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Seroprevalence of hantavirus infection in non-epidemic settings over four decades: a systematic review and meta-analysis

BMC Public Health volume 24, Article number: 2553 (2024) Cite this article

Abstract

Introduction

Hantavirus infection is a zoonotic disease from rodents to humans, necessitating seroprevalence assessment for disease burden clarification and control measure implementation. This study aimed to estimate global hantaviruses seroprevalence, examining variations by regions, populations or settings.

Methods

A comprehensive database search identified studies on human hantaviruses seroprevalence using IgG detection until january 2024. A random-effects meta-analysis estimated pooled seroprevalence, with subgroup analyses for geographical region, population, setting or occupation.

Results

Out of 3,382 abstracts reviewed, 110 studies were selected, comprising 81,815 observations and 3207 events. The global seroprevalence was calculated at 2.93% (2.34%-3.67%). In terms of geographical distribution, our analysis encompassed 61 studies from the Americas, where the seroprevalence was estimated at 2.43% (95% CI: 1.71%—3.46%), 33 studies from Europe indicating a seroprevalence of 2.98% (95% CI: 2.19%—4.06%), 10 studies from Asia revealing a seroprevalence of 6.84% (95% CI: 3.64%—12.50%), and 6 studies from Africa demonstrating a seroprevalence of 2.21% (95% CI: 1.82%—2.71%). Subgroup analysis underscored varying seroprevalence rates across different populations, settings, and occupations, highlighting the necessity for targeted interventions and preventive measures.

Conclusion

The analysis reveals a moderate global hantaviruses seroprevalence, emphasizing the viral family's complex transmission dynamics influenced by exposure and geographical factors. This highlights the need for targeted prevention and control strategies.

Peer Review reports

Introduction

Hantaviruses are negative stranded, tripartite RNA viruses belonging to a genus within the Bunyaviridae family. The natural reservoirs of pathogenic hantaviruses are certain rodents, in which chronic and asymptomatic infection occurs [1,2,3]. Hantaviruses are commonly transmitted from rodents to humans, mainly through inhalation of aerosols contaminated with feces, urine, or saliva of infected mice. The distribution of hantaviruses is solely dependent on the ecology of its reservoir. Therefore, if the distribution of virus-carrying rodents is known, the occurrence of human cases can be predicted [4,5,6,7,8]. A systematic review by Toledo et al. [9] has explored the evidence for human-to-human transmission of hantaviruses, particularly focusing on the Andes virus (ANDV). This review examines 22 studies and concludes that, while there is limited evidence supporting human-to-human transmission, it remains a possibility under certain conditions [9].

Human hantavirus infection can manifest in various clinical syndromes. In the Old World, severe hantavirus infections commonly manifest as hemorrhagic fever with renal syndrome with mortality rates ranging from 0.1% to 15%, whereas the New World species, such as ANDV, cause cardiopulmonary syndrome with a mortality rate of 40%. Furthermore, it was demonstrated that ANDV, a New World species, can be transmitted person to person. While assessments of occupational and environmental risks for hantavirus exposure have been carried out in certain regions, a critical gap remains in conducting a broader and more comprehensive evaluation of seroprevalence across diverse populations, occupational sectors, and environmental contexts [10,11,12,13,14,15].

Research on the overall seroprevalence of hantavirus infection in humans and the assessment of associated risk factors are pivotal in advancing our understanding of disease transmission dynamics. In this study, we conducted a comprehensive systematic review and meta-analysis to assess the global prevalence of hantaviruses antibodies in the human population. Understanding the dynamics of this disease is crucial for implementing effective measures against it. Seroprevalence data offer valuable insights into transmission patterns and prevalence rates, thereby guiding preventive strategies. By elucidating the extent of hantavirus exposure across diverse populations, our aim is to contribute to a deeper understanding of this infectious disease and facilitate the development of targeted preventive measures. Furthermore, we have explored the prevalence of these antibodies across various geographic regions, and in individuals with distinct population, occupation or setting [16, 17].

Methods

Systematic review and meta-analysis

We conducted this systematic review in accordance with the Meta-analysis of Observational Studies in Epidemiology (MOOSE) guidelines for systematic reviews of observational studies [18] and reported following PRISMA guidelines (Appendix 1). We registered the protocol in PROSPERO (CRD42022339202). Furthermore, we used an adaptation of the classic research PICO question framework for prevalence studies proposed by Munn et al [19].

Eligibility criteria and study selection

We included studies that tested hantaviruses specific IgG antibodies and reported seroprevalence in a sample of individuals. To comprehensively evaluate seroprevalence among asymptomatic individuals under typical circumstances, we deliberately omitted studies conducted during epidemic outbreaks and excluded symptomatic patients from our analysis. We did not impose restrictions on language or study design.

At least two of the authors (FT, GC, FP, and LL) independently and in pairs assessed articles during each screening stage, first by title and abstract and subsequently by full text. We resolved disagreements through discussion.

Search strategies

We searched MEDLINE, Embase, Cochrane Central Register of Controlled Trials (CENTRAL) in the Cochrane Library, Virtual Health Library, Epistemonikos, Scielo up to January 2, 2024. In addition, we screened the references of all included studies and contacted authors for information when necessary. A description of the search strategy is reported in Appendix 1.

Data extraction and management

Four reviewers (FT, GC, FP, and LL) independently and in duplicate, extracted study characteristics and information from the included studies using a standardized data extraction template. We resolved discrepancies through consensus.

Outcomes

The primary outcome of interest was the seroprevalence of hantavirus IgG-specific antibodies for specific hantavirus types across different regions and subpopulations. We selected studies employing ELISA for detecting hantaviruses IgG antibodies. Additionally, any diagnostic method assessing the presence of IgG against hantaviruses was recorded, including confirmatory methods such as IFA (Indirect Immunofluorescence Assay) or Western Blot.

Statistical analysis

We obtained the seropositivity prevalence estimate and variance (e.g., standard deviation) from each study. We then combined the results from all studies using meta-analysis to obtain a weighted mean. To pool and compare prevalence data, we used the inverse variance method (Dersimonian-Laird) [20,21,22]. Additionally, we performed a common effects model analysis in parallel, and both models were presented in the forest plots. We carried out subgroup analysis based on geographical region (Europe, America, Asia and Africa), and different population, occupation or setting categories. We presented the results in tables and graphically in forest plots [23,24,25]. We conducted all analyses using R programming language version 4.1.0 (R Core Team, 2021) and the RStudio integrated development environment version 2023.03.0 + 386 "Cherry Blossom" Release for Windows RStudio.

Risk of bias

Four reviewers (FT, GC, FP, and LL) independently and in pairs assessed the quality of the studies using the Risk of Bias in Prevalence Studies tool according to the RoB-SPEO guidelines. The assessment included a thorough review of study selection, measurement, comparability, and exposure-related aspects. Any differences in evaluation were resolved through consensus [26].

Certainty of the evidence

The evaluation of the certainty of evidence concerning prevalence across various populations, settings, and occupations in numerous studies was performed using the GRADE approach. This was augmented by the QoE-SPEO tool, specifically adapted for studies that assess exposure. This method evaluates various domains, including risk of bias, indirectness, inconsistency, imprecision, and publication bias. Summary of findings tables were generated, and the certainty of evidence was categorized as high, moderate, low, or very low based on the evaluation of each domain. Further details on the assessment of certainty of evidence are provided in Appendix 1 [27,28,29].

Results

Characteristics of included studies

The selection process for the studies is detailed in Fig. 1. We included a total of 110 studies [30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56,57,58,59,60,61,62,63,64,65,66,67,68,69,70,71,72,73,74,75,76,77,78,79,80,81,82,83,84,85,86,87,88,89,90,91,92,93,94,95,96,97,98,99,100,101,102,103,104,105,106,107,108,109,110,111,112,113,114,115,116,117,118,119,120,121,122,123,124,125,126,127,128,129,130,131,132,133,134,135,136,137,138,139,140], collectively reporting 81,815 observations, of which 3,207 events were recorded (positive IgG determinations). The global seroprevalence estimated across these studies was 3.88% (95% CI: 3.75% to 4.01%). The characteristics of the included can be observed in Table 1. Excluded studies with reasons can be observed in Appendix 1, Table of excluded studies.

Table 1 Characteristics of included studies
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Fig. 1
figure 1

PRISMA Flow Diagram

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Risk of bias of included studies

Despite the absence of confirmatory tests in many cases due to potential antibody cross-reactivity, we evaluated the body of evidence for seroprevalence as having a low risk of bias. Our assessment is based on the uniform application of testing methods across the majority of studies, which supports the reliability of the seroprevalence rates reported. Although most of the studies included likely had a high risk of misclassification and incomplete exposure data bias, we did not evaluate exposure risk nor assess it as an infection risk in the rest of the manuscript. Therefore, for the purposes of evaluating seroprevalence, this was not considered a high risk of bias. (See further details in Appendix 1: Table of Risk of Bias).

Regional seroprevalence stratified by population, setting and occupation

The seroprevalence results for each population or scenario, as well as the corresponding certainty in the estimated seroprevalence values, are presented in Table 2.

Table 2 Summary of findings table
Full size table

For the Americas, exploration into subgroups revealed varying seroprevalence rates across 61 studies and 33,156 observations. The overall prevalence was estimated at 2.43% (95% CI: 1.70%—3.46%) with high certainty (⨁⨁⨁⨁). Forestry workers exhibited a prevalence of 3.14% (95% CI: 1.15%—8.32%) with moderate certainty (⨁⨁⨁ ⊖) across 8 studies, the general population showed 2.39% (95% CI: 1.56%—3.65%) with high certainty (⨁⨁⨁⨁) across 29 studies, while Indigenous peoples and the rural population had rates of 3.77% (95% CI: 0.97%—13.59%) with very low certainty (⨁ ⊖  ⊖ ⊖) and 2.93% (2.34%-3.67) with moderate certainty (⨁⨁⨁ ⊖) respectively. Healthcare workers exhibited a lower prevalence of 0.54% (95% CI: 0.11%—2.57%) with low certainty (⨁⨁ ⊖ ⊖) based on data from 4 studies, and people exposed to rodents at work exhibited a prevalence of 0.86% (95% CI: 0.13%—5.33%) with low certainty (⨁⨁ ⊖ ⊖) across 5 studies (Fig. 2).

Fig. 2
figure 2

Forest plot, Subgroups by Geographical Region and population, setting or occupation: Americas

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In Europe, 33 studies were reviewed, with data from 40820 individuals, revealing a seroprevalence proportion of 2.98% (95% CI: 2.19%—4.06%) with high certainty (⨁⨁⨁⨁). Forestry workers exhibited a prevalence of 4.22% (95% CI: 3.35%—5.30%) with high certainty (⨁⨁⨁⨁) across 4 studies, while the rural population showed a prevalence of 7.00% (95% CI: 2.40%—18.76%) with low certainty (⨁⨁ ⊖ ⊖) across 2 studies. The general population demonstrated a prevalence of 2.70% (95% CI: 1.70%—4.28%) with high certainty (⨁⨁⨁⨁) across 14 studies. Individuals exposed to rodents at work exhibited a prevalence of 3.35% (95% CI: 1.64%—6.73%) with moderate certainty (⨁⨁⨁ ⊖) across 8 studies (Fig. 3).

Fig. 3
figure 3

Forest plot, Subgroups by Geographical Region and population, setting or occupation: Europe

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For Asia, 10 studies were analyzed, involving a total of 3219 patients, showing a seroprevalence proportion of 6.84% (95% CI: 3.64%—12.50%) with moderate certainty (⨁⨁ ⊖ ⊖). Subgroup analysis indicated diverse seroprevalence rates: among people exposed to rodents at work, the prevalence was 5.17% (95% CI: 1.99%—12.79%) with low certainty (⨁ ⊖  ⊖ ⊖) across 6 studies, while the general population exhibited a higher prevalence of 10.12% (95% CI: 5.66%—17.44%) with low certainty (⨁ ⊖  ⊖ ⊖) across 4 studies (Fig. 4).

Fig. 4
figure 4

Forest plot, Subgroups by Geographical Region and population, setting or occupation: Asia

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Lastly, for Africa, 6 studies were identified, comprising data from a total of 5253 patients, with a seroprevalence proportion of 2.21% (95% CI: 1.82%—2.71%) with high certainty (⨁⨁⨁⨁). Subgroup analysis revealed varying seroprevalence rates: among individuals with chronic kidney disease, the prevalence was notably higher at 9.89% (95% CI: 5.23%—17.93%) with low certainty (⨁ ⊖  ⊖ ⊖) based on data from one study. In contrast, the general population exhibited a lower prevalence of 1.83% (95% CI: 1.32%—2.53%) with high certainty (⨁⨁⨁⨁) across six studies (Fig. 5).

Fig. 5
figure 5

Forest plot, Subgroups by Geographical Region and population, setting or occupation: Africa

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Other analysis

Although we performed a subgroup analysis by viral species, these results, presented in Appendix 1 were evaluated using the ICEMAN tool [141] and were found not to be credible in terms of the subgroup effect.

Discussion

This systematic review offers valuable insights into the seroprevalence of hantavirus infections worldwide. The range of observed seroprevalence in multiple and varied regions around the globe was from 2.43% to 6.84%. The presence of these viruses across the world, even in areas where clinical cases are rare, suggests that widespread exposure has occurred globally, with many individuals likely coming into contact with the virus without developing severe illness [142, 143]. While occasional reports mention oligo symptomatic or asymptomatic illness among patients, the certainty regarding the existence of asymptomatic infections, particularly concerning hantaviruses species that induce hantavirus pulmonary syndrome, remains insufficiently established [108]. Furthermore, it is possible that unidentified hantaviruses species or groups circulating in rodent, shrew, bat, and other zoonotic reservoir populations may result in clinically insignificant asymptomatic infections, explaining some of the background seropositivity [144, 145].

Our results support the notion that rural populations, especially indigenous communities, are at a greater risk of coming into contact with these viruses. Clear examples include the Americas, where rural settings have a higher exposure risk compared to the general population, and Europe, where non-healthcare-related occupational risk surpasses that observed for the general population. Additionally, in Asia, distinct occupational categories reveal varying levels of seroprevalence, with some groups, like tribal members involved in rodent trapping, showing higher seroprevalence rates [3, 13, 15, 16].

On the other hand, healthcare workers, who are generally less exposed to rodents, consistently showed lower seroprevalence rates, further reinforcing the hypothesis that rodent contact remains the primary transmission route [9,10,11,12,13,14,15,16,17].

Our study also reinforces the understanding that hantavirus transmission primarily occurs through contact with rodents in interface areas between urban and rural environments, rather than through direct human-to-human transmission. This conclusion is based on the observation that occupations and residential areas with greater exposure to rodents, such as rural and indigenous communities, showed higher seroprevalence compared to other groups. Although less common, evidence of human to human transmission also exist, particularly in areas where Andes virus (ANDV) is endemic [146, 147]. For example, studies conducted in Chile and Argentina have documented probable cases of human-to-human transmission of ANDV, especially in close household contacts, such as sexual partners [146, 147]. These studies, though limited in number and with some methodological constraints, highlight that while most human contacts did not result in infections, there were instances where human-to-human transmission was likely.

The limitations of the present study highlight the geographic constraints of the available data. In particular, data from Africa and Asia are notably sparse, and even within the Americas and Europe, certain regions—such as the Caribbean—are underrepresented, with only two studies included. Additionally, the small number of studies and the high degree of variability significantly limit the interpretability of the subgroup analyses.

To our knowledge, this is the first systematic review to assess the global seroprevalence of hantaviruses. We conducted a comprehensive search and employed state-of-the-art methods for evidence synthesis and analysis. Our findings reveal a moderate global hantavirus seroprevalence, underscoring the complex transmission dynamics influenced by exposure and geographical factors. These results highlight the need for targeted prevention and control strategies.

Availability of data and materials

All data generated or analyzed during this study are publicly available in the Figshare repository under DOI: https://doi.org/10.6084/m9.figshare.26946898. This includes the datasets that underlie Figs. 1, 2, 3, 4, 5, Tables 1 and 2, and supplementary figures. The repository ensures long-term access and citation, allowing for further research and verification of the study's claims. Data are shared in compliance with relevant ethical standards and in line with repository best practices for transparency and accessibility.

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Funding

This work was supported by the Universidad de Río Negro. No additional external funding was received.

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Authors and Affiliations

  1. Carrera de Medicina, Universidad Nacional de Rio Negro, Rio Negro, Argentina

    Fernando Tortosa, Celia Tognetti, Gabriela Carrasco & German Guaresti

  2. Castro Rendón Hospital, Neuquen, Argentina

    Fernando Perre

  3. “Ramon Carrillo” Hospital, Bariloche, Rio Negro, Rio Negro, Argentina

    Lucia Lossetti, Ayelén Iglesias & Yesica Espasandin

  4. Universidad del Salvador, Buenos Aires, Argentina

    Ariel Izcovich

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F.T.: Conceived the study, led the research design and coordination, and substantively revised the manuscript. Also responsible for final approval of the version to be published. F.P.: Contributed to data acquisition and analysis, and assisted in drafting the manuscript. C.T.: Played a key role in the interpretation of data and critically revised the manuscript for important intellectual content. L.L.: Assisted with data collection and analysis and contributed to the drafting of the manuscript. G.C.: Involved in the data analysis and interpretation, provided critical revisions to the manuscript. G.G.: Contributed to the conception and design of the work, helped in the drafting and revision of the manuscript. A.I. and Y.E.: Both contributed equally to the acquisition and analysis of data and to drafting parts of the manuscript related to their expertise. A.I.: Oversaw the methodology, was involved in the critical revision of the manuscript for key intellectual content, and approved the final version to be published.

All authors agreed to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. All authors have read and agreed to the published version of the manuscript.

Author Consent Declaration:All listed authors have actively participated in the conception and design of this study, or analysis and interpretation of data, and/or have been involved in the drafting or revising of the manuscript critically for important intellectual content. Each author has provided explicit consent to submit the manuscript in its current form and has approved the final version to be published.

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Correspondence to Fernando Tortosa.

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As this study involves secondary data and does not include direct involvement of human participants, the requirement for ethics approval is not applicable.

Given that this study is a systematic review using secondary data, there were no direct human participants involved. Human Ethics and Consent to Participate declarations: not applicable.

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Tortosa, F., Perre, F., Tognetti, C. et al. Seroprevalence of hantavirus infection in non-epidemic settings over four decades: a systematic review and meta-analysis. BMC Public Health 24, 2553 (2024). https://doi.org/10.1186/s12889-024-20014-w

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Keywords

BMC Public Health

ISSN: 1471-2458

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