E-ISSN 2146-9369 | ISSN 2146-3158
 

Research Article


J. Microbiol. Infect. Dis., (2024), Vol. 14(1): 8–12

Original Research

10.5455/JMID.2024.v14.i1.2

First report of dengue virus among febrile malaria positive and negative patients in Nyala city, Western Sudan

Smah Ishag1, Abdel Rahim M. El Hussein2, Isam M. Elkhidir3 and Khalid Enan2*

1Department of Medical Microbiology, Faculty of Medical Laboratory Science, National University of Sudan, Khartoum, Sudan

2Department of Virology, Central Laboratory, The Ministry of Higher Education and Scientific Research, Khartoum, Sudan

3Department of Microbiology and Parasitology, Faculty of Medicine, University of Khartoum, Khartoum, Sudan

*Corresponding Author: Khalid Enan. Department of Virology, Central Laboratory, The Ministry of Higher Education and Scientific Research, Khartoum, Sudan. Email: khalid.enan [at] gmail.com

Submitted: 29/08/2023 Accepted: 24/03/2024, Published: 31/03/2024


Abstract

Background: The mosquito-borne dengue fever and malaria are major public health concerns in tropical settings. They are highly prevalent and considered one of the main etiology of febrile illnesses in Sudan.

Aim: This study aimed to determine the seroprevalence of dengue virus (DENV) among febrile malaria positive and negative patients in Nyala city, Western Sudan by using Enzyme linked immunosorbent assay (ELISA) to detect DENV IgM and IgG antibodies. It also aimed to study possible risk factors that may be associated with DENV and malaria infections.

Methods: This cross-sectional study was undertaken in different Hospitals in Nyala city, South Darfur state Sudan from June to December 2021. A total of 93 blood samples from febrile patients were collected in EDTA containers. Plasma was obtained by centrifugation and tested by ELISA (EUROIMMUN, Germany) according to manufacturer instructions for DENV IgG and IgM antibodies. Malaria parasites were detected using microscopy of stained blood smears. Generated data was analyzed using the statistical package (SPSS) version 21.

Results: Forty-six (49.5%) out of 93 febrile patients were found infected with malaria parasites using blood smear microscopy. Among these malaria-infected patients, the prevalence of dengue anti-virus IgG (49.5%) was higher than that of IgM (16.1%) but was statistically insignificant (p > 0.05). In the present study, dengue infection was higher in males than in females but was statistically insignificant (p > 0.05) and the age group 21–40 years was the most affected with DENV infection.

Conclusion: The present study showed a higher prevalence rate of dengue IgG among the participants of the study more than IgM but was statistically insignificant. There was no association between age and gender with seroprevalence of DENV among febrile patients with and without malaria. The frequent existence of infections of DENV requires improved surveillance and control measures to combat this disease in Nyala, Sudan.

Keywords: Dengue, Malaria, ELISA, Nyala City, Sudan.


Introduction

Dengue is a mosquito-borne arboviral disease with ever-increasing public health importance. Worldwide, dengue virus (DENV) is an arbovirus disease with increasing public health importance, the incidence of dengue has increased by 30-fold in the last half century (Hadinegoro, 2012). New countries are declining their first outbreaks that seriously disturb communities and drain economies (Shepard et al., 2011). Currently, dengue is reported as the most prevalent mosquito-borne viral infection worldwide, with substantial human health and economic costs (Guzman et al., 2010). Dengue is caused by any of the dengue serotypes (Chen et al., 2011). Dengue is mainly a tropical disease transmitted by mosquitoes of the genus Aedes (Ong et al., 2021). DENV is an RNA virus in the genus Flavivirus in the family Flaviviridae. The virus has four serotypes (Den-1, Den-2, Den-3, and Den-4), is transmitted principally by infected Aedes aegypti mosquito, and the disease is manifested as dengue, with or without normal dengue fever or as an aggravated disease. Classical dengue fever is the most prevalent type of the disease and, is manifested by sudden onset of headache, malaise, fever, anorexia, muscle and joint pains, lymphadenopathy, and rash (Kularatne et al., 2015). aggravated dengue is characterized by dengue-shocked disease leakage of plasma, hemorrhage, and signs of severe organ dysfunction, such as elevated hepatic enzymes and impaired consciousness (Chen et al., 2011). The case fatality rate of aggravated dengue can exceed 5% and figures as high as 44% have been documented (Withana et al., 2014). Half a million dengue infections are estimated to occur each year and approximately 2.5 billion people live in dengue-endemic countries (Bhatt et al., 2013). In Sudan, several epidemics of DENV infections have been recorded in Eastern Sudan (Red Sea and Kassala States) (Malik et al., 2011; Seidahmed et al., 2012; Abdullah et al., 2025). In Sudan, several epidemics of DENV infections have been reported in Eastern and Western. DENV-1 and DENV3 were associated with disease outbreaks in these States (Soghaier et al., 2014; Ahmed et al., 2019). DENV-1 and DENV-3 were reported in these States, while DENV serotype-1 and DENV serotype-2 were reported for the first time in the Red Sea State. Investigation into DENV incidence in Sudan has produced variable results due to geographic, temporal, and methodological differences. On the other hand, Malaria is a serious public health problem caused by Plasmodium spp. that is transmitted by the bite of female Anopheles mosquitoes (Pimenta et al., 2015). There are about 200 million annual cases and more than 400,000 deaths worldwide, and it affects populations in more than 100 countries. Most countries in tropical and subtropical areas, especially in sub-Saharan Africa, South America, and Southeast Asia, are the worst affected (Rebaudet et al., 2010; Kar et al., 2014). Five species of malaria parasites (Plasmodium falciparum, Plasmodium vivax, Plasmodium ovale, Plasmodium malariae and recently, Plasmodium knowlesi) are known to infect humans, of which P. falciparum and P. vivax are the most common. P. falciparum causes malaria with severe clinical symptoms. Fever, chills, headache, fatigue, nausea, and vomiting are some of the most encountered clinical indications of the disease (Bartoloni et al., 2012). As dengue fever and malaria are both prevalent and coexist over a wide range of their distribution, therefore, early differentiation between dengue and malaria febrile illnesses could help clinicians identify patients who should be closely monitored for signs of dengue hemorrhagic fever, dengue shock syndrome, or severe malaria.

The goal of this study was to evaluate the prevalence of DENV antibodies among febrile malaria positive and negative patients in Nyala city, Western Sudan by using Enzyme linked immunosorbent assay (ELISA) to detect DENV IgM and IgG antibodies.


Method and Materials

Study area

This study was conducted in different Hospitals (Health Insurance Centers, Aleithar Clinic, Alabrar Clinic) in Nyala city, South Darfur state, Sudan.

Study design

This is a cross-sectional study that was carried out during the period from June to December 2021.

Patients inclusion criteria and sample size

Ninety-three febrile patients who were either malaria positive or negative were included in the study, all participating patients were given written informed consent from adult patients, or from parents or legal guardians of children.

Blood sample collection

A blood sample was collected in EDTA containers. Plasma obtained was used for ELISA.

Determination of malaria infection

This was done by microscopic examination of blood films stained with Giemsa, stain.

ELISA

Commercial ELISA Kits (EUROIMMUN, Germany) were used according to manufactures’ instructions.

Data analysis

Generated results were analyzed using the statistical package (SPSS) version 21.

Ethical approval

The approval of this study was obtained by the Ethical Review Committee (ERC) of the Ministry of Health Khartoum State, Sudan.


Result

A total of 93 febrile patients were enrolled in this study comprising 38 males and 55 females, with a mean age of 29.6 ± 14.3 (Tables 1 and 2) Malaria parasites were detected in 46(49.5%) out of the patients and IgM antibodies were detected in 15(32.6%) of them, while all 46 were positive for IgG. There was no significant relation between IgG and Gender (p=0.383). The prevalence of dengue antibodies among malaria-negative patients was 46.8% and 40% for IgG and IgM respectively (Table 3).

Table 1. Correlation between gender and IgG and IgM positivity.

Table 2. Correlation between age groups and IgG and IgM positivity.

Table 3. Correlation between BFFM and IgG and IgM.

The relation between ag and IgG is shown in Table 1. There was no significant relation between IgG and age (p=0.465).

There was no significant relation between IgM and age respectively (p=0.904) (Table 2). Furthermore, there was no significant relation between IgG and IgM and BFFM positivity (Table 3).


Discussion

DENV is an important reemerging disease in tropical and sub-tropical countries. The differential diagnosis associated with dengue fever includes a wide variety of parasitic and bacterial infections that produce similar syndrome.

This study has shown that malaria is not the only mosquito-borne illness that is associated with fever in Nyala city, as evidenced by the fact that 15(16.1%) out of the 93 patients showed IgM antibodies indicating recent infection. This finding is higher than the 1.8% positivity reported by Idoko et al. (2015) in Nigeria.

Similarly, the high prevalence (49.5%) of dengue IgG antibodies obtained in this study may suggest that dengue fever has been occurring in the study area for some time.

The high IgG prevalence may also be due to the fact that we targeted febrile patients and that these patients may have passed the acute stage. Probably if the research recruited apparently healthy subjects, our finding might not differ from recent results obtained by Katnap et al. (2020) in Nigeria who reported an IgG prevalence of 2.7%.

In this study, the incidence of malaria was found to be 49.5%, which further confirms the endemicity of malaria in the Nyala city reported over the years. Of the 46 (49.5%) who had malaria, there was a statistically insignificant relation between dengue fever and malaria (p > 0.05) this finding is in agreement with Katnap et al. (2020) who found an insignificant relationship between dengue and malaria.

The correlation between age groups with dengue infection was found to be non-significant. In this study IgG was most noted in the age group 21–40 years (29.03%) with an average age of 29 years, followed by 41–60 years (10.7%) then 10–20 years (7.5%) and the least infected category was the 61–80 years (0%). This result may reflect the higher activity of young people that makes them more at risk of dengue fever infections.

In this study, IgM was also most observed in the age group 21–40 years (7.5%), then 41–60 years (4.3%), then 10–20 years (3.2%) and the least infected category was 61–80 years (0%). This result may again reflect the higher activity of young people These results were similar to Ayyub et al. (2006) and Madani et al. (2013).

However, there is an unstable relationship between dengue infection and the age groups. Serious dengue infection was reported among children and old people a fact that reflects the association between serious dengue infection and the human immune system (Pimenta et al., 2015).

Furthermore, the distribution of dengue infection was insignificantly higher in males (73%) than in females (60%) (p > 0.05). These findings are in line with other studies from Saudi Arabia and Yemen (Bin Ghouth et al., 2010).

Dengue vector(s) control is required to prevent the spread of the virus and to reduce the impact of disease burden in Sudan as well as in other African countries. Entomological studies are needed to determine the distribution of the vector in Southern Darfur to ease the control and management of the disease. Especially in the hot and dry weather of Nyala city, which presumably does not furnish a suitable habitat for the breeding of the mosquito vector.

This result is very important because Nyala city is one of the areas where investigation of febrile illnesses is limited to malaria and perhaps typhoid fever with complete neglect to viral infections.

To the best of our knowledge, this is the first report of DENV infection in Nyala city. This is probably due to the absence of large outbreaks that attract a lot of attention. This is probably will happen soon as has occurred in Eastern Sudan due to climate changes that can lead to environmental and social conditions suitable for vector reproduction and survival with increased arboviral transmission.


Conclusion

In the present study high rate of circulating DENV IgG was noted among the participants, albeit there was no association between age and gender in seroprevalence of DENV among febrile patients with and without malaria. The frequent occurrence of DENV infections emphasizes the need for improved surveillance programs and prevention measures to combat this important arboviral disease in the study area. The serotype(s) of the infecting DENV in the area is also urgently needed to be identified.


Acknowledgment

None.

Funding

This study was fully financially supported by the Central Laboratory, the Ministry of Higher Education and Scientific Research, Khartoum, Sudan.

Conflict of interest

The authors declare that there is no conflict of interest.

Data availability

All data are provided in the manuscript.

Authors contributions

All authors contributed to this study. All authors read and approved the final manuscript.


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How to Cite this Article
Pubmed Style

Ishag S, Hussein ARME, Elkhidir IM, Enan KA. First report of dengue virus among febrile malaria positive and negative patients in Nyala city, Western Sudan. J Microbiol Infect Dis. 2024; 14(1): 8-12. doi:10.5455/JMID.2024.v14.i1.2


Web Style

Ishag S, Hussein ARME, Elkhidir IM, Enan KA. First report of dengue virus among febrile malaria positive and negative patients in Nyala city, Western Sudan. https://www.jmidonline.org/?mno=167433 [Access: May 25, 2024]. doi:10.5455/JMID.2024.v14.i1.2


AMA (American Medical Association) Style

Ishag S, Hussein ARME, Elkhidir IM, Enan KA. First report of dengue virus among febrile malaria positive and negative patients in Nyala city, Western Sudan. J Microbiol Infect Dis. 2024; 14(1): 8-12. doi:10.5455/JMID.2024.v14.i1.2



Vancouver/ICMJE Style

Ishag S, Hussein ARME, Elkhidir IM, Enan KA. First report of dengue virus among febrile malaria positive and negative patients in Nyala city, Western Sudan. J Microbiol Infect Dis. (2024), [cited May 25, 2024]; 14(1): 8-12. doi:10.5455/JMID.2024.v14.i1.2



Harvard Style

Ishag, S., Hussein, . A. R. M. E., Elkhidir, . I. M. & Enan, . K. A. (2024) First report of dengue virus among febrile malaria positive and negative patients in Nyala city, Western Sudan. J Microbiol Infect Dis, 14 (1), 8-12. doi:10.5455/JMID.2024.v14.i1.2



Turabian Style

Ishag, Smah, Abdel Rahim M El Hussein, Isam M Elkhidir, and Khalid A Enan. 2024. First report of dengue virus among febrile malaria positive and negative patients in Nyala city, Western Sudan. Journal of Microbiology and Infectious Diseases, 14 (1), 8-12. doi:10.5455/JMID.2024.v14.i1.2



Chicago Style

Ishag, Smah, Abdel Rahim M El Hussein, Isam M Elkhidir, and Khalid A Enan. "First report of dengue virus among febrile malaria positive and negative patients in Nyala city, Western Sudan." Journal of Microbiology and Infectious Diseases 14 (2024), 8-12. doi:10.5455/JMID.2024.v14.i1.2



MLA (The Modern Language Association) Style

Ishag, Smah, Abdel Rahim M El Hussein, Isam M Elkhidir, and Khalid A Enan. "First report of dengue virus among febrile malaria positive and negative patients in Nyala city, Western Sudan." Journal of Microbiology and Infectious Diseases 14.1 (2024), 8-12. Print. doi:10.5455/JMID.2024.v14.i1.2



APA (American Psychological Association) Style

Ishag, S., Hussein, . A. R. M. E., Elkhidir, . I. M. & Enan, . K. A. (2024) First report of dengue virus among febrile malaria positive and negative patients in Nyala city, Western Sudan. Journal of Microbiology and Infectious Diseases, 14 (1), 8-12. doi:10.5455/JMID.2024.v14.i1.2