ABSTRACT.
Diagnostics for febrile illnesses other than malaria are not readily available in rural sub-Saharan Africa. This study assessed exposure to three mosquito-borne arboviruses—dengue virus (DENV), Zika virus (ZIKV), and chikungunya virus (CHIKV)—in southern Mali. Seroprevalence for DENV, CHIKV, and ZIKV was analyzed by detection of IgG antibodies and determined to be 77.2%, 31.2%, and 25.8%, respectively. Among study participants, 11.3% were IgG-positive for all three arboviruses. DENV had the highest seroprevalence rate at all sites; the highest seroprevalence of CHIKV and ZIKV was observed in Bamba. The seroprevalence for all three arboviruses increased with age, and the highest seroprevalence was observed among adults older than 50 years. The prevalence of Plasmodium spp. in the cohort was analyzed by microscopy and determined to be 44.5% (N = 600) with Plasmodium falciparum representing 95.1% of all infections. This study demonstrates the co-circulation of arboviruses in a region hyperendemic for malaria and highlights the needs for arbovirus diagnostics in rural sub-Saharan Africa.
INTRODUCTION
Febrile illnesses are a huge public health burden in many parts of sub-Saharan Africa, and the implementation of diagnostic capabilities remains a high priority. Plasmodium spp. and arboviruses are important human pathogens causing similar initial disease symptoms that cannot be clinically distinguished.1 Malaria remains the top cause of febrile diseases in sub-Saharan Africa, but the situation with arboviruses remains obscure. More than 500 arboviruses belonging to distinct virus families are currently listed, of which more than 100 are implicated in human disease.2 Some of these arboviruses are emerging/reemerging on the African continent, causing epidemics in multiple countries over recent years and leading to significant mortality.3–6 Because of the similar initial clinical presentation and a lack of diagnostics, arbovirus infections are often missed or misdiagnosed.
In Mali, despite significant progress in control efforts, malaria remains the number one differential diagnosis for febrile diseases and the leading cause of morbidity, accounting for roughly a third of all healthcare center visits.7 Other causes of febrile illnesses are not well studied, and cases are poorly documented. Mosquito-borne arboviral infections have been reported from Mali8 but are often misdiagnosed as malaria due to lack of appropriate diagnostic tools in rural settings. In recent years, infections with arboviruses have also become more frequently reported in other sub-Saharan African countries.6,8,9 With mosquito vectors cocirculating in malaria hyperendemic regions,10–12 dengue virus (DENV), chikungunya (CHIKV), Zika (ZIKV), and yellow fever (YFV) are considered major public health issues.4,13 In this study, we analyzed human serum samples from malaria hyperendemic areas in the Sikasso region of southern Mali. We report serological evidence for exposure to the mosquito-borne arboviruses DENV, CHIKV, and ZIKV.
MATERIALS AND METHODS
Ethics.
The research protocol was approved by the ethic committees of the Faculty of Medicine, Pharmacy and Odontostomatology, University of Bamako, and the U.S. National Institutes of Health (Protocol NIH No. 18-I8-N060). Community consent was obtained from local authorities, and individual consent was obtained from each participant before enrollment in the study.
Study population and sample collection.
The study was conducted in three villages (Soromba, Bamba, and Banzana), located in the commune of Sibirila, district of Bougouni, region of Sikasso in southern Mali (Figure 1). The population size in the three villages was 855, 1,751, and 4,822 habitants for Soromba, Bamba, and Banzana, respectively. Samples were collected during the month of February 2015 just after the end of the rainy season. Households were randomly selected in each village from a census list to compose a cohort of 200 participants of >6 months of age (600 participants in total). As previously reported,14 52.5% was female; the mean age was 22.6 years (range: 7 months–83 years), with 53.2% under 15 years of age. Approximately 1 mL capillary blood (finger prick for adults, heel prick for children <2 years of age) was obtained for blood smear and serological analysis. Serum was separated, aliquoted, and stored frozen in liquid nitrogen on site. All clinical specimens were sent to the Virology Laboratory at Point G in Bamako for further processing and analysis.
Figure 1.
Seroprevalence and parasitemia at study sites. The inset shows the map of the country Mali, whereas the larger map focuses on the regions south of the capital Bamako. The study locations in the Sibirila Community of Bougouni in southern Mali (Bamba, Banzana, and Soromba) are indicated. The charts provide the seroprevalence and parasitemia at each study site. CHIKV = Chikungunya virus; DENV = Dengue virus; ZIKV = Zika virus.
Malaria testing.
For malaria parasite identification, the thick and thin blood smears collected during the cross-sectional survey were stained on site with 10% Giemsa and examined under the 100× oil immersion objective lens of a light microscope by an experienced investigator. The number of asexual and sexual parasites was counted per 200 leukocytes.
Arbovirus serology.
For arbovirus serology, commercial ELISA for IgG antibody detection (CHIKV and ZIKV, Euroimmun kits [Luebeck, Schleswig-Holstein, Germany]; DENV, Quest Diagnostics [Cypress, CA] Dengue Virus IgG Dx Select™) were used. The kit for dengue detects serotypes 1–4. Serum was heat-treated at 56°C for 60 minutes. The reagents were brought to room temperature 30 minutes before testing, and ELISAs were run according to the protocols provided by the manufacturer. Testing for the three arboviruses was handled separately, but the data were compiled in one database.
Biosafety.
Laboratory tests were performed in a biosafety class IIa cabinet by trained personnel wearing proper personal protective equipment (N95 mask, face shield, Tyvek laboratory gowns, and two sets of gloves).
STATISTICAL ANALYSES
The data were entered in Excel and analyzed using SPS for Windows version 20.0 (SPSS, Chicago, IL). The figures were made using GraphPad Prism version 9.4.0 (San Diego, CA). The prevalence of Plasmodium ssp. and of combined IgG responses against DENV, CHIKV, and ZIKV are presented with 95% CIs. Prevalence comparison was done among the three study sites, sex, and five age groups using 95% CI overlaps. Multivariable regression analyses were performed to identify risk factors for Plasmodium ssp. parasitemia and for the IgG responses to DENV, CHIKV, and ZIKV (dependent variables scored 0 or 1). The independent variables were location (three study sites), sex (two levels), and age (five groups). The odds ratio (OR) with 95% CI were used to assess the strengths of the associations among variables. A two-tailed P value of <0.05 was considered statistically significant.15
RESULTS
Prevalence of Plasmodium ssp.
The overall prevalence of Plasmodium ssp. in the study population was 44.5% (273/600) with minor variations among the three study sites: Bamba (40.0%; 80/200), Banzana (45.0%; 90/200), and Soromba (48.5%; 97/200) (Table 1); these variations were not statistically significant (Bamba, reference site; Banzana, OR = 1.4, 95% CI = 0.9–2.1; Soromba, OR = 1.2, 95% CI = 0.8–1.7) (Table 2). Two malaria parasite species were identified with Plasmodium falciparum in 95.1% and Plasmodium malariae in 12.4% of study participants (7.5% coinfections with both species) (Figure 2A). The prevalence of Plasmodium ssp. was significantly higher in male (51.9%; 148/285) than female (37.8%; 119/315) participants (Table 1). Male participants were 1.8 times more likely to be infected with Plasmodium ssp. compared with female participants (OR = 1.8, 95% CI = 1.3–2.5) (Table 2). Most infections were found in children under the age of 14 years with rapidly decreasing positivity in the older age groups (Table 1).
Table 1.
Prevalence of Plasmodium ssp. and arbovirus IgG antibodies
| Variables | Plasmodium Positive/Total % Positive (95% CI) |
DENV Positive/Total % Positive (95% CI) |
CHIKV Positive/Total % Positive (95% CI) |
ZIKV Positive/Total % Positive (95% CI) |
|---|---|---|---|---|
| Site | ||||
| All sites | 273/600 44.5 (40.5–48.5) |
463/600 77.2 (73.8–80.5) |
187/600 31.2 (27.5–34.9) |
155/600 25.8 (22.3–29.3) |
| Bamba | 80/200 40.0 (33.2–46.8) |
149/200 74.5 (68.5–80.5) |
73/200 36.5 (29.8–43.2) |
68/200 34.0 (27.4–40.6) |
| Banzana | 90/200 45.0 (38.1–51.9) |
162/200 81.0 (75.6–86.4) |
66/200 33.0 (26.5–39.5) |
49/200 24.5 (18.5–30.5) |
| Soromba | 97/200 48.5 (41.6–55.4) |
152/200 76.0 (70.1–81.9) |
48/200 24.0 (18.1–29.9) |
38/200 19.0 (13.6–24.4) |
| Sex | ||||
| Female | 119/315 37.8 (32.4–43.1) |
245/315 77.8 (73.2–82.4) |
122/315 38.7 (33.4–44.1) |
92/315 29.2 (24.2–34.2) |
| Male | 148/285 51.9 (46.1–57.7) |
218/285 76.5 (71.6–81.4) |
65/285 22.8 (17.9–27.7) |
63/285 22.1 (17.3–26.9) |
| Age | ||||
| <5 | 63/95 66.3 (56.8–75.8) |
63/95 66.3 (56.8–75.8) |
3/95 3.2 (0.4–6.7) |
9/95 9.5 (3.6–15.4) |
| 5–14 | 149/214 69.6 (63.5–75.8) |
159/214 74.3 (68.5–80.2) |
11/214 5.1 (2.2–8.1) |
32/214 15.0 (10.2–19.8) |
| 15–29 | 30/95 31.2 (21.9–40.6) |
71/95 74.7 (66.0–84.5) |
37/95 39.0 (29.1–48.8) |
30/95 31.6 (22.2–40.9) |
| 30–49 | 17/124 13.4 (7.4–19.4) |
106/124 85.5 (79.3–91.7) |
88/124 71.0 (63.0–79.0) |
53/124 42.7 (34.0–51.5) |
| 50+ | 8/72 11.0 (3.8–18.2) |
64/72 88.9 (81.6–96.2) |
48/72 66.7 (55.8–77.6) |
31/72 43.2 (31.6–54.5) |
% = mean prevalence; 95% CI = CIs around the mean; CHIKV = Chikungunya virus; DENV = Dengue virus; ZIKV = Zika virus. Data are presented according to the study population, sex, and age groups.
Table 2.
Multivariate analysis of Plasmodium ssp. parasitemia and exposure to arbovirus IgG antibodies dependent on study sites, sex, and age
| Variables | Plasmodium spp. OR (95% CI) | DENV OR (95% CI) | CHIKV OR (95% CI) | ZIKV OR (95% CI) |
|---|---|---|---|---|
| Sites | ||||
| Bamba | 1* | 1 | 1 | 1 |
| Banzana | 1.4 (0.9–2.1) | 1.1 (0.7–1.7) | 0.6 (0.4–1.0) | 0.5 (0.3–0.7) |
| Soromba | 1.2 (0.8–1.7) | 0.7 (0.5–1.2) | 0.6 (0.4–0.9) | 0.7 (0.5–1.2) |
| Sex | ||||
| Females | 1* | 1 | 1 | 1 |
| Males | 1.8 (1.3–2.5) | 0.9 (0.6–1.3) | 0.5 (0.3–0.7) | 0.7 (0.5–1.0) |
| Age | ||||
| <5 | 1* | 1 | 1 | 1 |
| 5–14 | 1.1 (0.7–1.8) | 1.5 (0.9–2.5) | 1.7 (0.5–6.1) | 0.7 (0.8–3.7) |
| 15–29 | 0.2 (0.1–0.4) | 1.5 (0.8–2.8) | 19.6 (5.8–66.4) | 1.8 (2.0–9.9) |
| 30–49 | 0.1 (0.0–0.2) | 3.0 (1.6–5.8) | 75.0 (22.3–252.3) | 2.8 (3.3–15.5) |
| ≥50 | 0.1 (0.0–0.1) | 4.1 (1.7–9.5) | 61.3 (17.6–214.1) | 3.1 (3.2–16.6) |
95% CI = CIs around the mean; CHIKV = Chikungunya virus; DENV = Dengue virus; OR = odds ratio; ZIKV = Zika virus.
Reference group.
Figure 2.
Seroprevalence and parasitemia. (A) Plasmodium ssp. parasitemia. The chart shows the overall prevalence of parasitemia of Plasmodium falciparum, Plasmodium malariae, and both parasites. (B) Seroprevalence of mosquito-borne arboviruses. The graph shows the percentages of seropositivity for Dengue (DENV), Chikungunya (CHIKV), and Zika (ZIKV) viruses as well as seropositivity for two and three of the arboviruses.
Seroprevalence of DENV, CHIKV, and ZIKV.
We detected IgG antibodies to at least one of the three arboviruses (DENV, CHIKV, ZIKV) in 84.9% (522/600) of the participants. The highest seroprevalence was observed with DENV with 77.2% (463/600), followed by CHIKV with 31.2% (187/600), and ZIKV with 25.8% (155/600) (Table 1). Among the study participants, 42.3% (254/600) were only exposed to DENV, 3.0% (18/600) only to CHIKV, and 1.8% (11/600) only to ZIKV. In addition, 13.8% of participants were exposed to DENV and CHIKV, 9.7% to DENV and ZIKV, 3.0% to CHIKV and ZIKV; 11.3% were exposed to all the three viruses (Figure 2B). There was no significant difference among the three study sites regarding the seroprevalence of DENV with 74.5% (149/200) in Bamba, 81.0% (162/200) in Banzana, and 76.0% (152/200) in Soromba (Table 1). DENV seropositivity was not significantly different among sites (Bamba, reference site; Banzana (OR = 1.1, 95% CI = 0.7–1.7); Soromba (OR = 0.7, 95% CI = 0.5–1.2 (Table 2). We also found no significant difference in the prevalence of exposure to CHIKV between participants from Bamba (36.5%; 73/200) and Banzana (33.0%; 66/200), but those from Soromba (24.0%; 48/200) were significantly less exposed (OR = 0.6, 95% CI = 0.4–0.9) (Tables 1 and 2). As for DENV exposure, there was not a significant difference in exposure to ZIKV for the participants from the three sites with a seroprevalence of 34.0% (68/200) in Bamba, 24.5% (49/200) in Banzana, and 19.0% (38/200) in Soromba (Table 1). Participants from Banzana were 0.5 times less likely to be exposed to ZIKV than those from Bamba (OR = 0.5, 95% CI = 0.3–0.7) (Table 2).
Seroprevalence for IgG antibodies increased with age for all arboviruses tested. The highest seroprevalence was observed among adults older than 50 years with 88.9% (64/72) for DENV, 66.7% (48/72) for CHIKV, and 43.2% (31/72) ZIKV (Table 1). The lowest seroprevalences were observed in children under 5 years of age with 66.3% (63/95) for DENV, 3.2% (3/95) for CHIKV, and 9.5% (9/95) for ZIKV (Table 1). Data showed a higher seroprevalence rate in women for DENV, CHIKV, and ZIKV with 77.8% (245/315), 38.7% (122/315), and 29.2% (92/315) (Table 1), respectively. Male participants were 0.5 times less likely to be exposed to CHIKV (OR = 0.5, 95% CI = 0.3–0.7) (Table 2).
DISCUSSION
This study was carried out in three locations in southern Mali, an area hyperendemic for malaria.16 The region is known for a high density of mosquitos including Anopheles and Aedes spp., which are known to transmit Plasmodium spp. and certain arboviruses.17 Aedes aegypti populations are on the rise in this region and throughout Africa.18 In Mali and many African countries, accurate identification of arboviral infections is challenging, and fevers of unknown cause often tend to be misdiagnosed as malaria; hence, the burden of arboviral infections remains unknown.
Malaria is responsible for about one-third of all visits to health care facilities in Mali with 2.37 million clinical cases according to Local Health Information System.19 High prevalence of acute malaria was also found in this study cohort with P. falciparum causing the vast majority and P. malariae a minority of the infections. Co-circulation of these two species has previously been found in other African studies.20–22 The Malian malaria control program recommends the use of rapid diagnostic tests (RDT) targeting the histidine-rich protein 2 (HRP2) for routine diagnostics. However, only P. falciparum expresses the HRP-2 antigen, resulting in missing those infections caused by P. malariae. Therefore, confirmation by other tests should be considered for RDT HRP-2–negative suspect clinical malaria cases.23 This could be best achieved with molecular diagnostics, which also would determine the Plasmodium ssp., but availability and cost are likely prohibitive in rural sub-Saharan settings. Children showed the highest prevalence in our study supporting the established seasonal malaria chemoprevention program for children in Mali.24,25 Overall, our study attributes hyperendemicity of Plasmodium spp. in this southern Mali.
The overall prevalence of DENV IgG antibodies in the study population was high with no significant difference in seroprevalence among the three study sites. This may be explained by the high prevalence of A. aegypti, the main DENV vector, in Mali.26 Furthermore, DENV IgG antibodies persist for a long time explaining increased seropositivity at older age.27 Despite the high exposure risk to DENV in southern Mali, Dengue fever cases have rarely been reported.26 This is likely because of the lack of diagnostic testing and the biased clinical focus on malaria in the region. Awareness of DENV as a cause of febrile disease needs to be urgently established in medical communities as an important public health measure. All patients with clinical suspected Dengue fever (acute fever onset, headache, body aches, and rash starting from the trunk) should be tested for DENV nucleic acid or DENV antigen. In parallel, they should receive appropriate management and be monitored for more severe forms of DENV infection while waiting for final diagnosis.
Aedes aegypti also serves as the main vector for CHIKV17,26; IgG antibodies were found at lower levels than DENV antibodies in our study, however, a result that is supported by similar serosurveys from Kenya (34%)28 and Benin (36%).29 In Mali, we previously found a lower seroprevalence of 6.6% in people tested negative for yellow fever,8 and recently a CHIKV prevalence of 13% was reported.30 Notable is a higher CHIKV seroprevalence in women (38.7%) in our study, which has also been reported from Benin.29 A potential sex difference for CHIKV infections requires further investigation. Overall, CHIKV is an emerging neglected disease in Africa, and diagnostic capabilities are urgently needed for public health response.
Zika virus is another emerging arbovirus of medical importance. Serological evidence for ZIKV infections has previously been reported from Senegal (22.7%) and Burkina Faso (22.75%).31–33 Zika virus IgG seroprevalence was similar in our study cohort with increasing positivity in the older age groups. A study previously carried out in Mali reported a ZIKV seroprevalence of 12% with a similar age distribution.34 Interestingly, Aedes albopictus, an alternative vector of ZIKV, has recently been described in the Niger River region of Mali,35 a finding that may have future implications for public health. As with other arboviruses, ZIKV needs to be considered as a cause of febrile disease in southern Mali.
Overall, almost 85% of the study cohort was tested IgG seropositive for at least one of the three arboviruses investigated in this study, of which approximately 10% had evidence for exposure to all the three viruses. The co-circulation of the three arboviruses is explained by the presence of the mosquito vectors in the region studied. Indeed, a previous study in Mali using samples from acutely ill patients testing negative for malaria and yellow fever reported the presence of IgG antibodies of up to 40.0% and 8.4% for DENV and CHIKV, respectively.8 O’Hearn et al.36 found evidence for the presence of flavivirus (52.9%) and other hemorrhagic fever viruses in Sierra Leone. The presence of viral antibodies to multiple arboviruses in our study corresponded to the levels of exposure to different viral pathogens in the O’Hearn study.36 Thus, co-circulation of arboviruses in southern Mali is of medical and public health importance because some of the viruses have shown epidemic potential.
As discussed earlier, accumulation of IgG seroprevalence for the three arborviruses in older age is not surprising, but a significant seroprevalence of IgG antibodies against DENV, CHIKV, and ZIKV was already found in children under 5 years of age. This indicates exposure to mosquito-borne arboviruses early in life, reflecting maternal antibodies, exposure at very young age, or likely a combination of both.37–39
Our study has several limitations that need to be addressed in the future. The study cohort was small, and larger enrollment numbers could have changed the seroprevalence data. Acknowledging potential cross-reactivity among flaviviruses, especially DENV and ZIKV, virus neutralization assays should have been considered to distinguish among flavivirus infections, although acute arbovirus infections could have been detected by molecular assays or IgM seroprevalence. Unfortunately, both aspects could not be addressed because only a limited amount of serum remained for this study. Future, larger serosurveys on healthy individuals as well as febrile patients are planned.
CONCLUSION
Our study identified the co-circulation of three mosquito-borne arboviruses (DENV, CHIKV, and ZIKV) in southern Mali, an area hyperendemic for malaria. Therefore, arbovirus infections need to be considered as causes of febrile diseases. In addition, co-infections of arboviruses and Plasmodium ssp. are likely to occur, although we did not directly address this in our study. Diagnostics for arboviruses will be instrumental for future public health intervention and case patient management. Further studies are needed to gain a better understanding of the epidemiology and clinical significance of arbovirus infections in Mali and elsewhere in sub-Saharan Africa.
ACKNOWLEDGMENTS
We are indebted to the village chiefs and elders as well as the entire population of Soromba, Bamba, and Banzana for supporting our work in their communities. This study would not have been possible without the assistance of the local and regional medical personnel. We thank Richard Sakai, Joseph Shott, and Mark Pineda (all Division of Intramural Research [DIR], National Institute of Allergy and Infectious Diseases [NIAID], NIH at the time of the study) for logistical support.
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