Abstract
Background
Celiac disease (CD) is an autoimmune disorder characterized by gluten intolerance, primarily affecting the gastrointestinal system but potentially influencing cardiovascular health. Emerging evidence suggests an association between CD and myocardial infarction (MI), though studies have produced inconsistent results. This study aimed to systematically review and conduct a meta-analysis of existing literature to quantify the risk of MI in individuals diagnosed with CD.
Methods
A comprehensive literature search was performed across PubMed, Embase, and Web of Science up to August 2024. Studies were included if they investigated the association between CD and MI in adult populations and provided relevant effect estimates. Data from eligible studies were extracted, and a random-effects meta-analysis was conducted to calculate pooled hazard ratios (HRs) and odds ratios (ORs), along with an assessment of heterogeneity. Statistical analysis has been performed by R software (V 4.4).
Results
A total of 8 studies were included in the systematic review. Pooled HR analysis showed no significant association between CD and MI (HR = 1.143, 95% CI: 0.619–2.109), and pooled OR analysis also revealed non-significant results (OR = 0.879, 95% CI: 0.481–1.606). High heterogeneity was observed (I2 = 86% for HR, 99% for OR).
Conclusion
This meta-analysis found no significant association between CD and MI. However, substantial heterogeneity across studies indicates variability in results, highlighting the need for further research with larger, more homogeneous cohorts to better understand cardiovascular risks in CD patients. Future studies should explore subgroups and the impact of gluten-free diet adherence.
Supplementary Information
The online version contains supplementary material available at 10.1186/s12872-024-04340-w.
Keywords: Celiac disease, Myocardial infarction, Cardiovascular disease, Meta-analysis
Introduction
Celiac disease (CD) is an autoimmune condition marked by a lifelong sensitivity to gluten, which is a protein present in wheat, rye, and barley. [1]. In individuals with a genetic predisposition, consuming gluten prompts an improper immune reaction that results in inflammation and harm to the small intestine's lining, leading to poor nutrient absorption. It affects approximately 1% of the population globally [2], though the prevalence may vary across different regions and populations depending on genetic predisposition and dietary factors. There is high variability in clinical presentation of CD, ranging from classical symptoms such as abdominal pain, weight loss, and diarrhea to atypical or extraintestinal manifestations including anemia, osteoporosis, and neurological disorders [3]. The diagnosis of CD requires serological tests for certain antibodies, like anti-tissue transglutaminase and anti-endomysial antibodies, which are then confirmed by a small bowel biopsy. The sole effective treatment for CD is maintaining a lifelong gluten-free diet (GFD), leading to clinical improvement and histological recovery in the majority of patients. [4].
Although the primary pathological changes in CD occur within the gastrointestinal tract, emerging evidence suggests that CD may have systemic implications, particularly with respect to cardiovascular health [5]. Cardiovascular disease (CVD) remains the leading cause of mortality worldwide, with myocardial infarction (MI) being one of the most common and severe manifestations. MI, commonly referred to as a heart attack, results from the occlusion of coronary arteries, leading to necrosis and ischemia of cardiac tissue. Established risk factors for MI include hypertension, dyslipidemia, diabetes mellitus, smoking, and obesity. However, Recently, researchers have started investigating the connection between autoimmune disorders, chronic inflammation, and the risk of cardiovascular disease (CVD), including among those suffering from CD. [6].
The pathophysiological bridge between CD and an increased risk of cardiovascular events, particularly MI, is not yet fully understood but may be related to several factors. First, chronic systemic inflammation, which is a distinctive feature of untreated or poorly managed CD, has been implicated in the development of atherosclerosis, the underlying cause of most cases of MI [7]. Inflammation is key in the development and advancement of atherosclerotic plaques, and autoimmune disorders like CD can intensify this process via continuous immune activation. [8]. Second, nutrient deficiencies commonly seen in CD, particularly vitamin B12, folate, and iron deficiencies, may contribute to cardiovascular risk. For instance, deficiencies in B vitamins can enhance homocysteine levels, a known risk factor for cardiovascular events including MI [9]. Additionally, anemia, which is frequently observed in CD patients due to malabsorption of iron and other essential nutrients, has been linked to adverse cardiovascular outcomes, including increased risk of ischemic heart disease [5].
Studies reveal that people with untreated CD typically have atypical lipid profiles, characterized by reduced high-density lipoprotein (HDL) and elevated low-density lipoprotein (LDL) cholesterol and triglycerides. Such lipid imbalances can accelerate the development of atherosclerosis and heighten the risk of myocardial infarction (MI). [5]. Additionally, evidence suggests that CD may be associated with an increased risk of thromboembolic events, including venous thromboembolism and arterial thrombosis, both of which can lead to MI [10]. The prothrombotic state observed in some CD patients may be related to chronic inflammation, coagulation factors, and platelet function abnormalities [11].
The association between CD and MI has been explored in several observational studies, but the results have been inconsistent. For instance, Conroy et al. identified an elevated risk in a prospective cohort study involving 2,083 patients conducted in 2023. for MI in individuals with CD [12] while others have found no statistical significant association [13]. These discrepancies may be attributed to differences in study design, sample size, and patient populations, as well as varying degrees of adherence to a GFD.
This study aims to conduct a systematic review exploring the link between CD and MI, and to perform a meta-analysis of pertinent studies to quantify the risk of MI in individuals diagnosed with CD. This analysis provides more precise estimates of the risk and help to clarify the clinical implications of CD in the context of cardiovascular health.
Method
Study design
This systematic review and meta-analysis adhered to the guidelines set forth by the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) (Table S1). The objective of this study was to explore the relationship between CD and MI through a systematic review and synthesis of the existing literature. The protocol for the study was registered with the International Prospective Register of Systematic Reviews (PROSPERO).
Search strategy
A thorough search across several electronic databases such as PubMed, Embase, and Web of Science was carried out to locate studies released from their start up to 20 August 2024. The search strategy employed a mix of controlled vocabulary, such as MeSH terms, and free-text terms relevant to CD and MI. The following keywords and their synonyms were used in PubMed: ("myocardial infarction" OR "myocardial infarction"[MeSH Terms] OR "MI" OR "heart attack" OR "cardiac arrest" OR "ischemic heart*") AND ("Celiac disease" OR "Coeliac disease" OR "Celiac diseases" OR "Coeliac diseases" OR "Celiac sprue" OR "celiac*"). No language or type of article restriction was imposed in the search. The complete search strategy is presented in Table S2.
Eligibility criteria
Eligibility criteria for this systematic review and meta-analysis were set up to guarantee the inclusion of pertinent and high-quality studies. Studies were included if they met the following criteria: 1) they involved adult participants (18 years and older) diagnosed with CD based on serological tests or small bowel biopsy, 2) they examined the association between celiac disease and MI, 4) the studies provided clear data on cardiovascular events, including MI, with appropriate comparison groups, and 5) they were published in peer-reviewed journals and authored in English. Studies were excluded if they focused solely on pediatric populations, lacked a control group, did not provide sufficient data on the cardiovascular outcomes of interest, or included data on cardiovascular events without MI. Additionally, review articles, conference abstracts, and case reports were excluded.
Screening
We used semi-automated software (Nested-Knowledge, MN, USA) to streamline the study selection process, which involved deduplication and a two-phase screening process conducted by two independent reviewers. Initially, the software removed duplicate records across databases, ensuring a clean dataset for review. The first phase, title and abstract screening, involved each reviewer independently assessing studies based on predefined inclusion and exclusion criteria, allowing for a quick exclusion of irrelevant studies. Discrepancies at this stage were resolved through discussion, with a third reviewer consulted when consensus could not be reached. Studies deemed relevant were then subjected to full-text screening, where each study was evaluated in detail for methodological quality, relevance, and alignment with the research question. Any conflicts were resolved as in the previous phase.
Data extraction and risk of bias assessment
Data from the selected studies were independently extracted by two reviewers using a standardized form to ensure consistency and accuracy in data collection. The extracted information covered several key aspects of each study. Study characteristics included details such as the country, year of publication, first author where the study was conducted, the total sample size, and the study design. Population characteristics involved age, and gender distribution. Statistical data, including effect estimates like odds ratios (ORs) and Hazard ratio (HRs) and their corresponding 95% confidence intervals (CI), along with any adjustments for potential confounders, were also extracted. During the data extraction process, any disagreements were resolved through discussion, with a third reviewer being consulted as necessary to reach a consensus. The "tagging" function of the Nested-Knowledge software was utilized for data extraction [14].
The methodological quality of the included studies was independently evaluated by two reviewers using the Newcastle–Ottawa Scale (NOS). Each study was assessed based on participant selection, comparability of study groups, and the determination of exposure and outcomes. Also, we considered the score of 7 to 9 as high, 4 to 6 as moderate and below 3 as low.
Data synthesis and statistical analysis
A random-effects meta-analysis was performed to accommodate the variability among the included studies. The primary outcome measure was the pooled OR and HR of MI in individuals with CD, using a random-effects model [15]. Heterogeneity among studies was evaluated using the I2 statistic and Cochran's Q test. I2 values greater than 75% indicating substantial heterogeneity. Sensitivity analysis was performed by the leave-one-out approach [16, 17]. All analyses considered a p-value of less than 0.05 as statistically significant. The statistical analyses were carried out using R version 4.4.
Results
Study selection
A total of 2,118 records were initially identified through database searches across PubMed (313 records), Embase (1166 records), and Web of Science (639 records). After removing 530 duplicate records, 1,588 records remained for screening. After the screening process, 1450 records were excluded because their titles and abstracts did not fulfill the inclusion criteria. Upon full-text review, 131 articles were excluded for various reasons: 56 did not focus on the outcomes of interest, 15 were review articles, 10 were case reports, 17 were case series, and 32 were irrelevant articles. Finally, 8 [12, 13, 18–23] studies satisfied the inclusion criteria and were incorporated into the final systematic review and meta-analysis (Fig. 1).
Fig. 1.
PRISMA flowchart depicting article selection and screening process
Study characteristics
The eight included studies are from various countries, including the USA, UK, and China (Table 1). Out of these, six studies employed a retrospective cohort design, while one was prospective cohort and other one was Mendelian Randomization, indicating a mix of temporal approaches to explore the relationship between CD and MI. In most studies, CD was diagnosed primarily through serological testing (anti-tissue transglutaminase or anti-endomysial antibodies) in combination with small bowel biopsy. MI was identified using clinical records or ICD codes. The quality assessment of the studies is presented in Table S3.
Table 1.
Characteristics of included studies
| Study | Country | Study design | Population | Age | Effect size for MI (95% CI) | Male | Follow-up (years) |
|---|---|---|---|---|---|---|---|
| Abboud 2024 [18] | USA | Retrospective Cohort | Patients admitted with acute pancreatitis | Mean = 50.56 (SD = 0.28) | OR = 0.217 (0.116–0.406) | Non-CD = 52.1%, CD = 30.6% | NA |
| Cole 2022 [19] | USA | Retrospective Cohort | Patients with CD who underwent THA and TKA | Mean = 64.72 (SD = 9.96) | THA: OR = 1.45 (1.01–2.07), TKA: OR = 1.16 (0.88–1.52) | THA = 27%, TKA = 24% | 2 |
| Conroy 2023 [12] | UK | Prospective Cohort | Adults with coeliac disease | Mean = 58.1 (SD = 7.9) | HR = 1.59 (1.25–2.01) | 45% | 12.4 |
| Gajulapalli 2017 [20] | USA | Retrospective Cohort | Patients with CD | Mean = 50.6 | OR = 1.73 (1.65‑1.82) | 60% | 17 |
| [21, 21] | China | Mendelian Randomization | Patients with CD | NA | OR = 0.994 (0.959–1.030) | NA | NA |
| Naaraayan 2019 [22] | NA | Retrospective Cohort | Patients with CD | Median = 70.15 | OR = 0.78 (0.72–0.86) | NA | 9 |
| Pellegrini 2022 [23] | USA | Retrospective Cohort | Adults with diagnosed CD | 69.57 ± 13.21 | OR = 0.78; P < .05) | CD = 46.24, No CD = 61.53 | NA |
| West 2004 [13] | UK | Retrospective Cohort | Adults with diagnosed CD | 25 or older | HR = 0.85 (0.63–1.13) | 31.50% | 5.9 |
CD Celiac Disease, HR Hazard Ratio, MI Myocardial Infarction, NA Not Available, OR Odds Ratio, SD Standard Deviation, THA Total Hip Arthroplasty, TKA Total Knee Arthroplasty
Studies examining the relationship between CD and the risk of MI present a complex and, at times, paradoxical picture. Conroy et al. [12] and Gajulapalli et al. [20] point to an increased cardiovascular risk in individuals with CD, suggesting that chronic inflammation associated with the disease might drive a higher incidence of cardiovascular events, such as MI, independent of traditional risk factors. Conroy et al. [12] observed a 1.27-fold increased risk of cardiovascular events in CD patients (HR: 1.27; 95% CI: 1.11–1.45), despite their generally favorable cardiovascular profiles, such as lower body mass index (BMI) and systolic blood pressure. This paradoxical increase aligns with findings by Gajulapalli et al. [20], who reported nearly twice the prevalence of coronary artery disease (CAD) in CD patients compared to non-CD counterparts (OR: 2.09; 95% CI: 2.03–2.15), indicating that the systemic inflammation common in CD could accelerate atherosclerosis and contribute to MI risk. However, studies by West et al. [13] and Abboud et al. reported a lower prevalence of traditional risk factors among CD patients, such as hypertension and hypercholesterolemia, despite a persistently elevated risk of MI. Abboud et al. [18] further suggest protective factors in CD, with findings showing reduced mortality and complications, such as MI, in CD patients hospitalized with acute pancreatitis. Notably, CD patients hospitalized with acute pancreatitis had significantly lower odds of MI (OR 0.217; P < 0.05). Additionally, Pellegrini et al. [23] reported lower adjusted odds of MI (adjusted OR 0.78; P < 0.05) and related mortality in CD patients than in controls, particularly during acute hospitalizations. Cole et al. [19] found that CD patients undergoing total hip arthroplasty (THA) faced significantly higher rates of MI within 90 days post-operation (2.7% vs. 1.9%; OR 1.45; 95% CI: 1.01–2.07), showing an elevated risk of cardiovascular complications following surgical interventions for CD patients. Conversely, Huang et al.’s [21] Mendelian randomization analysis revealed no causal genetic link between CD and cardiovascular disease, including MI, ischemic stroke, and coronary artery disease, with an OR of 0.994 (95% CI: 0.959–1.030) for MI.
Meta-analysis
The pooled analysis of HR for the association between CD and MI showed no statistically significant relationship (Fig. 2). The combined HR was 1.143 (95% CI: 0.619–2.109), indicating that CD individuals did not have a significantly higher risk of MI compared to those without CD. However, the heterogeneity was substantial (I2 = 86%, p < 0.01), suggesting considerable variability between the studies, which may have impacted the overall pooled estimate.
Fig. 2.
Meta-analysis of pooled Hazard ratios showing the association of MI with CD
The meta-analysis of ORs also revealed no significant association between CD and MI, with a pooled OR of 0.879 (95% CI: 0.481–1.606) (Fig. 3). As with the HR analysis, the high level of heterogeneity (I2 = 99%, p < 0.01) indicates substantial variability between the included studies. This suggests that while some individual studies reported different outcomes, the overall pooled result does not show a clear link between CD and MI.
Fig. 3.
Meta-analysis of pooled odds ratios showing the association of MI with CD
Sensitivity analysis
Sensitivity analysis was performed by leave-one-out approach (Fig. 4). Each study was sequentially omitted, and the pooled OR was recalculated. The results demonstrated that omitting any individual study did not significantly alter the overall pooled OR, which remained at 0.879 (95% CI: 0.481–1.606). This suggests that no single study had a disproportionate influence on the results, confirming the stability and reliability of the meta-analysis findings.
Fig. 4.
Sensitivity analysis
Discussion
This systematic review and meta-analysis sought to elucidate the connection between CD and MI by synthesizing the available evidence. The primary finding from this meta-analysis is that there is no statistically significant association between CD and MI when data from various studies are pooled. Both HR and OR analyses revealed non-significant results, with pooled HR of 1.143 (95% CI: 0.619–2.109) and pooled OR of 0.879 (95% CI: 0.481–1.606). However, high heterogeneity was observed, particularly in the OR analysis (I2 = 99%), which indicates substantial variability in the study outcomes.
Despite the clear inflammatory component of CD and its known potential to induce systemic inflammation, which can contribute to cardiovascular disease, the pooled analysis does not show a definitive link between CD and MI. Several potential reasons may include the degree of heterogeneity observed across the included studies. This heterogeneity could stem from several factors, including differences in study design, variations in how CD and MI were diagnosed, and differences in population characteristics (such as geographic location, ethnicity, and age distribution). Some studies may have included patients with undiagnosed or subclinical CD, which could skew the results. Furthermore, differences in the length of follow-up and the extent to which CD was managed with a GFD could also influence cardiovascular outcomes. Additionally, many patients with CD follow a strict GFD, which can mitigate systemic inflammation and reduce cardiovascular risk factors such as dyslipidemia, hypertension, and chronic inflammation. Studies have shown that adherence to a GFD can lead to the normalization of lipid profiles, reduce inflammatory markers, and reverse certain risk factors for cardiovascular disease [4]. Cardiovascular disease, including MI, is multifactorial in nature, with established risk factors such as hypertension, smoking, diabetes, dyslipidemia, and obesity playing a crucial role [24]. Many of the included studies adjusted for these traditional cardiovascular risk factors, which may have diluted any potential independent effect of CD on MI.
A previous meta-analysis also showed similar results. They reported an OR of 1.12 (95% CI: 0.83–1.40) [25], similarly indicating a non-significant increased risk of MI in individuals with CD, as shown by our analysis. However, their meta-analysis involved only 4 studies, among which one study reported composite cardiovascular outcomes rather than MI alone. Our analysis included 7 studies that reported MI as a distinct outcome. Our analysis provided stronger evidence due to the inclusion of more studies. The findings of the previous meta-analysis, along with ours, suggest that, although CD may modestly elevate cardiovascular risk in general, the evidence supporting a clear and significant link between CD and MI is limited and inconsistent, warranting further research.
Future studies could benefit from larger, multi-national cohorts to provide more generalized and comprehensive insights. It is essential to conduct prospective studies with long-term follow-up to capture the full extent of cardiovascular outcomes in CD patients, particularly considering different degrees of adherence to a gluten-free diet and its impact on systemic inflammation and cardiovascular risk. Further research should also focus on the role of specific nutritional deficiencies and biomarkers of inflammation in CD patients that could influence cardiovascular risk. Identifying subgroups within the CD population, such as those with different levels of disease activity, varying durations of gluten exposure before diagnosis, or co-existing autoimmune conditions, would help in understanding the nuanced risks of cardiovascular diseases in these patients. Exploring the genetic predispositions that link CD and cardiovascular diseases could uncover new insights into pathophysiological mechanisms. Advanced analytical techniques, such as Mendelian randomization, could help ascertain causal relationships between CD and cardiovascular outcomes. Moreover, intervention studies examining the effects of gluten-free dietary adherence on cardiovascular risk markers in newly diagnosed CD patients could provide actionable insights into disease management and prevention strategies. These areas of future research could significantly refine our understanding and management of cardiovascular risks in individuals with celiac disease.
Our study has some limitations. Substantial heterogeneity was observed among the included studies, indicated by high I2 values. Such discrepancies can dilute the true effect size and potentially mask subtler associations. The studies included varied significantly in their adjustment for potential confounders. While some studies adjusted for traditional cardiovascular risk factors such as age, smoking, hypertension, and cholesterol levels, others did not, which might lead to residual confounding. The influence of diet, particularly adherence to a gluten-free diet among CD patients, which can significantly modify cardiovascular risk, was also not uniformly considered across studies. Another limitation is the reliance on observational data, which inherently limits the ability to draw causal inferences due to the potential for unmeasured confounding factors. Additionally, most included studies relied on medical records and administrative databases for the diagnosis of CD and MI, which may be subject to misclassification bias. Moreover, we could not perform subgroup analyses to explore the effects of gender, age at diagnosis, or the severity of CD, which might have provided deeper insights into specific high-risk subgroups within the CD population. The lack of individual patient data also prevented more refined analyses, such as assessing the impact of disease duration or the long-term adherence to a gluten-free diet on the risk of MI. Additionally, CD patients with comorbid autoimmune diseases or those who are diagnosed later in life may have an increased cardiovascular risk due to prolonged inflammation or other underlying conditions.
Conclusion
This meta-analysis found no significant link between CD and MI. However, the variability across studies shows the need for more robust, longitudinal research to better understand potential cardiovascular risks in specific subgroups of CD patients. Further research should focus on detailed subgroup analyses, the impact of gluten-free diet adherence, and the interaction of CD with other cardiovascular risk factors to refine our understanding and management of cardiovascular health in CD patients.
Supplementary Information
Acknowledgements
The authors acknowledge the Nested-Knowledge, MN, USA for providing the access to the software.
Clinical trial number
Not applicable.
Financial support and sponsorship
None.
Ethical considerations
Not applicable.
Authors' contributions
Muhammed Shabil and Mahalaqua Nazli Khatib, Nikhil Sharma led conceptualization and execution. Raj Pratap Singh and Mahendra Pratap Singh managed statistical analysis and interpretation. Ganesh Bushi handled data collection and analysis. Suhas Ballal, Pooja Bansal, and Kiran Bhopte drafted and revised the manuscript. Abhay M Gaidhane and Afukonyo Shidoiku Daniel supervised and reviewed revisions. Balvir S. Tomar, Ayash Ashraf, M Ravi Kumar, Ashish Singh Chauhan, and Sanjit Sah reviewed intellectual content. Rachna Kathuria reviewed methodology and the final manuscript.
Funding
This study received no funding.
Data availability
The data is with the authors and available on request.
Declarations
Ethics approval and consent to participate
Not applicable since this is a review and not involved any human.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Footnotes
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Nikhil Sharma and Mahalaqua Nazli Khatib contributed equally to this work.
Contributor Information
Abhay M. Gaidhane, Email: abhay.psm@dmiher.edu.in
Afukonyo Shidoiku Daniel, Email: afukonyoshidoiku@tsuniversity.edu.ng.
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Associated Data
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Supplementary Materials
Data Availability Statement
The data is with the authors and available on request.