01 billion infection prevalence in school age children in Asia (70%), Sub-Sharan Africa (16%) and Latin Ameriaca and Caribbian (13%) [11]. Declined food intake and/or an increase in nutrient wastage through blood loss, vomiting or diarrhea related to helminthes infections mostly affects the nutritional status of an individual or aggravate protein energy malnutrition, anemia and other nutrient deficiencies [12]. Chronic schistosomiasis contributes to anemia and under-nutrition, which, in turn, can lead to growth stunting, poor school performance, poor work productivity, and continued poverty while blood loss due to Hook worm infection can cause iron deficiency anemia and hypo-proteinaemia[13]. Ascariasis cause malnutrition in addition to pathology associated the worm migration in the body. Chronic dysentery associated with Trichriasis is also a major problem in health of school children [14]. Heavy S. mansoni infected children in Brazil(above 400 eggs/g of stool) showed 2.74 fold higher risk of stunting compared to uninfected children [15].

Ethiopia, second populous nation in Africa, has been classified as low income countries with 20% of poverty in both urban and rural areas [16]. The prevalence of wasting in Ethiopia was 12% in under 5 years children in 2011 and  stunting reduced  from 64% in 1990 to 47% in 2008 [1, 16, 17]. Of the total 4, 921 under five children analyzed in 2014 to determine their nutritional status, the percentages of stunted, underweight and wasted were 40.4%, 25.2% and 8.7% respectively [18]. Low socio-economic status or low accessibility of food (poverty) in Ethiopia could be the main cause of malnutrition [19, 20]. Factors that increase the risk of intestinal parasitic infections such as swimming, bar foot walking (lack of shoes), bad hand washing habits and low Education status of parents were also reports to be associated with malnutrition  [19, 21, 22].  In Ethiopia, intestinal parasitic infections in under 5 years children were reported to cause malnutrition, anemia, and growth retardation [23, 24].  Researches describing the role of helminth infections and their intensity on nutritional status, anemia and normal hematological and biochemical values of primary school children are rare. The aims of this research was to evaluate the nutritional status of school children in Azezo primary school in Gondar town and compared it to WHO standards in addition to analyzing the impact of intestinal helminthes (infections and intensities) on normal growth, normal hematological and biochemical values in the school children.

Results

Stunting was statistically significantly associated with poor family status (without enough available food) compared to other factors (table 1). Intestinal helminth infections were highly prevalent in rural (57.1%) compared to urban residence (30.1%) in statistically significant different (p=0.000) manner. But, stunning or wasting were not associated with urban or rural residence (p>0.05). Swimming or washing in the rivers was more common for rural residences (p=0.04), but it was not associated with intestinal helminth infections or stunting. Almost all the community has shoes wearing  and hand washing habits.   Stunting, wasting and anaemia were not associated with these behaviour  (p>0.05)(Table 1).

Table 1 .Risk factor analysis table.Bionomial regression analysis was used to relate low accessibility of food, residence, education status of parents, shoes wearing habit, hand washing habits, Intestinal helminth infections and swimming or washing in the rivers as possible risk factors associated with stunting and wasting

Table 2.Regression analysis between nutritional status and haematological and biochemical values. The table indicates binomial regression analysis toshow relationship among growth status of school children and  haematological and biochemical values.

The overall prevalence of helminthes infections in the school children was 45.8% (178/384) with the leading Ascaris infection (20.6% or 79/384). The second and third leading infections wereSchistosomamansoni and Hook worm infections with prevalence of 17.4% (67/384) and 13.3% (51/384) respectively. The prevalent of the remaining Tricuristrichura, Hymenolopis nana and Taeniaspp were 3.4%, 1% and 0.3% respectively. Of the total 178 school children found infected, 37(9.6%) were with double infections (16 Ascaris – Schistosoma, 12 Ascaris – Hookworm, 4  Schistosoma – Hookworm and 5 Ascaris and others)  and  2.8%(5/178) triple  infections (4 Ascaris -Schistosoma –others and 1 Ascaris - Hook worm - Tricuristrichura). 

Ascarislumbericoides, Schistosomamansoni and  Hook worm mono-infection or Ascarislubericoides – Schistosomamansoni and Ascarislumbericoides – Hook worm co-infections were statistically significantly associated (P≤0.001) with protein malnutrition (hypoproteinemia) and Anaemia (Table 3) compared to non-infected school children. The overall infection was also statistically significantly associated with hypogycocemia, hypoproteinaemia and anemia (p=0.000).

Table 3.Table indicating multiple regression regression analysis to show relationship of different intestinal helminth infections with age groups, stunted and normal, hypo-proteinemic and hypo-glycemic school children.

Of total 384 school children, 209 were none infected compared to 56 light infections, 47 moderate infections and 75 heavy infections. Of total 47 stunted school children, the percentage with light, moderate, heavy and none infections were 34%, 4.3% 12.8% and 48.9% respectively.  Of 337 school children who were not stunted, the percentage with light, moderate, heavy and none infections were 11.9%, 13.4%, 20.5% and 54.3% respectively. intestinalhelminthes infection, intensity, mono or co-infection between stunted and normal school children were not statistically significantly different (P>0.05)(Table 4). Kruskal Wallis and Mann – Whitney analysis of variance indicated intestinal helminth infections were not statistically significantly different (p>0.05) for different Gender (Table 4). 

Table 4  Comparison of variance in Helminth infections, intensity and mono and co-infection in school children. Mann -Whitney Test (ANOVA test)  was used to lack statistically significantly difference  between male and female with prevalence of helminth infections, intensity of infection, mono or co-infections in addition to prevalence of anaemia and stunting.

Discussion

The prevalence of intestinal helminthes infections in this study (45.8%) has showed helminthes as one of the important parasites in school age children in Gondar as already reported in Gondar University Community Primary School (34.2%) [21]and Azezo Primary School (72.9%) [22]. These previous investigations were conducted before the Gondar City Administration Health office started regular deworming program in all primary schools. The difference in prevalence of intestinal parasites between the two previous studies could be related with relatively better standard of life of the University community and other people living in Central Gondar compared with semi-rural conditions in the peripheral Azezo areas where most students were

coming from the surrounding rural villages. The prevalence of Schistosomamansoni and Ascarislumbercoides decreased from 43.5% and 28.8% in 2008 [22] to 17.4% and 20.6% in 2018 by this study respectively in the same Azezo primary school.  Lack of elimination of intestinal helminth infections in school children, after regular annual deworming practices, had  indicated the magnitude of problems associated with helminthes re-infections in school children. This is an indication for inability of deworming program alone to control soil transmitted helminthiasis. Targeted hygiene education, sanitation measures and clean water supply could be among measures to be done in integration with deworming program to control helminth infections in school children as already reported[37]. Poor hand washing habits, unhygienic conditions, swimming habits, waking bar foot and education status of parents were reported for high incidence of intestinal infections which worsen the situation of malnutrition in children [19, 21, 22]. In this study, higher incidence (p-0.00) for intestinal helminth infections was observed for rural residence. Rural and urban conditions, with no difference in poverty level, did not show difference in stunting or wasting in school children (p>0.05)(Table 1). But, stunting was associated with low accessibility of food in poor families compared with families without shortage of food availability (p=0.000).Malnutrition due to low accessibility of food could be  the main source stunting in the study area. In   Ethiopia low accessibility of food due to low income of parents were reported to be statistically significant associated with stunting, wasting and underweight in school children [19, 20  33, 34]. The prevalence stunting and thinness including wasting in school children in different part of Ethiopia were ranged from 11 to 41 % for stunting and from 8.7- 34 % for thinness or underweight [19 24, 33-36].

In Ethiopia, intestinal parasitic infections in children reported to be associated with malnutrition, anaemia, and growth retardation [23]. Intestinal parasitic infections could result in malnutrition as they decline appetite for food, increase nutrient wastage through blood loss, vomiting and diarrhea and result in protein and energy deficiencies, anaemia and other nutrient deficiencies

Except 1 school children (0.3%), there was no problem of overweight. Only 34.9% of the school children were within WHO normal range based on BAZ scores. Majority (65%) were in state of thinness or underweight (thin, wasted or sever wasted).  Thinness (underweight) or stunting were not statistically significantly associated (p>0.05) with Age, sex, age groups, Haematological and biochemical values. All these results could show malnutrition was very common in all children and might be related with the low socio-economic background of the community in Azezo areas. But, 97.9% of stunting was found in 10 - 15 years age group (P=0.000). A statistically significantly differently different (p=0.000) high stunting prevalence (56.4 %) in 10-15 age group compared to lower (33.6%) in 5-10 age group was reported in school children in Macha district in Northwest Ethiopia [24].  A total of  50.1% stunting in  12-14 age group School children  compared to  36.9% in 6-11 age group (p=0.000) was also reported in Arbaminch town (Southern Ethiopia)[38]. Frequent stunting in children above 10 years compared to those under 10 was reported in Angola due to prolonged problem of food shortage during previous war time [39].  From the fact that anemia prevalence, glucose or protein malnutrition were not different between the age groups (p>0.05)( almost the same  probability) in addition to lack of difference in incidence of intestinal helminth infections between stunted and normal school children (P=0.49) at present study (Table 2), most probably, stunting was the result of prolonged malnutrition related to poverty and parasitic infection during childhood. Stunting may not be restricted to areas with war and prolonged shortage of food as indicated by Olivera et al. [39]. School feeding is highly recommended in countries like Ethiopia where the nation is classified as low income county with majority of rural and urban people living in poverty.

Ascarislumbericoides, Schistosomamansoni and  Hook worm mono-infection or Ascarislubericoides – Schistosomamansoni, Ascarislumbericoides– Hook worm co-infections and overall infections were statistically significantly associated (P ≤ 0.001) with protein malnutrition (hypo-proteinemia) and anaemia (Table 3). This type of association between severe malnutrition and infections reported to be common in children[40]. Intestinal helminthes infections could aggravate the situation of malnutrition. Prevalence of stunting and anaemia were reported higher in male than in female [41]. But, gender did not show any difference (p>0.05) for prevalence of stunting or anaemia in school children studied (Table 3). Intensity of infection and species of intestinal helminth infections were affected the prevalence of anaemia in statistically significant ways (p=0.000) compared with none infected school children (Table 4). The likelihood of anemia in school children, when it was compared with uninfected, increased 148 times for both Ascarislumbericoides-Schistosomamansoni co-infection, 38 times for Hook worm, 20 times for Schistosomamansoni and 3 times for Ascarislumbericoidesmono-infection (Table 4). But in Kenya S. mansoni mono-infection was reported to associate with anaemia and the likelihood of anemia in Schistosoma infection was 3.68 times compared with non- infected children [41].  Probably, Swimming habits of school children in the rivers in the study areas, unhygienic and bare foot walking  habits mentioned as risk factor for high incidence of Intestinal infections in the school children(Mengistu et al 2010) [22]might have contributed for such very high incidence of anemia in Azezo school children. Ascarislumbercoides, Schistosomamansoni and Hook worm infections were statistically significantly associated with lower MCH values (P≤0.001). Similarly, Schistosomamansoni and Hook worm infections were associated with below normal MCHC level (p=.000). Below normal concentration of MCH and MCHC were statistically significantly associated with anaemia (Table 2). Similar study in Thailand has indicated statistically significantly lower (P<0.000) MCH, and MCHC levels in helminthes infected group compared to the helminth-free group [42].

Conclusions

Helminthes infection is associated anaemia and hypo-proteinaemia, lower MCH and MCHC levels. The likelihood of anemia is very high in mono-and co-infected compared to uninfected school children. Stunting is the product of prolonged malnutrition and repeated reinfection of intestinal helminth infections in school children. Intestinal helminthes most probably aggravate the malnutrition in school children with low accessibility of food supply due to week economic background.  Regular monitoring of nutritional status of school children and screening intestinal Helminthes, integrated control which involve school feeding, deworming, clean water supply and public health awareness are required.

Abbreviations

BAZ – Body mass index for age Z-score

EPG – Egg per gram

 HAZ – Height for age Z-score

SD – Standard Deviation

 WBC - white blood cells

 RBC - red blood cells

Hgb- hemoglobin concentration

PCV - packed cell volume 

MCV-mean corpuscular volume

MCH-mean corpuscular hemoglobin

MCHC-mean corpuscular hemoglobinconcentration

Declarations

Ethics approval and consent to participate

Ethical clearance was obtained from Gondar University after proposal was reviewed by ethical review board of the University.

Consent for publication

The author consents to Editorial Board of the journal BMC to publish the paper. The author(s) accept responsibility for publishing this material in his own name, if any.

Availability of data and materials

The data analysed is available in   the corresponding author and could be available on reasonable request.

Competing interests

The authors declare that he has no competing interests.

Funding

University of Gondar office of research and community service and University    has funded this research.

Authors' contributions

 MB, DT and LW designed the research and participated in the research. DT collected the samples  and processed them.  MB and WL supervised the processes.  DT and WL analuzed the data. WL prepared this manuscript.

Acknowledgements      

University of Gondar is acknowledged for funding the research and Gondar university research Ethics review board and Gondar City Health Bureau for providing ethical clearance. Our thanks also goes to Azezo district health clinic for provision of free health service and drug treatment for parasite positive school children. 

Authors' contributions

DT, MB and WL developed the proposal and designed the study.  DT collected the samples and MB and WL supervised the processes. WL prepared this manuscript.

References

1. Food and Agriculture Organization, 2009.The State of Food Insecurity in the World Economic crises – impacts and lessonslearned. Rome, Food and Agriculture of the United Nations, 2009.http://www.fao.org/publications/sofi/en/.

2. Bain LE, Awah PK, Geraldine N, Kindong NP, Siga Y, Bernard,N, et al. Malnutrition in Sub – Saharan Africa: burden, causes and prospects Pan African Medical Journal. 2013; 15:120. doi:10.11604/pamj.2013.15.120.2535 online at: http://www.panafrican-med-journal.com/content/ article/15/120/full/

3. UNICEF, WHO and World Bank Group, 2015. UNICEF, World Health Organization, & the World Bank. (2012, September 20). Key facts and figures. UNICEF/WHO/World Bank Group Joint Child Malnutrition Estimates. http://www.who.int/nutgrowthdb/

4. Health Organization (2016) Global Health Observatory (GHO) data. Retrieved from http://www.who.int/gho/child_health/mortality/mortality_under_five/en/.

5. World Food Programme (2012) Two minutes to learn about: School Meals.Retrieved from https://documents.wfp.org/stellent/groups/public/documents/ communications/wfp220221.pdf?_ga=2.263020492.1314642926.1528665631-1013504369.1528665631.

6. United Nations ,2015. The Millennium Development Goals Report. UN, 2015. IFPRI: Washington DC.

7. Stewart, C.P.; Lannotti, L.; Dewey, K.G.; Michaelsen, K.F.; Onyango, A.W. Contextualizing complementary feeding in a broader framework for stunting prevention. Matern. Child Nutr. 2013, 9, 27–45.

8. , T., Africa’s Food and Nutrition Security Situation Where Are We and How Did We Get Here?, in 2020 Discussion Series. 2004, IFPRI: Washington DC.

9. World Health Organization (2018) Nutrition. Retrieved from http://www.who.int/nutrition/double-burden-malnutrition/infographics/en/.

10. Stephenson LS.Helminth parasites, a major factor in malnutrition. World Health Forum. 1994; 15(2):169-72

11. Pullan RL, Smith JL, Jasrasaria R, Brooker SJ. Global numbers of infection and disease burden of soil helminth infections in 2010. Parasit Vectors. 2014; 7:37. Epub 2014/01/23. https://doi.org/10.1186/1756-3305-7-37 PMID: 24447578; PubMed Central PMCID: PMCPMC3905661

12. Stephenson, L.S.; Holland, C. Reference. In: Impact of Helminth Infections on Human Nutrition; Aylor and Francis Ltd.: New York, NY, USA, 1987.

13. King CH. Parasites and poverty: the case of schistosomiasis. Acta Tropica. 2010;113(2):95-104.

14. Taren DL, Nesheim MC, Crompton DW, Holland CV, Barbeau I, Rivera G, et al. Contributions of Ascariasis to poor nutritional status in children from Chiriqui Province, Republic of Panama. Parasitology. 1987; 95:603–13.

15. Assis AMO, Prado MS, Barreto ML, Reis MG, Conceic¸a˜o Pinheiro1 SM, Parraga IM, et al.Schistosomamansoni infection and inadequate dietary intake Childhood stunting in Northeast Brazil: the role of Schistosomamansoni infection and inadequate dietary intake Eur J ClinNutr. 2004; 58: 1022–1029.

16. World Health Organization and UNICEF, 2009. Child growth standards and the identification of severe acute malnutrition in infants and children.A Joint Statement by the World Health Organization and the United Nations.Fund 2009

17. Sanchez-Montero M, SalseUbachN , 2010.Undernutrition: what works? A review of policy andpractise, S. M, Editor. 2010, ACF International Network and Tripode: Madrid.

18. . Akombi1 BJ, Kingsley EA, Merom D, Renzaho AM, Hall JJ. Child malnutrition in sub-Saharan Africa: A meta-analysis of demographic and health surveys (2006-2016). PLoS ONE.2017; 12(5): e0177338. https://doi.org/10.1371 /journal. pone.0177338

19. TamiratHailegebriel. Undernutrition, intestinal parasitic infection and associated risk factors among selected primary school children in Bahir Dar, Ethiopia. BMC Inf Dis. 2018;18:394https://doi.org/10.1186/s12879-018-3306-3

20. Mekonnen H, Tadesse T, Kisi T.Malnutrition and its Correlates among Rural Primary School Children ofFogera District, Northwest Ethiopia J Nutr Disorders Ther S12: 002. doi:10.4172/2161-0509.S12-002

21. Gelaw A, Anagaw B, Nigussie B, Silesh B, 3, Yirga A, Alem M, et al. Prevalence of intestinal parasitic infections and risk factors among schoolchildren at the University of Gondar Community School, Northwest Ethiopia: a cross-sectional study BMC Public Health 2013, 13:304 http://www. biomedcentral.com/1471-2458/13/304

22. Endris M, LemmaW, BelyhunY, Moges B, Gelaw A, Anagaw B, et al.Prevalence of intestinal parasites and associated risk factors among students of Atsefasil general elementary school Azezo, northwest Ethiopia. Ethiopia. J. Health Biomed Science Vol.3, No.1

23. Yirga G, Degarege A, Erko B. Prevalence of intestinal parasitic infections among children under five years of age with emphasis on Schistosomamansoni in WonjiShoa Sugar Estate, Ethiopia. PLoS One. 2014; 9(10):e109793. https://doi.org/10.1371/journal.pone.0109793 PMID: 25296337; PubMed Central PMCID: PMCPMC4190315.

24. Mazengia AL, Biks, GA. Predictors of Stunting among School-Age Children in Northwestern Ethiopia. J NutriMetab2018.https://doi.org/10.1155/2018/7521751

25. Ethiopian Statistical authority. ESA, 2007.

26. Ethiopian Meteorological Authority. EMA, 2015

27. WHO AnthroPlus for personal computers Manual: Software for assessing growth of the world’s children and adolescents. http://www.who.int/ growthref/tools/en/] Geneva, Switzerland: WHO; 2009. webcite.

28. Victora, CG (1991) The association between wasting and stunting: An international perspective’, The Journal of Nutrition122(5), 1105–1110.

29. De Onis M, Onyango AW, Borghi E, Garza C, Yang H (2006) Comparison of the World Health Organization (WHO) child growth standards and the National Centre for Health Statistics/WHO international growth reference: implications for child health programmes’. Pub Health Nutri. 2006; 9(7), 942–947. http://dx.doi. org/10.1017/PHN20062005.

30. Katz N, Pellegrino JS. Simple device for quantitative determinations’ of S. mansoni eggs in faeces examined by the thick smear technique. Rev Inst Med. Trop. 1972; 14, 397–400.

31. WHO (1994) Bench Aids for the diagnosis of intestinal parasites. World Health Organization, Geneva 1994.

32. Soldin, SJ, Brugnara C, Wong, EC.Pediatric reference ranges (4th ed.). Washington, DC: AACC Press.2005

33. Wolde M, Berhan Y, Chala W. Determinants of underweight, stunting and wasting among school children BMC Public Health;2005;15:8 DOI 10.1186/s12889-014-1337-2

34. Mekonnen Z, MekaS, Zeynudin A, Suleman, S.Schistosomamansoni infection and undernutrition among school age children in Fincha’a sugar estate, rural part of West Ethiopia. BMC Research Notes 2014, 7:763 http://www.biomedcentral.com/1756-0500/7/763

35. Birmeka M, Urga K, Petros, B () Intestinal Parasitic Infection and Nutritional Status of Elementary School children Aged 7 - 14 in Enemorena-Ener District, Gurage Zone, Ethiopia EC Nutrition.2017; 9.3: 129-141.

36. Kabeta A, Assefa S, Hailu D, Berhanu G. (). Intestinal parasitic infections and nutritional status of pre-school children in HawassaZuria District, South Ethiopia. Afr J MicrobiolResearch. 2017;11(31):1243-1251, 21 August, 2017 DOI: 10.5897/AJMR2017.8597

37. Jia T-W, Melville S,Utzinger J, King CH, Zhou X-N. Soil-transmitted helminth reinfection after drug treatment: a systematic review and meta-analysis. PLoSNegl Trop Dis. 2012;6(5):e1621.

38. TarikuIEZ, Abebe GA, Melketsedik ZA, Gutema, BT. Prevalence and factors associated with stunting and thinness among school-age children in Arba Minch Health and Demographic Surveillance Site, Southern Ethiopia PLoS ONE 2018;13(11): e0206659. https://doi.org/10.1371/journal.pone.0206659

39. Oliveira D, Filip F, Atouguia J, Fortes F, Guerra A, Centeno-Lima S. Infection by Intestinal Parasites, Stunting Anemia in School-Aged Children from Southern Angola. PLoS ONE; 2015: 10 (9): e0137327. doi:10.1371/journal. bpone.0137327

40. Krawinkel MB. Interaction of Nutrition and Infections globally. Ann NutrMetab2012; 61 (suppl 1):39–45 DOI: 10.1159/000345162

41. Butler SE, Muok EM, Montgomery SP, Odhiambo K, Mwinzi PM, Secor WE, et al. Mechanism of Anemia in Schistosoma mansoni–Infected School Children in Western Kenya. The American journal of tropical medicine and hygiene.2012;87(5):862-7.

42. Watthanakulpanich D, Maipanich W, Pubampen S, Sa-nguankiat S, PooudouanS, Chantaranipapong Y. Impact of Hookworm deworming on anemia and nutritional status among children in Thailand. Southeast Asian J Trop Med Public Health 2011; 42:782-792.

Tables

Table 1

Table 2

Table 3

Table 4