Skip to main content
Top
Published in: Malaria Journal 1/2020

01-12-2020 | Falciparum Malaria | Research

Uncomplicated falciparum malaria among schoolchildren in Bajil district of Hodeidah governorate, west of Yemen: association with anaemia and underweight

Authors: Talal S. Alwajeeh, Rashad Abdul-Ghani, Amal F. Allam, Hoda F. Farag, Safia S. M. Khalil, Amel Y. Shehab, Mona H. El-Sayad, Raed A. Alharbi, Shaia S. R. Almalki, Ahmed A. Azazy

Published in: Malaria Journal | Issue 1/2020

Login to get access

Abstract

Background

Malaria, malnutrition and anaemia are major public health problems in Yemen, with Hodeidah being the most malaria-afflicted governorate. To address the lack of relevant studies, this study was conducted to determine the prevalence of Plasmodium falciparum and its relation to nutritional status and haematological indices among schoolchildren in Bajil district of Hodeidah governorate, west of Yemen.

Methods

A cross-sectional study was conducted among 400 schoolchildren selected randomly from four schools in Bajil district. Data about demographic characteristics, risk factors and anthropometric measurements of age, height and weight were collected. Duplicate thick and thin blood films were prepared, stained with Giemsa and examined microscopically for malaria parasites. The density of P. falciparum asexual stages was estimated on thick films. EDTA-blood samples were examined for the haematological indices of haemoglobin (Hb) and blood cell counts.

Results

Plasmodium falciparum was prevalent among 8.0% (32/400) of schoolchildren with a mean parasite density of 244.3 ± 299.3/µL of blood and most infections showing low-level parasitaemia, whereas Plasmodium vivax was detected in one child (0.25%). Residing near water collections was a significant independent predictor of falciparum malaria [adjusted odds ratio (AOR) = 2.6, 95.0% CI 1.20–5.72; p = 0.016] in schoolchildren. Mild anaemia was prevalent among more than half of P. falciparum-infected schoolchildren and significantly associated with falciparum malaria (AOR = 5.8, 95.0% CI 2.39–14.17; p < 0.001), with a mean Hb concentration of 10.7 ± 1.0 g/dL. Although the mean values of the total white blood cells, monocytes and platelets were significantly lower in infected than non-infected schoolchildren, they were within normal ranges. More than half of the children were malnourished, with stunting (39.3%) and underweight (36.0%) being the most prevalent forms of malnutrition; 6.3% of children were wasted. Underweight (AOR = 5.3, 95.0% CI 2.09–13.62; p < 0.001) but not stunting or wasting, was a significant predictor of falciparum malaria among schoolchildren.

Conclusion

Asymptomatic falciparum malaria is prevalent among schoolchildren in Bajil district of Hodeidah Governorate, with predominance of low parasitaemic infections and significant association with mild anaemia and underweight. Residence near water collection is a significant predictor of infection with falciparum malaria among schoolchildren. Further studies among children with severe malaria and those with high parasite densities are recommended.
Literature
1.
go back to reference WHO. World malaria report 2019. Geneva: World Health Organization; 2019. WHO. World malaria report 2019. Geneva: World Health Organization; 2019.
2.
go back to reference Abdul-Ghani R. Malaria research priorities in Yemen: paving the way for malaria elimination. Yemeni J Med Sci. 2015;9:1–5.CrossRef Abdul-Ghani R. Malaria research priorities in Yemen: paving the way for malaria elimination. Yemeni J Med Sci. 2015;9:1–5.CrossRef
3.
go back to reference IOM. Malaria in Yemen: needs assessment. Amman: Regional MER Project Management Unit, International Organization for Migration; 2017. IOM. Malaria in Yemen: needs assessment. Amman: Regional MER Project Management Unit, International Organization for Migration; 2017.
6.
go back to reference WHO Expert Committee. Physical status: the use and interpretation of anthropometry. Geneva: WHO; 1995. WHO Expert Committee. Physical status: the use and interpretation of anthropometry. Geneva: WHO; 1995.
7.
go back to reference WHO. WHO child growth standards: length/height-for-age, weight-for-age, weight-for-length, weight-for-height and body mass index-for-age: methods and development. Geneva: World Health Organization; 2006. WHO. WHO child growth standards: length/height-for-age, weight-for-age, weight-for-length, weight-for-height and body mass index-for-age: methods and development. Geneva: World Health Organization; 2006.
8.
go back to reference Shankar AH. Nutritional modulation of malaria morbidity and mortality. J Infect Dis. 2000;182(Suppl 1):S37–53.PubMedCrossRef Shankar AH. Nutritional modulation of malaria morbidity and mortality. J Infect Dis. 2000;182(Suppl 1):S37–53.PubMedCrossRef
9.
go back to reference Das D, Grais R, Okiro E, Stepniewska K, Mansoor R, Van Der Kam S, Terlouw D, et al. Complex interactions between malaria and malnutrition: a systematic literature review. BMC Med. 2018;16:186.PubMedPubMedCentralCrossRef Das D, Grais R, Okiro E, Stepniewska K, Mansoor R, Van Der Kam S, Terlouw D, et al. Complex interactions between malaria and malnutrition: a systematic literature review. BMC Med. 2018;16:186.PubMedPubMedCentralCrossRef
10.
go back to reference Ehrhardt S, Burchard GD, Mantel C, Cramer JP, Kaiser S, Kubo M, et al. Malaria, anemia, and malnutrition in African children—defining intervention priorities. J Infect Dis. 2006;194:108–14.PubMedCrossRef Ehrhardt S, Burchard GD, Mantel C, Cramer JP, Kaiser S, Kubo M, et al. Malaria, anemia, and malnutrition in African children—defining intervention priorities. J Infect Dis. 2006;194:108–14.PubMedCrossRef
11.
go back to reference Friedman JF, Kwena AM, Mirel LB, Kariuki SK, Terlouw DJ, Phillips-Howard PA, et al. Malaria and nutritional status among pre-school children: results from cross-sectional surveys in western Kenya. Am J Trop Med Hyg. 2005;73:698–704.PubMedCrossRef Friedman JF, Kwena AM, Mirel LB, Kariuki SK, Terlouw DJ, Phillips-Howard PA, et al. Malaria and nutritional status among pre-school children: results from cross-sectional surveys in western Kenya. Am J Trop Med Hyg. 2005;73:698–704.PubMedCrossRef
13.
go back to reference Verhoef H, West CE, Veenemans J, Beguin Y, Kok FJ. Stunting may determine the severity of malaria-associated anemia in African children. Pediatrics. 2002;110:e48.PubMedCrossRef Verhoef H, West CE, Veenemans J, Beguin Y, Kok FJ. Stunting may determine the severity of malaria-associated anemia in African children. Pediatrics. 2002;110:e48.PubMedCrossRef
14.
go back to reference Alexandre MA, Benzecry SG, Siqueira AM, Vitor-Silva S, Melo GC, Monteiro WM, et al. The association between nutritional status and malaria in children from a rural community in the Amazonian region: a longitudinal study. PLoS Negl Trop Dis. 2015;9:e0003743.PubMedPubMedCentralCrossRef Alexandre MA, Benzecry SG, Siqueira AM, Vitor-Silva S, Melo GC, Monteiro WM, et al. The association between nutritional status and malaria in children from a rural community in the Amazonian region: a longitudinal study. PLoS Negl Trop Dis. 2015;9:e0003743.PubMedPubMedCentralCrossRef
15.
go back to reference Fillol F, Sarr JB, Boulanger D, Cisse B, Sokhna C, Riveau G, et al. Impact of child malnutrition on the specific anti-Plasmodium falciparum antibody response. Malar J. 2009;8:116.PubMedPubMedCentralCrossRef Fillol F, Sarr JB, Boulanger D, Cisse B, Sokhna C, Riveau G, et al. Impact of child malnutrition on the specific anti-Plasmodium falciparum antibody response. Malar J. 2009;8:116.PubMedPubMedCentralCrossRef
16.
go back to reference Genton B, Al-Yaman F, Ginny M, Taraika J, Alpers MP. Relation of anthropometry to malaria morbidity and immunity in Papua New Guinean children. Am J Clin Nutr. 1998;68:734–41.PubMedCrossRef Genton B, Al-Yaman F, Ginny M, Taraika J, Alpers MP. Relation of anthropometry to malaria morbidity and immunity in Papua New Guinean children. Am J Clin Nutr. 1998;68:734–41.PubMedCrossRef
17.
go back to reference Gari T, Loha E, Deressa W, Solomon T, Lindtjørn B. Malaria increased the risk of stunting and wasting among young children in Ethiopia: results of a cohort study. PLoS ONE. 2018;13:e0190983.PubMedPubMedCentralCrossRef Gari T, Loha E, Deressa W, Solomon T, Lindtjørn B. Malaria increased the risk of stunting and wasting among young children in Ethiopia: results of a cohort study. PLoS ONE. 2018;13:e0190983.PubMedPubMedCentralCrossRef
18.
go back to reference WHO. Malaria control in complex emergencies. Geneva: World Health Organization; 2005. WHO. Malaria control in complex emergencies. Geneva: World Health Organization; 2005.
19.
20.
go back to reference Kotepui M, Phunphuech B, Phiwklam N, Chupeerach C, Duangmano S. Effect of malarial infection on haematological parameters in population near Thailand-Myanmar border. Malar J. 2014;13:218.PubMedPubMedCentralCrossRef Kotepui M, Phunphuech B, Phiwklam N, Chupeerach C, Duangmano S. Effect of malarial infection on haematological parameters in population near Thailand-Myanmar border. Malar J. 2014;13:218.PubMedPubMedCentralCrossRef
21.
go back to reference Maina RN, Walsh D, Gaddy C, Hongo G, Waitumbi J, Otieno L, et al. Impact of Plasmodium falciparum infection on haematological parameters in children living in Western Kenya. Malar J. 2010;9(Suppl 3):S4.PubMedPubMedCentralCrossRef Maina RN, Walsh D, Gaddy C, Hongo G, Waitumbi J, Otieno L, et al. Impact of Plasmodium falciparum infection on haematological parameters in children living in Western Kenya. Malar J. 2010;9(Suppl 3):S4.PubMedPubMedCentralCrossRef
22.
go back to reference CSO. Population census of Yemen. Sana'a: Central Statistical Organization; 2004. CSO. Population census of Yemen. Sana'a: Central Statistical Organization; 2004.
23.
go back to reference Cheesbrough M. District laboratory practice in tropical countries: part 1. 2nd ed. Cambridge: Cambridge University Press; 2005.CrossRef Cheesbrough M. District laboratory practice in tropical countries: part 1. 2nd ed. Cambridge: Cambridge University Press; 2005.CrossRef
24.
go back to reference WHO. Basic malaria microscopy. Part 1. Learner's guide. 2nd ed. Geneva: World Health Organization; 2010. WHO. Basic malaria microscopy. Part 1. Learner's guide. 2nd ed. Geneva: World Health Organization; 2010.
25.
go back to reference WHO. Haemoglobin concentrations for the diagnosis of anaemia and assessment of severity. Geneva: World Health Organization; 2011. WHO. Haemoglobin concentrations for the diagnosis of anaemia and assessment of severity. Geneva: World Health Organization; 2011.
26.
go back to reference Cantor AB. Thrombocytopoiesis. In: Hoffman R, Benz EJ, Silberstein LE, Heslop HE, Weitz J, Anastasi J, et al., editors. Hematology: basic principles and practice. 7th ed. Philadelphia: Elsevier; 2017. p. 334–349. Cantor AB. Thrombocytopoiesis. In: Hoffman R, Benz EJ, Silberstein LE, Heslop HE, Weitz J, Anastasi J, et al., editors. Hematology: basic principles and practice. 7th ed. Philadelphia: Elsevier; 2017. p. 334–349.
27.
go back to reference Dibley MJ, Goldsby JB, Staehling NW, Trowbridge FL. Development of normalized curves for the international growth reference: historical and technical considerations. Am J Clin Nutr. 1987;46:736–48.PubMedCrossRef Dibley MJ, Goldsby JB, Staehling NW, Trowbridge FL. Development of normalized curves for the international growth reference: historical and technical considerations. Am J Clin Nutr. 1987;46:736–48.PubMedCrossRef
28.
go back to reference Al-Maktari MT, Bassiouny HK, Al-Hamd ZS, Assabri AM, El-Massry AG, Shatat HZ. Malaria status in Al-Hodeidah Governorate, Yemen: malariometric parasitic survey & chloroquine resistance P. falciparum local strain. J Egypt Soc Parasitol. 2003;33:361–72.PubMed Al-Maktari MT, Bassiouny HK, Al-Hamd ZS, Assabri AM, El-Massry AG, Shatat HZ. Malaria status in Al-Hodeidah Governorate, Yemen: malariometric parasitic survey & chloroquine resistance P. falciparum local strain. J Egypt Soc Parasitol. 2003;33:361–72.PubMed
29.
go back to reference Al-Mekhlafi AM, Fong MY, Azazy AA, Mahdy MA. Study on the prevalence of malaria among patients with fever in Hodiedah Province, Yemen. In: the 45th annual scientific seminar of the Malaysian Society of Parasitology and Tropical Medicine, Mar 18–19. Kuala Lumpur, Malaysia; 2009. Al-Mekhlafi AM, Fong MY, Azazy AA, Mahdy MA. Study on the prevalence of malaria among patients with fever in Hodiedah Province, Yemen. In: the 45th annual scientific seminar of the Malaysian Society of Parasitology and Tropical Medicine, Mar 18–19. Kuala Lumpur, Malaysia; 2009.
30.
go back to reference Alkadi HO, Al-Maktari MT, Nooman MA. Chloroquine-resistant Plasmodium falciparum local strain in Taiz Governorate. Repub Yemen Chemother. 2006;52:166–70.CrossRef Alkadi HO, Al-Maktari MT, Nooman MA. Chloroquine-resistant Plasmodium falciparum local strain in Taiz Governorate. Repub Yemen Chemother. 2006;52:166–70.CrossRef
31.
go back to reference Azazy AA, Raja'a YA. Malaria and intestinal parasitosis among children presenting to the paediatric centre in Sana'a. Yemen East Mediterr Health J. 2003;9:1048–53.PubMed Azazy AA, Raja'a YA. Malaria and intestinal parasitosis among children presenting to the paediatric centre in Sana'a. Yemen East Mediterr Health J. 2003;9:1048–53.PubMed
32.
go back to reference Bamaga OA, Mahdy MA, Mahmud R, Lim YA. Malaria in Hadhramout, a southeast province of Yemen: prevalence, risk factors, knowledge, attitude and practices (KAPs). Parasites Vectors. 2014;7:351.PubMedPubMedCentralCrossRef Bamaga OA, Mahdy MA, Mahmud R, Lim YA. Malaria in Hadhramout, a southeast province of Yemen: prevalence, risk factors, knowledge, attitude and practices (KAPs). Parasites Vectors. 2014;7:351.PubMedPubMedCentralCrossRef
33.
go back to reference Kimbi HK, Sumbele IU, Nweboh M, Anchang-Kimbi JK, Lum E, Nana Y, et al. Malaria and haematologic parameters of pupils at different altitudes along the slope of Mount Cameroon: a cross-sectional study. Malar J. 2013;12:193.PubMedPubMedCentralCrossRef Kimbi HK, Sumbele IU, Nweboh M, Anchang-Kimbi JK, Lum E, Nana Y, et al. Malaria and haematologic parameters of pupils at different altitudes along the slope of Mount Cameroon: a cross-sectional study. Malar J. 2013;12:193.PubMedPubMedCentralCrossRef
34.
go back to reference Nankabirwa J, Wandera B, Kiwanuka N, Staedke SG, Kamya MR, Brooker SJ. Asymptomatic Plasmodium infection and cognition among primary schoolchildren in a high malaria transmission setting in Uganda. Am J Trop Med Hyg. 2013;88:1102–8.PubMedPubMedCentralCrossRef Nankabirwa J, Wandera B, Kiwanuka N, Staedke SG, Kamya MR, Brooker SJ. Asymptomatic Plasmodium infection and cognition among primary schoolchildren in a high malaria transmission setting in Uganda. Am J Trop Med Hyg. 2013;88:1102–8.PubMedPubMedCentralCrossRef
35.
go back to reference Kim M-J, Jung B-K, Chai J-Y, Eom KS, Yong T-S, Min D-Y, et al. High malaria prevalence among schoolchildren on Kome Island, Tanzania. Korean J Parasitol. 2015;53:571–3.PubMedPubMedCentralCrossRef Kim M-J, Jung B-K, Chai J-Y, Eom KS, Yong T-S, Min D-Y, et al. High malaria prevalence among schoolchildren on Kome Island, Tanzania. Korean J Parasitol. 2015;53:571–3.PubMedPubMedCentralCrossRef
36.
go back to reference Mathanga DP, Halliday KE, Jawati M, Verney A, Bauleni A, Sande J, et al. The high burden of malaria in primary school children in southern Malawi. Am J Trop Med Hyg. 2015;93:779–89.PubMedPubMedCentralCrossRef Mathanga DP, Halliday KE, Jawati M, Verney A, Bauleni A, Sande J, et al. The high burden of malaria in primary school children in southern Malawi. Am J Trop Med Hyg. 2015;93:779–89.PubMedPubMedCentralCrossRef
37.
go back to reference Sumbele IU, Bopda OS, Kimbi HK, Ning TR, Nkuo-Akenji T. Nutritional status of children in a malaria meso endemic area: cross sectional study on prevalence, intensity, predictors, influence on malaria parasitaemia and anaemia severity. BMC Public Health. 2015;15:1099.PubMedPubMedCentralCrossRef Sumbele IU, Bopda OS, Kimbi HK, Ning TR, Nkuo-Akenji T. Nutritional status of children in a malaria meso endemic area: cross sectional study on prevalence, intensity, predictors, influence on malaria parasitaemia and anaemia severity. BMC Public Health. 2015;15:1099.PubMedPubMedCentralCrossRef
38.
go back to reference Kepha S, Nikolay B, Nuwaha F, Mwandawiro CS, Nankabirwa J, Ndibazza J, et al. Plasmodium falciparum parasitaemia and clinical malaria among school children living in a high transmission setting in western Kenya. Malar J. 2016;15:157.PubMedPubMedCentralCrossRef Kepha S, Nikolay B, Nuwaha F, Mwandawiro CS, Nankabirwa J, Ndibazza J, et al. Plasmodium falciparum parasitaemia and clinical malaria among school children living in a high transmission setting in western Kenya. Malar J. 2016;15:157.PubMedPubMedCentralCrossRef
39.
go back to reference Chacky F, Runge M, Rumisha SF, Machafuko P, Chaki P, Massaga JJ, et al. Nationwide school malaria parasitaemia survey in public primary schools, the United Republic of Tanzania. Malar J. 2018;17:452.PubMedPubMedCentralCrossRef Chacky F, Runge M, Rumisha SF, Machafuko P, Chaki P, Massaga JJ, et al. Nationwide school malaria parasitaemia survey in public primary schools, the United Republic of Tanzania. Malar J. 2018;17:452.PubMedPubMedCentralCrossRef
40.
go back to reference Gitonga CW, Karanja PN, Kihara J, Mwanje M, Juma E, Snow RW, et al. Implementing school malaria surveys in Kenya: towards a national surveillance system. Malar J. 2010;9:306.PubMedPubMedCentralCrossRef Gitonga CW, Karanja PN, Kihara J, Mwanje M, Juma E, Snow RW, et al. Implementing school malaria surveys in Kenya: towards a national surveillance system. Malar J. 2010;9:306.PubMedPubMedCentralCrossRef
41.
go back to reference Worku L, Damtie D, Endris M, Getie S, Aemero M. Asymptomatic malaria and associated risk factors among school children in Sanja town, Northwest Ethiopia. Int Sch Res Not. 2014;2014:302369. Worku L, Damtie D, Endris M, Getie S, Aemero M. Asymptomatic malaria and associated risk factors among school children in Sanja town, Northwest Ethiopia. Int Sch Res Not. 2014;2014:302369.
42.
go back to reference Kern SE, Tiono AB, Makanga M, Gbadoe AD, Premji Z, Gaye O, et al. Community screening and treatment of asymptomatic carriers of Plasmodium falciparum with artemether-lumefantrine to reduce malaria disease burden: a modelling and simulation analysis. Malar J. 2011;10:210.PubMedPubMedCentralCrossRef Kern SE, Tiono AB, Makanga M, Gbadoe AD, Premji Z, Gaye O, et al. Community screening and treatment of asymptomatic carriers of Plasmodium falciparum with artemether-lumefantrine to reduce malaria disease burden: a modelling and simulation analysis. Malar J. 2011;10:210.PubMedPubMedCentralCrossRef
43.
go back to reference Koepfli C, Yan G. Plasmodium gametocytes in field studies: do we measure commitment to transmission or detectability? Trends Parasitol. 2018;34:378–87.PubMedPubMedCentralCrossRef Koepfli C, Yan G. Plasmodium gametocytes in field studies: do we measure commitment to transmission or detectability? Trends Parasitol. 2018;34:378–87.PubMedPubMedCentralCrossRef
44.
go back to reference Al Serouri AW, Grantham-McGregor SM, Greenwood B, Costello A. Impact of asymptomatic malaria parasitaemia on cognitive function and school achievement of schoolchildren in the Yemen Republic. Parasitology. 2000;121(Pt 4):337–45.PubMedCrossRef Al Serouri AW, Grantham-McGregor SM, Greenwood B, Costello A. Impact of asymptomatic malaria parasitaemia on cognitive function and school achievement of schoolchildren in the Yemen Republic. Parasitology. 2000;121(Pt 4):337–45.PubMedCrossRef
46.
go back to reference Beadle C, McElroy PD, Oster CN, Beier JC, Oloo AJ, Onyango FK, et al. Impact of transmission intensity and age on Plasmodium falciparum density and associated fever: implications for malaria vaccine trial design. J Infect Dis. 1995;172:1047–54.PubMedCrossRef Beadle C, McElroy PD, Oster CN, Beier JC, Oloo AJ, Onyango FK, et al. Impact of transmission intensity and age on Plasmodium falciparum density and associated fever: implications for malaria vaccine trial design. J Infect Dis. 1995;172:1047–54.PubMedCrossRef
48.
go back to reference Stevenson JC, Stresman GH, Gitonga CW, Gillig J, Owaga C, Marube E, et al. Reliability of school surveys in estimating geographic variation in malaria transmission in the western Kenyan highlands. PLoS ONE. 2013;8:e77641.PubMedPubMedCentralCrossRef Stevenson JC, Stresman GH, Gitonga CW, Gillig J, Owaga C, Marube E, et al. Reliability of school surveys in estimating geographic variation in malaria transmission in the western Kenyan highlands. PLoS ONE. 2013;8:e77641.PubMedPubMedCentralCrossRef
49.
go back to reference Swana EK, Yav TI, Ngwej LM, Mupemba BN, Suprianto, Mukeng CK, et al. School-based malaria prevalence: informative systematic surveillance measure to assess epidemiological impact of malaria control interventions in the Democratic Republic of the Congo. Malar J. 2018;17:141.PubMedPubMedCentralCrossRef Swana EK, Yav TI, Ngwej LM, Mupemba BN, Suprianto, Mukeng CK, et al. School-based malaria prevalence: informative systematic surveillance measure to assess epidemiological impact of malaria control interventions in the Democratic Republic of the Congo. Malar J. 2018;17:141.PubMedPubMedCentralCrossRef
50.
go back to reference Carneiro I, Roca-Feltrer A, Griffin JT, Smith L, Tanner M, Schellenberg JA, et al. Age-patterns of malaria vary with severity, transmission intensity and seasonality in sub-Saharan Africa: a systematic review and pooled analysis. PLoS ONE. 2010;5:e8988.PubMedPubMedCentralCrossRef Carneiro I, Roca-Feltrer A, Griffin JT, Smith L, Tanner M, Schellenberg JA, et al. Age-patterns of malaria vary with severity, transmission intensity and seasonality in sub-Saharan Africa: a systematic review and pooled analysis. PLoS ONE. 2010;5:e8988.PubMedPubMedCentralCrossRef
51.
go back to reference Teh RN, Sumbele IUN, Meduke DN, Ojong ST, Kimbi HK. Malaria parasitaemia, anaemia and malnutrition in children less than 15 years residing in different altitudes along the slope of Mount Cameroon: prevalence, intensity and risk factors. Malar J. 2018;17:336.PubMedPubMedCentralCrossRef Teh RN, Sumbele IUN, Meduke DN, Ojong ST, Kimbi HK. Malaria parasitaemia, anaemia and malnutrition in children less than 15 years residing in different altitudes along the slope of Mount Cameroon: prevalence, intensity and risk factors. Malar J. 2018;17:336.PubMedPubMedCentralCrossRef
52.
go back to reference Al-Eryani SMA, Mahdy MAK, Al-Mekhlafi AM, Abdul-Ghani R. Access to and use of long-lasting insecticidal nets and factors associated with non-use among communities in malaria-endemic areas of Al Hudaydah governorate in the Tihama region, west of Yemen. Malar J. 2017;16:244.PubMedPubMedCentralCrossRef Al-Eryani SMA, Mahdy MAK, Al-Mekhlafi AM, Abdul-Ghani R. Access to and use of long-lasting insecticidal nets and factors associated with non-use among communities in malaria-endemic areas of Al Hudaydah governorate in the Tihama region, west of Yemen. Malar J. 2017;16:244.PubMedPubMedCentralCrossRef
53.
go back to reference Akiyama T, Pongvongsa T, Phrommala S, Taniguchi T, Inamine Y, Takeuchi R, et al. Asymptomatic malaria, growth status, and anaemia among children in Lao People’s Democratic Republic: a cross-sectional study. Malar J. 2016;15:499.PubMedPubMedCentralCrossRef Akiyama T, Pongvongsa T, Phrommala S, Taniguchi T, Inamine Y, Takeuchi R, et al. Asymptomatic malaria, growth status, and anaemia among children in Lao People’s Democratic Republic: a cross-sectional study. Malar J. 2016;15:499.PubMedPubMedCentralCrossRef
54.
go back to reference Nyakeriga AM, Troye-Blomberg M, Chemtai AK, Marsh K, Williams TN. Malaria and nutritional status in children living on the coast of Kenya. Am J Clin Nutr. 2004;80:1604–10.PubMedCrossRef Nyakeriga AM, Troye-Blomberg M, Chemtai AK, Marsh K, Williams TN. Malaria and nutritional status in children living on the coast of Kenya. Am J Clin Nutr. 2004;80:1604–10.PubMedCrossRef
55.
go back to reference Hess FI, Nukuro E, Judson L, Rodgers J, Nothdurft HD, Rieckmann KH. Anti-malarial drug resistance, malnutrition and socio-economic status. Trop Med Int Health. 1997;2:721–8.PubMedCrossRef Hess FI, Nukuro E, Judson L, Rodgers J, Nothdurft HD, Rieckmann KH. Anti-malarial drug resistance, malnutrition and socio-economic status. Trop Med Int Health. 1997;2:721–8.PubMedCrossRef
56.
go back to reference Bashawri LA, Mandil AA, Bahnassy AA, Ahmed MA. Malaria: hematological aspects. Ann Saudi Med. 2002;22:372–6.PubMedCrossRef Bashawri LA, Mandil AA, Bahnassy AA, Ahmed MA. Malaria: hematological aspects. Ann Saudi Med. 2002;22:372–6.PubMedCrossRef
57.
go back to reference Casals-Pascual C, Kai O, Cheung JO, Williams S, Lowe B, Nyanoti M, et al. Suppression of erythropoiesis in malarial anemia is associated with hemozoin in vitro and in vivo. Blood. 2006;108:2569–77.PubMedCrossRef Casals-Pascual C, Kai O, Cheung JO, Williams S, Lowe B, Nyanoti M, et al. Suppression of erythropoiesis in malarial anemia is associated with hemozoin in vitro and in vivo. Blood. 2006;108:2569–77.PubMedCrossRef
58.
go back to reference Lamikanra AA, Merryweather-Clarke AT, Tipping AJ, Roberts DJ. Distinct mechanisms of inadequate erythropoiesis induced by tumor necrosis factor alpha or malarial pigment. PLoS ONE. 2015;10:e0119836.PubMedPubMedCentralCrossRef Lamikanra AA, Merryweather-Clarke AT, Tipping AJ, Roberts DJ. Distinct mechanisms of inadequate erythropoiesis induced by tumor necrosis factor alpha or malarial pigment. PLoS ONE. 2015;10:e0119836.PubMedPubMedCentralCrossRef
60.
go back to reference McKenzie FE, Prudhomme WA, Magill AJ, Forney JR, Permpanich B, Lucas C, et al. White blood cell counts and malaria. J Infect Dis. 2005;192:323–30.PubMedCrossRef McKenzie FE, Prudhomme WA, Magill AJ, Forney JR, Permpanich B, Lucas C, et al. White blood cell counts and malaria. J Infect Dis. 2005;192:323–30.PubMedCrossRef
61.
go back to reference Moulin F, Lesage F, Legros AH, Maroga C, Moussavou A, Guyon P, et al. Thrombocytopenia and Plasmodium falciparum malaria in children with different exposures. Arch Dis Child. 2003;88:540–1.PubMedPubMedCentralCrossRef Moulin F, Lesage F, Legros AH, Maroga C, Moussavou A, Guyon P, et al. Thrombocytopenia and Plasmodium falciparum malaria in children with different exposures. Arch Dis Child. 2003;88:540–1.PubMedPubMedCentralCrossRef
62.
go back to reference Al-Salahy M, Shnawa B, Abed G, Mandour A, Al-Ezzi A. Parasitaemia and its relation to hematological parameters and liver function among patients malaria in Abs, Hajjah, Northwest Yemen. Interdiscip Perspect Infect Dis. 2016;2016:5954394.PubMedPubMedCentralCrossRef Al-Salahy M, Shnawa B, Abed G, Mandour A, Al-Ezzi A. Parasitaemia and its relation to hematological parameters and liver function among patients malaria in Abs, Hajjah, Northwest Yemen. Interdiscip Perspect Infect Dis. 2016;2016:5954394.PubMedPubMedCentralCrossRef
63.
go back to reference George I, Ewelike-Ezeani C. Haematological changes in children with malaria infection in Nigeria. J Med Med Sci. 2011;2:768–71. George I, Ewelike-Ezeani C. Haematological changes in children with malaria infection in Nigeria. J Med Med Sci. 2011;2:768–71.
64.
go back to reference Mensah-Brown HE, Abugri J, Asante KP, Dwomoh D, Dosoo D, Atuguba F, et al. Assessing the impact of differences in malaria transmission intensity on clinical and haematological indices in children with malaria. Malar J. 2017;16:96.PubMedPubMedCentralCrossRef Mensah-Brown HE, Abugri J, Asante KP, Dwomoh D, Dosoo D, Atuguba F, et al. Assessing the impact of differences in malaria transmission intensity on clinical and haematological indices in children with malaria. Malar J. 2017;16:96.PubMedPubMedCentralCrossRef
Metadata
Title
Uncomplicated falciparum malaria among schoolchildren in Bajil district of Hodeidah governorate, west of Yemen: association with anaemia and underweight
Authors
Talal S. Alwajeeh
Rashad Abdul-Ghani
Amal F. Allam
Hoda F. Farag
Safia S. M. Khalil
Amel Y. Shehab
Mona H. El-Sayad
Raed A. Alharbi
Shaia S. R. Almalki
Ahmed A. Azazy
Publication date
01-12-2020
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2020
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-020-03431-1

Other articles of this Issue 1/2020

Malaria Journal 1/2020 Go to the issue