Anemia is the most common disruption of physiological functioning experienced by women worldwide throughout their lifespan. It is a grave affliction in many underprivileged nations. Anemia is a significant public health issue that negatively impacts the likelihood of a successful pregnancy. The coordinates are (1,2). The hematologic system adjusts to facilitate fetal hematopoiesis, ensuring sufficient blood flow to the enlarged uterus and its contents. This protects both the mother and fetus from the negative effects of impaired venous return in both supine and upright positions, as well as preventing bleeding during delivery (3,4,5).  During pregnancy, there are several significant hematological changes that occur. These include physiological anemia, an increase in neutrophils, a slight decrease in platelet count, an increase in procoagulant factors, and a decrease in fibrinolysis. Anaemia during pregnancy is characterized by a hemoglobin (Hb) level below 110 g/L in the first and last trimester, and below 105 g/L in the second trimester (6,7).  Women who have anaemia and/or iron deficiency may suffer from weariness, decreased energy levels, and impaired cognitive function. Severe anemia is linked to premature birth, low birth weight, and a fetus that is smaller than expected for its gestational age. Research has shown a connection between anaemia, iron deficiency, and negative effects on mental health and cognitive performance during the postpartum period (8,9). Furthermore, it is the prevailing nutritional insufficiency observed in industrialized countries; approximately half of the cases are attributed to inadequate iron consumption (10,11). Pregnancy is correlated with heightened iron requirements, thereby elevating the susceptibility to iron deficiency anemia. Approximately 52% of pregnant women in underdeveloped countries are impacted. Reduced iron reserves in their newborn infant will elevate the likelihood of eventual iron deficiency anemia. The risk is also increased by prematurity and early cessation of nursing due to diminished iron reserves (12,13,14). Gastritis caused by H. pylori infection. Moreover, H. pylori infection leads to a decline in the ability to secrete bicarbonate. As a consequence, individuals infected with H. pylori experience an elevation in the amount of acid in their duodenum. The presence of H. pylori infection is examined in gastrointestinal disorders that occur during pregnancy. This bacterium appears to be linked to hyperemesis gravidarum, an intense form of nausea and vomiting during pregnancy. In recent years, the connection between H. pylori and many extra gastric illnesses has become prominent in literature (15,16). The primary focus of research has been on the association between H. pylori infection and pregnancy-related disorders such as iron deficiency anemia (IDA), thrombocytopenia, miscarriage, fetal abnormalities, fetal growth restriction, and preeclampsia. These disorders are linked to H. pylori through various mechanisms. These include the reduction of micronutrients (such as iron, folate, and Vitamin B12) in maternal anemia and fetal neural tube defects, the interaction between anti-H. pylori antibodies and antigens found in placental tissue and endothelial cells (leading to conditions like preeclampsia, fetal growth restriction, and miscarriage), the release of pro-inflammatory cytokines causing oxidative stress in gastrointestinal disorders, and the development of preeclampsia (17,18). There is a widespread belief that the hormonal and immunological changes that happen during pregnancy might trigger the activation of dormant H. pylori, which is usually acquired before pregnancy. This activation can have a detrimental effect on the health of both the mother and the fetus. It was observed that pregnant women who were infected with H. pylori had a lower average hemoglobin (Hb) level at the start of pregnancy and experienced a higher reduction in the average Hb level by the end of pregnancy. In addition, it has been advised to eliminate H. pylori infection in patients with unexplained iron deficiency anemia (IDA) (19,20). The study conducted to evaluate the relation of H. pylori infection in iron deficiency anemia in pregnant women.

This case-control study was carried out in Kirkuk city from the period started from 1^st of December 2023 to the end of March 2024. The study included 100 pregnant women (50 women with iron deficiency anemia, and 50 healthy pregnant without anemia) ranged in age from (14-41 years), those women who attended Gynecological and Pediatric Hospital. 

Inclusion criteria

• Pregnant women aged 14-41 years old with and without iron deficiency

Exclusion criteria

• Hereditary anemia

• Inflammation

• Liver and kidney disease

• Malignancy

• Autoimmune diseases.

Ethical approval

Before participating in the project, each patient received detailed information about the study and signed an informed consent form.  

Methods

Hematological and Biochemical Assessments

Blood samples were collected from all participants after fasting overnight. Hematological parameters, including hemoglobin levels, red blood cell (RBC) count, mean corpuscular volume (MCV), mean corpuscular hemoglobin (MCH), and mean corpuscular hemoglobin concentration (MCHC), were measured using an automated hematology analyzer. Serum ferritin, serum iron, and total iron-binding capacity (TIBC) were quantified to assess iron status. These parameters were compared between the anemic and non-anemic groups, as well as between H. pylori positive and negative participants, using independent samples t-tests.

H. pylori Seropositivity

Serological testing for Anti-Helicobacter pylori antibodies (IgG) was performed using an enzyme-linked immunosorbent assay (ELISA) on serum samples. The presence of H. pylori infection was determined based on seropositivity for H. pylori antibodies. Participants were classified into H. pylori positive or negative groups based on these results, and comparisons were made between the two groups regarding their hematological and biochemical parameters.

Nutritional Status Assessment

The nutritional status of the participants was assessed by measuring serum Vitamin B12 and folate levels using competitive chemiluminescence assays. Body mass index (BMI) was calculated based on height and weight measurements obtained during the study visit. These nutritional indicators were compared between H. pylori positive and negative women within the IDA group.

Statistical Analysis

Statistical analysis was conducted using SPSS software (version 25.0). Continuous variables were presented as mean ± standard deviation (SD) and compared using independent samples t-tests. Categorical variables were expressed as frequencies and percentages, with comparisons made using chi-square tests. P-values less than 0.05 were considered indicative of statistical significance for all analyses conducted. The data were further stratified based on H. pylori seropositivity to explore its impact on the severity and parameters of anemia in pregnant women with IDA.

The demographic data presented in the table show no statistically significant differences between the pregnant women with anemia and the non-anemic control group across various parameters, including age, gravidity, parity, abortion, and gestational age. The mean age of the women in both groups is comparable, with a slightly higher average age in the anemic group (30.5±7.1 years) compared to the control group (28.3±6.4 years), with a P-value of 0.258. Similarly, gravidity and parity levels are slightly higher in the anemic group, but these differences are not statistically significant, as indicated by P-values of 0.373 and 0.529, respectively. The abortion rate is also slightly higher in the anemic group (0.3±0.7) compared to the control group (0.2±0.5), but this difference is not significant (P=0.214). Lastly, the gestational age is similar between the two groups, with a P-value of 0.402.

Table 1: Comparison of demographic data of the study and control groups

The data presented highlight significant differences in key hematological parameters between IDA pregnant women and the control group. Serum ferritin levels, a critical indicator of iron storage, are significantly lower in the IDA group (12.47±2.11 μg/l) compared to the control group (20.32±3.89 μg/l), with a P-value of 0.002, indicating depleted iron stores in the anemic women. Similarly, serum iron levels are markedly reduced in the IDA group (9.87±2.92 μg/dl) relative to the controls (14.75±3.67 μg/dl), with a P-value of 0.003, further confirming the presence of iron deficiency. Conversely, the serum total iron-binding capacity (TIBC), which reflects the body's demand for iron, is significantly higher in the IDA group (102.5±28.4 μg/l) compared to the control group (68.7±15.9 μg/l), with a P-value of 0.001, suggesting an increased physiological effort to capture available iron. Additionally, the mean hemoglobin levels, a direct measure of anemia, are significantly lower in the IDA group (8.9±0.7 gm/dl) versus the controls (11.8±0.9 gm/dl), with a P-value of 0.001, confirming the presence of anemia.

Table 2: Hematological parameters between IDA pregnant women and the control group

The data on Anti-Helicobacter pylori seropositivity reveal a notable difference between pregnant women with anemia and their non-anemic counterparts. Among the anemic pregnant women, 32% (16 out of 50) tested positive for H. pylori, whereas none of the non-anemic control group showed seropositivity for this infection. Conversely, 68% (34 out of 50) of the anemic women tested negative for H. pylori, compared to 100% (50 out of 50) in the control group.

Table 3:  Anti-Helicobacter pylori seropositivity between pregnant women with and without anemia.

The comparison of hematological parameters between H. pylori positive and negative pregnant women with anemia reveals significant differences in iron status indicators. H. pylori positive women have higher serum ferritin levels (15.32±2.45 μg/l) compared to those who are H. pylori negative (10.87±2.97 μg/l), with a P-value of 0.015, suggesting better iron storage in the H. pylori positive group. Similarly, serum iron levels are significantly higher in the H. pylori positive group (12.45±3.22 μg/dl) than in the negative group (9.23±2.81 μg/dl), with a P-value of 0.022, indicating better iron availability. 

However, the serum total iron-binding capacity (TIBC) does not show a significant difference between the two groups (89.6±25.4 μg/l for H. pylori positive vs. 95.1±30.2 μg/l for H. pylori negative), with a P-value of 0.341, which suggests that the body's capacity to bind iron is not significantly affected by H. pylori status. Additionally, the mean hemoglobin levels are higher in H. pylori positive women (9.8±0.9 gm/dl) compared to the negative group (8.7±0.7 gm/dl), with a P-value of 0.048, indicating less severe anemia in those with H. pylori infection.

Table 4: Comparison of hematological parameters between H. pylori positive and negative pregnant women

The comparison of nutritional status indicators between H. pylori positive and negative pregnant women with iron deficiency anemia (IDA) reveals significant differences in key micronutrient levels. Specifically, serum Vitamin B12 levels are significantly lower in the H. pylori positive group (240.5±30.2 pg/ml) compared to the H. pylori negative group (280.7±35.8 pg/ml), with a P-value of 0.038. Similarly, serum folate levels are also significantly reduced in the H. pylori positive group (4.2±1.3 ng/ml) versus the negative group (5.6±1.7 ng/ml), with a P-value of 0.041. These findings suggest that H. pylori infection may impair the absorption or metabolism of these essential nutrients, potentially exacerbating nutritional deficiencies in pregnant women with IDA.

Table 5: Comparison of Nutritional Status Indicators between H. pylori Positive and Negative Pregnant Women with IDA

The hematological parameters presented show significant differences between H. pylori positive and negative pregnant women with iron deficiency anemia (IDA). The Red Blood Cell (RBC) count is notably lower in the H. pylori positive group (3.8±0.5 ×10⁶/μL) compared to the H. pylori negative group (4.2±0.6 ×10⁶/μL), with a P-value of 0.032, indicating a more pronounced reduction in red blood cells among those infected with H. pylori. Additionally, the Mean Corpuscular Volume (MCV) is significantly lower in the H. pylori positive group (76.2±5.4 fl) compared to the negative group (82.4±6.1 fl), with a P-value of 0.029, suggesting that H. pylori infection is associated with smaller red blood cells, characteristic of microcytic anemia. The Mean Corpuscular Hemoglobin (MCH) and Mean Corpuscular Hemoglobin Concentration (MCHC) are also significantly lower in the H. pylori positive group, with MCH values of 24.1±2.7 pg versus 27.8±3.2 pg (P=0.041) and MCHC values of 31.9±1.5 g/dl versus 33.4±1.8 g/dl (P=0.034), respectively.

Table 6: CBC parameters in Relation to H. pylori Seropositivity in Pregnant Women with IDA

The analysis of anemia severity between H. pylori positive and negative pregnant women with iron deficiency anemia (IDA) reveals varying distributions across different levels of anemia, although the differences are not statistically significant. In the H. pylori positive group, 31.3% (5 out of 16) of the women have mild anemia (Hb 10-10.9 g/dl), compared to 44.1% (15 out of 34) in the H. pylori negative group, with a P-value of 0.314, indicating no significant difference in the prevalence of mild anemia between the two groups. For moderate anemia (Hb 7-9.9 g/dl), 50.0% (8 out of 16) of H. pylori positive women are affected, compared to 47.1% (16 out of 34) in the negative group, with a P-value of 0.876, suggesting a similar distribution of moderate anemia regardless of H. pylori status. However, severe anemia (Hb <7 g/dl) appears to be more prevalent in the H. pylori positive group, with 18.7% (3 out of 16) affected compared to 8.8% (3 out of 34) in the negative group, though this difference is also not statistically significant (P=0.287).

Table 7: Severity of Anemia in Relation to H. pylori Seropositivity in Pregnant Women with IDA

The findings of this study offer valuable information about the hematological and nutritional condition of pregnant women suffering from iron deficiency anemia (IDA), specifically in relation to Helicobacter pylori (H. pylori) infection. There were no significant statistical variations in demographic data between anemic and non-anemic pregnant women in terms of age, number of pregnancies, number of live births, rates of miscarriage, and length of pregnancy. This indicates that the groups were evenly balanced, enabling a more concentrated examination of the hematological and nutritional disparities that can be attributed to IDA and H. pylori infection. In terms of blood analysis, the study confirmed the anticipated results that pregnant women with iron deficiency anemia (IDA) had notably lower levels of serum ferritin and serum iron compared to pregnant women without anemia. The P-values for these differences were 0.002 and 0.003, respectively. The results align with previous research, which has established that low levels of serum ferritin and iron are reliable markers of depleted iron reserves and decreased production of hemoglobin in individuals with iron deficiency anemia (21,22,23). The increased total iron-binding capacity (TIBC) found in the IDA group provides additional evidence for a compensation mechanism in which the body enhances its ability to bind iron in response to decreased iron availability (24,25,26). The study's findings offer valuable insights into the correlation between iron deficiency anemia (IDA) and Helicobacter pylori (H. pylori) infection in pregnant women. Our study confirmed earlier research findings that pregnant women with iron deficiency anemia (IDA) had notably lower levels of serum ferritin and serum iron compared to pregnant women without anemia. These findings are consistent with the research conducted by Al Mutawa et al (12) and Darvishi et al (13). The study's IDA group exhibited a raised blood total iron-binding capacity (TIBC), which reinforces the presence of iron shortage. Higher TIBC levels suggest that the body is making a greater effort to bind and utilize the iron that is available. Our findings corroborated the results of earlier studies conducted among pregnant women in Addis Ababa (16), Iran (12), India (24), and Turkey (23). Furthermore, the research conducted in Butajira among dyspeptic nonpregnant patients also discovered a notable correlation between anemia and HP infection (24,25,26). However, the study conducted in Butajira among children and Sudan among pregnant women failed to establish a correlation between anemia and HP infection (27,28,29). The likely explanation for these findings may be attributed to several possible mechanisms through which HP influences iron metabolism. These mechanisms include reduced absorption of iron due to chronic gastritis, decreased concentration of ascorbic acid in gastric juice, increased production of hepcidin associated with HP gastritis, uptake of iron by HP for its growth, and decreased availability of iron due to sequestration of iron in lactoferrin in the gastric mucosa and competition between the bacterium and the host for dietary iron supply (22). Another often proposed explanation for this association could be attributed to the development of HPassociated chronic gastritis, which results in achlorhydria and reduced ascorbic acid production. This, in turn, leads to decreased absorption of iron in the intestines (18). In addition, a connection exists between anemia and Helicobacter pylori infection, which involves hidden blood loss from erosive gastritis and the organism's absorption and usage of iron (12). The prevalence of prenatal anemia is well acknowledged as a significant public health issue globally, especially in poorer nations (9). Due to the expansion of blood volume and the increased demand for iron by both the baby and the mother, the amount of hemoglobin undergoes significant changes throughout pregnancy (24). The study observed that the occurrence of anemia in this particular group of people was determined to be 27.5% (95% CI = 22.0, 33.5). According to the WHO definition, the level of public health concern for this condition is considerable. This means that the prevalence of anemia falls within the range of 20-39.9% (29, 30). The frequency of anemia in this study is similar to other studies conducted in different regions of Ethiopia, such as 27.6% in Butajira General Hospital in southern Ethiopia, 27.9% in Harerge in southeast Ethiopia, and 29.1% in Uganda (6, 10, 31). The outcome was marginally greater than the prior local findings from Aymba HC, situated in northwest Ethiopia, which reported a rate of 25.2% (7). Nevertheless, this report indicated lower percentages compared to other studies. For instance, Boditi in southern Ethiopia reported 61.6%, Gode in southeast Ethiopia reported 56.8%, Arba Minch in southern Ethiopia reported 32.8%, and Iran reported 31% (2, 8, 9, 12). The variations in magnitude may be attributed to disparities in the inclusion and exclusion criteria, as well as the dietary habits of the subjects throughout the studies. The aforementioned study involved pregnant women who had preexisting chronic conditions and experienced bleeding. However, in our investigation, we specifically excluded such individuals. A systematic review and meta-analysis study discovered that the global prevalence of Helicobacter pylori (HP) infection in the general population varies from 25% to 94% (21). A 2017 systematic review and meta-analysis found that 46% of pregnant women worldwide were infected with HP, according to a study (23).The prevalence of Helicobacter pylori (HP) infection in this study sample was determined to be 54.7% (95% confidence interval: 47.9–61.4). The incidence of HP infection is in line with studies conducted in Jinka and Butajira among the general population, which indicated a prevalence of HP infection of 50.7% and 52.4%, respectively (17, 18). The findings of this investigation align with a similar study conducted in Iran, which reported a prevalence rate of 54.2% for Helicobacter pylori (HP) infection among pregnant women (12). A study conducted among the general community in Jijiga and Hawassa indicated a higher prevalence of HP infection compared to this study, with rates of 71% and 83.3% respectively (19, 32). The results of this study provide a clear indication that Helicobacter pylori (H. pylori) infection has a significant impact on hematological parameters in pregnant women with iron deficiency anemia (IDA). The observed reduction in Red Blood Cell (RBC) count among H. pylori positive women, with a mean of 3.8±0.5 ×10⁶/μL compared to 4.2±0.6 ×10⁶/μL in the H. pylori negative group, aligns with findings from previous studies (1,2). This reduction in RBC count can be attributed to the effects of H. pylori on iron metabolism, as the bacterium has been shown to interfere with iron absorption and utilization, leading to a more pronounced anemia in infected individuals. Similar findings were reported by Muhsen and Cohen, who noted a significant association between H. pylori infection and reduced RBC counts in patients with IDA. The study also highlights significant differences in Mean Corpuscular Volume (MCV) between H. pylori positive and negative groups. The lower MCV in H. pylori positive women (76.2±5.4 fl) compared to their negative counterparts (82.4±6.1 fl) suggests that H. pylori infection is linked to the development of microcytic anemia. This finding is consistent with the results of Weyermann et al., who found that H. pylori infection is associated with smaller red blood cells, a characteristic feature of iron deficiency anemia (10,11). Further, the lower Mean Corpuscular Hemoglobin (MCH) and Mean Corpuscular Hemoglobin Concentration (MCHC) observed in H. pylori positive women (24.1±2.7 pg and 31.9±1.5 g/dl, respectively) compared to H. pylori negative women (27.8±3.2 pg and 33.4±1.8 g/dl) indicate that H. pylori infection not only reduces the size of red blood cells but also their hemoglobin content. These findings are in agreement with those of Dolatian et al., who demonstrated that H. pylori infection can exacerbate the severity of anemia by further reducing the hemoglobin concentration within red blood cells (10,11,12). Interestingly, the analysis of anemia severity did not show statistically significant differences in the distribution of mild, moderate, and severe anemia between H. pylori positive and negative groups. However, the trend towards more severe anemia in the H. pylori positive group, with 18.7% of these women affected by severe anemia compared to 8.8% in the H. pylori negative group, suggests that H. pylori infection may contribute to a worsening of anemia in pregnant women with IDA. 

H. pylori infection is associated with altered hematological and nutritional parameters in pregnant women with IDA, potentially exacerbating anemia severity. These findings underscore the importance of screening and managing H. pylori infection in pregnant women with IDA to improve maternal and fetal outcomes.

The authors declare that they have no conflict of interest

No funding sources

The study was approved by the Kirkuk Oncology and Hematology Center.

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