Advertisement
  • Loading metrics

Systematic review and meta-analysis of the epidemiology of Lassa virus in humans, rodents and other mammals in sub-Saharan Africa

  • Sebastien Kenmoe,

    Roles Conceptualization, Data curation, Formal analysis, Methodology, Project administration, Supervision, Validation, Writing – original draft, Writing – review & editing

    Affiliation Department of Virology, Centre Pasteur of Cameroon, Yaoundé, Cameroon

  • Serges Tchatchouang,

    Roles Data curation, Methodology, Writing – review & editing

    Affiliation Department of Virology, Centre Pasteur of Cameroon, Yaoundé, Cameroon

  • Jean Thierry Ebogo-Belobo,

    Roles Data curation, Methodology, Writing – review & editing

    Affiliation Medical Research Centre, Institut of Medical Research and Medicinal Plants Studies, Yaoundé, Cameroon

  • Aude Christelle Ka'e,

    Roles Data curation, Methodology, Writing – review & editing

    Affiliation Virology Department, Chantal Biya International Reference Centre, Yaoundé, Cameroon

  • Gadji Mahamat,

    Roles Data curation, Methodology, Writing – review & editing

    Affiliation Department of Microbiology, Faculty of Science, The University of Yaounde I, Yaoundé, Cameroon

  • Raïssa Estelle Guiamdjo Simo,

    Roles Data curation, Methodology, Writing – review & editing

    Affiliation Department of Microbiology, Faculty of Science, The University of Yaounde I, Yaoundé, Cameroon

  • Arnol Bowo-Ngandji,

    Roles Data curation, Methodology, Writing – review & editing

    Affiliation Department of Microbiology, Faculty of Science, The University of Yaounde I, Yaoundé, Cameroon

  • Cynthia Paola Demeni Emoh,

    Roles Data curation, Methodology, Writing – review & editing

    Affiliation Department of Microbiology, Faculty of Science, The University of Yaounde I, Yaoundé, Cameroon

  • Emmanuel Che,

    Roles Data curation, Methodology, Writing – review & editing

    Affiliation Vaccinology and Biobank, Chantal Biya International Reference Centre, Yaounde, Cameroon

  • Dimitri Tchami Ngongang,

    Roles Data curation, Methodology, Writing – review & editing

    Affiliation Department of Microbiology, Faculty of Science, The University of Yaounde I, Yaoundé, Cameroon

  • Marie Amougou-Atsama,

    Roles Data curation, Methodology, Writing – review & editing

    Affiliations Department of Virology, Centre Pasteur of Cameroon, Yaoundé, Cameroon, Medical Research Centre, Institut of Medical Research and Medicinal Plants Studies, Yaoundé, Cameroon

  • Nathalie Diane Nzukui,

    Roles Data curation, Methodology, Writing – review & editing

    Affiliation School of Health Sciences-Catholic University of Central Africa, Department of Medical Microbiology, Yaoundé, Cameroon

  • Chris Andre Mbongue Mikangue,

    Roles Data curation, Methodology, Writing – review & editing

    Affiliation Department of Microbiology, Faculty of Science, The University of Yaounde I, Yaoundé, Cameroon

  • Donatien Serge Mbaga,

    Roles Data curation, Methodology, Writing – review & editing

    Affiliation Department of Microbiology, Faculty of Science, The University of Yaounde I, Yaoundé, Cameroon

  • Sorel Kenfack,

    Roles Data curation, Methodology, Writing – review & editing

    Affiliation Department of Microbiology, Faculty of Science, The University of Yaounde I, Yaoundé, Cameroon

  • Sandrine Rachel Kingue Bebey,

    Roles Data curation, Methodology, Writing – review & editing

    Affiliation Department of Microbiology, Faculty of Science, The University of Yaounde I, Yaoundé, Cameroon

  • Nathalie Amvongo Adjia,

    Roles Data curation, Methodology, Writing – review & editing

    Affiliation Medical Research Centre, Institut of Medical Research and Medicinal Plants Studies, Yaoundé, Cameroon

  • Atembeh Noura Efietngab,

    Roles Data curation, Methodology, Writing – review & editing

    Affiliation Medical Research Centre, Institut of Medical Research and Medicinal Plants Studies, Yaoundé, Cameroon

  • Hervé Raoul Tazokong,

    Roles Data curation, Methodology, Writing – review & editing

    Affiliation Department of Microbiology, Faculty of Science, The University of Yaounde I, Yaoundé, Cameroon

  • Abdou Fatawou Modiyinji,

    Roles Data curation, Methodology, Writing – review & editing

    Affiliations Department of Virology, Centre Pasteur of Cameroon, Yaoundé, Cameroon, Department of Animals Biology and Physiology, Faculty of Science, The University of Yaoundé I, Yaoundé, Cameroon

  • Cyprien Kengne-Nde,

    Roles Data curation, Formal analysis, Methodology, Writing – review & editing

    Affiliation Epidemiological Surveillance, Evaluation and Research Unit, National AIDS Control Committee, Yaoundé, Cameroon

  • Serge Alain Sadeuh-Mba,

    Roles Methodology, Writing – review & editing

    Affiliation Department of Virology, Centre Pasteur of Cameroon, Yaoundé, Cameroon

  •  [ ... ],
  • Richard Njouom

    Roles Conceptualization, Project administration, Supervision, Writing – review & editing

    njouom@pasteur-yaounde.org, njouom@yahoo.com

    Affiliation Department of Virology, Centre Pasteur of Cameroon, Yaoundé, Cameroon

  • [ view all ]
  • [ view less ]

Systematic review and meta-analysis of the epidemiology of Lassa virus in humans, rodents and other mammals in sub-Saharan Africa

  • Sebastien Kenmoe, 
  • Serges Tchatchouang, 
  • Jean Thierry Ebogo-Belobo, 
  • Aude Christelle Ka'e, 
  • Gadji Mahamat, 
  • Raïssa Estelle Guiamdjo Simo, 
  • Arnol Bowo-Ngandji, 
  • Cynthia Paola Demeni Emoh, 
  • Emmanuel Che, 
  • Dimitri Tchami Ngongang
PLOS
x

Abstract

Accurate data on the Lassa virus (LASV) human case fatality rate (CFR) and the prevalence of LASV in humans, rodents and other mammals are needed for better planning of actions that will ultimately reduce the burden of LASV infection in sub-Saharan Africa. In this systematic review with meta-analysis, we searched PubMed, Scopus, Africa Journal Online, and African Index Medicus from 1969 to 2020 to obtain studies that reported enough data to calculate LASV infection CFR or prevalence. Study selection, data extraction, and risk of bias assessment were conducted independently. We extracted all measures of current, recent, and past infections with LASV. Prevalence and CFR estimates were pooled using a random-effect meta-analysis. Factors associated with CFR, prevalence, and sources of between-study heterogeneity were determined using subgroup and metaregression analyses. This review was registered with PROSPERO, CRD42020166465. We initially identified 1,399 records and finally retained 109 reports that contributed to 291 prevalence records from 25 countries. The overall CFR was 29.7% (22.3–37.5) in humans. Pooled prevalence of LASV infection was 8.7% (95% confidence interval: 6.8–10.8) in humans, 3.2% (1.9–4.6) in rodents, and 0.7% (0.0–2.3) in other mammals. Subgroup and metaregression analyses revealed a substantial statistical heterogeneity explained by higher prevalence in tissue organs, in case-control, in hospital outbreak, and surveys, in retrospective studies, in urban and hospital setting, in hospitalized patients, and in West African countries. This study suggests that LASV infections is an important cause of death in humans and that LASV are common in humans, rodents and other mammals in sub-Saharan Africa. These estimates highlight disparities between sub-regions, and population risk profiles. Western Africa, and specific key populations were identified as having higher LASV CFR and prevalence, hence, deserving more attention for cost-effective preventive interventions.

Author summary

Lassa virus (LASV) infection constitutes a major public health threat as it has a direct impact on the mortality of febrile patients, healthcare workers, pregnant women, visitors of endemic countries with a consequential negative impact on national and individual economies. It is necessary to have accurate epidemiological data on LASV infection, in order to prioritize the policies, funding for public health interventions, and health-care planning, especially in sub-Saharan Africa (SSA). Data concerning virus occurrence in rodents and other mammal species can also assist in guiding control of Lassa fever from an ecological perspective. This could include preventive measures such as the protection of food fields by anti-rodent barriers, the protection of rodent predatory fauna, the sanitation of home and particularly the food storage place and the blocking of rodent access to home and food stored. Our systematic review and meta-analysis of LASV infection in SSA has contemporarily and comprehensively summarized the prevalence of current, recent, and past infection both in humans, rodents and other mammals. Broadly, the study showed relatively high CFR estimates in humans. Additionally, Western Africa presented the highest burden of LASV infections compared to other regions. This study emphasized various populations of SSA with relatively high burden of LASV infection. We have identified specific populations at high risk of LASV infection, who may urgently benefit from routine screening, detection and management programmes. Beyond, preventive strategies should be promoted, by educating and raising people’s awareness about LASV infection, and strengthening practitioners’ capacities towards adequate diagnosis and proper management of this infection in SSA.

Introduction

At least 75% of emerging and re-emerging infectious diseases have an animal origin [1]. Lassa virus (LASV) is a zoonotic re-emerging pathogen and a member of the family Arenaviridae and the genus Mammarenaviruses (viruses that infect mammals). The main natural reservoir of LASV is the rodent Mastomys natalensis that lives in proximity with humans [24]. A recent study showed that up to 37.7 million people in 14 countries in sub-Saharan Africa (SSA), particularly in West Africa, were living in areas that were prone to LASV zoonotic transmission, because of the presence of rodent reservoirs in these countries [5]. The LASV is also found in other rodents and mammals species in the West Africa [6]. This presence of LASV in non-reservoirs could however represent transient or spillover infections [7]. Humans are infected either by direct contact with infected tissues, urine or excrement of rodents or indirectly through vectors such as cereals dried on the ground. Lassa virus is also transmitted from human to human by direct contact with secretions or infected blood, especially in hospitals with relatively high case fatality rates [8,9].

The LASV was isolated for the first time from two missionary nurses in the city of Lassa in north-eastern Nigeria in 1969 [10]. It is estimated that Lassa fever is responsible for 2 million infections annually in West Africa [11]. A systematic review has shown that 21 Lassa fever outbreaks recorded in Nigeria from 1969 to 2017 have been associated with approximately 6,000 suspected cases, 800 confirmed cases and nearly 700 deaths [12]. These epidemics of Lassa fever pose a constant problem in health facilities with nosocomial transmissions to health care workers and visitors of infected cases [8]. Another recent review reported 33 patients with imported cases of LASV returning from 7 West African countries and 9 other countries between 1969 and 2016 [13]. A total of 39% (12/31) of the patients with known outcomes were deceased. Lassa fever virus is listed among the WHO priority diseases in need of urgent research and development efforts and it is classified as a category “A” bioterrorism agent that can serve as biological weapons [14].

Lassa virus infection includes a wide variety of clinical presentations resulting in mild or severe forms that require medical attention and often lead to death. Asymptomatic infections also seem common. The early phase of Lassa fever is indistinguishable from other common febrile syndromes such as malaria, typhoid fever or haemorrhagic fevers caused by other viruses. Laboratory-based surveillance programs are essential for the prevention, management and control of outbreaks of LASV infections [15]. Early diagnosis and treatment are associated with better outcomes for patients with LASV [16]. Molecular assays are widely used in reference laboratories for LASV diagnosis [15,17]. However, there are still many challenges to the laboratory diagnosis of LASV including the wide diversity of LASV strains and sequences, the low sensitivity and specificity of immunoassays, and the low number of approved rapid diagnostic tests. Furthermore, there is also a possibility of cross-reaction between LASV and other Arenaviruses strains. Although promising results have been reported in the preclinical phase of the vaccine development [18], there are currently no approved vaccines against LASV infection [19]. The management of LASV fever patients is primarily mainly based on alleviating symptoms. However, encouraging results have been obtained with the administration of ribavirin in the initial phase (first week) of the disease [16].

It is recognized that the fight against zoonotic diseases can be done ideally according to the One Health approach [20]. To this end, epidemiological data from zoonotic viruses such as LASV in humans and animals are crucial in guiding common responses to this health threat. Furthermore, a recent study reported that the detection rate of the LASV in asymptomatic individuals and the identification of populations at high risk were at crucial importance [21]. We explored both the case fatality rate of the LASV in various category of human populations and the prevalence of LASV in humans, rodents and others mammals. This is important information that can inform priorities in focussing prevention efforts. Data concerning virus occurrence in rodents and other mammal species can also assist in guiding control of Lassa fever from an ecological perspective.

Methods

Design and inclusion criteria

The preferred reporting items for systematic reviews and meta–analyses (PRISMA) checklist was used for the design of this systematic review (S1 Table) [22]. This review was published to Prospero under the identification CRD42020166465. Inclusion criteria were met for studies including subjects of all ages and gender with any illness, apparently healthy individuals, rodents or other mammals. The LASV clinical case definitions present a wide variability on multiple factors such as the definition of fever, other symptoms considered, non-response to treatment for other febrile illnesses endemic in sub-Saharan Africa, past contact with confirmed, suspect or probable cases of LASV patients or rodents and the organisation considered for guidelines. We therefore categorized the types of participants according to the inclusion criteria of the included studies. We classified the other mammals according to the highest level listed in the included articles and in agreement with the mammal classification proposed by Wilson and Reeder in 2005 [23]. Studies reporting the prevalence of LASV (virus, antigen, RNA, IgM and/or IgG) or data to calculate this estimate were included. Lassa virus prevalence was determined using any detection assays including indirect immunofluorescence, complement fixation, culture, Reverse Transcription Polymerase Chain Reaction (RT-PCR) or Enzyme Linked Immunosorbent Assay (ELISA). We selected studies conducted in SSA, as defined by the United Nations Statistics Division (UNSD), that represent the habitat of Mastomys natalensis, natural hosts of LASV [5]. All study types published in peer-reviewed journals, observational or interventional, providing cross-sectional records on the prevalence of one or more LASV markers were included. We used a conceptual definition for the included study designs, considering surveys and surveillance as a cross-sectional study. Given that epidemic context is usually associated with high prevalences, we presented epidemics as community outbreak and hospital outbreak. Studies reporting imported case data, case reports, reports, reviews, systematic reviews and meta-analyses, comments and duplicate were excluded.

Data sources and search strategy

A comprehensive search strategy designed to allow exhaustive identification of relevant studies was applied to the Pubmed, Scopus, African Journals Online, and African Index Medicus databases. Databases were consulted from 1969 to 2020 for studies published in English and French languages. The electronic search strategy was adapted to each database. S2 Table displays the details of the search strategy applied in the Pubmed database. The list of references from the included studies and other relevant articles were manually screened for other relevant studies.

Selection and extraction of data from included studies

Duplicates identified from the complete list of studies were removed. The titles and abstracts of the eligible studies were independently examined by two study authors (SK and JTEB) for the selection of relevant studies. The differing opinions of the investigators regarding the selection of the studies were resolved by discussion, consensus and intervention of a third arbitrator if necessary. Data from the included studies was extracted using a google form by 18 study authors and verified by SK. The extracted data were the name of the first author, the year of publication, the study design, the inclusion criteria (ill, apparently healthy, rodent or other mammals), country, sampling method, study period, LASV detection assay, LASV detection marker (virus, antigen, RNA, IgM or IgG), type of sample used for LASV detection, age and gender of study participants, sample size, number of positive for LASV, and number of deaths within LASV positive. Disagreements observed during data extraction were resolved by discussion and consensus.

Study definitions

Studies performed in several hospitals or cities were defined as multicentric and those in a single hospital or city were defined as monocentric. We grouped the countries in accordance with the breakdown of the UNSD [24]. We considered studies that performed analysis on acute and convalescent samples in order to give a diagnosis of the infection by the rise in the IgG antibody titer. Past infections were considered for articles with unspecified antibodies or IgG positive subjects. Recent infections, contact lasting up to 12 months, were considered for articles with IgM or IgM and IgG positive subjects. Current infections were considered for studies with antigen, RNA, virus positives or subjects with an increase in antibody titer between acute and convalescent samples. People with regular contacts with any animal were defined as high risk individuals. We assumed the data of the various population categories from the same article as several individual prevalences.

Evaluation of the quality of studies and synthesis of data

The quality of the included studies was independently assessed by all study authors using a dedicated scale for prevalence studies that is based on 10 components divided into two groups: internal and external validity of the study (S3 Table) [25]. The scores of 0 or 1 were assigned to each question in the assessment tool for a total score of 10 per study. The scores of 0–3, 4–6 and 7–10 represented a high, moderate and low risk of bias, respectively. The disagreements were resolved by discussion and consensus. The R version 3.6.0 software (package "meta" and "metafor") through the RStudio interface was used to perform all meta-analyses [26,27]. Heterogeneity between studies was estimated by the Cochran Q test, and the I2 and the H statistics [28]. Studies were considered to lack of evidence on heterogeneity if the p value for Q test was greater than 0.05. The I2 value was indicative of the degree of heterogeneity with values ​​of 0%, 18%, 45%, and 75% considered for none, low, moderate and high heterogeneity respectively [29]. H values ​​close to 1 indicated lack of evidence on heterogeneity between studies and these values ​​were inversely correlated with degree of heterogeneity. Prevalence, 95% confidence intervals (95% CI), and prediction intervals were estimated by random effect models (DerSimonian-Laird method) [30]. The instability of the variance and the problem of the 95% CIs excluded from the range 0 to 1 were solved by the Freeman-Tukey double arcsine stabilization. Potential reasons for heterogeneity were investigated by subgroup and metaregression analyses by study design, the sampling method, the timing of data collection, the country, the UNSD region, the setting, the hospitalization, and the sample types. The dependent variable was the LASV prevalence or case fatality rate. We considered only dependent variables with at least 3 studies divided into two or more categories of the independent variables in subgroup analyses and metaregression. The independent variables were evaluated in both a univariate and a multivariate metaregression model (if p <0.2 in the univariate model). The statistical significance threshold was 0.05 in multivariate meta-regression analysis. The publication bias was assessed by visual inspection of the asymmetry of the funnel plot and the Egger test with the value of p <0.1 indicating a potential bias [31]. As cross-sectional studies are best for prevalence studies [32], a sensitivity analysis that included only low-risk of bias and cross-sectional studies was performed.

Results

Literature search

A total of 1,399 articles were identified by electronic search in the databases and 178 duplicates eliminated (Fig 1 and S4 Table). A group of 1,014 were eliminated after examination of the titles and abstracts, leaving a total of 207 articles to be examined completely. Of the 207 articles examined completely, 109 (291 prevalence records) met the inclusion criteria, including 159 in humans, 116 in rodents, and 16 in other mammals [24,6,8,9,33135].

Study quality assessment

The majority of articles in humans had a moderate risk of bias (112/159; 70.4%), followed by studies with a low risk of bias (46/159; 28.9%), and a high risk of bias (1/159; 0.6%). All articles in rodents and other mammals had a moderate risk of bias (S5 Table). No study was representative of the population of a country, no study described the rate of non-respondents and only 16 performed probabilistic sampling approach.

Characteristics of studies included in meta-analysis.

Twenty-five countries in SSA were represented in this review. Most of the prevalence records were from West Africa (86.6%; 252/291) and more particularly in Nigeria (31.3%; 91/291) (S6 Table). Study participants were recruited between 1965 and 2019. Two hundred and fifty-eight (88.6%; 258/291) prevalence records were cross-sectional, 106 (36.4%) were rural, 192 (66.0%) were community based, 99 (34.0%) had tested for antibodies by indirect immunofluorescence, 225 (77.3%), and had tested for LASV in serum alone. Fifty-seven prevalence records (35.9%; 57/159) focused on apparently healthy individuals and 13 (11.2%; 13/116) on Mastomys natalensis rodents. Only 23 of the human included studies gave a LASV suspected or probable case definition of the recruited participants. Individual data from included studies are presented in the S7 Table.

Meta-analysis

The included studies in this review recruited 114,848 participants, including 91,275 humans, 21,891 rodents, and 1,348 other mammals.

Case fatality rate of Lassa virus infections in humans.

A total of 3063 participants recruited from 20 studies conducted in West Africa gave an overall fatality rate of 29.6% (95% CI; 22.3–37.5) (Fig 2) [8,34,37,47,49,52,53,65,70,75,87,89,100,101,109,116,117,120,123,132]. All categories of participants with common, recent or old infections had relatively high case fatality rates ranging from 9.1 to 46.7%. We obtained decreasing case fatality records from participants with current LASV infections in LASV suspected cases 34.7% (95% CI; 25.0–45.1), pregnant women 27.0% (95% CI; 12.9–43.9), febrile patients 22.1% (95% CI; 9.4–37.7), and patients with haemorrhagic symptoms 13.2% (95% CI; 0.0–53.4).

thumbnail
Fig 2. Human case fatality rate due to Lassa virus in sub-Saharan Africa.

https://doi.org/10.1371/journal.pntd.0008589.g002

Prevalence of Lassa virus infections in humans

A total of 88,212 participants enrolled in 82 studies gave an overall prevalence of LASV of 8.7% (95% CI; 6.8–10.8) (Figs 3 and S1) [8,9,3446,4850,52,53,5661,6567,6770,7284,8789,9197,99,100,105108,110,113,115123,126130,132136]. Regardless of the type of infection; current, recent or past, LASV suspected cases and febrile patients had the highest prevalence. In studies with participants with evidence of LASV current infection, healthcare workers (11.1%) had high prevalence. In studies with participants with evidence of LASV recent infection, apparently healthy individuals (12.6%) had high prevalence. In studies with participants with evidence of previous LASV infection patients with any disease (16.9%) had high prevalence. Apart from West Africa where current and recent LASV infections have been recorded, only past infections evidence has been recorded in other regions of SSA including Central Africa (Cameroon, Central African Republic, Guinea Equatorial, Republic of Congo and Democratic Republic of Congo), Eastern Africa (Zimbabwe and Uganda) and Northern Africa (Sudan).

thumbnail
Fig 3. Prevalence of Lassa virus infections in humans in sub-Saharan Africa.

https://doi.org/10.1371/journal.pntd.0008589.g003

Prevalence of Lassa virus infections in rodents

A total of 21,891 rodents trapped in 29 studies gave an overall prevalence of LASV of 3.2% (95% CI; 2.0–4.6) (Figs 4 and S2) [24,6,33,43,45,49,51,54,55,6264,69,85,86,90,94,102104,111,112,114,124,125,129,130]. Besides the Mastomys species, more particularly Mastomys natalensis, many other rodent species had evidence of current or previous contacts with LASV. In one study, the species Hylomyscus pamfi showed the highest prevalence of current contact at 41.7% [6]. In terms of current and past contacts, Mus species have also shown relatively high prevalence of LASV [3,63,103,125]. Lemniscomys striatus, Rattus rattus, and Praomys species also had relatively high evidence of previous contact with LASV [63,103].

thumbnail
Fig 4. Prevalence of Lassa virus infections in rodents in sub-Saharan Africa.

*Negative rodents include Gerbilliscus species, Lemniscomys species, Praomys daltoni, Praomys species, Rattus rattus, Uranomys ruddi, Nannomys minutoides/mattheyi, Myomys daltoni, Praomys rostratus, Lemniscomys striatus, Praomys cf. rostratus, Crocodura species, Lophuromys sikapusi, Tatera cf. guinea, Gerbilliscus kempi, Praomys jacksoni, Mus setulosus, and Mus minutoides. #Negative rodents include Gerbilliscus kempi, Mus setulosus, Praomys jacksoni, Lemniscomys bellieri/zebra, Uranomys ruddi, Crocidura buettikoferi, Gerbilliscus guineae, Lophuromys sikapusi, and Mus mattheyi.

https://doi.org/10.1371/journal.pntd.0008589.g004

Prevalence of Lassa virus infections in other mammals

A total of 1645 other mammals recruited in 8 studies gave an overall prevalence of LASV of 0.7% (95% CI; 0.0–2.3) (Fig 5) [4,49,68,71,77,81,98,103]. Only primates, carnivora and Eulipotyphla showed evidence of current or previous contact with LASV [68,71,98,103].

thumbnail
Fig 5. Prevalence of Lassa virus infections in other mammals in sub-Saharan Africa.

https://doi.org/10.1371/journal.pntd.0008589.g005

Sensitivity, heterogeneity and publication bias analysis

The overall case fatality rate in humans and the overall prevalence of LASV in humans, rodents and other mammals were similar to those estimated for cross-sectional and low risk of bias studies for the vast majority of categories (Table 1). The differences were mainly observed in the categories of febrile patients. Most study categories in rodents and other mammals had a small number of studies (<5 studies) and did not allow an objective estimate of heterogeneity. Substantial heterogeneity was recorded in the remaining included human, rodent and other mammal studies. In agreement with the funnel plot symmetry and the Egger test p value, there was no publication bias in case fatality rate in humans (p-value Egger test = 0.510), LASV prevalence in humans (p-value Egger test = 0.715), and LASV prevalence in other mammals (p-value Egger test = 0.647) analyses and evidence of publication bias in LASV prevalence in rodents (p-value Egger test = 0.045) analyses (S3S6 Figs).

thumbnail
Table 1. Summary of meta-analysis results for prevalence of Lassa virus in humans, rodents, and other mammals in sub-Saharan Africa.

https://doi.org/10.1371/journal.pntd.0008589.t001

Subgroup analysis and metaregression

All LASV deaths have been recorded only in West Africa including Nigeria, Guinea, and Sierra Leone (Fig 6) [34,37,47,53,65,70,120,123]. Only the case fatality rate category in LASV suspected cases fulfilled the conditions for subgroup analyses (at least 3 studies divided into two or more categories). The case fatality rate was significantly higher in studies on community outbreak (p = 0.036), with a retrospective design (p = 0.018) [47,53,89,101,116,117], conducted in rural areas (p <0.001) [53], and in the community (p = 0.039) (S8 Table) [47]. S9 Table displayed the results of the meta-regression analysis. The final model of the case fatality rate in current LASV infection suspected cases explained 32.5% of the heterogeneity. In this model only retrospective studies presented significantly high case fatality rates (p = 0.002).

The LASV prevalence in current infections in humans was statistically higher in hospitalized febrile patients (p = 0.001), in febrile patients in Liberia and Sierra Leone (p <0.001), in febrile patients in urban areas (p = 0.049) and in LASV suspected cases in rural areas (p = 0.048), and in case-control studies for LASV suspected cases (p <0.001). In febrile patients, the final meta-regression model explained 0% heterogeneity for the prevalence of the current LASV infection. Case control and hospital/community-based studies showed the highest prevalence.

The LASV seroprevalence in recent infections in humans was statistically higher in Sierra Leone in apparently healthy individuals (p <0.001) and in LASV suspected cases (p <0.001), in urban areas in apparently healthy individuals (p = 0.015), and in case-control studies in febrile patients (p = 0.036). In apparently healthy individuals, the final meta-regression model explained 60.3% heterogeneity for the seroprevalence of recent LASV infection and Sierra Leone had the highest prevalence.

The seroprevalence of LASV in past infections in humans was statistically higher in West African countries including Guinea, Sierra Leone, Nigeria, Mali, Ivory Coast, in context urban, especially in apparently healthy individuals/ patients with any disease and LASV suspected cases. In apparently healthy individuals, the final meta-regression model explained 75.9% heterogeneity for the seroprevalence of past LASV infection. West Africa and hospital/community-based studies showed the highest prevalences. In febrile patients, the final meta-regression model explained 54.1% heterogeneity for the seroprevalence of past LASV infection. Non-probabilistic and West Africa studies showed the highest prevalences. In LASV suspected cases, the final meta-regression model explained 99.0% heterogeneity for the seroprevalence of past LASV infection and studies conducted in urban setting showed the highest prevalences. In patients with any disease, the final meta-regression model explained 100% heterogeneity for the seroprevalence of past LASV infection and studies conducted in hospitals showed the highest prevalences. In patients with diseases other than fever, the final meta-regression model explained 100% heterogeneity for the seroprevalence of past LASV infection and studies conducted in West Africa showed the highest prevalences.

The LASV prevalence in current infections in Mastomys species was statistically higher in West African countries (p <0.001) including Guinea and Sierra Leone and in spleen samples (p = 0.004). In the Mastomys species, the final meta-regression model explained 100% heterogeneity for the prevalence of the current LASV infection and the studies conducted in Sierra Leone presented the highest prevalences.

The LASV seroprevalence in past infections in Mastomys natalensis was statistically higher in Nigeria (p = 0.001). In Mastomys natalensis, the final meta-regression model explained 82.0% heterogeneity for the prevalence of the current LASV infection and the studies conducted in Guinea showed the highest prevalences.

thumbnail
Fig 6. Lassa virus case fatality rate in humans and Lassa virus prevalence in humans, rodents, and other mammals in sub-Saharan Africa, 1970–2020.

LASV: Lassa virus prevalence; Past contacts denote articles with unspecified antibodies or IgG positive subjects. Recent contacts denote articles with IgM or IgM and IgG positive subjects. Current contacts denote studies with antigen, RNA, virus positives or subjects with an increase in antibody titer between acute and convalescent samples. Current, recent and past contacts are indicated by shades of red, blue and green respectively. Lines 1, 2, 3, 4 and 5 indicate the LASV case fatality rate in humans, the prevalence of LASV in humans, Mastomys natalensis, non-Mastomys natalensis rodents and other mammals respectively.

https://doi.org/10.1371/journal.pntd.0008589.g006

Discussion

Our study presents the most comprehensive records to date on the LASV human case fatality rate and LASV prevalence in humans, rodents, and other mammals. We estimated an overall LASV case fatality rate of around 30% and a LASV prevalence around 10%, 3%, and 1% in humans, rodents, and other mammals respectively. The prevalence of LASV infections was higher in West African region, in LASV suspect cases, febrile patients, patients with haemorrhagic symptoms, healthcare workers, apparently healthy patients, and patient with any diseases. In addition to Mastomys natalensis, the main reservoir of LASV [137], this study clarifies the LASV current contact estimated mainly by RT-PCR and culture assays in Hylomyscus pamfi, Mus baoulei, Mastomys erythroleucus, and Mus (Nannomys) species. In the present work, the primates have shown evidence of LASV antigen and antibodies. Carnivora and Eulipotyphla have shown evidence of past contact with LASV through antibody detection.

This relatively high overall case fatality rate of around 30% due to LASV infections is surprising in this era of availability of antivirals such as ribavirin which have been shown to be effective in the early phase of LASV infections in individuals with of elevated aspartate aminotransferase [138]. The case fatality rate of 27.1% observed in pregnant women in this study is comparable to that of a recent meta-analysis which also included this same population [139]. This meta-analysis had however included studies with pregnant women with suspected or probable LASV infections [140,141]. Patients who died with past LASV infections presented in this work may be those IgM and/or IgG positive in the early stage of infection rather than sequelae of mortality from an old infection. Indeed, it has been shown that IgM is produced from the 4th day and rarely persists beyond one month in LASV infections [142144]. Immunoglobulin G appear around the 8th day after the onset of symptoms and persist longer. Although reported in only two studies, compared to other subgroups, it was surprising to record a relatively low case fatality rate of 13,2% among participants with haemorrhagic symptoms, since bleeding is known as a predictor of bad outcomes in viral haemorrhagic symptoms [145]. This could be explained by several factors including the management and the treatment delay implemented in these studies with patients with haemorrhagic symptoms.

The various stakeholders in human and animal health should make concerted efforts to fight LASV. This fight should not be limited to healthcare professionals, but should also include funding agencies, politicians, citizens and all relevant stakeholders. This study shows that studies using direct methods of detecting LASV have been conducted only in West Africa. Thus, additional research using direct detection assays for current LASV infections are needed outside West Africa where past and recent LASV infections have been reported. On human side, Lassa fever should be taken into account in the differential diagnosis of febrile illnesses across West Africa in addition to the common febrile illnesses such as malaria, typhoid fever and dengue. This study highlights the need to educate people in SSA about the signs and symptoms of Lassa fever and to keep dwellings safe from rodents by creating adequate food storage spaces. All LASV infections in healthcare workers could have been reduced or avoided through actions such as 1) educating healthcare workers about Lassa fever guidelines and the risk of infection during their activity, 2) strengthening the use of personal protective equipment; and 3) training in the adequate use of personal protective equipment. Findings from this study point out the need to establish LASV laboratory-based surveillance programs across West Africa. The construction of well-equipped laboratories and research centre would help to quickly diagnose and treat Lassa fever. To this end, the development of a simple rapid diagnostic test would be of great added value for the diagnosis of patients. Additional research on viral factors (viral load, genotype), biomarkers, clinical and socio-demographic factors associated with mortality from the LASV is necessary. We identified a single study with LASV prevalence record among pregnant women. This suggests an urgent need to provide more data on the proportion of pregnant women with LASV infections. This study clearly demonstrates that LASV is a highly lethal pathogen, so the paradox of infections recorded in apparently asymptomatic individuals remains to be elucidated in particular their role in the transmission chain of LASV infection.

The results of this study suggest that apart from Mastomys natalensis, other rodent species may be involved in the LASV transmission. Most IgG-positive results detected in small mammals outside the LASV-endemic zone beyond West Africa during this study are probably signatures of the several arenaviruses other than Lassa that continue to be described across sub Saharan Africa of late. Nevertheless, these results are equally crucial for portrayal in a manuscript like this; as these arenaviruses are related by varying degrees to LASV and their epidemiological significance needs to be further understood. An effort should be directed towards the sequencing and phylogenetic characterization of the LASV strains identified. The promotion of research on the development of vaccines in rodents or other mammals sensitive to LASV which can subsequently be adapted for human vaccination is necessary. There should be a recognition of LASV surveillance in rodents and other mammals to better control the risk of human infection.

Most of the included studies used the Josiah strain as an antigen for the detection of antibodies in serological methods. Due to the great variability of LASV, however, it may have antibodies that do not recognize the Josiah antigen. This suggests the possibility of having false negative results in some included studies. There is a high probability of cross-reactions between Arenavirus species [146,147]. Although plaque reduction neutralisation test which is the most specific assay in serological detection has been used to assess result in 19 included studies, the potential cross reactions associated with other serological methods suggests the possibility of false positive results in some studies included. Another important weakness to highlight in this study is the absence or variability in the case definitions of LASV infections in the included studies.

These results regarding the vector role of LASV for non-Mastomys natalensis rodents should be interpreted with caution, because these infections could rather reflect a spillover infection or a misclassification of rodents due to the same number of chromosomes in certain species [7]. It should also be noted that all of the studies on current LASV detected in non-Mastomys rodents have used either RT-PCR, culture or Antigen detection by ELISA. Regarding the detection of RNA by RT-PCR, none of these studies sequenced the viruses detected and could therefore be subject to false positive results [146,147]. The only study that isolated LASV by culture raised the possibility of an incorrect classification of rodent species [124]. Antibodies suggesting past contacts with LASV in Mastomys natalensis and non-Mastomys natalensis rodents have been reported in the present study. These antibodies could, however, be acquired transplacentally or by lactation in young rodents [148]. The ages of trapped rodents were unfortunately not reported in most included studies.

Conclusions

Despite its limitations, this systematic review provides a comprehensive overview of the case fatality rate due to LASV in humans and the prevalence of LASV in humans, rodents and other mammals. We carried out a categorization of meta-analyses according to the different categories of population and target of the LASV sought. Meta-analyses suggest a relatively high case fatality rate and a prevalence of LASV infection influenced by geographic locations. The results of the study suggest that LASV is widespread in West Africa. It also appears that apart from Mastomys natalensis, other rodents could serve as reservoirs for LASV.

Supporting information

S1 Table. Preferred reporting items for systematic reviews and meta-analyses checklist.

https://doi.org/10.1371/journal.pntd.0008589.s001

(PDF)

S2 Table. Search strategy in Medline (Pubmed).

https://doi.org/10.1371/journal.pntd.0008589.s002

(PDF)

S3 Table. Items for risk of bias assessment.

https://doi.org/10.1371/journal.pntd.0008589.s003

(PDF)

S4 Table. Main reasons of exclusion of eligible studies.

https://doi.org/10.1371/journal.pntd.0008589.s004

(PDF)

S6 Table. Characteristics of included studies.

https://doi.org/10.1371/journal.pntd.0008589.s006

(PDF)

S7 Table. Individual characteristics of included studies.

https://doi.org/10.1371/journal.pntd.0008589.s007

(PDF)

S8 Table. Subgroup of human case fatality rate and prevalence of Lassa virus in humans, rodents, and other animals in sub-Saharan Africa.

https://doi.org/10.1371/journal.pntd.0008589.s008

(PDF)

S9 Table. Univariable and multivariable meta‐regression analysis on the human case fatality rate and prevalence of Lassa virus in humans, rodents, and other animals.

https://doi.org/10.1371/journal.pntd.0008589.s009

(PDF)

S1 Fig. Prevalence of Lassa virus infections in humans in sub-Saharan Africa.

https://doi.org/10.1371/journal.pntd.0008589.s010

(PDF)

S2 Fig. Prevalence of Lassa virus infections in rodents in sub-Saharan Africa.

https://doi.org/10.1371/journal.pntd.0008589.s011

(PDF)

S3 Fig. Funnel plot for publication for Lassa virus case fatality rate in humans.

https://doi.org/10.1371/journal.pntd.0008589.s012

(PDF)

S4 Fig. Funnel plot for publication for Lassa virus prevalence in humans.

https://doi.org/10.1371/journal.pntd.0008589.s013

(PDF)

S5 Fig. Funnel plot for publication for Lassa virus prevalence in rodents.

https://doi.org/10.1371/journal.pntd.0008589.s014

(PDF)

S6 Fig. Funnel plot for publication for Lassa virus prevalence in other mammals.

https://doi.org/10.1371/journal.pntd.0008589.s015

(PDF)

References

  1. 1. OIE. OneHealth: OIE—World Organisation for Animal Health. [cited 13 Jun 2020]. Available: https://www.oie.int/en/for-the-media/onehealth/
  2. 2. Kouadio L, Nowak K, Akoua-Koffi C, Weiss S, Allali BK, Witkowski PT, et al. Lassa Virus in Multimammate Rats, Côte d’Ivoire, 2013. Emerg Infect Dis. 2015;21: 1481–1483. pmid:26196447
  3. 3. Lecompte E, Fichet-Calvet E, Daffis S, Koulémou K, Sylla O, Kourouma F, et al. Mastomys natalensis and Lassa Fever, West Africa. Emerg Infect Dis. 2006;12: 1971–1974. pmid:17326956
  4. 4. Monath TP, Newhouse VF, Kemp GE, Setzer HW, Cacciapuoti A. Lassa virus isolation from Mastomys natalensis rodents during an epidemic in Sierra Leone. Science. 1974;185: 263–265. pmid:4833828
  5. 5. Mylne AQN, Pigott DM, Longbottom J, Shearer F, Duda KA, Messina JP, et al. Mapping the zoonotic niche of Lassa fever in Africa. Trans R Soc Trop Med Hyg. 2015;109: 483–492. pmid:26085474
  6. 6. Olayemi A, Cadar D, Magassouba N, Obadare A, Kourouma F, Oyeyiola A, et al. New Hosts of The Lassa Virus. Sci Rep. 2016;6: 25280. pmid:27140942
  7. 7. Granjon L, Duplantier J-M, Catalan J, Britton-Davidian J. Systematics of the genus Mastomys (Thomas, 1915) (Rodentia: Muridae): a review. Belgian Journal of Zoology. 1997;127: 7–18.
  8. 8. Fisher-Hoch SP, Tomori O, Nasidi A, Perez-Oronoz GI, Fakile Y, Hutwagner L, et al. Review of cases of nosocomial Lassa fever in Nigeria: the high price of poor medical practice. BMJ. 1995;311: 857–859. pmid:7580496
  9. 9. Monath TP, Mertens PE, Patton R, Moser CR, Baum JJ, Pinneo L, et al. A hospital epidemic of Lassa fever in Zorzor, Liberia, March-April 1972. Am J Trop Med Hyg. 1973;22: 773–779. pmid:4745236
  10. 10. Frame JD, Jr JMB, Gocke DJ, Troup JM. Lassa Fever, a New Virus Disease of Man from West Africa. The American Journal of Tropical Medicine and Hygiene. 1970;19: 670–676. pmid:4246571
  11. 11. McCormick JB. Lassa Fever. Emergence and Control of Rodent-Borne Viral Diseases. Elsevier; 1999. pp. 177–195.
  12. 12. Okwor TJ, Ndu AC, Okeke TA, Aguwa EN, Arinze-Onyia SU, Chinawa A, et al. A review of Lassa fever outbreaks in Nigeria From 1969 to 2017: Epidemiologic profile, determinants and public health response. Nigerian Journal of Medicine. 2018;27: 219–233–233.
  13. 13. Kofman A, Choi MJ, Rollin PE. Lassa Fever in Travelers from West Africa, 1969–2016. Emerg Infect Dis. 2019;25: 236–239. pmid:30666924
  14. 14. Mehand MS, Al-Shorbaji F, Millett P, Murgue B. The WHO R&D Blueprint: 2018 review of emerging infectious diseases requiring urgent research and development efforts. Antiviral Res. 2018;159: 63–67. pmid:30261226
  15. 15. Mazzola LT, Kelly-Cirino C. Diagnostics for Lassa fever virus: a genetically diverse pathogen found in low-resource settings. BMJ Global Health. 2019;4: e001116. pmid:30899575
  16. 16. McCormick JB, King IJ, Webb PA, Scribner CL, Craven RB, Johnson KM, et al. Lassa fever. Effective therapy with ribavirin. N Engl J Med. 1986;314: 20–26. pmid:3940312
  17. 17. Takah NF, Brangel P, Shrestha P, Peeling R. Sensitivity and specificity of diagnostic tests for Lassa fever: a systematic review. BMC Infect Dis. 2019;19: 647. pmid:31324229
  18. 18. Mateo M, Reynard S, Carnec X, Journeaux A, Baillet N, Schaeffer J, et al. Vaccines inducing immunity to Lassa virus glycoprotein and nucleoprotein protect macaques after a single shot. Sci Transl Med. 2019;11. pmid:31578242
  19. 19. Salami K, Gouglas D, Schmaljohn C, Saville M, Tornieporth N. A review of Lassa fever vaccine candidates. Curr Opin Virol. 2019;37: 105–111. pmid:31472333
  20. 20. Videla OE, Urzua JO. The benefits of incorporating the One Health concept into the organisation of Veterinary Services. Rev—Off Int Epizoot. 2014;33: 401–406, 393–399. pmid:25707170
  21. 21. Sigfrid L, Moore C, Salam AP, Maayan N, Hamel C, Garritty C, et al. A rapid research needs appraisal methodology to identify evidence gaps to inform clinical research priorities in response to outbreaks—results from the Lassa fever pilot. BMC Med. 2019;17. pmid:30764819
  22. 22. Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred Reporting Items for Systematic Reviews and Meta-Analyses: The PRISMA Statement. PLoS Med. 2009;6. pmid:19621072
  23. 23. Wilson DE, Reeder DM. Mammal Species of the World. A Taxonomic and Geographic Reference. 3rd ed. Johns Hopkins University Press; 2005. Available: http://www.press.jhu.edu
  24. 24. United Nations Statistics Division—Millennium Indicators. [cited 6 Mar 2020]. Available: https://unstats.un.org/unsd/mi/africa.htm
  25. 25. Hoy D, Brooks P, Woolf A, Blyth F, March L, Bain C, et al. Assessing risk of bias in prevalence studies: modification of an existing tool and evidence of interrater agreement. J Clin Epidemiol. 2012;65: 934–939. pmid:22742910
  26. 26. Schwarzer G. meta: An R package for meta-analysis. R News. 2007;7: 40–5.
  27. 27. R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2017 [cited 28 Sep 2018]. Available: https://www.r-project.org/
  28. 28. Cochran WG. The Combination of Estimates from Different Experiments. Biometrics. 1954;10: 101–129.
  29. 29. Veroniki AA, Jackson D, Viechtbauer W, Bender R, Bowden J, Knapp G, et al. Methods to estimate the between‐study variance and its uncertainty in meta‐analysis. Res Synth Methods. 2016;7: 55–79. pmid:26332144
  30. 30. Barendregt JJ, Doi SA, Lee YY, Norman RE, Vos T. Meta-analysis of prevalence. J Epidemiol Community Health. 2013;67: 974–978. pmid:23963506
  31. 31. Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997;315: 629–634. pmid:9310563
  32. 32. Noordzij M, Dekker FW, Zoccali C, Jager KJ. Study designs in clinical research. Nephron Clin Pract. 2009;113: c218–221. pmid:19690439
  33. 33. Agbonlahor DE, Erah A, Agba IM, Oviasogie FE, Ehiaghe AF, Wankasi M, et al. Prevalence of Lassa virus among rodents trapped in three South-South States of Nigeria. J Vector Borne Dis. 2017; 5.
  34. 34. Akhuemokhan OC, Ewah-Odiase RO, Akpede N, Ehimuan J, Adomeh DI, Odia I, et al. Prevalence of Lassa Virus Disease (LVD) in Nigerian children with fever or fever and convulsions in an endemic area. PLoS Negl Trop Dis. 2017;11. pmid:28671959
  35. 35. Akoua-Koffi C, Ter Meulen J, Legros D, Akran V, Aïdara M, Nahounou N, et al. [Detection of anti-Lassa antibodies in the Western Forest area of the Ivory Coast]. Med Trop (Mars). 2006;66: 465–468.
  36. 36. Arnold RB, Gary GW. A neutralization test survey for Lassa fever activity in Lassa, Nigeria. Transactions of the Royal Society of Tropical Medicine and Hygiene. 1977;71: 152–154. pmid:560072
  37. 37. Asogun DA, Adomeh DI, Ehimuan J, Odia I, Hass M, Gabriel M, et al. Molecular Diagnostics for Lassa Fever at Irrua Specialist Teaching Hospital, Nigeria: Lessons Learnt from Two Years of Laboratory Operation. PLoS Negl Trop Dis. 2012;6. pmid:23029594
  38. 38. Babalola SO, Babatunde JA, Remilekun OM, Amaobichukwu AR, Abiodun AM, Jide I, et al. Lassa virus RNA detection from suspected cases in Nigeria, 2011–2017. Pan Afr Med J. 2019;34. pmid:31819792
  39. 39. Bajani MD, Tomori O, Rollin PE, Harry TO, Bukbuk ND, Wilson L, et al. A survey for antibodies to Lassa virus among health workers in Nigeria. Transactions of the Royal Society of Tropical Medicine and Hygiene. 1997;91: 379–381. pmid:9373625
  40. 40. Baumann J, Knüpfer M, Ouedraogo J, Traoré BY, Heitzer A, Kané B, et al. Lassa and Crimean-Congo Hemorrhagic Fever Viruses, Mali. Emerging Infect Dis. 2019;25: 999–1002. pmid:31002054
  41. 41. Bausch DG, Demby AH, Coulibaly M, Kanu J, Goba A, Bah A, et al. Lassa fever in Guinea: I. Epidemiology of human disease and clinical observations. Vector Borne Zoonotic Dis. 2001;1: 269–281. pmid:12653127
  42. 42. Blackburn NK, Searle L, Taylor P. Viral haemorrhagic fever antibodies in Zimbabwe schoolchildren. Transactions of the Royal Society of Tropical Medicine and Hygiene. 1982;76: 803–805. pmid:6761909
  43. 43. Boiro I, Lomonossov NN, Sotsinski VA, Constantinov OK, Tkachenko EA, Inapogui AP, et al. [Clinico-epidemiologic and laboratory research on hemorrhagic fevers in Guinea]. Bull Soc Pathol Exot Filiales. 1987;80: 607–612. pmid:3440310
  44. 44. Bonney JHK, Osei-Kwasi M, Adiku TK, Barnor JS, Amesiya R, Kubio C, et al. Hospital-Based Surveillance for Viral Hemorrhagic Fevers and Hepatitides in Ghana. Kasper M, editor. PLoS Negl Trop Dis. 2013;7: e2435. pmid:24069490
  45. 45. Bowen GS, Wulff H, Casals J, Noonan A, Downs WG. Lassa fever in Onitsha, East Central State, Nigeria, in 1974. 1975; 6.
  46. 46. Branco LM, Grove JN, Boisen ML, Shaffer JG, Goba A, Fullah M, et al. Emerging trends in Lassa fever: redefining the role of immunoglobulin M and inflammation in diagnosing acute infection. Virol J. 2011;8: 478. pmid:22023795
  47. 47. Buba MI, Dalhat MM, Nguku PM, Waziri N, Mohammad JO, Bomoi IM, et al. Mortality Among Confirmed Lassa Fever Cases During the 2015–2016 Outbreak in Nigeria. Am J Public Health. 2018;108: 262–264. pmid:29267063
  48. 48. Bukbuk DN, Fukushi S, Tani H, Yoshikawa T, Taniguchi S, Iha K, et al. Development and validation of serological assays for viral hemorrhagic fevers and determination of the prevalence of Rift Valley fever in Borno State, Nigeria. Transactions of The Royal Society of Tropical Medicine and Hygiene. 2014;108: 768–773. pmid:25344695
  49. 49. Carey DE, Kemp GE, White HA, Pinneo L, Addy RF, Fom ALMD, et al. Lassa fever Epidemiological aspects of the 1970 epidemic, Jos, Nigeria. Trans R Soc Trop Med Hyg. 1972;66: 402–408. pmid:5046380
  50. 50. Clements TL, Rossi CA, Irish AK, Kibuuka H, Eller LA, Robb ML, et al. Chikungunya and O’nyong-nyong Viruses in Uganda: Implications for Diagnostics. Open Forum Infectious Diseases. 2019;6. pmid:31660384
  51. 51. Coulibaly-N’Golo D, Allali B, Rieger T, Akoua-Koffi C. Novel Arenavirus Sequences in Hylomyscus sp. and Mus (Nannomys) setulosus from Coˆ te d’Ivoire: Implications for Evolution of Arenaviruses in Africa. PLoS ONE. 2011;6: 9.
  52. 52. Dan-Nwafor CC, Ipadeola O, Smout E, Ilori E, Adeyemo A, Umeokonkwo C, et al. A cluster of nosocomial Lassa fever cases in a tertiary health facility in Nigeria: Description and lessons learned, 2018. International Journal of Infectious Diseases. 2019;83: 88–94. pmid:30930184
  53. 53. Dahmane A, van Griensven J, Van Herp M, Van den Bergh R, Nzomukunda Y, Prior J, et al. Constraints in the diagnosis and treatment of Lassa Fever and the effect on mortality in hospitalized children and women with obstetric conditions in a rural district hospital in Sierra Leone. Trans R Soc Trop Med Hyg. 2014;108: 126–132. pmid:24535150
  54. 54. Demartini JC, Green DE, Monath TP. Lassa virus infection in Mastomys natalensis in Sierra Leone. 1975; 12.
  55. 55. Demby AH, Inapogui A, Kargbo K, Koninga J, Kourouma K, Kanu J, et al. Lassa fever in Guinea: II. Distribution and prevalence of Lassa virus infection in small mammals. Vector Borne Zoonotic Dis. 2001;1: 283–297. pmid:12653128
  56. 56. Demby AH, Chamberlain J, Brown DW, Clegg CS. Early diagnosis of Lassa fever by reverse transcription-PCR. Journal of Clinical Microbiology. 1994;32: 2898–2903. pmid:7883875
  57. 57. Ehichioya DU, Asogun DA, Ehimuan J, Okokhere PO, Pahlmann M, Ölschläger S, et al. Hospital-based surveillance for Lassa fever in Edo State, Nigeria, 2005–2008: Lassa fever in Edo State, Nigeria. Tropical Medicine & International Health. 2012;17: 1001–1004. pmid:22594713
  58. 58. Emmerich P, Günther S, Schmitz H. Strain-specific antibody response to Lassa virus in the local population of west Africa. Journal of Clinical Virology. 2008;42: 40–44. pmid:18164653
  59. 59. Emmerich P, Thome-Bolduan C, Drosten C, Gunther S, Ban E, Sawinsky I, et al. Reverse ELISA for IgG and IgM antibodies to detect Lassa virus infections in Africa. Journal of Clinical Virology. 2006;37: 277–281. pmid:16996789
  60. 60. Fabiyi A, Tomori O, Pinneo P. Lassa fever antibodies in hospital personnel in the Plateau State of Nigeria. Niger Med J. 1979;9: 23–25. pmid:463337
  61. 61. Fabiyi A. Use of the complement fixation (CF) test in Lassa fever surveillance. 1975; 4.
  62. 62. Fair J, Jentes E, Inapogui A, Kourouma K, Goba A, Bah A, et al. Lassa Virus-Infected Rodents in Refugee Camps in Guinea: A Looming Threat to Public Health in a Politically Unstable Region. Vector-Borne and Zoonotic Diseases. 2007;7: 167–171. pmid:17627434
  63. 63. Fichet-Calvet E, Becker-Ziaja B, Koivogui L, Günther S. Lassa Serology in Natural Populations of Rodents and Horizontal Transmission. Vector-Borne and Zoonotic Diseases. 2014;14: 665–674. pmid:25229705
  64. 64. Fichet-Calvet E, Lecompte E, Koivogui L, Soropogui B, Doré A, Kourouma F, et al. Fluctuation of Abundance and Lassa Virus Prevalence in Mastomys natalensis in Guinea, West Africa. Vector-Borne and Zoonotic Diseases. 2007;7: 119–128. pmid:17627428
  65. 65. Fisher-Hoch S, McCormick JB, Sasso D, Craven RB. Hematologic dysfunction in Lassa fever. J Med Virol. 1988;26: 127–135. pmid:3183637
  66. 66. Frame JD, Jahrling PB, Yalley-Ogunro JE, Monson MH. Endemic Lassa fever in Liberia. II. Serological and virological findings in hospital patients. Trans R Soc Trop Med Hyg. 1984;78: 656–660. pmid:6390808
  67. 67. Frame JD, Casals J, Dennis EA. Lassa virus antibodies in hospital personnel in western Liberia. Transactions of the Royal Society of Tropical Medicine and Hygiene. 1979;73: 219–224. pmid:382467
  68. 68. Georges AJ, Gonzalez JP, Abdul-Wahid S, Saluzzo JF, Meunier DMY, McCormick JB. Antibodies to Lassa and lassa-like viruses in man and mammals in the Central African Republic. Transactions of the Royal Society of Tropical Medicine and Hygiene. 1985;79: 78–79. pmid:2986324
  69. 69. Gonzalez JP, Josse R, Johnson ED, Merlin M, Georges AJ, Abandja J, et al. Antibody prevalence against haemorrhagic fever viruses in randomized representative central African populations. Research in Virology. 1989;140: 319–331. pmid:2505350
  70. 70. Hamblion EL, Raftery P, Wendland A, Dweh E, Williams GS, George RNC, et al. The challenges of detecting and responding to a Lassa fever outbreak in an Ebola-affected setting. International Journal of Infectious Diseases. 2018;66: 65–73. pmid:29138016
  71. 71. Haun BK, Kamara V, Dweh AS, Garalde-Machida K, Forkay SSE, Takaaze M, et al. Serological evidence of Ebola virus exposure in dogs from affected communities in Liberia: A preliminary report. Rimoin AW, editor. PLoS Negl Trop Dis. 2019;13: e0007614. pmid:31329600
  72. 72. Helmick C, Scribner C, Webb P, Krebs J, Mccormick J. NO EVIDENCE FOR INCREASED RISK OF LASSA FEVER INFECTION IN HOSPITAL STAFF. The Lancet. 1986;328: 1202–1205.
  73. 73. Henderson BE, Gary GW, Kissling RE, Frame JD, Carey DE. Lassa fever virological and serological studies. Transactions of the Royal Society of Tropical Medicine and Hygiene. 1972;66: 409–416. pmid:4625715
  74. 74. Ibekwe T, Nwegbu M, Okokhere P, Adomeh D, Asogun D. The sensitivity and specificity of Lassa virus IgM by ELISA as screening tool at early phase of Lassa fever infection. Niger Med J. 2012;53: 196. pmid:23661877
  75. 75. Ipadeola O, Furuse Y, Ilori EA, Dan-Nwafor CC, Akabike KO, Ahumibe A, et al. Epidemiology and case-control study of Lassa fever outbreak in Nigeria from 2018 to 2019. Journal of Infection. 2020; S0163445320300013. pmid:31926184
  76. 76. Isere EE, Fatiregun A, Ilesanmi O, Ijarotimi I, Egube B, Adejugbagbe A, et al. Lessons Learnt from Epidemiological Investigation of Lassa Fever Outbreak in a Southwest State of Nigeria December 2015 to April 2016. PLoS Curr. 2018 [cited 25 Feb 2020]. pmid:30094105
  77. 77. Ivanoff’ B, Duquesnoy’ P, Languillat’ G, Saluzzo’ JF, Georges’ A, Gonzalez’ JP, et al. Haemorrhagic fever in Gabon. I. Incidence of Lassa, Ebola and Marburg viruses in Haut-Ogoou6. 1982; 2.
  78. 78. Jahrling PB, Frame JD, Smith SB, Monson MH. Endemic Lassa fever in Liberia. III. Characterization of Lassa virus isolates. Transactions of the Royal Society of Tropical Medicine and Hygiene. 1985;79: 374–379. pmid:3898483
  79. 79. Johnson BK, Ocheng D, Gichogo A, Okiro M, Libondo D, Tukei PM, et al. Antibodies against haemorrhagic fever viruses in Kenya populations. Transactions of the Royal Society of Tropical Medicine and Hygiene. 1983;77: 731–733. pmid:6419422
  80. 80. Johnson BK, Ocheng D, Gitau LG, Gichogo A, Tukei PM, Ngindu A, et al. Viral Haemorrhagic Fever Surveillance in Kenya, 1980–198. 1983; 1.
  81. 81. Johnson’ BK, Gitau LG, Gichogop A, Tukei’ M, Else’ JG, Suleman MA, et al. Marburg, Ebota and Rift Valley fever virus antibodies in East African primates. Transactions of the Royal Society of Tropical Medicine and Hygiene. 1982; 4. pmid:7043806
  82. 82. Keane E, Gilles HM. Lassa fever in Panguma Hospital, Sierra Leone, 1973–6. BMJ. 1977;1: 1399–1402. pmid:861652
  83. 83. Kernéis S, Koivogui L, Magassouba N, Koulemou K, Lewis R, Aplogan A, et al. Prevalence and Risk Factors of Lassa Seropositivity in Inhabitants of the Forest Region of Guinea: A Cross-Sectional Study. Aksoy S, editor. PLoS Negl Trop Dis. 2009;3: e548. pmid:19924222
  84. 84. Klempa B, Koulemou K, Auste B, Emmerich P, Thomé-Bolduan C, Günther S, et al. Seroepidemiological study reveals regional co-occurrence of Lassa- and Hantavirus antibodies in Upper Guinea, West Africa. Trop Med Int Health. 2012; n/a-n/a. pmid:23279760
  85. 85. Lalis A, Leblois R, Lecompte E, Denys C, ter Meulen J, Wirth T. The Impact of Human Conflict on the Genetics of Mastomys natalensis and Lassa Virus in West Africa. Mores CN, editor. PLoS ONE. 2012;7: e37068. pmid:22615894
  86. 86. Leski TA, Stockelman MG, Moses LM, Park M, Stenger DA, Ansumana R, et al. Sequence Variability and Geographic Distribution of Lassa Virus, Sierra Leone—Volume 21, Number 4—April 2015—Emerging Infectious Diseases journal—CDC. 2015 [cited 26 Oct 2019]. pmid:25811712
  87. 87. Li W-G, Chen W-W, Li L, Ji D, Ji Y-J, Li C, et al. The etiology of Ebola virus disease-like illnesses in Ebola virusnegative patients from Sierra Leone. Oncotarget. 2016;7. pmid:26683705
  88. 88. Lukashevich IS, Clegg JC, Sidibe K. Lassa virus activity in Guinea: distribution of human antiviral antibody defined using enzyme-linked immunosorbent assay with recombinant antigen. J Med Virol. 1993;40: 210–217. pmid:8355019
  89. 89. Maigari IM, Jibrin YB, Umar MS, Lawal SM, Gandi AY. Descriptive features of Lassa fever in Bauchi, Northeastern Nigeria—a retrospective review. Research Journal of Health Sciences. 2018;6: 149.
  90. 90. Mariën J, Borremans B, Gryseels S, Soropogui B, De Bruyn L, Bongo GN, et al. No measurable adverse effects of Lassa, Morogoro and Gairo arenaviruses on their rodent reservoir host in natural conditions. Parasites Vectors. 2017;10: 210. pmid:28449693
  91. 91. Mathiot CC, Fontenille D, Georges AJ, Coulanges P. Antibodies to haemorrhagic fever viruses in Madagascar populations. Transactions of the Royal Society of Tropical Medicine and Hygiene. 1989;83: 407–409. pmid:2515626
  92. 92. McCarthy MC, Haberberger RL, Salib AW, Soliman BA, El-Tigani A, Watts DM. Evaluation of arthropod‐borne viruses and other infectious disease pathogens as the causes of febrile illnesses in the Khartoum Province of Sudan. 1996; 6.
  93. 93. McCormick JB, King IJ, Webb PA, Johnson KM, O’Sullivan R, Smith ES, et al. A Case-Control Study of the Clinical Diagnosis and Course of Lassa Fever. J Infect Dis. 1987;155: 445–455. pmid:3805772
  94. 94. McCormick JB, Webb PA, Krebs JW, Johnson KM, Smith ES. A Prospective Study of the Epidemiology and Ecology of Lassa Fever. J Infect Dis. 1987;155: 437–444. pmid:3805771
  95. 95. Meunier DM, Johnson ED, Gonzalez JP, Georges-Courbot MC, Madelon MC, Georges AJ. [Current serologic data on viral hemorrhagic fevers in the Central African Republic]. Bull Soc Pathol Exot Filiales. 1987;80: 51–61. pmid:3607998
  96. 96. Nakounné E, Selekon B, Morvan J. Veille microbiologique: les fièvres hémorragiques virales en République centrafricaine; 2000; 8.
  97. 97. Nimo-Paintsil SC, Fichet-Calvet E, Borremans B, Letizia AG, Mohareb E, Bonney JHK, et al. Rodent-borne infections in rural Ghanaian farming communities. Schieffelin J, editor. PLoS ONE. 2019;14: e0215224. pmid:31017931
  98. 98. Ogunro BN, Olugasa BO, Kayode A, Ishola OO, Kolawole ON, Odigie EA, et al. Detection of Antibody and Antigen for Lassa Virus Nucleoprotein in Monkeys from Southern Nigeria. JEGH. 2019 [cited 25 Feb 2020]. pmid:31241870
  99. 99. O’Hearn AE, Voorhees MA, Fetterer DP, Wauquier N, Coomber MR, Bangura J, et al. Serosurveillance of viral pathogens circulating in West Africa. Virol J. 2016;13: 163. pmid:27716429
  100. 100. Okogbenin S, Okoeguale J, Akpede G, Colubri A, Barnes KG, Mehta S, et al. Retrospective Cohort Study of Lassa Fever in Pregnancy, Southern Nigeria. Emerg Infect Dis. 2019;25: 1494–1500. pmid:31310586
  101. 101. Okokhere P, Colubri A, Azubike C, Iruolagbe C, Osazuwa O, Tabrizi S, et al. Clinical and laboratory predictors of Lassa fever outcome in a dedicated treatment facility in Nigeria: a retrospective, observational cohort study. The Lancet Infectious Diseases. 2018;18: 684–695. pmid:29523497
  102. 102. Okoror LE, Esumeh FI, Agbonlahor DE, Umolu PI. Lassa virus: Seroepidemiological survey of rodents caught in Ekpoma and environs. Trop Doct. 2005;35: 16–17. pmid:15712534
  103. 103. Olayemi A, Oyeyiola A, Obadare A, Igbokwe J, Adesina AS, Onwe F, et al. Widespread arenavirus occurrence and seroprevalence in small mammals, Nigeria. Parasites Vectors. 2018;11: 416. pmid:30005641
  104. 104. Olayemi A, Obadare A, Oyeyiola A, Igbokwe J, Fasogbon A, Igbahenah F, et al. Arenavirus Diversity and Phylogeography of Mastomys natalensis Rodents, Nigeria. Emerg Infect Dis. 2016;22: 687–690. pmid:26926035
  105. 105. Oloniniyi OK, Unigwe US, Okada S, Kimura M, Koyano S, Miyazaki Y, et al. Genetic characterization of Lassa virus strains isolated from 2012 to 2016 in southeastern Nigeria. PLoS Negl Trop Dis. 2018;12. pmid:30500827
  106. 106. Omilabu SA, Badaru SO, Okokhere P, Asogun D, Drosten C, Emmerich P, et al. Lassa Fever, Nigeria, 2003 and 2004. Emerg Infect Dis. 2005;11: 1642–1644. pmid:16355508
  107. 107. Paix MA, Poveda JD, Malvy D, Bailly C, Merlin M, Fleury HJ. [Serological study of the virus responsible for hemorrhagic fever in an urban population of Cameroon]. Bull Soc Pathol Exot Filiales. 1988;81: 679–682. pmid:3064937
  108. 108. Panning M, Emmerich P, Ölschläger S, Bojenko S, Koivogui L, Marx A, et al. Laboratory Diagnosis of Lassa Fever, Liberia. Emerg Infect Dis. 2010;16: 1041–1043. pmid:20507774
  109. 109. Price ME, Fisher-Hoch SP, Craven RB, McCormick JB. A prospective study of maternal and fetal outcome in acute Lassa fever infection during pregnancy. 1988;297: 4.
  110. 110. Rodhain F, Gonzalez JP, Mercier E, Helynck B, Larouze B, Hannoun C. Arbovirus infections and viral haemorrhagic fevers in Uganda: a serological survey in Karamoja district, 1984. Transactions of the Royal Society of Tropical Medicine and Hygiene. 1989;83: 851–854. pmid:2559514
  111. 111. Safronetz D, Sogoba N, Lopez JE, Maiga O, Dahlstrom E, Zivcec M, et al. Geographic Distribution and Genetic Characterization of Lassa Virus in Sub-Saharan Mali. PLoS Negl Trop Dis. 2013;7. pmid:24340119
  112. 112. Safronetz D, Lopez JE, Sogoba N, Traore’ SF, Raffel SJ, Fischer ER, et al. Detection of Lassa virus, Mali. Emerging Infect Dis. 2010;16: 1123–1126. pmid:20587185
  113. 113. Salu OB, James AB, Bankolé HS, Agbla JM, Da Silva M, Gbaguidi F, et al. Molecular confirmation and phylogeny of Lassa fever virus in Benin Republic 2014–2016. African Journal of Laboratory Medicine. 2019;8. pmid:31534915
  114. 114. Saluzzo JF, Adam F, McCormick JB, Digoutte JP. Lassa Fever Virus in Senegal. Journal of Infectious Diseases. 1988;157: 605–605. pmid:3343533
  115. 115. Schoepp RJ, Rossi CA, Khan SH, Goba A, Fair JN. Undiagnosed Acute Viral Febrile Illnesses, Sierra Leone. Emerg Infect Dis. 2014;20: 1176–1182. pmid:24959946
  116. 116. Shaffer JG, Schieffelin JS, Gbakie M, Alhasan F, Roberts NB, Goba A, et al. A medical records and data capture and management system for Lassa fever in Sierra Leone: Approach, implementation, and challenges. Verdonck K, editor. PLoS ONE. 2019;14: e0214284. pmid:30921383
  117. 117. Shehu NY, Gomerep SS, Isa SE, Iraoyah KO, Mafuka J, Bitrus N, et al. Lassa Fever 2016 Outbreak in Plateau State, Nigeria—The Changing Epidemiology and Clinical Presentation. Front Public Health. 2018;6: 232. pmid:30211144
  118. 118. Smith EA, Fabiyi A, Kuteyi OE, Tomori O. Epidemiological aspect of the 1976 Pankshin Lassa fever outbreak. Niger Med J. 1979;9: 20–22. pmid:463336
  119. 119. Sogoba N, Rosenke K, Adjemian J, Diawara SI, Maiga O, Keita M, et al. Lassa Virus Seroprevalence in Sibirilia Commune, Bougouni District, Southern Mali. Emerg Infect Dis. 2016;22: 657–663. pmid:26981786
  120. 120. ter Meulen J, Koulemou K, Wittekindt T, Windisch K, Strigl S, Conde S, et al. Detection of Lassa Virus Antinucleoprotein Immunoglobulin G (IgG) and IgM Antibodies by a Simple Recombinant Immunoblot Assay for Field Use. Journal of Clinical Microbiology. 1998;36: 3143–3148. pmid:9774554
  121. 121. Tomori O, Fabiyi A, Sorungbe A, Smith A, McCormick JB. Viral hemorrhagic fever antibodies in Nigerian populations. Am J Trop Med Hyg. 1988;38: 407–410. pmid:3128130
  122. 122. Van der Waals FW, Pomeroy KL, Goudsmit J, Asher DM, Gajdusek DC. Hemorrhagic fever virus infections in an isolated rainforest area of central Liberia. Limitations of the indirect immunofluorescence slide test for antibody screening in Africa. Trop Geogr Med. 1986;38: 209–214. pmid:3092415
  123. 123. Webb PA, McCormick JB, King IJ, Bosman I, Johnson KM, Elliott LH, et al. Lassa fever in children in Sierra Leone, West Africa. Trans R Soc Trop Med Hyg. 1986;80: 577–582. pmid:3810792
  124. 124. Wulff H, Fabiyi A, Monath TP. Recent isolations of Lassa virus from Nigerian rodents. Bull World Health Organ. 1975;52: 609–613. pmid:1085216
  125. 125. Yadouleton A, Agolinou A, Kourouma F, Saizonou R, Pahlmann M, Bedié SK, et al. Lassa Virus in Pygmy Mice, Benin, 2016–2017. Emerg Infect Dis. 2019;25: 1977–1979. pmid:31365854
  126. 126. Yalley-Ogunro JE, Frame JD, Hanson AP. Endemic Lassa fever in Liberia. VI. Village serological surveys for evidence of Lassa virus activity in Lofa County, Liberia. Transactions of the Royal Society of Tropical Medicine and Hygiene. 1984;78: 764–770. pmid:6398530
  127. 127. Cummins D, McCormick JB, Bennett D, Samba JA, Farrar B, Machin SJ, et al. Acute sensorineural deafness in Lassa fever. JAMA. 1990;264: 2093–2096. pmid:2214077
  128. 128. Frame JD, Yalley-Ogunro JE, Hanson AP. Endemic Lassa fever in Liberia. V. Distribution of Lassa virus activity in Liberia: hospital staff surveys. Transactions of the Royal Society of Tropical Medicine and Hygiene. 1984;78: 761–763. pmid:6398529
  129. 129. Gonzalez JP, McCormick JB, Saluzzo JF, Herve JP, Georges AJ, Johnson KM. An arenavirus isolated from wild-caught rodents (Pramys species) in the Central African Republic. Intervirology. 1983;19: 105–112. pmid:6862813
  130. 130. Keenlyside RA, McCormick JB, Webb PA, Smith E, Elliott L, Johnson KM. Case-control study of Mastomys natalensis and humans in Lassa virus-infected households in Sierra Leone. Am J Trop Med Hyg. 1983;32: 829–837. pmid:6881432
  131. 131. Meulen JT, Lukashevich I, Sidibe K, Inapogui A, Marx M, Dorlemann A, et al. Hunting of Peridomestic Rodents and Consumption of Their Meat as Possible Risk Factors for Rodent-to-Human Transmission of Lassa Virus in the Republic of Guinea. The American Journal of Tropical Medicine and Hygiene. 1996;55: 661–666. pmid:9025695
  132. 132. Troup JM, White HA, Fom AL, Carey DE. An outbreak of Lassa fever on the Jos plateau, Nigeria, in January-February 1970. A preliminary report. Am J Trop Med Hyg. 1970;19: 695–696. pmid:4987549
  133. 133. Bloch A. A serological survey of Lassa fever in Liberia. 1978; 3.
  134. 134. Dan-Nwafor CC, Furuse Y, Ilori EA, Ipadeola O, Akabike KO, Ahumibe A, et al. Measures to control protracted large Lassa fever outbreak in Nigeria, 1 January to 28 April 2019. Eurosurveillance. 2019;24. pmid:31115314
  135. 135. Johnson ED, Gonzalez JP, Georges A. Haemorrhagic fever virus activity in equatorial Africa: distribution and prevalence of filovirus reactive antibody in the Central African Republic. Transactions of the Royal Society of Tropical Medicine and Hygiene. 1993;87: 530–535. pmid:8266402
  136. 136. ter Meulen J, Lenz O, Koivogui L, Magassouba N, Kaushik SK, Lewis R, et al. Short communication: Lassa fever in Sierra Leone: UN peacekeepers are at risk. Trop Med Int Health. 2001;6: 83–84. pmid:11251899
  137. 137. Ogbu O, Ajuluchukwu E, Uneke CJ. Lassa fever in West African sub-region: an overview. J Vector Borne Dis. 2007;44: 1–11. pmid:17378212
  138. 138. Eberhardt KA, Mischlinger J, Jordan S, Groger M, Günther S, Ramharter M. Ribavirin for the treatment of Lassa fever: A systematic review and meta-analysis. International Journal of Infectious Diseases. 2019;87: 15–20. pmid:31357056
  139. 139. Kayem ND, Benson C, Aye CYL, Barker S, Tome M, Kennedy S, et al. Lassa fever in pregnancy: a systematic review and meta-analysis. Transactions of The Royal Society of Tropical Medicine and Hygiene. 2020; traa011. pmid:32125412
  140. 140. Monson MH, Cole AK, FRAME JD, SERWINT JR, ALEXANDER S, JAHRLINGI PB. Pediatric Lassa Fever: A Review of 33 Liberian Cases. The American Journal of Tropical Medicine and Hygiene. 1987;36: 408–415. pmid:3826501
  141. 141. Frame JD. Clinical Features of Lassa Fever in Liberia. Clinical Infectious Diseases. 1989;11: S783–S789. pmid:2749109
  142. 142. Wulff H, Johnson KM. Immunoglobulin M and G responses measured by immunofluorescence in patients with Lassa or Marburg virus infections. Bulletin of the World Health Organization. 1979;57: 631–635. pmid:118812
  143. 143. Branco LM, Boisen ML, Andersen KG, Grove JN, Moses LM, Muncy IJ, et al. Lassa hemorrhagic fever in a late term pregnancy from northern sierra leone with a positive maternal outcome: case report. Virol J. 2011;8: 404. pmid:21843352
  144. 144. Bausch DG, Rollin PE, Demby AH, Coulibaly M, Kanu J, Conteh AS, et al. Diagnosis and Clinical Virology of Lassa Fever as Evaluated by Enzyme-Linked Immunosorbent Assay, Indirect Fluorescent-Antibody Test, and Virus Isolation. Journal of Clinical Microbiology. 2000;38: 2670–2677. pmid:10878062
  145. 145. Laoprasopwattana K, Chaimongkol W, Pruekprasert P, Geater A. Acute Respiratory Failure and Active Bleeding Are the Important Fatality Predictive Factors for Severe Dengue Viral Infection. Ooi EE, editor. PLoS ONE. 2014;9: e114499. pmid:25460594
  146. 146. Amanat F, Duehr J, Oestereich L, Hastie KM, Ollmann Saphire E, Krammer F. Antibodies to the Glycoprotein GP2 Subunit Cross-React between Old and New World Arenaviruses. mSphere. 2018;3. pmid:29720525
  147. 147. La Posta VJ, Auperin DD, Kamin-Lewis R, Cole GA. Cross-protection against lymphocytic choriomeningitis virus mediated by a CD4+ T-cell clone specific for an envelope glycoprotein epitope of Lassa virus. J Virol. 1993;67: 3497–3506. pmid:7684468
  148. 148. Jiménez de Oya N, Alonso-Padilla J, Blázquez A-B, Escribano-Romero E, Escribano JM, Saiz J-C. Maternal transfer of antibodies to the offspring after mice immunization with insect larvae-derived recombinant hepatitis E virus ORF-2 proteins. Virus Research. 2011;158: 28–32. pmid:21376089