RSS-Feed abonnieren

DOI: 10.1055/s-0041-1740465
Prevalence of Helicobacter pylori Infection among Anemic School-Age Children in Egypt: A Cross-Sectional Population-Based Study
Funding None.
Abstract
Anemia and Helicobacter pylori infection in school-age children are important public health problems. The association between H. pylori infection and the development of anemia, especially iron deficiency anemia, has been previously studied and until now it is still a matter of argument. This study aimed to determine the prevalence of anemia and H. pylori infection among school-age children and to find the association between H. pylori infection and anemia in school-age children. We conducted this population-based cross-sectional study in six Egyptian primary schools over a 12-month-period, including 1,200 students from all grades who fulfilled the inclusion criteria. The study participants were subjected to the following: medical history, clinical examination, and laboratory investigations included complete blood count and H. pylori antigen in stool, and according to the level of hemoglobin (Hb), we divided the students into two groups; the anemic group with Hb level <11.5 g/dL and nonanemic group with Hb level ≥11.5 g/dL, and the serum ferritin levels were measured only for the anemic group as the best indicator for iron status. The overall prevalence of H. pylori infection was 25%. The overall prevalence of anemia was 13.25%, of which hypochromic microcytic anemia represented 87.4% of the anemic group, and the mean ferritin level in the anemic group was 18.56 ± 9.96 ng/mL. The prevalence of anemia among H. pylori-infected patients (62.3%) was significantly (p < 0.001) higher than in noninfected children (37.7%). In the anemic group, the mean ferritin level in H. pylori-infected children was significantly lower than the mean level in the noninfected children (p <0.001). Furthermore, the anemic group had a significantly higher incidence of H. pylori infection and a lower age (p <0.001) in comparison with the nonanemic group. The dominant type of anemia in H. pylori-infected children was the microcytic hypochromic anemia, with a significantly higher incidence in comparison to other types of anemia (p <0.001). The findings of this study demonstrate a significant association between H. pylori infection and anemia in school-aged children, especially iron deficiency anemia, as the incidence of H. pylori infection was greater in anemic children than in non-anemic children.
Keywords
anemia - iron deficiency anemia - Helicobacter pylori infection - school-age children - ferritin levelAuthors' Contributions
M.A., T.A.A., and E.G.B. designed the study, collected, and interpreted data, and wrote the manuscript. M.A., T.A.A., E.G.B., and D.H. collected, evaluated the patient's interpreted data, and wrote the manuscript. All the authors evaluated the patient's interpreted data and wrote the manuscript. All the authors critically contributed to the discussion and data interpretation, reviewed, and approved the final manuscript.
Publikationsverlauf
Eingereicht: 03. Juli 2021
Angenommen: 12. Oktober 2021
Artikel online veröffentlicht:
13. Dezember 2021
© 2021. The Author(s). This is an open access article published by Thieme under the terms of the Creative Commons Attribution License, permitting unrestricted use, distribution, and reproduction so long as the original work is properly cited. (https://creativecommons.org/licenses/by/4.0/)
Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany
-
References
- 1 Aref MI, Khalifa HO. Prevalence of anemia and associated factors among school-age children in al-haram zone, Giza governorate, Egypt. Azhar Med J 2019; 48 (02) 165-176
- 2 Mattiello V, Schmugge M, Hengartner H, von der Weid N, Renella R. SPOG Pediatric Hematology Working Group. Diagnosis and management of iron deficiency in children with or without anemia: consensus recommendations of the SPOG Pediatric Hematology Working Group. Eur J Pediatr 2020; 179 (04) 527-545
- 3 Tiwari S, Aggarwal S, Kaushik S, Kumar S. Iron deficiency anemia. J Assoc Physicians India 2020; 68 (01) 101-112
- 4 Stevens GA, Finucane MM, De-Regil LM. et al; Nutrition Impact Model Study Group (Anaemia). Global, regional, and national trends in haemoglobin concentration and prevalence of total and severe anaemia in children and pregnant and non-pregnant women for 1995-2011: a systematic analysis of population-representative data. Lancet Glob Health 2013; 1 (01) e16-e25
- 5 Franceschi F, Annalisa T, Teresa DR. et al. Role of Helicobacter pylori infection on nutrition and metabolism. World J Gastroenterol 2014; 20 (36) 12809-12817
- 6 Gheibi Sh, Farrokh-Eslamlou HR, Noroozi M, Pakniyat A. Refractory iron deficiency anemia and Helicobacter pylori infection in pediatrics: a review. Iran J Ped Hematol Oncol 2015; 5 (01) 50-64
- 7 Pasricha SR, Tye-Din J, Muckenthaler MU, Swinkels DW. Iron deficiency. Lancet 2020
- 8 Rayan P, Verghese S, McDonnell PA. Geographical location and age affects the incidence of parasitic infestations in school children. Indian J Pathol Microbiol 2010; 53 (03) 498-502
- 9 DiLorenzo C, Colletti RB, Lehmann HP, Boyle JT, Gerson WT, Hyams JS. Technical report: chronic abdominal pain in children. J Pediatr Gastroenterol Nutr 2005; 40 (03) 249-261
- 10 WHO. The Global Prevalence of Anaemia in 2011. Geneva: World Health Organization; 2015
- 11 Musallam KM, Taher AT. Iron deficiency beyond erythropoiesis: should we be concerned?. Curr Med Res Opin 2018; 34 (01) 81-93
- 12 Polin V, Coriat R, Perkins G. et al. Iron deficiency: from diagnosis to treatment. Dig Liver Dis 2013; 45 (10) 803-809
- 13 Wang YK, Kuo FC, Liu CJ. et al. Diagnosis of Helicobacter pylori infection: current options and developments. World J Gastroenterol 2015; 21 (40) 11221-11235
- 14 Kiran U, Kumar V. Etiology of anemia, iron deficiency among young children and strategies to overcome. Int J Physiol 2020; 8 (02) 171-176
- 15 Kato S, Shimizu T, Toyoda S. et al; Japanese Society for Pediatric Gastroenterology, Hepatology and Nutrition. The updated JSPGHAN guidelines for the management of Helicobacter pylori infection in childhood. Pediatr Int (Roma) 2020; 62 (12) 1315-1331
- 16 Pivina L, Semenova Y, Doşa MD, Dauletyarova M, Bjørklund G. Iron deficiency, cognitive functions, and neurobehavioral disorders in children. J Mol Neurosci 2019; 68 (01) 1-10
- 17 Zamani A, Shariat M, Oloomi Yazdi Z, Bahremand S, Akbari Asbagh P, Dejakam A. Relationship between Helicobacter pylori infection and serum ferritin level in primary school children in Tehran-Iran. Acta Med Iran 2011; 49 (05) 314-318
- 18 Naous A, Al-Tannir M, Naja Z, Ziade F, El-Rajab M. Fecoprevalence and determinants of Helicobacter pylori infection among asymptomatic children in Lebanon. J Med Liban 2007; 55 (03) 138-144
- 19 Ali B, Chloë W, Mehmet A. et al. Presence of gastric Helicobacter species in children suffering from gastric disorders in Southern Turkey. Helicobacter 2018; 23 (05) e12511
- 20 Łaszewicz W, Iwańczak F, Iwańczak B. Task Force of the Polish Society of Gastroenterology, Task Force of the Polish Society of Gastroenterology. Seroprevalence of Helicobacter pylori infection in Polish children and adults depending on socioeconomic status and living conditions. Adv Med Sci 2014; 59 (01) 147-150
- 21 Galal YS, Ghobrial CM, Labib JR, Abou-Zekri ME. Helicobacter pylori among symptomatic Egyptian children: prevalence, risk factors, and effect on growth. J Egypt Public Health Assoc 2019; 94 (01) 17
- 22 Deeb MM, Bahbah WA, Abou-Elela DH, Hessen MM. Seroprevalence of Helicobacter pylori infection among school children in Al Qulubia governorate. Menoufia Med J 2018; 31 (03) 963
- 23 Abdulqawi K, El-Mahalaway AM, Abdelhameed A, Abdelwahab AA. Correlation of serum antibody titres with invasive methods for rapid detection of Helicobacter pylori infections in symptomatic children. Int J Exp Pathol 2012; 93 (04) 295-304
- 24 Mohammad MA, Hussein L, Coward A, Jackson SJ. Prevalence of Helicobacter pylori infection among Egyptian children: impact of social background and effect on growth. Public Health Nutr 2008; 11 (03) 230-236
- 25 Hasosah M, Satti M, Shehzad A. et al. Prevalence and risk factors of Helicobacter pylori infection in Saudi children: a three-year prospective controlled study. Helicobacter 2015; 20 (01) 56-63
- 26 Iwańczak BM, Buchner AM, Iwańczak F. Clinical differences of Helicobacter pylori infection in children. Adv Clin Exp Med 2017; 26 (07) 1131-1136
- 27 Awuku YA, Simpong DL, Alhassan IK, Tuoyire DA, Afaa T, Adu P. Prevalence of helicobacter pylori infection among children living in a rural setting in Sub-Saharan Africa. BMC Public Health 2017; 17 (01) 360
- 28 Zhou Y, Ye Z, Huang J, Huang Y, Yan W, Zhang Y. High prevalence and low spontaneous eradication rate of Helicobacter pylori infection among schoolchildren aged 7-12 years. Acta Paediatr 2018; 107 (09) 1624-1628
- 29 da Silva Roque IJR, Machado II RS, Rodrigues III D, Rech IV P, Kawakami VE. Prevalence of Helicobacter pylori infection in an indigenous community in São Paulo and associated factors: cross-sectional study. JUNTOS PARA TRANSFORMAR. 2017; 135 (02) 140-145
- 30 Duque X, Vilchis J, Mera R. et al. Natural history of Helicobacter pylori infection in Mexican schoolchildren: incidence and spontaneous clearance. J Pediatr Gastroenterol Nutr 2012; 55 (02) 209-216
- 31 Andriastuti M, Ilmana G, Nawangwulan SA, Kosasih KA. Prevalence of anemia and iron profile among children and adolescent with low socio-economic status. Int J Pediatr Adolesc Med 2020; 7 (02) 88-92
- 32 Getaneh Z, Enawgaw B, Engidaye G. et al. Prevalence of anemia and associated factors among school children in Gondar town public primary schools, northwest Ethiopia: a school-based cross-sectional study. PLoS One 2017; 12 (12) e0190151
- 33 Pektaş E, Aral YZ, Yenisey Ç. The prevalence of anemia and nutritional anemia in primary school children in the City of Aydın. Meandros Med J 2015; 16: 97-107
- 34 Wu J, Hu Y, Li M. et al. Prevalence of anemia in Chinese children and adolescents and its associated factors. Int J Environ Res Public Health 2019; 16 (08) 1416
- 35 Mansour RE, Abu Zeid A, Bahaa El Din RM. Cross sectional study to assess Malnutrition and associated risk factors among primary school children in Kafr Sakr, Sharqia, Egypt. Zagazig Univ Med J 2020; 26 (05) 725-734
- 36 Salama RA, Labib MR. The prevalence of anemia among informal primary school children: a community based study in Rural Upper Egypt. Epidemiol Biostat Public Health 2016;13(01):
- 37 Suzan M, Salah M, Aliaa M, Hasnaa A. Iron deficiency and iron deficiency anemia in adolescent girls in Rural Upper Egypt. Int Blood Res Rev 2016; 5 (04) 1-6
- 38 Gonete KA, Tariku A, Wami SD, Derso T. Prevalence and associated factors of anemia among adolescent girls attending high schools in Dembia District, Northwest Ethiopia, 2017. Arch Public Health 2018; 76: 79
- 39 Ngui R, Ravindran S, Ong DB. et al. Intestinal parasitic infections and the level of immunosuppression in HIV seropositive individuals with diarrhoea in Kilimanjaro, Tanzania: a cross-sectional study. PLoS Negl Trop Dis 2013; 18 (03) 122-139
- 40 Oliveira D, Ferreira FS, Atouguia J, Fortes F, Guerra A, Centeno-Lima S. Infection by intestinal parasites, stunting and anemia in school-aged children from Southern Angola. PLoS One 2015; 10 (09) e0137327
- 41 Benoist BD, McLean E, Egll I, Cogswell M. Worldwide Prevalence of Anaemia 1993–2005: WHO Global Database on Anaemia. Geneva: WHO Global Database on Anaemia; 2008
- 42 Baker RD, Greer FR. Committee on Nutrition American Academy of Pediatrics. Diagnosis and prevention of iron deficiency and iron-deficiency anemia in infants and young children (0-3 years of age). Pediatrics 2010; 126 (05) 1040-1050
- 43 Elhakim N, Laillou A, El Nakeeb A, Yacoub R, Shehata M. Fortifying baladi bread in Egypt: reaching more than 50 million people through the subsidy program. Food Nutr Bull 2012; 33 (4, Suppl): S260-S271
- 44 Hurrell R, Ranum P, de Pee S. et al. Revised recommendations for iron fortification of wheat flour and an evaluation of the expected impact of current national wheat flour fortification programs. Food Nutr Bull 2010; 31 (1, Suppl): S7-S21
- 45 World Health Organization. Serum Ferritin Concentrations for the Assessment of Iron Status and Iron Deficiency in Populations. Geneva: World Health Organization; 2011
- 46 Mohamed E, Ahmed O, Youssef A. Iron deficiency and anemia in rural school children in a coastal area of Morocco. Pak J Nutr 2008; 7: 400-403
- 47 Abdel-Rasoul GM, El Bahnasy RE, El Shazly HM, Gabr HM, Abdel-Aaty NB. Epidemiology of iron-deficiency anemia among primary school children (6–11 years), Menoufia governorate, Egypt. Menoufia Med J 2015; 28 (03) 663
- 48 Achouri I, Aboussaleh Y, Sbaibi R, Ahami A, El Hioui M. Prevalence of iron deficiency anaemia among school children in Kenitra. Pak J Biol Sci 2015; 18 (04) 191-195
- 49 Le Nguyen BK, Le Thi H, Nguyen Do VA. et al. Double burden of undernutrition and overnutrition in Vietnam in 2011: results of the SEANUTS study in 0.5–11-year-old children. Br J Nutr 2013; 110: S45-S56
- 50 Li L, Luo R, Medina A, Rozelle S. The prevalence of anemia in central and eastern China: evidence from the China health and nutrition survey. Southeast Asian J Trop Med Public Health 2015; 46 (02) 306-321
- 51 Egbi G, Steiner-Asiedu M, Kwesi FS. et al. Anaemia among school children older than five years in the Volta Region of Ghana. Pan Afr Med J 2014; 17 (Suppl. 01) 10
- 52 Maiti D, Acharya S, Basu S. Recognizing missed opportunities to diagnose and treat iron deficiency anemia: a study based on prevalence of anemia among children in a teaching hospital. J Family Med Prim Care 2019; 8 (03) 899-903
- 53 Sahana KS, Ghaliyah K, Anitha P, Prakash S. A study of anemia in hospitalised infants at a tertiary care hospital. Natl J Community Med 2015; 6: 22-27
- 54 Manohar Reddy CV, Sai Geeta C. Evaluation of anemia in hospitalised infants at a tertiary care hospital. Int J Med Res Prof. 2017; 3: 208-210
- 55 Mourad-Baars PE, Verspaget HW, Mertens BJ, Mearin ML. Low prevalence of Helicobacter pylori infection in young children in the Netherlands. Eur J Gastroenterol Hepatol 2007; 19 (03) 213-216
- 56 Hassan MA, Kasem IA, Ali AS. Correlation between Helicobacter pylori infection and iron deficiency anemia in school-aged children. Egypt J Hosp Med 2020; 81 (02) 1489-1498
- 57 Baggett HC, Parkinson AJ, Muth PT, Gold BD, Gessner BD. Endemic iron deficiency associated with Helicobacter pylori infection among school-aged children in Alaska. Pediatrics 2006; 117 (03) e396-e404
- 58 Hudak L, Jaraisy A, Haj S, Muhsen K. An updated systematic review and meta-analysis on the association between Helicobacter pylori infection and iron deficiency anemia. Helicobacter 2017; 22 (01) 12330-12333
- 59 Zahmatkeshan M, Karimi M, Geramizadeh B, Eslaminasab S, Esmailnejad A, Safarpour AR. Association between Helicobacter pylori infection and iron deficiency anemia in school-aged Iranian children. Indian Pediatr 2019; 56 (05) 387-389
- 60 Sarker SA, Mahmud H, Davidsson L. et al. Causal relationship of Helicobacter pylori with iron-deficiency anemia or failure of iron supplementation in children. Gastroenterology 2008; 135 (05) 1534-1542
- 61 Vendt N, Kool P, Teesalu K, Lillemäe K, Maaroos HI, Oona M. Iron deficiency and Helicobacter pylori infection in children. Acta Paediatr 2011; 100 (09) 1239-1243
- 62 Santos IS, Boccio J, Davidsson L. et al. Helicobacter pylori is not associated with anaemia in Latin America: results from Argentina, Brazil, Bolivia, Cuba, Mexico and Venezuela. Public Health Nutr 2009; 12 (10) 1862-1870
- 63 El-Kady HM, Al-Kahiry W, Abdelsalam HS. Burden of Helicobacter pylori infections and associated risk factors among cases of iron deficiency anaemia in Egypt. Microbiol Res J Int 2020; 80-91
- 64 Osman HA, Hasan H, Suppian R. et al. Evaluation of the Atlas Helicobacter pylori stool antigen test for diagnosis of infection in adult patients. Asian Pac J Cancer Prev 2014; 15 (13) 5245-5247
- 65 Shatla MM. Treatment of Helicobacter Pylori associated iron deficiency anemia: does iron supplementation make difference. Eur J Preventive Med 2016; 4 (02) 50-55
- 66 Abou-Taleb A, Allam A, Elsamman M. Association between Helicobacter pylori infection and iron deficiency anemia among school-age children in Sohag University hospital, Upper Egypt. Open J Blood Dis 2017; 7: 36-46
- 67 Queiroz DMM, Harris PR, Sanderson IR. et al. Iron status and Helicobacter pylori infection in symptomatic children: an international multi-centered study. PLoS One 2013; 8 (07) e68833
- 68 Muhsen K, Barak M, Henig C, Alpert G, Ornoy A, Cohen D. Is the association between Helicobacter pylori infection and anemia age dependent?. Helicobacter 2010; 15 (05) 467-472
- 69 Afifi RA, Ali DK, Shaheen IA. A localized case-control study of extra-gastric manifestations of Helicobacter pylori infection in children. Indian J Pediatr 2011; 78 (04) 418-422
- 70 Soylu ÖB, Ozturk Y. Helicobacter pylori infection: effect on malnutrition and growth failure in dyspeptic children. Eur J Pediatr 2008; 167 (05) 557-562
- 71 Sh M, Al-Ani MH. Coexistence of iron deficiency anemia with Helicobacter pylori infection among children aged 6 to 12 years in Erbil city. Med J Tikrit Univers 2019; 25 (02) 121-130
- 72 Haghi-Ashtiani MT, Monajemzadeh M, Motamed F. et al. Anemia in children with and without Helicobacter pylori infection. Arch Med Res 2008; 39 (05) 536-540
- 73 Hoseinzadeh M, Khosravi A, Sayemiri K, Rasoli MH, Mohaveri A. The antibody titers to Helicobacter pylori in 7 - 12 year old iron deficiency anemic children, in Ilam. J Res Med Sci 2010; 15 (06) 324-330
- 74 Chiu NC, Lin CY, Chi H. et al. Helicobacter pylori infection is not associated with failure to thrive: a case control study. Ther Clin Risk Manag 2017; 13: 273-278
- 75 Gravina AG, Zagari RM, De Musis C, Romano L, Loguercio C, Romano M. Helicobacter pylori and extragastric diseases: a review. World J Gastroenterol 2018; 24 (29) 3204-3221
- 76 Zhang F, Pu K, Wu Z. et al. Prevalence and associated risk factors of Helicobacter pylori infection in the Wuwei cohort of north-western China. Trop Med Int Health 2021; 26 (03) 290-300