Prevalence and determinants of hyperemesis gravidarum among pregnant women in Ethiopia: A systematic review and meta-analysis

Abstract

Background

Studies focusing on the occurrence and correlates of hyperemesis gravidarum in Ethiopia have reported varied values in different regions of the country. Additionally, there is no systematic review and meta-analysis summarizing the prevalence of hyperemesis gravidarum and its determinants in Ethiopia. Hence, this systematic review and meta-analysis aimed to estimate the overall prevalence of hyperemesis gravidarum and explore its determinants in Ethiopia.

Methods

Cross-sectional or case-control studies conducted in Ethiopia, written in English, and reporting the prevalence or the determinant of hyperemesis gravidarum among pregnant women were included in the review. International databases (PubMed, Scopus, Cochrane Library, Google Scholar, Science Direct, African Journal Online, Directory of Open Access Journal, and African Index Medicus) and Ethiopian university repositories (Jimma, Addis Ababa, Haramaya, Hawassa, and Gondar Universities) were searched from September 4–15, 2023, to identify articles published on the topic. The pooled prevalence of hyperemesis gravidarum with a 95% confidence interval was presented using the forest plots. The heterogeneity of the studies was checked by I² with its corresponding p-values and the Galbraith plot. Subgroup analysis and meta-regression were performed to identify sources of heterogeneity. Funnel plot, Egger, and Begg’s tests were used to assess publication bias.

Results

A total of 11 articles with a 3510-sample size were included in this systematic review and meta-analysis. The pooled prevalence of hyperemesis gravidarum among pregnant women in Ethiopia was 7.12% with a 95% CI (4.09–10.15) and a high level of heterogeneity (I² = 86.5%, p<0.001). Subgroup analyses revealed the overall prevalence of hyperemesis gravidarum was highest in the Amhara region with 11.30%, 95% CI (8.20–14.40), and lowest in Oromia with 3.40%, 95% CI (1.94–4.85). Having a previous history of hyperemesis gravidarum (POR = 3.828, 95% CI: 1.673–5.983), being in the first trimester of pregnancy (POR = 8.476, 95% CI: 5.047–11.905), and Helicobacter pylori infection (POR = 3.924, 95% CI: 2.027–5.821) were found to be significantly associated with hyperemesis gravidarum in Ethiopia.

Conclusion

The prevalence of hyperemesis gravidarum among pregnant women in Ethiopia is high. Targeting pregnant women in the first trimester, with a previous history of hyperemesis gravidarum, and those with Helicobacter pylori infection during prenatal counseling on how to manage and reduce hyperemesis gravidarum is very helpful to avert related complications.

Registration

The review was registered in the International Prospective Register of Systematic Reviews (PROSPERO) with the registration number “CRD42023461808”, on September 19, 2023.

Introduction

Nausea and vomiting in pregnancy (NVP) is a common disorder characterized by symptoms of nausea, vomiting, or dry retching commencing in the first trimester without an identifiable cause other than pregnancy [1]. It has a complex and unclear origin that involves genetic, hormonal, endocrine, gastrointestinal, immune, metabolic, environmental, and psychosocial factors [2]. Hyperemesis gravidarum (HG) is the most severe form of unrelenting nausea and vomiting that leads to dehydration, electrolyte and metabolic imbalance, ketonuria, significant weight loss of more than 5% of the pre-pregnancy weight, and impaired daily functioning [3–7].

HG is affecting 0.3%-3.6% of pregnant women globally [8]. The prevalence is notably high in China (8.9%), and Northeast Nigeria (44.9%), and varies in Ethiopia from 3.2% in Hararghe to 11.7% in Addis Ababa [5, 9–15].

Hyperemesis gravidarum is more likely in women who are young, single, primigravida, carrying a girl or a molar pregnancy, have a previous or family history of HG, have a history of abortion or multiple gestations [5, 7, 9–11, 14–28]. Additionally, gestational age, maternal nutritional status, history of gastrointestinal disease, asthma, previous history of urinary infection, H. pylori infection, and stress were factors reported by literature to be associated with hyperemesis gravidarum [10, 12, 24, 26, 29–37].

Women with hyperemesis are at increased risk of having medical and obstetric problems during pregnancy as well as a higher rate of maternal and fetal complications. These include failure to gain weight, hypertensive disorders, anemia, preterm birth, low birth weight, post-partum hemorrhage, placental abruption, and neonatal intensive care unit admission [38–44]. It may also increase the likelihood of psychological and emotional distress during and after pregnancy, and some women may have suicidal thoughts or consider ending their wanted pregnancies [45–52]. The health-related quality of life of women with moderate to severe NVP is comparable to those with breast cancer or myocardial infarction [53, 54]. Children exposed to HG in utero may have increased risks of various health problems later in life, such as hormonal imbalances, metabolic disorders, growth and neurodevelopmental impairment [41, 55–61].

A comprehensive understanding of the condition, improving healthcare provider awareness, and providing appropriate psychological support, prompt and timely recognition, identification, and treatment are essential to minimize or prevent associated long-term maternal and fetal morbidity/complications [7, 42, 62, 63].

Studies focusing on the occurrence and correlates of hyperemesis gravidarum in Ethiopia have reported varied values in different regions of the country. Additionally, there is no systematic review and meta-analysis summarizing the prevalence of hyperemesis gravidarum and its determinants in Ethiopia. Hence, the objective of this systematic review and meta-analysis is to estimate the overall prevalence of hyperemesis gravidarum and explore its determinants in Ethiopia. Understanding the burden of the problem and identification of the determinant factors are important in pre-pregnancy counseling to detect early and minimize related complications and adverse outcomes. The findings of this systematic review and meta-analysis will be used by the concerned stakeholders to reduce the prevalence of hyperemesis gravidarum and design evidence-based interventions.

Methods

Reporting and protocol registration

The research database and Prospective Register of Systematic Reviews (PROSPERO) have been searched to check if the topic has been reviewed previously or if an ongoing review exists to avoid re-inventing the wheel. Hence, no systematic review or meta-analysis on this topic was published or registered. The updated Preferred Reporting Items for Systematic Reviews and Meta-analysis guideline (PRISMA-P) protocol was followed for conducting and reporting this systematic review and meta-analysis (S1 Table). The review protocol has been registered in PROSPERO, the University of York Centre for Reviews and Dissemination, with the registration number “CRD42023461808”, as of September 19, 2023.

Eligibility criteria

Cross-sectional or case-control studies conducted in Ethiopia, written in English, and reporting the prevalence or determinant factors of hyperemesis gravidarum among pregnant women were included in the review. Cross-sectional studies were used to calculate the pooled prevalence of hyperemesis gravidarum. Duplicated studies, articles without abstract and full text, and studies that do not report the odds ratio of the factors were excluded.

Information source

International online databases (such as PubMed, Scopus, Cochrane Library, Google Scholar, Science Direct, African Journal Online, Directory of Open Access Journal, and African Index Medicus) and Ethiopian university repositories (Jimma, Addis Ababa, Haramaya, Hawassa, and Gondar Universities) were searched for articles on prevalence and determinants of hyperemesis gravidarum from September 4–15, 2023.

Search strategy

Search terms based on Population, Intervention, Comparison, Outcome (PICO) questions, and medical subject heading (MeSH) terms; Boolean operators "AND" and "OR" were used. “Hyperemesis gravidarum” OR “hyperemesis” AND “gravidarum” OR “nausea and vomiting in pregnancy” OR “nausea” OR “vomiting” OR “pregnancy complications” OR “maternal morbidity” AND “prevalence” OR “magnitude” OR “burden” AND “determinants” OR “risk factors” OR “associated factors” OR “predictors” AND “Ethiopia” were used to search articles on the databases. In addition to consultation with the subject matter experts, the list of references for the included articles was also searched to find potential articles (S2 Table). EndNote™ 20 reference manager software was used to organize search results and remove duplicate articles. The study selection process was presented in a PRISMA flowchart (Fig 1).

[Figure omitted. See PDF.]

Selection process

To determine the eligibility of the studies for the review, independent reviewers applied the pre-defined inclusion criteria. Two authors (GA & AW) independently screened and selected the articles, and resolved any disagreement by consulting with a third author (ND).

Data collection process

Once eligible studies were identified from the databases, the data extraction format was prepared on a Microsoft Excel spreadsheet and used to extract the data from the articles. The data extraction format included the name of the author, the year it was published, the region and specific location where the study was conducted, the type of study design employed, and the sample size of participants. The prevalence of hyperemesis gravidarum and the odds ratio of the selected variables were also recorded.

Outcome measurement

This study considered two major outcomes of interest. First, the percentage of pregnant women who suffered from hyperemesis gravidarum. The second one was the factors that influenced the occurrence of hyperemesis gravidarum, expressed by the odds ratio with the confidence intervals. Although there is no clear consensus on how to define hyperemesis gravidarum, all the studies that were included in this review used the same criteria: “Pregnant women who had frequent nausea and vomiting not related to other causes and/or who had dehydration, electrolyte abnormalities, ketonuria on urine analysis, or weight loss of at least 5% of their pre-pregnancy weight.”

Study risk of bias assessment

To assess the risk of bias in the included studies, Joanna Briggs Institute’s (JBI) quality appraisal tool was used, with eight criteria rated as yes, no, not applicable, and classified risks of bias as low, moderate, or high.

Effect measures

The effect measures for the synthesis and presentation of the results were the precomputed prevalence and odds ratio, along with their respective confidence intervals.

Synthesis methods

We calculated the pooled prevalence of hyperemesis gravidarum by analyzing cross-sectional studies that measured its occurrence. The odds ratio of the factors associated with hyperemesis gravidarum was determined from both cross-sectional and case-control studies. The data from the studies were extracted using a Microsoft Excel 2021 spreadsheet, and then meta-analyses were conducted using Stata MP 17. To address the missing values identified in the primary data for key outcomes or variables essential to the meta-analysis, we contacted the authors of the original studies. We minimized the risk of introducing bias by obtaining the missing information directly from the source.

The estimated prevalence of each study and analysis of determinant factors were presented using the forest plots with a 95% confidence interval. The heterogeneity of the studies was checked by I² with its corresponding p-values and the Galbraith plot. Analysis of the random effect model was used because of the high evidence of heterogeneity. To explore possible sources of heterogeneity among the studies, subgroup analyses and meta-regression were performed. Sensitivity analysis was conducted to understand the effect of a single study on the pooled estimate value. The results of the study were presented using narration, tables, and graphs.

Publication/reporting bias assessment

Funnel plot and Egger and Begg’s regression asymmetry tests with a p-value of <0.05 were used to assess and decide reporting or publication bias.

Results

Study selection

The PRISMA flowchart (Fig 1) shows the study selection process.

Study characteristics

A total of 11 articles with a 3510-sample size were included in this systematic review and meta-analysis. Six of the included studies were cross-sectional, and the remaining five were case-control studies. The pooled prevalence was calculated from the cross-sectional studies (S3 Table), and the factors were identified from both cross-sectional and case-control studies (S4 Table). Concerning their regional distribution, four were conducted in the Oromia region, three in Addis Ababa city, two in the Amhara region, one in South Ethiopia, and one in the Tigray region (Table 1).

[Figure omitted. See PDF.]

Risk of bias in studies

The risk of bias in the included studies was evaluated by Joanna Briggs Institute’s (JBI) quality appraisal tools, using eight criteria rated as yes, no, not applicable, and classified risks of bias as low, moderate, or high. Thus, all the included articles were assessed and found to have a low risk of bias. The details of the risk of bias assessment for the included studies are displayed below (Table 2).

[Figure omitted. See PDF.]

Prevalence of hyperemesis gravidarum in Ethiopia

Based on the random effect model, the pooled prevalence of hyperemesis gravidarum among pregnant women in Ethiopia is 7.12% with a 95% CI (4.09–10.15) and a high level of heterogeneity, (I² = 86.5%, p<0.001). The graphical display of the prevalence of the individual studies and the result of the synthesis is presented in the forest plot (Fig 2).

[Figure omitted. See PDF.]

Heterogeneity analysis

As observed from I² of 86.5% as displayed on the forest plot and the Galbraith plot (Fig 3) there is high heterogeneity among the included studies.

[Figure omitted. See PDF.]

To identify the source of heterogeneity, subgroup analyses of the prevalence of hyperemesis gravidarum were further calculated based on the geographical locations of the included studies. Accordingly, the overall prevalence of hyperemesis gravidarum is highest in the Amhara region with 11.30%, 95% CI (8.20–14.40), and lowest in the region of Oromia with 3.40%. 95% CI (1.94–4.85) (Fig 4).

[Figure omitted. See PDF.]

We also performed a meta-regression analysis to examine the effects of the year of publication and the sample size. However, none of these variables showed statistically significant association with a p-value of 0.150 for the publication year and 0.432 for the sample size (Table 3).

[Figure omitted. See PDF.]

Determinants of hyperemesis gravidarum in Ethiopia

The pooled analysis of the studies revealed that having a previous history of hyperemesis gravidarum, being in the first trimester of pregnancy, and having a Helicobacter pylori infection were determinants associated with hyperemesis gravidarum. Pregnant women who have a previous history of hyperemesis gravidarum are almost four times more likely to have hyperemesis gravidarum compared to those who do not have a previous history of hyperemesis gravidarum, with a pooled OR of 3.83 and a 95% CI of 1.67–5.98. Compared to those who are in the third trimester of pregnancy, pregnant women in the first trimester are more than eight times more likely to have hyperemesis gravidarum, with a pooled OR of 8.48, 95% CI (5.05–11.91). Pregnant women who have a Helicobacter pylori infection are almost four times more likely to have hyperemesis gravidarum compared to those who are negative for Helicobacter pylori, with a pooled OR of 3.92 and a 95% CI of 2.03–5.82 (Table 4).

[Figure omitted. See PDF.]

Publication bias

The presence of reporting or publication bias was evaluated visually using funnel plot asymmetry and statistically using Egger and Begg’s test for small study effects. As observed from the plot, there is some sort of asymmetry, which might be due to the detected heterogeneity or simply by chance. Regression-based Egger’s and Begg’s tests were used to test whether the funnel-plot asymmetry was greater than what had been expected by chance. Thus, Egger’s test (p = 0.2117) and Begg’s test (p = 7071) were not statistically significant, confirming no reporting bias and indicating the funnel plot asymmetry might be observed by chance (Fig 5).

[Figure omitted. See PDF.]

Sensitivity analysis

According to the result of sensitivity analysis, using leave-one-out meta-analysis, no single study in this systematic review and meta-analysis dominated the overall prevalence of hyperemesis gravidarum in Ethiopia (Fig 6).

[Figure omitted. See PDF.]

Discussion

This systematic review and meta-analysis estimated the overall prevalence of hyperemesis gravidarum in Ethiopia and explored its determinants. Hence, 7.12%, with a 95% CI (4.09–10.15), of pregnant women have hyperemesis gravidarum in Ethiopia. Subgroup analyses, based on the geographical locations where the included studies were conducted, revealed the highest and lowest prevalence of Hyperemesis gravidarum documented in the Amhara and Oromia regions, respectively. This is much lower than the study conducted in Nigeria, where almost half of the study participants had hyperemesis gravidarum, and more than the study conducted in Finland, where 1.3% of pregnancies resulting in delivery had been diagnosed with hyperemesis gravidarum [64]. The difference might be due to how hyperemesis was measured. The study in Finland measured hyperemesis gravidarum as an incidence among pregnancies that ended in delivery. However, the studies included in this review measured hyperemesis among all pregnant women, irrespective of their outcomes [14, 65].

The prevalence of hyperemesis gravidarum (HG) observed in our meta-analysis is lower than the study conducted at comprehensive specialized hospitals in northwest Ethiopia which reported 16.8% prevalence. This discrepancy may be attributed to the study setting, as the latter was conducted at specialized hospitals where most patients were referred, potentially leading to a higher concentration of severe cases [66].

Having a previous history of hyperemesis gravidarum, being in the first trimester of pregnancy, and helicobacter pylori infection were determinant factors associated with hyperemesis gravidarum among pregnant women in Ethiopia. Pregnant women who have a previous history of hyperemesis gravidarum are more likely to experience hyperemesis gravidarum compared to those who do not have a previous history of hyperemesis gravidarum. This finding was in line with the studies conducted in Australia, Finland, Nigeria, and Ethiopia, where women with a previous history of hyperemesis gravidarum are more likely to experience hyperemesis gravidarum. The increased risk of hyperemesis gravidarum in subsequent pregnancies among women with a prior history of the condition may be attributed to several factors. These may include psychological stress due to the anticipation of recurrent HG, the persistence of risk factors from previous pregnancies, and the possibility of genetic predisposition to HG [14, 17, 21, 66, 67].

Compared to those who are in the third trimester of pregnancy, pregnant women in the first trimester are more likely to have hyperemesis gravidarum. The same finding was observed in a study conducted in Indonesia, where women in their first trimester were more likely to be affected by hyperemesis gravidarum [68]. This might be because the level of human chorionic gonadotropin is higher in the first trimester of pregnancy, resulting in excess nausea and vomiting. This justification is supported by other related literature [69–71].

Pregnant women who have a Helicobacter pylori infection are more likely to have hyperemesis gravidarum compared to those who are negative for Helicobacter pylori. Similar results were reported by studies conducted in Turkiye, Iraq, Pakistan, Egypt, and Ethiopia, where Helicobacter pylori infection was found to have a statistically significant association with hyperemesis gravidarum. The potential mechanisms underlying this association may include the inflammatory response triggered by H. pylori infection in the gastric mucosa, leading to gastrointestinal disturbances such as gastritis and peptic ulcers. This inflammation can exacerbate symptoms of nausea and vomiting. Additionally, H. pylori infection may be linked to elevated levels of gastrin hormone, resulting in increased gastric acidity. The infection may also induce the release of cytokines such as interleukin-6 and tumor necrosis factor-alpha, which contribute to gastrointestinal symptoms. These cytokines can affect the central nervous system and gastrointestinal motility [72–75]. Hence, pregnant women with persistent hyperemesis gravidarum should be investigated for active Helicobacter pylori infection, and eradication therapy has to be initiated [29, 31–33, 35, 36].

While our study provides valuable insights, it is not without limitations. Firstly, the small sample size in some included studies may affect the meta-analysis findings. Secondly, the inclusion of factors identified from cross-sectional studies introduces the potential for confounding variables to influence the estimates. The possibility of unexamined confounders may contribute to the observed heterogeneity.

Conclusion

A high proportion of pregnant women in Ethiopia experience hyperemesis gravidarum. The pooled prevalence of hyperemesis gravidarum among pregnant women in Ethiopia is high. Having a previous history of hyperemesis gravidarum, being in the first trimester of pregnancy, and helicobacter pylori infection were significant determinant factors associated with hyperemesis gravidarum among pregnant women in Ethiopia.

Hence, targeting pregnant women in the first trimester with a previous history of hyperemesis gravidarum and those with Helicobacter pylori infection during prenatal counseling on how to manage and reduce hyperemesis gravidarum is very helpful to avert related complications.

Supporting information

S1 Table. PRISMA checklist for reporting hyperemesis gravidarum among pregnant women in Ethiopia, 2023.

https://doi.org/10.1371/journal.pone.0314783.s001

(DOCX)

S2 Table. Total studies identified and retrieved in the literature search, and assessed for eligibility for the systematic review and meta-analysis of hyperemesis gravidarum among pregnant women in Ethiopia, 2023.

https://doi.org/10.1371/journal.pone.0314783.s002

(DOCX)

S3 Table. Studies included in the analysis of prevalence hyperemesis gravidarum among pregnant women in Ethiopia, 2023.

https://doi.org/10.1371/journal.pone.0314783.s003

(DOCX)

S4 Table. Studies included in the analysis of determinants of hyperemesis gravidarum among pregnant women in Ethiopia, 2023.

https://doi.org/10.1371/journal.pone.0314783.s004

(DOCX)

Acknowledgments

We are very thankful for all authors of the primary studies that are included in this systematic review and meta-analysis.

References

1. 1. Lowe S, Bowyer L, Beech A, Robinson H, Armstrong G, Marnoch C, et al. Guideline for the Management of Nausea and Vomiting in Pregnancy and Hyperemesis gravidarum. Society of Obstetric Medicine of Australia and New Zealand. 2019.

* View Article

* Google Scholar

2. 2. Maltepe C, Koren G. The management of nausea and vomiting of pregnancy and hyperemesis gravidarum-a 2013 update. Journal of Population Therapeutics and Clinical Pharmacology. 2013;20(2). pmid:23863612

* View Article

* PubMed/NCBI

* Google Scholar

3. 3. Tian R, MacGibbon K, Martin B, Mullin P, Fejzo M. Analysis of pre-and post-pregnancy issues in women with hyperemesis gravidarum. Autonomic Neuroscience. 2017;202:73–8. pmid:27460690

* View Article

* PubMed/NCBI

* Google Scholar

4. 4. Sobhi Ahmed A, Abd-Elhakeem Hasneen S, Ouda Abd-Elmoniem S, Abd-Elwahab Afifi O. Assessment of knowledge and practices of pregnant women regarding hyperemesis gravidarum. Journal of Nursing Science Benha University. 2022;3(1):445–59.

* View Article

* Google Scholar

5. 5. Kuma T, Yusuf L, Negash S. Assessment of nausea and vomiting of pregnancy on antenatal clients of Addis Ababa. Ethiopian Journal of Health Development. 2013;27(3):200–7.

* View Article

* Google Scholar

6. 6. Laitinen L. Nausea and Vomiting of Pregnancy—Studies with Pregnancy-Unique Quantification of Emesis Questionnaire. 2023.

* View Article

* Google Scholar

7. 7. Castillo MJ, Phillippi JC. Hyperemesis gravidarum: A Holistic Overview and Approach to Clinical Assessment and Management. The Journal of perinatal & neonatal nursing. 2015;29(1):12–22. pmid:25534678

* View Article

* PubMed/NCBI

* Google Scholar

8. 8. Einarson TR, Piwko C, Koren G. Quantifying the global rates of nausea and vomiting of pregnancy: a meta-analysis. Journal of population therapeutics and clinical pharmacology. 2013;20(2). pmid:23863575

* View Article

* PubMed/NCBI

* Google Scholar

9. 9. Fessehaye A, Abate D. Prevalence of Nausea and Vomiting of Pregnancy and its Associated Factors at Three Teaching Hospitals in Ethiopia. Annals Gynecol Obstet. 2021;5(1):133–7.

* View Article

* Google Scholar

10. 10. Adane KD, Zerga AA, Gebeyehu FB, Ayele FY. Proportion of hyperemesis gravidarum and associated factors among pregnant women admitted into the obstetrics ward at Akesta general hospital, North East Ethiopia. Plos one. 2023;18(2):e0281433. pmid:36745599

* View Article

* PubMed/NCBI

* Google Scholar

11. 11. Gelmesa MO, Kenay A, Weldegebreal F, Degefa M. Prevalence and Associated Factors of Nausea and Vomiting in Pregnancy among Pregnant Women in Hararghe Health and Demographic Surveillance System, Eastern Ethiopia: Haramaya university; 2021.

12. 12. Segni H, Ayana D, Jarso H. Prevalence of hyperemesis gravidarum and associated factors among pregnant women at Jimma University medical center, South West Ethiopia: a cross-sectional study. EC Gynaecol. 2016;3(5):376–87.

* View Article

* Google Scholar

13. 13. Kejela G, Getu S, Gebretsdik T, Wendimagegn T. Prevalence of Hyperemesis Gravidarum and Associated Factors in Arba Minch General Hospital, Gamo Gofa Zone, Southern Ethiopia. Clin Mother Child Health. 2018;15(10.4172):2090–7214.1000285.

* View Article

* Google Scholar

14. 14. Aminu MB, Alkali M, Audu BM, Abdulrazak T, Bathna D. Prevalence of hyperemesis gravidarum and associated risk factors among pregnant women in a tertiary health facility in Northeast, Nigeria. International Journal of Reproduction, Contraception, Obstetrics and Gynecology. 2020;9(9):2320–1770.

* View Article

* Google Scholar

15. 15. Cheng W, Li L, Long Z, Ma X, Chen F, Ma L, et al. Association between Dietary Patterns and the Risk of Hyperemesis Gravidarum. Nutrients. 2023;15(15):3300. pmid:37571237

* View Article

* PubMed/NCBI

* Google Scholar

16. 16. Fejzo MS, Ingles SA, Wilson M, Wanga W, MacGibbon K, Romero R, et al. High Prevalence of Severe Nausea and Vomiting of Pregnancy and Hyperemesis Gravidarum Among Relatives of Affected Individuals. Obstetrical & Gynecological Survey. 2009;64(3):148–9.

* View Article

* Google Scholar

17. 17. Lindstrom VS, Laitinen LM, Nurmi JMA, Koivisto MA, Polo-Kantola P. Hyperemesis gravidarum: Associations with personal and family history of nausea. Acta Obstet Gynecol Scand. 2023;102(9):1176–82. pmid:37431247

* View Article

* PubMed/NCBI

* Google Scholar

18. 18. Colodro-Conde L, Jern P, Johansson A, Sánchez-Romera JF, Lind PA, Painter JN, et al. Nausea and vomiting during pregnancy is highly heritable. Behavior genetics. 2016;46(4):481–91. pmid:26801654

* View Article

* PubMed/NCBI

* Google Scholar

19. 19. Solomon D, Morka G, Wayessa ZJ. Determinants of hyperemesis gravidarum among pregnant women in public hospitals of Guji, West Guji, and Borana zones, Oromia, Ethiopia. SAGE Open Medicine. 2022;11:1–11.

* View Article

* Google Scholar

20. 20. Nithiyasri P, Monika S, Leelashree T, Lokesh G, Priya DJ. Prevalance and Risk Factors of Hyperemesis Gravidarum: A Retrospective Study. Medico-legal Update. 2020;20(2):132–35.

* View Article

* Google Scholar

21. 21. Duarsa ABS, Widiyanto A, Arjita IPD, Atmojo JT, Anulus A, Putri SI, et al. Risk factors of Hyperemesis gravidarum: Meta-analysis from Retrospective cohort studies. Malaysian Journal of Public Health Medicine. 2022;22(3):296–309.

* View Article

* Google Scholar

22. 22. Thakur M, Gautam J, Dangal G. Severity of hyperemesis gravidarum and associated maternal factors. Journal of Nepal Health Research Council. 2019;17(3):293–6. pmid:31735920

* View Article

* PubMed/NCBI

* Google Scholar

23. 23. González Valdivia C. The gut microbiome and nausea in pregnancy. 2023.

* View Article

* Google Scholar

24. 24. Asrade L, Misikir D, Alemu H, Belachew A, Almaw H. Determinants of hyperemesis gravidarum among pregnant women attending antenatal care at public and private hospitals in Bahir Dar City, North-West Ethiopia, 2022: a multicenter unmatched case control study. BMC Womens Health. 2023;23(1):225. pmid:37138281

* View Article

* PubMed/NCBI

* Google Scholar

25. 25. Ashebir G, Nigussie H, Glagn M, Beyene K, Getie A. Determinants of hyperemesis gravidarum among pregnant women attending health care service in public hospitals of Southern Ethiopia. PLoS One. 2022;17(4):e0266054. pmid:35472152

* View Article

* PubMed/NCBI

* Google Scholar

26. 26. Tefera Z, Assefaw M. Determinants of Hyperemesis Gravidarum Among Pregnant Women in Public Hospitals of Mekelle City, North Ethiopia, 2019: Unmatched Case-Control Study. 2021.

27. 27. Oktaviani T. Association between Pregnant women’s Characteristics with Hyperemesis Gravidarum Event. Jurnal Asuhan Ibu dan Anak. 2023;8(1):29–36.

* View Article

* Google Scholar

28. 28. Nurfadillah W, Rosyidah R, Rinata E, Purwanti Y. Risk Factor of hyperemesis gravidarum incidence. Indonesian Journal of Nursing and Midwifery. 2023;11(2):116–26.

* View Article

* Google Scholar

29. 29. Tuzcuoğlu S, İnal HA, Soysal ME. The Prevalence of Helicobacter pylori in the Stools of Pregnant Women with Hyperemesis Gravidarum. The Anatolian Journal of Family Medicine. 2023;6(2):69–74.

* View Article

* Google Scholar

30. 30. Aleem NSA, El-Dakhakhni RA, Hazzaa SM, Aglaan NI, Borg HM. Comparative Study between Patients with Hyperemesis Gravidarum and Normal Pregnancy Regarding Presence of Helicobacter Pylori Antibodies. 2021.

* View Article

* Google Scholar

31. 31. Ayub JU, Qaisar A, Shah AZ, Amin S, Fayaz H, Khan UA. Association between H Pylori and Hyperemesis Gravidarum: A Cross Sectional Study. Journal of Saidu Medical College, Swat. 2023;13(2):67–71.

* View Article

* Google Scholar

32. 32. Zakaria AMM, Abdel Moneim M. The Association Between Helicobacter Pylori Seropositivity And Risk Of Hyperemesis Gravidarum During Pregnancy. Al-Azhar International Medical Journal. 2022;3(4):66–70.

* View Article

* Google Scholar

33. 33. Rasin BH, Aboud RS. Association between Hyperemesis Gravidarum in Iraqi Women with Helicobacter pylori Infection. The Egyptian Journal of Hospital Medicine. 2022;89(1):5653–9.

* View Article

* Google Scholar

34. 34. Yilikal A. Association of Helicobacter pylori infection and hyperemesis gravidarum women; a case control study in selected hospital and two health centers in Kirkos Sub-City, Addis Ababa, Ethiopia. Addis Ababa University, Addis Ababa, Ethiopia. 2017.

35. 35. Kitila KT, Sori LM, Desalegn DM, Tullu KD. Burden of Helicobacter pylori infections and associated risk factors among women of child bearing age in Addis Ababa, Ethiopia. International journal of chronic diseases. 2018;2018. pmid:30538998

* View Article

* PubMed/NCBI

* Google Scholar

36. 36. Nasr AA, Aboulfoutouh I, Nada A, Younan MA, Saed M, El-Khayat W. Is there an association between Helicobacter pylori infection and hyperemesis gravidarum among Egyptian women? Journal of Evidence-Based Women’s Health Journal Society. 2012;2(3):100–3.

* View Article

* Google Scholar

37. 37. Kjeldgaard HK, Eberhard-Gran M, Benth JŠ, Nordeng H, Vikanes ÅV. History of depression and risk of hyperemesis gravidarum: a population-based cohort study. Archives of women’s mental health. 2017;20(3):397–404. pmid:28064341

* View Article

* PubMed/NCBI

* Google Scholar

38. 38. Abdurke Kure M, Abdo Komicha M, Egata G. Magnitude of low birth weight and associated factors among women who gave birth in public hospitals of Harari Regional State, Eastern Ethiopia. J Women’s Health Care. 2021;10(534):2167–0420.21.

* View Article

* Google Scholar

39. 39. Mital TK, Waikar M. A cross-sectional and questionnaire-based study of prevalence of gastro-intestinal symptoms during pregnancy at tertiary care centre. International Journal of Clinical Obstetrics and Gynaecology. 2022;6.

* View Article

* Google Scholar

40. 40. Horasanlı JE, Şengül N. Examination of Placental Dysfunction and Neonatal Outcomes in Hospitalized Patients who have Hyperemesis Gravidarum Diagnosis. Journal of Contemporary Medicine. 2023;13(4):1–5.

* View Article

* Google Scholar

41. 41. Gabra A. Complications of hyperemesis gravidarum; a disease of both mother and fetus, review article. Crit Care Obst Gyne. 2018;5(1):1.

* View Article

* Google Scholar

42. 42. Mahato S, Shrestha A, Younjan S, Mahato A, Mahaseth A, Gautam R. Hyperemesis Gravidarum: fetal and maternal complications in a Tertiary Hospital in Nepal. International Journal of Public Health Asia Pacific. 2023.

* View Article

* Google Scholar

43. 43. Asi M, Aisa S, Usman AN. Eating habits and history of hyperemesis gravidarum as a risk factor of preeclampsia. Gaceta Sanitaria. 2021;35:S501–S5. pmid:34929886

* View Article

* PubMed/NCBI

* Google Scholar

44. 44. Fejzo MS, Poursharif B, Korst LM, Munch S, MacGibbon KW, Romero R, et al. Symptoms and pregnancy outcomes associated with extreme weight loss among women with hyperemesis gravidarum. Journal of women’s health. 2009;18(12):1981–7. pmid:20044860

* View Article

* PubMed/NCBI

* Google Scholar

45. 45. Mitchell-Jones N, Lawson K, Bobdiwala S, Farren JA, Tobias A, Bourne T, et al. Association between hyperemesis gravidarum and psychological symptoms, psychosocial outcomes and infant bonding: a two-point prospective case–control multicentre survey study in an inner city setting. BMJ open. 2020;10(10):e039715. pmid:33051235

* View Article

* PubMed/NCBI

* Google Scholar

46. 46. Nasir AHAA. Depression in hyperemesis gravidarum: Determinants and extent in Al-Nasiriyah, across sectional study. European Journal of Molecular & Clinical Medicine. 2020;7(1):35–43.

* View Article

* Google Scholar

47. 47. Hizli D, Kamalak Z, Kosus A, Kosus N, Kurt G. Hyperemesis gravidarum and depression in pregnancy: is there an association? Journal of Psychosomatic Obstetrics & Gynecology. 2012;33(4):171–5.

* View Article

* Google Scholar

48. 48. Kjeldgaard HK, Eberhard-Gran M, Benth JŠ, Vikanes ÅV. Hyperemesis gravidarum and the risk of emotional distress during and after pregnancy. Archives of women’s mental health. 2017;20:747–56. pmid:28842762

* View Article

* PubMed/NCBI

* Google Scholar

49. 49. Elgathafi A, Elharary F, Al Shawbaki M, Boubataina H. Prevalence & Risk Factors of Anxiety and Depression among Cases of Hyperemesis Gravidarum. The Scientific Journal of University of Benghazi. 2023;36(1).

* View Article

* Google Scholar

50. 50. Anshory VLS, Hasanah N, Ngo NF. Literature Review about the Relationship Between Psychology on the Hyperemesis Gravidarum Occurrence. Jurnal Sains dan Kesehatan. 2022;4(1):89–98.

* View Article

* Google Scholar

51. 51. Senturk MB, Yıldız G, Yıldız P, Yorguner N, Çakmak Y. The relationship between hyperemesis gravidarum and maternal psychiatric well-being during and after pregnancy: controlled study. The Journal of Maternal-Fetal & Neonatal Medicine. 2017;30(11):1314–9.

* View Article

* Google Scholar

52. 52. Yilmaz E, Yilmaz Z, Cakmak B, Karsli MF, Gultekin IB, Dogan NG, et al. Nausea and vomiting in early pregnancy of adolescents: relationship with depressive symptoms. Journal of pediatric and adolescent gynecology. 2016;29(1):65–8. pmid:26143555

* View Article

* PubMed/NCBI

* Google Scholar

53. 53. Heitmann K, Nordeng H, Havnen GC, Solheimsnes A, Holst L. The burden of nausea and vomiting during pregnancy: severe impacts on quality of life, daily life functioning and willingness to become pregnant again–results from a cross-sectional study. BMC pregnancy and childbirth. 2017;17(1):1–12.

* View Article

* Google Scholar

54. 54. Tahta T, Yilmaz FA. The Effect of Hyperemesis Gravidarum on Acceptance of Pregnancy and Quality of Life: A Comparative Study. Current Women’s Health Reviews. 2023;19(4):14–21.

* View Article

* Google Scholar

55. 55. Mullin P, Bray A, Vu V, Schoenberg-Paik F, MacGibbon K, Romero R, et al. Prenatal exposure to hyperemesis gravidarum linked to increased risk of psychological and behavioral disorders in adulthood. Journal of Developmental Origins of Health and Disease. 2012;3(5):375–9.

* View Article

* Google Scholar

56. 56. Fejzo MS, Schoenberg FP, Macgibbon K, Magtira A, Martin B, Mullin PM. Long-term health effects in children exposed in utero to hyperemesis gravidarum. Clin Obstet Gynecol Reprod Med. 2016;2(2):150–4.

* View Article

* Google Scholar

57. 57. Fejzo MS, Magtira A, Schoenberg FP, Macgibbon K, Mullin PM. Neurodevelopmental delay in children exposed in utero to hyperemesis gravidarum. European Journal of Obstetrics & Gynecology and Reproductive Biology. 2015;189:79–84.

* View Article

* Google Scholar

58. 58. Mullin PM, Ching C, Schoenberg F, MacGibbon K, Romero R, Goodwin TM, et al. Risk factors, treatments, and outcomes associated with prolonged hyperemesis gravidarum. The Journal of Maternal-Fetal & Neonatal Medicine. 2012;25(6):632–6.

* View Article

* Google Scholar

59. 59. Ayyavoo A, Derraik JG, Hofman PL, Biggs J, Bloomfield FH, Cormack BE, et al. Severe hyperemesis gravidarum is associated with reduced insulin sensitivity in the offspring in childhood. The Journal of Clinical Endocrinology & Metabolism. 2013;98(8):3263–8.

* View Article

* Google Scholar

60. 60. Vikanes Å, Skjærven R, Grjibovski AM, Gunnes N, Vangen S, Magnus P. Recurrence of hyperemesis gravidarum across generations: population based cohort study. Bmj. 2010;340. pmid:21030362

* View Article

* PubMed/NCBI

* Google Scholar

61. 61. Getahun D, Fassett MJ, Jacobsen SJ, Xiang AH, Takhar HS, Wing DA, et al. Autism spectrum disorders in children exposed in utero to hyperemesis gravidarum. American Journal of Perinatology. 2019;38(03):265–72. pmid:31581303

* View Article

* PubMed/NCBI

* Google Scholar

62. 62. Bello IS, Sonibare OO, Olajubu TO, Olajubu AO, Orji EO, Dean C. Assessment of the management of nausea and vomiting of pregnancy (NVP) by primary care providers in Nigerian primary care settings: A descriptive study. Journal of Interprofessional Education & Practice. 2022;27:100513.

* View Article

* Google Scholar

63. 63. Joshi A, Chadha G, Narayanan P. From Discomfort to Distress: A Critical Analysis of Hyperemesis Gravidarum in the Emergency Room. Cureus. 2023;15(8). pmid:37746494

* View Article

* PubMed/NCBI

* Google Scholar

64. 64. Nurmi M, Rautava P, Gissler M, Vahlberg T, Polo-Kantola P. Incidence and risk factors of hyperemesis gravidarum: A national register-based study in Finland, 2005–2017. Acta Obstet Gynecol Scand. 2020;99(8):1003–13.

* View Article

* Google Scholar

65. 65. Nurmi M. Hyperemesis gravidarum. Incidence, recurrence, hospitalizations, outpatient care and effect on family planning. 2022.

* View Article

* Google Scholar

66. 66. Mohammed Seid A, Mehari EA, Bekalu AF, Dula Sema F, Limenh LW, Geremew DT, et al. Prevalence of hyperemesis gravidarum and associated factors among pregnant women at comprehensive specialized hospitals in northwest Ethiopia: Multicenter cross-sectional study. SAGE Open Med. 2024;12:20503121241257163. pmid:38846512

* View Article

* PubMed/NCBI

* Google Scholar

67. 67. Pont S, Bond DM, Shand AW, Khan I, Zoega H, Nassar N. Risk factors and recurrence of hyperemesis gravidarum: A population-based record linkage cohort study. Acta Obstet Gynecol Scand. 2024. pmid:39258527

* View Article

* PubMed/NCBI

* Google Scholar

68. 68. Citrawati NK, Arwidiana DP. Characteristic description of emesis gravidarum case to pregnant woman in 1st trimester. Indonesian Journal of Global Health Research. 2023;5.

* View Article

* Google Scholar

69. 69. Tan PC, Tan NC, Omar SZ. Effect of high levels of human chorionic gonadotropin and estradiol on the severity of hyperemesis gravidarum. Clinical Chemistry and Laboratory Medicine. 2009;47(2):165–71. pmid:19191722

* View Article

* PubMed/NCBI

* Google Scholar

70. 70. Derbent AU, Yanik FF, Simavli S, Atasoy L, Urun E, EsraKuscu U, et al. First trimester maternal serum PAPP-A and free β-HCG levels in hyperemesis gravidarum. Prenatal Diagnosis. 2011 31:450–3.

* View Article

* Google Scholar

71. 71. Yıldız G, Mat E, Gündoğdu EC, Kurt D, Kuru B, Yıldız P, et al. Hyperemesis Gravidarum and Its Relationship with Placental Thickness, PAPP-A, and Free Beta-HCG: A Case–Control Study. South Clin Ist Euras. 2022;33:406–12.

* View Article

* Google Scholar

72. 72. Mansour GM, Nashaat EH. Role of Helicobacter pylori in the pathogenesis of hyperemesis gravidarum. Archives of Gynecology and Obstetrics. 2011;284(4):843–7. pmid:21079980

* View Article

* PubMed/NCBI

* Google Scholar

73. 73. Hussein KS. Hyperemesis Gravidarum in First-Trimester Pregnant Saudi Women: Is Helicobacter pylori a Risk Factor? Frontiers in Physiology. 2020;11. pmid:32676034

* View Article

* PubMed/NCBI

* Google Scholar

74. 74. London V, Grube S, Sherer DM, Abulafia O. Hyperemesis Gravidarum: A Review of Recent Literature. Pharmacology. 2017;100(3–4):161–71. pmid:28641304

* View Article

* PubMed/NCBI

* Google Scholar

75. 75. Verberg MFG, Gillott DJ, Al-Fardan N, Grudzinskas JG. Hyperemesis gravidarum, a literature review. Human Reproduction Update. 2005;11(5):527–39. pmid:16006438

* View Article

* PubMed/NCBI

* Google Scholar

Citation: Beyene GA, Ayele ND, Kasahun AW (2024) Prevalence and determinants of hyperemesis gravidarum among pregnant women in Ethiopia: A systematic review and meta-analysis. PLoS ONE 19(12): e0314783. https://doi.org/10.1371/journal.pone.0314783

About the Authors:

Girma Alemayehu Beyene

Roles: Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Software, Validation, Visualization, Writing – original draft, Writing – review & editing

E-mail: [email protected]

Affiliation: Department of Public Health, College of Medicine and Health Sciences, Wolkite University, Welkite, Ethiopia

ORICD: https://orcid.org/0000-0002-7184-4572

Nitsuh D. Ayele

Roles: Data curation, Formal analysis, Software, Validation, Visualization, Writing – original draft, Writing – review & editing

Affiliation: Department of Internal Medicine, College of Medicine and Health Sciences, Wolkite University, Welkite, Ethiopia

ORICD: https://orcid.org/0009-0000-0943-9616

Abebaw Wasie Kasahun

Roles: Conceptualization, Data curation, Formal analysis, Methodology, Software, Validation, Visualization, Writing – original draft, Writing – review & editing

Affiliation: Department of Public Health, College of Medicine and Health Sciences, Wolkite University, Welkite, Ethiopia

[/RAW_REF_TEXT]

[/RAW_REF_TEXT]

[/RAW_REF_TEXT]

References

1. Lowe S, Bowyer L, Beech A, Robinson H, Armstrong G, Marnoch C, et al. Guideline for the Management of Nausea and Vomiting in Pregnancy and Hyperemesis gravidarum. Society of Obstetric Medicine of Australia and New Zealand. 2019.

2. Maltepe C, Koren G. The management of nausea and vomiting of pregnancy and hyperemesis gravidarum-a 2013 update. Journal of Population Therapeutics and Clinical Pharmacology. 2013;20(2). pmid:23863612

3. Tian R, MacGibbon K, Martin B, Mullin P, Fejzo M. Analysis of pre-and post-pregnancy issues in women with hyperemesis gravidarum. Autonomic Neuroscience. 2017;202:73–8. pmid:27460690

4. Sobhi Ahmed A, Abd-Elhakeem Hasneen S, Ouda Abd-Elmoniem S, Abd-Elwahab Afifi O. Assessment of knowledge and practices of pregnant women regarding hyperemesis gravidarum. Journal of Nursing Science Benha University. 2022;3(1):445–59.

5. Kuma T, Yusuf L, Negash S. Assessment of nausea and vomiting of pregnancy on antenatal clients of Addis Ababa. Ethiopian Journal of Health Development. 2013;27(3):200–7.

6. Laitinen L. Nausea and Vomiting of Pregnancy—Studies with Pregnancy-Unique Quantification of Emesis Questionnaire. 2023.

7. Castillo MJ, Phillippi JC. Hyperemesis gravidarum: A Holistic Overview and Approach to Clinical Assessment and Management. The Journal of perinatal & neonatal nursing. 2015;29(1):12–22. pmid:25534678

8. Einarson TR, Piwko C, Koren G. Quantifying the global rates of nausea and vomiting of pregnancy: a meta-analysis. Journal of population therapeutics and clinical pharmacology. 2013;20(2). pmid:23863575

9. Fessehaye A, Abate D. Prevalence of Nausea and Vomiting of Pregnancy and its Associated Factors at Three Teaching Hospitals in Ethiopia. Annals Gynecol Obstet. 2021;5(1):133–7.

10. Adane KD, Zerga AA, Gebeyehu FB, Ayele FY. Proportion of hyperemesis gravidarum and associated factors among pregnant women admitted into the obstetrics ward at Akesta general hospital, North East Ethiopia. Plos one. 2023;18(2):e0281433. pmid:36745599

11. Gelmesa MO, Kenay A, Weldegebreal F, Degefa M. Prevalence and Associated Factors of Nausea and Vomiting in Pregnancy among Pregnant Women in Hararghe Health and Demographic Surveillance System, Eastern Ethiopia: Haramaya university; 2021.

12. Segni H, Ayana D, Jarso H. Prevalence of hyperemesis gravidarum and associated factors among pregnant women at Jimma University medical center, South West Ethiopia: a cross-sectional study. EC Gynaecol. 2016;3(5):376–87.

13. Kejela G, Getu S, Gebretsdik T, Wendimagegn T. Prevalence of Hyperemesis Gravidarum and Associated Factors in Arba Minch General Hospital, Gamo Gofa Zone, Southern Ethiopia. Clin Mother Child Health. 2018;15(10.4172):2090–7214.1000285.

14. Aminu MB, Alkali M, Audu BM, Abdulrazak T, Bathna D. Prevalence of hyperemesis gravidarum and associated risk factors among pregnant women in a tertiary health facility in Northeast, Nigeria. International Journal of Reproduction, Contraception, Obstetrics and Gynecology. 2020;9(9):2320–1770.

15. Cheng W, Li L, Long Z, Ma X, Chen F, Ma L, et al. Association between Dietary Patterns and the Risk of Hyperemesis Gravidarum. Nutrients. 2023;15(15):3300. pmid:37571237

16. Fejzo MS, Ingles SA, Wilson M, Wanga W, MacGibbon K, Romero R, et al. High Prevalence of Severe Nausea and Vomiting of Pregnancy and Hyperemesis Gravidarum Among Relatives of Affected Individuals. Obstetrical & Gynecological Survey. 2009;64(3):148–9.

17. Lindstrom VS, Laitinen LM, Nurmi JMA, Koivisto MA, Polo-Kantola P. Hyperemesis gravidarum: Associations with personal and family history of nausea. Acta Obstet Gynecol Scand. 2023;102(9):1176–82. pmid:37431247

18. Colodro-Conde L, Jern P, Johansson A, Sánchez-Romera JF, Lind PA, Painter JN, et al. Nausea and vomiting during pregnancy is highly heritable. Behavior genetics. 2016;46(4):481–91. pmid:26801654

19. Solomon D, Morka G, Wayessa ZJ. Determinants of hyperemesis gravidarum among pregnant women in public hospitals of Guji, West Guji, and Borana zones, Oromia, Ethiopia. SAGE Open Medicine. 2022;11:1–11.

20. Nithiyasri P, Monika S, Leelashree T, Lokesh G, Priya DJ. Prevalance and Risk Factors of Hyperemesis Gravidarum: A Retrospective Study. Medico-legal Update. 2020;20(2):132–35.

21. Duarsa ABS, Widiyanto A, Arjita IPD, Atmojo JT, Anulus A, Putri SI, et al. Risk factors of Hyperemesis gravidarum: Meta-analysis from Retrospective cohort studies. Malaysian Journal of Public Health Medicine. 2022;22(3):296–309.

22. Thakur M, Gautam J, Dangal G. Severity of hyperemesis gravidarum and associated maternal factors. Journal of Nepal Health Research Council. 2019;17(3):293–6. pmid:31735920

23. González Valdivia C. The gut microbiome and nausea in pregnancy. 2023.

24. Asrade L, Misikir D, Alemu H, Belachew A, Almaw H. Determinants of hyperemesis gravidarum among pregnant women attending antenatal care at public and private hospitals in Bahir Dar City, North-West Ethiopia, 2022: a multicenter unmatched case control study. BMC Womens Health. 2023;23(1):225. pmid:37138281

25. Ashebir G, Nigussie H, Glagn M, Beyene K, Getie A. Determinants of hyperemesis gravidarum among pregnant women attending health care service in public hospitals of Southern Ethiopia. PLoS One. 2022;17(4):e0266054. pmid:35472152

26. Tefera Z, Assefaw M. Determinants of Hyperemesis Gravidarum Among Pregnant Women in Public Hospitals of Mekelle City, North Ethiopia, 2019: Unmatched Case-Control Study. 2021.

27. Oktaviani T. Association between Pregnant women’s Characteristics with Hyperemesis Gravidarum Event. Jurnal Asuhan Ibu dan Anak. 2023;8(1):29–36.

28. Nurfadillah W, Rosyidah R, Rinata E, Purwanti Y. Risk Factor of hyperemesis gravidarum incidence. Indonesian Journal of Nursing and Midwifery. 2023;11(2):116–26.

29. Tuzcuoğlu S, İnal HA, Soysal ME. The Prevalence of Helicobacter pylori in the Stools of Pregnant Women with Hyperemesis Gravidarum. The Anatolian Journal of Family Medicine. 2023;6(2):69–74.

30. Aleem NSA, El-Dakhakhni RA, Hazzaa SM, Aglaan NI, Borg HM. Comparative Study between Patients with Hyperemesis Gravidarum and Normal Pregnancy Regarding Presence of Helicobacter Pylori Antibodies. 2021.

31. Ayub JU, Qaisar A, Shah AZ, Amin S, Fayaz H, Khan UA. Association between H Pylori and Hyperemesis Gravidarum: A Cross Sectional Study. Journal of Saidu Medical College, Swat. 2023;13(2):67–71.

32. Zakaria AMM, Abdel Moneim M. The Association Between Helicobacter Pylori Seropositivity And Risk Of Hyperemesis Gravidarum During Pregnancy. Al-Azhar International Medical Journal. 2022;3(4):66–70.

33. Rasin BH, Aboud RS. Association between Hyperemesis Gravidarum in Iraqi Women with Helicobacter pylori Infection. The Egyptian Journal of Hospital Medicine. 2022;89(1):5653–9.

34. Yilikal A. Association of Helicobacter pylori infection and hyperemesis gravidarum women; a case control study in selected hospital and two health centers in Kirkos Sub-City, Addis Ababa, Ethiopia. Addis Ababa University, Addis Ababa, Ethiopia. 2017.

35. Kitila KT, Sori LM, Desalegn DM, Tullu KD. Burden of Helicobacter pylori infections and associated risk factors among women of child bearing age in Addis Ababa, Ethiopia. International journal of chronic diseases. 2018;2018. pmid:30538998

36. Nasr AA, Aboulfoutouh I, Nada A, Younan MA, Saed M, El-Khayat W. Is there an association between Helicobacter pylori infection and hyperemesis gravidarum among Egyptian women? Journal of Evidence-Based Women’s Health Journal Society. 2012;2(3):100–3.

37. Kjeldgaard HK, Eberhard-Gran M, Benth JŠ, Nordeng H, Vikanes ÅV. History of depression and risk of hyperemesis gravidarum: a population-based cohort study. Archives of women’s mental health. 2017;20(3):397–404. pmid:28064341

38. Abdurke Kure M, Abdo Komicha M, Egata G. Magnitude of low birth weight and associated factors among women who gave birth in public hospitals of Harari Regional State, Eastern Ethiopia. J Women’s Health Care. 2021;10(534):2167–0420.21.

39. Mital TK, Waikar M. A cross-sectional and questionnaire-based study of prevalence of gastro-intestinal symptoms during pregnancy at tertiary care centre. International Journal of Clinical Obstetrics and Gynaecology. 2022;6.

40. Horasanlı JE, Şengül N. Examination of Placental Dysfunction and Neonatal Outcomes in Hospitalized Patients who have Hyperemesis Gravidarum Diagnosis. Journal of Contemporary Medicine. 2023;13(4):1–5.

41. Gabra A. Complications of hyperemesis gravidarum; a disease of both mother and fetus, review article. Crit Care Obst Gyne. 2018;5(1):1.

42. Mahato S, Shrestha A, Younjan S, Mahato A, Mahaseth A, Gautam R. Hyperemesis Gravidarum: fetal and maternal complications in a Tertiary Hospital in Nepal. International Journal of Public Health Asia Pacific. 2023.

43. Asi M, Aisa S, Usman AN. Eating habits and history of hyperemesis gravidarum as a risk factor of preeclampsia. Gaceta Sanitaria. 2021;35:S501–S5. pmid:34929886

44. Fejzo MS, Poursharif B, Korst LM, Munch S, MacGibbon KW, Romero R, et al. Symptoms and pregnancy outcomes associated with extreme weight loss among women with hyperemesis gravidarum. Journal of women’s health. 2009;18(12):1981–7. pmid:20044860

45. Mitchell-Jones N, Lawson K, Bobdiwala S, Farren JA, Tobias A, Bourne T, et al. Association between hyperemesis gravidarum and psychological symptoms, psychosocial outcomes and infant bonding: a two-point prospective case–control multicentre survey study in an inner city setting. BMJ open. 2020;10(10):e039715. pmid:33051235

46. Nasir AHAA. Depression in hyperemesis gravidarum: Determinants and extent in Al-Nasiriyah, across sectional study. European Journal of Molecular & Clinical Medicine. 2020;7(1):35–43.

47. Hizli D, Kamalak Z, Kosus A, Kosus N, Kurt G. Hyperemesis gravidarum and depression in pregnancy: is there an association? Journal of Psychosomatic Obstetrics & Gynecology. 2012;33(4):171–5.

48. Kjeldgaard HK, Eberhard-Gran M, Benth JŠ, Vikanes ÅV. Hyperemesis gravidarum and the risk of emotional distress during and after pregnancy. Archives of women’s mental health. 2017;20:747–56. pmid:28842762

49. Elgathafi A, Elharary F, Al Shawbaki M, Boubataina H. Prevalence & Risk Factors of Anxiety and Depression among Cases of Hyperemesis Gravidarum. The Scientific Journal of University of Benghazi. 2023;36(1).

50. Anshory VLS, Hasanah N, Ngo NF. Literature Review about the Relationship Between Psychology on the Hyperemesis Gravidarum Occurrence. Jurnal Sains dan Kesehatan. 2022;4(1):89–98.

51. Senturk MB, Yıldız G, Yıldız P, Yorguner N, Çakmak Y. The relationship between hyperemesis gravidarum and maternal psychiatric well-being during and after pregnancy: controlled study. The Journal of Maternal-Fetal & Neonatal Medicine. 2017;30(11):1314–9.

52. Yilmaz E, Yilmaz Z, Cakmak B, Karsli MF, Gultekin IB, Dogan NG, et al. Nausea and vomiting in early pregnancy of adolescents: relationship with depressive symptoms. Journal of pediatric and adolescent gynecology. 2016;29(1):65–8. pmid:26143555

53. Heitmann K, Nordeng H, Havnen GC, Solheimsnes A, Holst L. The burden of nausea and vomiting during pregnancy: severe impacts on quality of life, daily life functioning and willingness to become pregnant again–results from a cross-sectional study. BMC pregnancy and childbirth. 2017;17(1):1–12.

54. Tahta T, Yilmaz FA. The Effect of Hyperemesis Gravidarum on Acceptance of Pregnancy and Quality of Life: A Comparative Study. Current Women’s Health Reviews. 2023;19(4):14–21.

55. Mullin P, Bray A, Vu V, Schoenberg-Paik F, MacGibbon K, Romero R, et al. Prenatal exposure to hyperemesis gravidarum linked to increased risk of psychological and behavioral disorders in adulthood. Journal of Developmental Origins of Health and Disease. 2012;3(5):375–9.

56. Fejzo MS, Schoenberg FP, Macgibbon K, Magtira A, Martin B, Mullin PM. Long-term health effects in children exposed in utero to hyperemesis gravidarum. Clin Obstet Gynecol Reprod Med. 2016;2(2):150–4.

57. Fejzo MS, Magtira A, Schoenberg FP, Macgibbon K, Mullin PM. Neurodevelopmental delay in children exposed in utero to hyperemesis gravidarum. European Journal of Obstetrics & Gynecology and Reproductive Biology. 2015;189:79–84.

58. Mullin PM, Ching C, Schoenberg F, MacGibbon K, Romero R, Goodwin TM, et al. Risk factors, treatments, and outcomes associated with prolonged hyperemesis gravidarum. The Journal of Maternal-Fetal & Neonatal Medicine. 2012;25(6):632–6.

59. Ayyavoo A, Derraik JG, Hofman PL, Biggs J, Bloomfield FH, Cormack BE, et al. Severe hyperemesis gravidarum is associated with reduced insulin sensitivity in the offspring in childhood. The Journal of Clinical Endocrinology & Metabolism. 2013;98(8):3263–8.

60. Vikanes Å, Skjærven R, Grjibovski AM, Gunnes N, Vangen S, Magnus P. Recurrence of hyperemesis gravidarum across generations: population based cohort study. Bmj. 2010;340. pmid:21030362

61. Getahun D, Fassett MJ, Jacobsen SJ, Xiang AH, Takhar HS, Wing DA, et al. Autism spectrum disorders in children exposed in utero to hyperemesis gravidarum. American Journal of Perinatology. 2019;38(03):265–72. pmid:31581303

62. Bello IS, Sonibare OO, Olajubu TO, Olajubu AO, Orji EO, Dean C. Assessment of the management of nausea and vomiting of pregnancy (NVP) by primary care providers in Nigerian primary care settings: A descriptive study. Journal of Interprofessional Education & Practice. 2022;27:100513.

63. Joshi A, Chadha G, Narayanan P. From Discomfort to Distress: A Critical Analysis of Hyperemesis Gravidarum in the Emergency Room. Cureus. 2023;15(8). pmid:37746494

64. Nurmi M, Rautava P, Gissler M, Vahlberg T, Polo-Kantola P. Incidence and risk factors of hyperemesis gravidarum: A national register-based study in Finland, 2005–2017. Acta Obstet Gynecol Scand. 2020;99(8):1003–13.

65. Nurmi M. Hyperemesis gravidarum. Incidence, recurrence, hospitalizations, outpatient care and effect on family planning. 2022.

66. Mohammed Seid A, Mehari EA, Bekalu AF, Dula Sema F, Limenh LW, Geremew DT, et al. Prevalence of hyperemesis gravidarum and associated factors among pregnant women at comprehensive specialized hospitals in northwest Ethiopia: Multicenter cross-sectional study. SAGE Open Med. 2024;12:20503121241257163. pmid:38846512

67. Pont S, Bond DM, Shand AW, Khan I, Zoega H, Nassar N. Risk factors and recurrence of hyperemesis gravidarum: A population-based record linkage cohort study. Acta Obstet Gynecol Scand. 2024. pmid:39258527

68. Citrawati NK, Arwidiana DP. Characteristic description of emesis gravidarum case to pregnant woman in 1st trimester. Indonesian Journal of Global Health Research. 2023;5.

69. Tan PC, Tan NC, Omar SZ. Effect of high levels of human chorionic gonadotropin and estradiol on the severity of hyperemesis gravidarum. Clinical Chemistry and Laboratory Medicine. 2009;47(2):165–71. pmid:19191722

70. Derbent AU, Yanik FF, Simavli S, Atasoy L, Urun E, EsraKuscu U, et al. First trimester maternal serum PAPP-A and free β-HCG levels in hyperemesis gravidarum. Prenatal Diagnosis. 2011 31:450–3.

71. Yıldız G, Mat E, Gündoğdu EC, Kurt D, Kuru B, Yıldız P, et al. Hyperemesis Gravidarum and Its Relationship with Placental Thickness, PAPP-A, and Free Beta-HCG: A Case–Control Study. South Clin Ist Euras. 2022;33:406–12.

72. Mansour GM, Nashaat EH. Role of Helicobacter pylori in the pathogenesis of hyperemesis gravidarum. Archives of Gynecology and Obstetrics. 2011;284(4):843–7. pmid:21079980

73. Hussein KS. Hyperemesis Gravidarum in First-Trimester Pregnant Saudi Women: Is Helicobacter pylori a Risk Factor? Frontiers in Physiology. 2020;11. pmid:32676034

74. London V, Grube S, Sherer DM, Abulafia O. Hyperemesis Gravidarum: A Review of Recent Literature. Pharmacology. 2017;100(3–4):161–71. pmid:28641304

75. Verberg MFG, Gillott DJ, Al-Fardan N, Grudzinskas JG. Hyperemesis gravidarum, a literature review. Human Reproduction Update. 2005;11(5):527–39. pmid:16006438