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Prevalence of Helicobacter pylori infection among asymptomatic children in southeastern Brazil: a cross-sectional study

ABSTRACT

BACKGROUND:

The prevalence of Helico bacter pylori (H. pylori) infection is decreasing worldwide, but is still high in developing countries. We previously observed an H. pylori infection rate of 52% among children and adolescents with chronic non-ulcer dyspepsia.

OBJECTIVE:

To investigate the prevalence of H. pylori infection among asymptomatic children living in a single region and to evaluate the risk factors for this infection.

DESIGN AND SETTING:

Cross-sectional study in which 161 children aged 5-13 years (mean age 7.8 years), at a public school in Botucatu, state of São Paulo, southeastern Brazil, were assessed.

METHOD:

The children's H. pylori infection status was determined through the urea breath test and the risk factors for acquisition of the infection were determined based on a sociodemographic questionnaire.

RESULTS:

The overall prevalence of H. pylori infection was 20.5%: 18.7% among females and 22.2% among males. The results from the sociodemographic survey did not differ between children with and without H. pylori infection. 30.9% of the children had previous records of upper gastrointestinal symptoms, which consisted of H. pylori infection in only 26.5% of these cases. Family histories of gastritis and peptic ulcer disease were found in relation to 50% and 32.3% of the children with H. pylori infection respectively.

CONCLUSION:

The prevalence of H. pylori infection among asymptomatic children in southeastern Brazil is lower than that recorded among symptomatic children in the same region and similar to the prevalence of H. pylori infection observed in developed countries.

KEYWORDS (MeSH terms):
Helicobacter pylori ; Child; Prevalence

AUTHORS’ KEYWORDS:
Children; Prevalence of H. pylori infection; Urea breath test

INTRODUCTION

The prevalence of Helicobacter pylori (H. pylori) infection is decreasing worldwide, but is still high in developing countries.11 Hooi JKY, Lai WY, Ng WK, et al. Global Prevalence of Helicobacter pylori Infection: Systematic Review and Meta-Analysis. Gastroenterology. 2017;153(2):420-9. PMID: 28456631; https://doi.org/10.1053/j.gastro.2017.04.022.
https://doi.org/10.1053/j.gastro.2017.04...
33 Leja M, Grinberga-Derica I, Bilgilier C, Steininger C. Review: Epidemiology of Helicobacter pylori infection. Helicobacter. 2019; 24 Suppl.1:e12635. PMID: 31486242; https://doi.org/10.1111/hel.12635.
https://doi.org/10.1111/hel.12635...
In Brazil, epidemiological studies have shown that the rates of H. pylori infection vary widely across different regions; for example, the highest rates have been reported in northern and northeastern regions (up to 90%), in contrast to lower prevalence in the southeastern region (less than 36%).44 Basílio ILD, Catão MFC, Carvalho JDS, et al. Risk factors of Helicobacter pylori infection in an urban community in Northeast Brazil and the relationship between the infection and gastric diseases. Rev Soc Bras Med Trop. 2018;51(2):183-9. PMID: 29768551; https://doi.org/10.1590/0037-8682-0412-2016.
https://doi.org/10.1590/0037-8682-0412-2...
,55 Toscano EP, Madeira FF, Dutra-Rulli MP, et al. Epidemiological and Clinical-Pathological Aspects of Helicobacter pylori Infection in Brazilian Children and Adults. Gastroent Res Pract. 2018;2018:8454125. Erratum in: Gastroenterol Res Pract. 2019;2019:5632935. PMID: 30254670; https://doi.org/10.1155/2018/8454125.
https://doi.org/10.1155/2018/8454125...

We previously observed an H. pylori infection rate of 52% among children and adolescents with chronic non-ulcer dyspepsia in southeastern Brazil.66 Carvalho MA, Machado NC, Ortolan EV, Rodrigues MA. Upper gastrointestinal histopathological findings in children and adolescents with nonulcer dyspepsia with Helicobacter pylori infection. J Pediatr Gastroenterol Nutr. 2012;55(5):523-9. PMID: 22684348; https://doi.org/10.1097/MPG.0b013e3182618136.
https://doi.org/10.1097/MPG.0b013e318261...
,77 Correa Silva RG, Machado NC, Carvalho MA, Rodrigues MA. Helicobacter pylori infection is high in paediatric nonulcer dyspepsia but not associated with specific gastrointestinal symptoms. Acta Paediatr. 2016;105(5):228-31. PMID: 26821362; https://doi.org/10.1111/apa.13347.
https://doi.org/10.1111/apa.13347...
This prompted us to investigate the prevalence of H. pylori infection among asymptomatic children living in a single community.

OBJECTIVE

To investigate the prevalence of H. pylori infection among asymptomatic children using the urea breath test. Sociodemographic data and previous records of gastrointestinal symptoms were assessed to investigate risk factors for this infection.

METHODS

This cross-sectional prospective study was conducted among children at a public school in the city of Botucatu city, São Paulo, southeastern Brazil, from October 2019 to February 2020. They were aged between 5 and 13 years and were living in the same geographical area as those of a previous study on symptomatic children66 Carvalho MA, Machado NC, Ortolan EV, Rodrigues MA. Upper gastrointestinal histopathological findings in children and adolescents with nonulcer dyspepsia with Helicobacter pylori infection. J Pediatr Gastroenterol Nutr. 2012;55(5):523-9. PMID: 22684348; https://doi.org/10.1097/MPG.0b013e3182618136.
https://doi.org/10.1097/MPG.0b013e318261...
,77 Correa Silva RG, Machado NC, Carvalho MA, Rodrigues MA. Helicobacter pylori infection is high in paediatric nonulcer dyspepsia but not associated with specific gastrointestinal symptoms. Acta Paediatr. 2016;105(5):228-31. PMID: 26821362; https://doi.org/10.1111/apa.13347.
https://doi.org/10.1111/apa.13347...
The exclusion criteria were occurrences of therapy with antibiotics or antisecretory drugs within the preceding four weeks. A sociodemographic questionnaire was administered to the parents. Questions asking about previous records of upper gastrointestinal symptoms in the last year, like nausea, vomiting, epigastric pain, post-prandial fullness and nocturnal pain, were included in the questionnaire.

H. pylori infection was evaluated through the urea breath test. This was applied to the children in the school, in the morning, before the recess, when the children had had a fasting time of approximately two hours. A baseline breath sample was collected, and then the children received a solution containing 1313 Mezmale L, Coelho LG, Bordin D, Leja M. Review: Epidemiology of Helicobacter pylori. Helicobacter. 2020;25 Suppl.1:e12734. PMID: 32918344; https://doi.org/10.1111/hel.12734.
https://doi.org/10.1111/hel.12734...
C-labeled urea (1313 Mezmale L, Coelho LG, Bordin D, Leja M. Review: Epidemiology of Helicobacter pylori. Helicobacter. 2020;25 Suppl.1:e12734. PMID: 32918344; https://doi.org/10.1111/hel.12734.
https://doi.org/10.1111/hel.12734...
C-urea): 50 mg for children ≤ 30 kg and 75 mg for children > 30 kg, dissolved in 80 ml of water. After 15 minutes, the final breath sample was collected. The samples were analyzed using an Automated Breath 1313 Mezmale L, Coelho LG, Bordin D, Leja M. Review: Epidemiology of Helicobacter pylori. Helicobacter. 2020;25 Suppl.1:e12734. PMID: 32918344; https://doi.org/10.1111/hel.12734.
https://doi.org/10.1111/hel.12734...
C Analyzer Isotope Ratio Mass Spectrometer (ABCA-IRMS) (SerCon-Cheshire, United Kingdom) at the Stable Isotope Center, at the Universidade Estadual de São Paulo (UNESP). The cutoff value for H. pylori infection to be considered present was 4‰ for the difference between the values obtained from the final and baseline breath samples

The data were analyzed using the R statistical software, version 4.0.3 (public domain). The significance level was taken to be P < 0.05.

This study was approved by the local Research Ethics Committee (CAAE 25856119.7.0000.5411) on December 4, 2019.

RESULTS

The study sample consisted of 161 asymptomatic children (80 males and 81 females). The age range was 5-13 years, and the mean age was 7.8 ± 1.7 years. H. pylori infection was identified in 33/161 children (20.5%), i.e. 15/80 females (18.7%) and 18/81 males (22.2%). Half of the children were male and 45.3% were between 5 and 7 years of age (Table 1). The results regarding sociodemographic, economic and sanitary condition data did not differ between children with and without H. pylori infection (Table 1).

Table 1
Sociodemographic characteristics of the study sample in relation to presence or absence of H. pylori (Hp) infection

30.4% of the children had previous records of upper gastrointestinal symptoms, which consisted of H. pylori infection in only 26.5% of these cases. The frequency of prior gastrointestinal symptoms was 39.4% among children with H. pylori infection and 28.1% in the non-infected group (P > 0.05).

A family history of gastritis was reported in relation to 50% of the children with H. pylori infection and 48.2% of the non-infected children (P > 0.05). Presence of a peptic ulcer was reported in relation to 32.3% of the children with H. pylori infection and 20.2% in the non-infected group (P > 0.05).

DISCUSSION

In this study, we found that the H. pylori infection rate was 20.5% among 161 asymptomatic school children living in a single community. This was significantly lower than the H. pylori infection rate of 52% previously recorded among symptomatic children living in the same region, despite the differences in age and diagnostic methods between the groups of symptomatic and asymptomatic children.66 Carvalho MA, Machado NC, Ortolan EV, Rodrigues MA. Upper gastrointestinal histopathological findings in children and adolescents with nonulcer dyspepsia with Helicobacter pylori infection. J Pediatr Gastroenterol Nutr. 2012;55(5):523-9. PMID: 22684348; https://doi.org/10.1097/MPG.0b013e3182618136.
https://doi.org/10.1097/MPG.0b013e318261...
,77 Correa Silva RG, Machado NC, Carvalho MA, Rodrigues MA. Helicobacter pylori infection is high in paediatric nonulcer dyspepsia but not associated with specific gastrointestinal symptoms. Acta Paediatr. 2016;105(5):228-31. PMID: 26821362; https://doi.org/10.1111/apa.13347.
https://doi.org/10.1111/apa.13347...

A recent systematic review and meta-analysis on the prevalence of H. pylori infection in Latin America and the Caribbean reported an H. pylori infection rate of 48.3% among children and adolescents.88 Curado MP, de Oliveira MM, de Araújo Fagundes M. Prevalence of Helicobacter pylori infection in Latin America and the Caribbean populations: A systematic review and meta-analysis. Cancer Epidemiol. 2019;60:141-8. PMID: 31009922; https://doi.org/10.1016/j.canep.2019.04.003.
https://doi.org/10.1016/j.canep.2019.04....
Similar rates have been registered in this age group in Brazilian studies conducted in São Paulo.99 Kawakami E, Machado RS, Reber M, Patrício F. 13C-Urea Breath Test With Infrared Spectroscopy for Diagnosing Helicobacter pylori Infection in Children and Adolescents. J Pediatr Gastroenterol Nutr. 2002;35(1):39-43. PMID: 12142808; https://doi.org/10.1097/00005176-200207000-00010.
https://doi.org/10.1097/00005176-2002070...
,1010 Miranda AC, Machado RS, Silva EM, Kawakami E. Seroprevalence of Helicobacter pylori infection among children of low socioeconomic level in São Paulo. Sao Paulo Med J. 2010;128(4):187-91. PMID: 21120427; https://doi.org/10.1590/S1516-31802010000400002.
https://doi.org/10.1590/S1516-3180201000...
Prevalence rates higher than 40% have been reported among asymptomatic children up to six years of age in the northeastern region.1111 Rodrigues MN, Queiroz DM, Rodrigues RT, et al. Prevalence of Helicobacter pylori infection in Fortaleza, Northeastern Brazil. Rev Saude Publica. 2005;39(5):847-9. PMID: 16254664; https://doi.org/10.1590/S0034-89102005000500022.
https://doi.org/10.1590/S0034-8910200500...
,1212 Braga AB, Fialho AM, Rodrigues MN, et al. Helicobacter pylori Colonization Among Children up to 6 Years: Results of a Community-based Study from Northeastern Brazil. J Trop Pediatr. 2007;53(6):393-7. PMID: 17578847; https://doi.org/10.1093/tropej/fmm051.
https://doi.org/10.1093/tropej/fmm051...
In these studies, low socioeconomic status and poor hygiene conditions were the main risk factors for H. pylori infection.

The 20.5% rate of H. pylori infection identified in the present study is similar to the values recorded in developed countries, such as 22.1% in Denmark, 24.6% in Australia and 25.4% in the United States.11 Hooi JKY, Lai WY, Ng WK, et al. Global Prevalence of Helicobacter pylori Infection: Systematic Review and Meta-Analysis. Gastroenterology. 2017;153(2):420-9. PMID: 28456631; https://doi.org/10.1053/j.gastro.2017.04.022.
https://doi.org/10.1053/j.gastro.2017.04...
,22 Zamani M, Ebrahimtabar F, Zamani V, et al. Systematic review with meta-analysis: the worldwide prevalence of Helicobacter pylori infection. Aliment Pharmacol Ther. 2018;47(7): 868-76. PMID: 29430669; https://doi.org/10.1111/apt.14561.
https://doi.org/10.1111/apt.14561...
,1313 Mezmale L, Coelho LG, Bordin D, Leja M. Review: Epidemiology of Helicobacter pylori. Helicobacter. 2020;25 Suppl.1:e12734. PMID: 32918344; https://doi.org/10.1111/hel.12734.
https://doi.org/10.1111/hel.12734...
Our result is lower than the 32.6% worldwide prevalence of H. pylori infection among children, reported by Zamani et al. According to these authors, the rate of H. pylori infection can be considered to be an additional benchmark for the socioeconomic and health status of a region or a country.22 Zamani M, Ebrahimtabar F, Zamani V, et al. Systematic review with meta-analysis: the worldwide prevalence of Helicobacter pylori infection. Aliment Pharmacol Ther. 2018;47(7): 868-76. PMID: 29430669; https://doi.org/10.1111/apt.14561.
https://doi.org/10.1111/apt.14561...

In the present study, only 14.3% of all the children and 12.1% of the children with H. pylori infection had parents whose educational level was low. Thus, the educational background of most of our study population was good. Moreover, we did not find differences in family income, number of people in the household, number of children or occurrence of bed-sharing, between children with and without H. pylori infection. The similarity between the two groups of children may be explained by particular conditions of the city of Botucatu, which is located in the most developed region of Brazil and has one of the highest human development indexes (HDIs) of the country (0.8), similar to the HDI reference values of developed countries.1414 IBGE. Índice de desenvolvimento humano, 2010. Available from: https://cidades.ibge.gov.br/brasil/sp/botucatu/pesquisa/37/30255. Accessed in 2022 (Mar 9).
https://cidades.ibge.gov.br/brasil/sp/bo...
,1515 UNDP (United Nations Development Programme). Human Development Report 2020. The Next Frontier. Human Development and the Anthropocene. Available from: http://report.hdr.undp.org. Accessed in 2022 (Mar 9).
http://report.hdr.undp.org...
These findings document the adequate socioeconomic and hygiene conditions of the study population and highlight the relevance of socioeconomic status and family education in relation to protection against H. pylori infection.22 Zamani M, Ebrahimtabar F, Zamani V, et al. Systematic review with meta-analysis: the worldwide prevalence of Helicobacter pylori infection. Aliment Pharmacol Ther. 2018;47(7): 868-76. PMID: 29430669; https://doi.org/10.1111/apt.14561.
https://doi.org/10.1111/apt.14561...
,1616 Bastos J, Peleteiro B, Barros R, et al. Sociodemographic determinants of prevalence and incidence of Helicobacter pylori infection in Portuguese adults. Helicobacter. 2013;18(6):413-22. PMID: 23725608; https://doi.org/10.1111/hel.12061.
https://doi.org/10.1111/hel.12061...

In this study, previous reports of gastrointestinal symptoms were observed in relation to 30.4% of the children, which consisted of H. pylori infection in only 26.5% of these cases. Thus, the majority of the children with previous records of gastrointestinal symptoms did not have H. pylori infection. These findings are in agreement with previous studies, which did not find any relationship between gastrointestinal symptoms and H. pylori infection.77 Correa Silva RG, Machado NC, Carvalho MA, Rodrigues MA. Helicobacter pylori infection is high in paediatric nonulcer dyspepsia but not associated with specific gastrointestinal symptoms. Acta Paediatr. 2016;105(5):228-31. PMID: 26821362; https://doi.org/10.1111/apa.13347.
https://doi.org/10.1111/apa.13347...
,1717 Spee LA, Madderom MB, Pijpers M, van Leeuwen Y, Berger MY. Association between Helicobacter pylori and gastrointestinal symptoms in children. Pediatrics. 2010;125(3):e651-69. PMID: 20156901; https://doi.org/10.1542/peds.2010-0941.
https://doi.org/10.1542/peds.2010-0941...

A family history of gastritis was reported in half of the children with H. pylori infection, and peptic ulcer disease in 32.3% of the children with H. pylori. These findings highlight the importance of transmission from one human to another, as the main route for acquisition and transmission of H. pylori infection.1818 Zaman C, Osaki T, Furuta Y, et al. Enhanced infectivity of strains of Helicobacter pylori isolated from children compared with parental strains. J Med Microbiol. 2019;68(4):633-41. PMID: 30806617; https://doi.org/10.1099/jmm.0.000918.
https://doi.org/10.1099/jmm.0.000918...

CONCLUSION

The prevalence of H. pylori infection among asymptomatic children in southeastern Brazil is lower than the prevalence recorded among symptomatic children living in the same region and similar to the rates of H. pylori infection observed in developed countries.

  • Faculdade de Medicina de Botucatu (FMB), Universidade Estadual Paulista (UNESP), Botucatu (SP), Brazil
  • Events or congresses: This study was presented by Ana Beatriz Marques Carlos to obtain the master's degree in science in the Postgraduate Program of the Faculdade de Medicina de Botucatu da Universidade Estadual Paulista (UNESP), 2021. This study was presented at the 34th Workshop of the European Helicobacter and Microbiota Study Group, 2021
  • Sources of funding: Ana Beatriz Marques Carlos received a fellowship from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) – no. 134212/2019-3

REFERENCES

  • 1
    Hooi JKY, Lai WY, Ng WK, et al. Global Prevalence of Helicobacter pylori Infection: Systematic Review and Meta-Analysis. Gastroenterology. 2017;153(2):420-9. PMID: 28456631; https://doi.org/10.1053/j.gastro.2017.04.022
    » https://doi.org/10.1053/j.gastro.2017.04.022
  • 2
    Zamani M, Ebrahimtabar F, Zamani V, et al. Systematic review with meta-analysis: the worldwide prevalence of Helicobacter pylori infection. Aliment Pharmacol Ther. 2018;47(7): 868-76. PMID: 29430669; https://doi.org/10.1111/apt.14561
    » https://doi.org/10.1111/apt.14561
  • 3
    Leja M, Grinberga-Derica I, Bilgilier C, Steininger C. Review: Epidemiology of Helicobacter pylori infection. Helicobacter. 2019; 24 Suppl.1:e12635. PMID: 31486242; https://doi.org/10.1111/hel.12635
    » https://doi.org/10.1111/hel.12635
  • 4
    Basílio ILD, Catão MFC, Carvalho JDS, et al. Risk factors of Helicobacter pylori infection in an urban community in Northeast Brazil and the relationship between the infection and gastric diseases. Rev Soc Bras Med Trop. 2018;51(2):183-9. PMID: 29768551; https://doi.org/10.1590/0037-8682-0412-2016
    » https://doi.org/10.1590/0037-8682-0412-2016
  • 5
    Toscano EP, Madeira FF, Dutra-Rulli MP, et al. Epidemiological and Clinical-Pathological Aspects of Helicobacter pylori Infection in Brazilian Children and Adults. Gastroent Res Pract. 2018;2018:8454125. Erratum in: Gastroenterol Res Pract. 2019;2019:5632935. PMID: 30254670; https://doi.org/10.1155/2018/8454125
    » https://doi.org/10.1155/2018/8454125
  • 6
    Carvalho MA, Machado NC, Ortolan EV, Rodrigues MA. Upper gastrointestinal histopathological findings in children and adolescents with nonulcer dyspepsia with Helicobacter pylori infection. J Pediatr Gastroenterol Nutr. 2012;55(5):523-9. PMID: 22684348; https://doi.org/10.1097/MPG.0b013e3182618136
    » https://doi.org/10.1097/MPG.0b013e3182618136
  • 7
    Correa Silva RG, Machado NC, Carvalho MA, Rodrigues MA. Helicobacter pylori infection is high in paediatric nonulcer dyspepsia but not associated with specific gastrointestinal symptoms. Acta Paediatr. 2016;105(5):228-31. PMID: 26821362; https://doi.org/10.1111/apa.13347
    » https://doi.org/10.1111/apa.13347
  • 8
    Curado MP, de Oliveira MM, de Araújo Fagundes M. Prevalence of Helicobacter pylori infection in Latin America and the Caribbean populations: A systematic review and meta-analysis. Cancer Epidemiol. 2019;60:141-8. PMID: 31009922; https://doi.org/10.1016/j.canep.2019.04.003
    » https://doi.org/10.1016/j.canep.2019.04.003
  • 9
    Kawakami E, Machado RS, Reber M, Patrício F. 13C-Urea Breath Test With Infrared Spectroscopy for Diagnosing Helicobacter pylori Infection in Children and Adolescents. J Pediatr Gastroenterol Nutr. 2002;35(1):39-43. PMID: 12142808; https://doi.org/10.1097/00005176-200207000-00010
    » https://doi.org/10.1097/00005176-200207000-00010
  • 10
    Miranda AC, Machado RS, Silva EM, Kawakami E. Seroprevalence of Helicobacter pylori infection among children of low socioeconomic level in São Paulo. Sao Paulo Med J. 2010;128(4):187-91. PMID: 21120427; https://doi.org/10.1590/S1516-31802010000400002
    » https://doi.org/10.1590/S1516-31802010000400002
  • 11
    Rodrigues MN, Queiroz DM, Rodrigues RT, et al. Prevalence of Helicobacter pylori infection in Fortaleza, Northeastern Brazil. Rev Saude Publica. 2005;39(5):847-9. PMID: 16254664; https://doi.org/10.1590/S0034-89102005000500022
    » https://doi.org/10.1590/S0034-89102005000500022
  • 12
    Braga AB, Fialho AM, Rodrigues MN, et al. Helicobacter pylori Colonization Among Children up to 6 Years: Results of a Community-based Study from Northeastern Brazil. J Trop Pediatr. 2007;53(6):393-7. PMID: 17578847; https://doi.org/10.1093/tropej/fmm051
    » https://doi.org/10.1093/tropej/fmm051
  • 13
    Mezmale L, Coelho LG, Bordin D, Leja M. Review: Epidemiology of Helicobacter pylori. Helicobacter. 2020;25 Suppl.1:e12734. PMID: 32918344; https://doi.org/10.1111/hel.12734
    » https://doi.org/10.1111/hel.12734
  • 14
    IBGE. Índice de desenvolvimento humano, 2010. Available from: https://cidades.ibge.gov.br/brasil/sp/botucatu/pesquisa/37/30255 Accessed in 2022 (Mar 9).
    » https://cidades.ibge.gov.br/brasil/sp/botucatu/pesquisa/37/30255
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    UNDP (United Nations Development Programme). Human Development Report 2020. The Next Frontier. Human Development and the Anthropocene. Available from: http://report.hdr.undp.org Accessed in 2022 (Mar 9).
    » http://report.hdr.undp.org
  • 16
    Bastos J, Peleteiro B, Barros R, et al. Sociodemographic determinants of prevalence and incidence of Helicobacter pylori infection in Portuguese adults. Helicobacter. 2013;18(6):413-22. PMID: 23725608; https://doi.org/10.1111/hel.12061
    » https://doi.org/10.1111/hel.12061
  • 17
    Spee LA, Madderom MB, Pijpers M, van Leeuwen Y, Berger MY. Association between Helicobacter pylori and gastrointestinal symptoms in children. Pediatrics. 2010;125(3):e651-69. PMID: 20156901; https://doi.org/10.1542/peds.2010-0941
    » https://doi.org/10.1542/peds.2010-0941
  • 18
    Zaman C, Osaki T, Furuta Y, et al. Enhanced infectivity of strains of Helicobacter pylori isolated from children compared with parental strains. J Med Microbiol. 2019;68(4):633-41. PMID: 30806617; https://doi.org/10.1099/jmm.0.000918
    » https://doi.org/10.1099/jmm.0.000918

Publication Dates

  • Publication in this collection
    29 Aug 2022
  • Date of issue
    Sep-Oct 2022

History

  • Received
    25 Aug 2021
  • Reviewed
    27 Jan 2022
  • Accepted
    03 Mar 2022
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