Introduction
Hemoglobin (Hb) is the protein contained in red blood cells that is responsible for delivery of oxygen to the tissues, and when the hemoglobin level is low, the patient has anemia1. Anemia—a condition in which the red blood cell count is decreased, impairing the body's ability to meet the oxygen needs of tissues—is a public health problem [
1,
2] where women are some of the most affected; in 2019, the World Health Organization reported around 30% of women 15-49 years of age worldwide had anemia [
3]. The WHO-defined hemoglobin (Hb) cut-offs, specific to age, sex, and pregnancy status, are most widely used to diagnose anemia, with the threshold being <120 g/L for non-pregnant and <110 g/L for pregnant women of 15–49 years of age [
4]. Anemia also has a high association within low-income countries, notably in Africa, where, in 2019, an estimated 106 million women were affected by anemia [
5].
Among pregnant women, maternal anemia can cause symptoms such as headaches and fatigue along with more severe cases, hemoglobin levels <6g/dL, causing a possibility of more dangerous effects secondary to decreased tissue oxygenation [
6]. Pregnant and lactating women are especially susceptible to decline in hemoglobin [
7], thus, it is important to analyze all risk factors that may have an impact on this. Beyond this, low maternal hemoglobin levels during pregnancy can also cause lasting effects such as fetal deaths [
6,
8] and an increased risk of limited cognitive development for infants after birth [
9]. There are many risk factors that have been associated with the prevalence of maternal anemia and maternal hemoglobin decline such as education [
10], income [
11], and diet [
12], however, research on the association between maternal hemoglobin and environmental factors is in its infancy.
Only a handful of studies have shown the relationship between environmental pollutants and maternal hemoglobin or anemia. One study showed that exposure levels to PM
10, SO
2, and CO for one and two years were significantly associated with decreased hemoglobin concentrations (all p < 0.05) [
13]. In this study, exposure levels to PM10, for instance, had an OR of 1.039 [95% CI : 1.001–1.079], highlighting the link between air pollutants and decreased hemoglobin [
13]. Additionally, carbon monoxide (CO) exposure during a two year period was closely related to anemia OR = 1.046 [95% CI: 1.004–1.091] [
13]. On the other hand, a study involving particulate matter
2.5 (PM
2.5) found no association with anemia prevalence during the one year exposure period [
13], yet other studies have found a negative association with hemoglobin levels which may contribute to maternal hemoglobin decline [
14,
15]. Fine toxic pollutants such as PM
2.5, primarily from vehicle emissions and industrial activities, are more likely to travel into and deposit on the surface of the deeper parts of the lung, which can induce tissue damage16. Furthermore, a previous study found that PM
2.5 particles can lead to a biological response due to motor emissions that can penetrate deep into the lungs, enter the bloodstream, and induce systemic inflammation [
17,
18]. Addressing these environmental factors and their impact on hemoglobin is crucial for improving maternal health outcomes and developing effective public health interventions.
This study aims to address regional differences in Africa and the association between PM2.5 and maternal reproductive hemoglobin. Our hypothesis is that PM2.5 will have varying effects on reproductive maternal hemoglobin levels based on different regions of Africa. The findings from this study can serve as a foundation for developing future policies aimed at improving maternal hemoglobin levels.
Methods
This is a population-based study for Africa from 2000-2019. Data for the annual mean prevalence hemoglobin (in grams per litre) of reproductive women between the ages of 15-49 years for 43 African nations. This outcome data was obtained from the World Health Organization (WHO). Aside from our primary outcome, exposure data for country-specific annual mean particulate matter
2.5 (PM
2.5) from 2000-2019 was obtained from World Bank:
https://www.stateofglobalair.org/data/#/air/plot.
We included covariate data on country-specific annual mean air pollution (specifically household air pollutants as percentage), cereal yield (in tonnes per hectare), gross domestic product (GDP), prevalence of reproductive women with anemia (moderate levels), low body-mass index (<18.5 kg/m2) of whole population, and annual trend.
We modelled the region-specific associations between the annual prevalence of reproductive women hemoglobin levels and annual PM2.5 using generalized linear model, specifically negative binomial regression using autocorrelation order 1 (i.e. AR1). This is because the outcome’s variance was much greater than its mean, leading to overdispersion of data. Model coefficients were exponentiated to be interpreted as rate ratios (RR) for each 10 μg/m3 rise in pollution levels. 95% confidence intervals were evaluated at P<0.05 using Student’s two-sided t-tests. Microsoft Excel (V.2021) and RStudio (V.4.1.1) were used for computation, analyses and figure composition.
Results
Over the twenty years of our study from 43 countries, within four regions of Africa, the average prevalence of hemoglobin among reproductive maternal is 120.8 g/L.
On a geographic perspective, the prevalence of reproductive women hemoglobin is lowest over Western Africa and highest over Southern Africa (
Figure 1A). Similarly annual mean PM
2.5 are highest in Western Africa throughout the 2000 to 2019 period (
Figure 1B).
Our models suggest that for each annual 10 μg/m3 rise in PM2.5 the RR for reproductive maternal hemoglobin found was no association for Western, Eastern, and Southern Africa, yet only Central Africa had the significant results [0.999 (P=0.035)]. The main findings from this suggests that countries of Central African regions had a negative association between prevalence of maternal reproductive women and PM2.5 from 2000-2019.
Discussion
The results of our study found that only Central Africa is statistically significant in the effect of PM
2.5 on maternal hemoglobin levels, whereas other regions were insignificant, hence suggesting regional differences in Africa. In a past study that analyzed the pregnancy conditions of Chinese women [20-45 years, n=7932] delivering between 2015-2018, it was found that an increase in PM
2.5 concentration for all pregnant women (mean: 69.56 μg/m³, standard deviation: 15.24 μg/m³) by one interquartile range increase (19.37 μg/m³) was associated with a decrease in hemoglobin levels in multiparous women (mean age: 32.77±3.75 years, n=2609), but not for primiparous women (mean age: 28.78±3.25 years, n=5323)
14. Exposure to PM
2.5 was associated with decreased hemoglobin in the third trimester of multiparous women, but not detrimental to the degree of being associated with anemia [
14].
The link between PM
2.5 exposure and decreased maternal hemoglobin levels is believed to be driven by inflammation as a biological response [
14]. PM
2.5 particles can deeply penetrate the lungs through motor emissions, enter the bloodstream, and trigger systemic inflammation, leading to oxidative stress and vascular dysfunction [
17,
18]. Pregnant and lactating women are especially vulnerable to hemoglobin decline, which has severe consequences for maternal health, and infant development, including impacts on cognitive function [
7]. Additionally, a previous study also shows that decreased hemoglobin levels are linked to cardiovascular disease in pregnant women, which further worsens the effect of PM
2.5 [
19,
20]. These factors underscore the importance of addressing PM
2.5 in strategies aimed at improving hemoglobin levels, particularly among maternal women in regions with poor air quality, such as Africa.
Several epidemiologic studies have confirmed that PM
2.5 harms pregnant women and leads to more severe impacts on hemoglobin levels [
13]. It is
confirmed based on availability of data that a mother with low hemoglobin was at risk of delivering a newborn with stunted growth [
21]
. Additionally, in Africa, a lack of dietary and malnutrition variety during pregnancy doubles the odds of developing maternal anemia, which in turn leads to low child birth weight and therefore low hemoglobin levels [
22].
The association between PM
2.5 and maternal hemoglobin levels observed in this study is limited by confounding factors, such as exposure to other air pollutants like PM1, PM10, and NO2, which have also been linked to decreased hemoglobin levels [
12]. Since these pollutants are formed from emissions such as those from motor vehicles, it is difficult to isolate PM
2.5 from other pollutants that may also affect hemoglobin levels [
16]. Moreover, socioeconomic status is another confounding factor that can influence both exposure to air pollution and access to healthcare, which further affects the relationship between PM
2.5 and hemoglobin levels [
2]3. The lack of nutrition education and iron rich food has been associated with decreased hemoglobin levels, which we were not able to control for [
24]. This study does not fully reflect the true prevalence or severity of low maternal hemoglobin, and interventions may be less effective due to African areas with limited healthcare access [
25].
Nevertheless, this study adds value to the literature that focuses on a specific region - Africa - discussing the association between PM
2.5 and maternal hemoglobin [
11]. This study highlights the regional variance and indicates that PM
2.5 is negatively associated with hemoglobin levels in maternal women. The study further helps to confirm our hypothesis that PM
2.5 increases the likelihood of maternal anemia. This is a concern since rising levels of PM
2.5 are exacerbated with further climate changes leading to clinical implications or reduced hemoglobin levels [
26].
Figure 1.
A) Annual country-specific reproductive maternal women (15-49 years) hemoglobin prevalence; B) annual mean PM2.5 from 2000-2019.
Figure 1.
A) Annual country-specific reproductive maternal women (15-49 years) hemoglobin prevalence; B) annual mean PM2.5 from 2000-2019.
Conclusion
Therefore, we found regional effects of PM2.5 on maternal hemoglobin. In future research, the scope can be expanded to other low-income regions to determine whether this hypothesis holds true globally. Additionally, the study can be used to collaborate with specific African regions’ governments to create considerable and lasting regulations. These regulations may decrease the prevalence of anemia among maternal women, reducing the chances of maternal health complications that arise in response to exposure from PM2.5.
Author Contributions
Dr. Muhammed Saeed: Original Idea, Paper Review, Data Collection, Data Review, Writing, Final Review. Harris Majid: Original Idea, Paper Review, Data Collection, Writing, Final Review. Mohammad R. Saeed: Data Collection, Writing of draft, Data Review and administration. Harris Khokar: Data Collection; Writing of draft. Adeena Zaidi: Data Collection; Writing of draft and administration. Arav Lohe: Data Collection Writing of draft. Olivea Ali: Data Collection; Draft Writing and administration. Mashael Sayed: Data Collection; Writing of draft and administration.
References
- Billett, H.H. Hemoglobin and Hematocrit. In: Walker HK, Hall WD, Hurst JW, eds. Clinical Methods: The History, Physical, and Laboratory Examinations. 3rd ed. Boston: Butterworths; 1990.
- Owais, A.; Merritt, C.; Lee, C.; Bhutta, Z.A. Anemia among Women of Reproductive Age: An Overview of Global Burden, Trends, Determinants, and Drivers of Progress in Low- and Middle-Income Countries. Nutrients 2021, 13, 2745. [Google Scholar] [CrossRef] [PubMed]
- World Health Organization. Anaemia [Internet]. www.who.int. World Health Organisation; 2024. Available from: https://www.who.int/health-topics/anaemia#tab=tab_1.
- WHO. Haemoglobin Concentrations for the Diagnosis of Anaemia and Assessment of Severity. World Health Organization; Geneva, Switzerland: 2011.
- World Health Organization. Anaemia [Internet]. www.who.int. 2023. Available from: https://www.who.int/news-room/fact-sheets/detail/anaemia.
- Sifakis, S.; Pharmakide, G. Anemia in Pregnancy. Annals of the New York Academy of Sciences. 2006, 900, 125–36. [Google Scholar] [CrossRef] [PubMed]
- Basrowi, R.W.; Zulfiqqar, A.; Sitorus, N.L. Anemia in Breastfeeding Women and Its Impact on Offspring’s Health in Indonesia: A Narrative Review. Nutrients 2024, 16, 1285. [Google Scholar] [CrossRef] [PubMed]
- Young, M.F.; Oaks, B.M.; Tandon, S.; Martorell, R.; Dewey, K.G.; Wendt, A.S. Maternal hemoglobin concentrations across pregnancy and maternal and child health: a systematic review and meta-analysis. Annals of the New York Academy of Sciences. 2019, 1450, 47–68. [Google Scholar] [CrossRef] [PubMed]
- Mireku, M.O.; Davidson, L.L.; Koura, G.K.; Ouédraogo, S.; Boivin, M.J.; Xiong, X.; Accrombessi, M.M.K.; Massougbodji, A.; Cot, M.; Bodeau-Livinec, F. Prenatal Hemoglobin Levels and Early Cognitive and Motor Functions of One-Year-Old Children. Pediatrics 2015, 136, e76–e83. [Google Scholar] [CrossRef] [PubMed]
- Stephen, G.; Mgongo, M.; Hashim, T.H.; Katanga, J.; Stray-Pedersen, B.; Msuya, S.E. Anaemia in Pregnancy: Prevalence, Risk Factors, and Adverse Perinatal Outcomes in Northern Tanzania. Anemia 2018, 2018, 1–9. [Google Scholar] [CrossRef] [PubMed]
- Idris, I.B.; Isa, Z.M.; Rahman, R.A.; Mahdy, Z.A. The Prevalence and Risk Factors of Iron Deficiency Anemia Among Pregnant Women in Malaysia: A Systematic Review. Front. Nutr. 2022, 9, 847693. [Google Scholar] [CrossRef]
- Gibore, N.S.; Ngowi, A.F.; Munyogwa, M.J.; Ali, M.M. Dietary Habits Associated with Anemia in Pregnant Women Attending Antenatal Care Services. Curr. Dev. Nutr. 2020, 5, nzaa178. [Google Scholar] [CrossRef] [PubMed]
- Hwang, J.; Kim, H.-J. Association of ambient air pollution with hemoglobin levels and anemia in the general population of Korean adults. BMC Public Heal. 2024, 24, 1–11. [Google Scholar] [CrossRef] [PubMed]
- Xie, G.; Yue, J.; Yang, W.; Yang, L.; Xu, M.; Sun, L.; Zhang, B.; Guo, L.; Chung, M.C. Effects of PM2.5 and its constituents on hemoglobin during the third trimester in pregnant women. Environ. Sci. Pollut. Res. 2022, 29, 35193–35203. [Google Scholar] [CrossRef] [PubMed]
- He, C.; Xie, L.; Gu, L.; Yan, H.; Feng, S.; Zeng, C.; et al. Anemia is associated with long-term exposure to PM2.5 and its components: a large population-based study in Southwest China. Therapeutic Advances in Hematology. 2023 Jan 1 [cited 2024 Sep 8];14.
- Inhalable Particulate Matter and Health (PM2.5 and PM10) | California Air Resources Board [Internet]. ww2.arb.ca.gov. Available from: https://ww2.arb.ca.gov/resources/inhalable-particulate-matter-and-health#:~:text=5%3F-.
- Miller, M.R. Oxidative stress and the cardiovascular effects of air pollution. Free. Radic. Biol. Med. 2020, 151, 69–87. [Google Scholar] [CrossRef]
- Thangavel, P.; Park, D.; Lee, Y.-C. Recent Insights into Particulate Matter (PM2.5)-Mediated Toxicity in Humans: An Overview. Int. J. Environ. Res. Public Heal. 2022, 19, 7511. [Google Scholar] [CrossRef] [PubMed]
- Lanser, L.; Fuchs, D.; Scharnagl, H.; Grammer, T.; Kleber, M.E.; März, W.; Weiss, G.; Kurz, K. Anemia of Chronic Disease in Patients With Cardiovascular Disease. Front. Cardiovasc. Med. 2021, 8. [Google Scholar] [CrossRef] [PubMed]
- Basith, S.; Manavalan, B.; Shin, T.H.; Park, C.B.; Lee, W.-S.; Kim, J.; Lee, G. The Impact of Fine Particulate Matter 2.5 on the Cardiovascular System: A Review of the Invisible Killer. Nanomaterials 2022, 12, 2656. [Google Scholar] [CrossRef] [PubMed]
- Nadhiroh, S.R.; Micheala, F.; Tung, S.E.H.; Kustiawan, T.C. Association between maternal anemia and stunting in infants and children aged 0–60 months: A systematic literature review. Nutrition [Internet]. 2023, 115, 112094, Available from: https://www.sciencedirect.com/science/article/pii/S0899900723001235#:~:. [Google Scholar] [CrossRef] [PubMed]
- Seid, A.; Fufa, D.D.; Weldeyohannes, M.; Tadesse, Z.; Fenta, S.L.; Bitew, Z.W.; Dessie, G. Inadequate dietary diversity during pregnancy increases the risk of maternal anemia and low birth weight in Africa: A systematic review and meta-analysis. Food Sci. Nutr. 2023, 11, 3706–3717. [Google Scholar] [CrossRef] [PubMed]
- Alaba, O.A.; Chiwire, P.; Siya, A.; Saliu, O.A.; Nhakaniso, K.; Nzeribe, E.; Okova, D.; Lukwa, A.T. Socio-Economic Inequalities in the Double Burden of Malnutrition among under-Five Children: Evidence from 10 Selected Sub-Saharan African Countries. Int. J. Environ. Res. Public Heal. 2023, 20, 5489. [Google Scholar] [CrossRef] [PubMed]
- Sunuwar, D.R.; Sangroula, R.K.; Shakya, N.S.; Yadav, R.; Chaudhary, N.K.; Pradhan, P.M.S. Effect of nutrition education on hemoglobin level in pregnant women: A quasi-experimental study. PLOS ONE 2019, 14, e0213982. [Google Scholar] [CrossRef] [PubMed]
- Musa, S.M.; Haruna, U.A.; Manirambona, E.; Eshun, G.; Ahmad, D.M.; Dada, D.A.; Gololo, A.A.; Musa, S.S.; Abdulkadir, A.K.; Iii, D.E.L.-P. Paucity of Health Data in Africa: An Obstacle to Digital Health Implementation and Evidence-Based Practice. Public Heal. Rev. 2023, 44, 1605821. [Google Scholar] [CrossRef] [PubMed]
- Shi, L.; Liu, P.; Zanobetti, A.; Schwartz, J. Climate Penalty. Environmental Epidemiology. 2019, 3, 365. [Google Scholar]
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