Authors:
Md. Abdur Rob Department of Medicine, Chittagong Medical College, Chattogram-4203, Bangladesh
Asperia Health Research and Development Foundation, Chattogram-4203, Bangladesh

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Mohabbat Hossain Department of Genetic Engineering and Biotechnology, University of Chittagong, Chattogram-4331, Bangladesh

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M.A. Sattar Department of Medicine, Chittagong Medical College, Chattogram-4203, Bangladesh

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Istiaq Uddin Ahmed Asperia Health Research and Development Foundation, Chattogram-4203, Bangladesh

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Abul Faisal Md. Nuruddin Chowdhury Department of Medicine, Chittagong Medical College, Chattogram-4203, Bangladesh

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H.M. Hamidullah Mehedi Department of Medicine, 250 Bedded General Hospital Chattogram, Chattogram-4000, Bangladesh

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Noor Mohammed Department of Medicine, Chittagong Medical College, Chattogram-4203, Bangladesh

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Mohammed Maruf ul Quader Department of Paediatric Nephrology, Chittagong Medical College, Chattogram-4203, Bangladesh

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Md. Zakir Hossain Department of Microbiology, Bangladesh Institute of Tropical & Infectious Diseases (BITID), Chattogram-4317, Bangladesh

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Mustafizur Rahman Virology Laboratory, Infectious Diseases Division, Icddr,b, Mohakhali, Dhaka 1212, Bangladesh

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Kallyan Chakma Department of Genetic Engineering and Biotechnology, University of Chittagong, Chattogram-4331, Bangladesh
Next Generation Sequencing, Research and Innovation Lab Chittagong (NRICh), Biotechnology Research & Innovation Centre (BRIC), University of Chittagong, Chattogram-4331, Bangladesh

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Susmita Barua Department of Genetic Engineering and Biotechnology, University of Chittagong, Chattogram-4331, Bangladesh
Next Generation Sequencing, Research and Innovation Lab Chittagong (NRICh), Biotechnology Research & Innovation Centre (BRIC), University of Chittagong, Chattogram-4331, Bangladesh

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Silvia Naznin Etu Department of Genetic Engineering and Biotechnology, University of Chittagong, Chattogram-4331, Bangladesh
Next Generation Sequencing, Research and Innovation Lab Chittagong (NRICh), Biotechnology Research & Innovation Centre (BRIC), University of Chittagong, Chattogram-4331, Bangladesh

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Uschash Sikder Department of Genetic Engineering and Biotechnology, University of Chittagong, Chattogram-4331, Bangladesh
Next Generation Sequencing, Research and Innovation Lab Chittagong (NRICh), Biotechnology Research & Innovation Centre (BRIC), University of Chittagong, Chattogram-4331, Bangladesh

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Afroza Akter Tanni Department of Genetic Engineering and Biotechnology, University of Chittagong, Chattogram-4331, Bangladesh
Next Generation Sequencing, Research and Innovation Lab Chittagong (NRICh), Biotechnology Research & Innovation Centre (BRIC), University of Chittagong, Chattogram-4331, Bangladesh

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Adnan Mannan Department of Genetic Engineering and Biotechnology, University of Chittagong, Chattogram-4331, Bangladesh
Next Generation Sequencing, Research and Innovation Lab Chittagong (NRICh), Biotechnology Research & Innovation Centre (BRIC), University of Chittagong, Chattogram-4331, Bangladesh

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Open access

Abstract

Dengue is a serious epidemic for Bangladesh affecting thousands of lives. This study aimed to identify and determine the prevalence of the circulating variants of dengue virus (DENV) and their association with demographics and clinical manifestations among the dengue-infected patients. A total of 711 participants with NS1 antigen positivity were enrolled, followed by viral RNA extraction from the collected blood samples and a multiplex real-time reverse transcription-polymerase chain reaction (RT-PCR) assay to determine the dengue virus serotypes. Of 711 dengue-infected patients, 503 (70.7%) were male. Among different age groups, most of the patients were 21–30 years old (n = 255, 35.9%). The DENV2 (n = 483, 67.9%) serotype was more prevalent than the DENV3 (n = 144, 20.3%) and DENV1 (n = 84, 11.8%). The duration of fever was highest in the DENV-1 patients (4.79 ± 1.84 days) in contrast to DENV-3 (4.48 ± 1.68 days) and DENV-2 (4.33 ± 1.45 days) (P = 0.039). Importantly, five highly populated areas were identified as dengue hotspots in Chittagong metropolitan city. Our results provide crucial insights into the patterns of dengue virus transmission and severity among southern Bangladeshi population, thereby aiding in the development of targeted public health interventions and management strategies to combat future outbreaks.

Abstract

Dengue is a serious epidemic for Bangladesh affecting thousands of lives. This study aimed to identify and determine the prevalence of the circulating variants of dengue virus (DENV) and their association with demographics and clinical manifestations among the dengue-infected patients. A total of 711 participants with NS1 antigen positivity were enrolled, followed by viral RNA extraction from the collected blood samples and a multiplex real-time reverse transcription-polymerase chain reaction (RT-PCR) assay to determine the dengue virus serotypes. Of 711 dengue-infected patients, 503 (70.7%) were male. Among different age groups, most of the patients were 21–30 years old (n = 255, 35.9%). The DENV2 (n = 483, 67.9%) serotype was more prevalent than the DENV3 (n = 144, 20.3%) and DENV1 (n = 84, 11.8%). The duration of fever was highest in the DENV-1 patients (4.79 ± 1.84 days) in contrast to DENV-3 (4.48 ± 1.68 days) and DENV-2 (4.33 ± 1.45 days) (P = 0.039). Importantly, five highly populated areas were identified as dengue hotspots in Chittagong metropolitan city. Our results provide crucial insights into the patterns of dengue virus transmission and severity among southern Bangladeshi population, thereby aiding in the development of targeted public health interventions and management strategies to combat future outbreaks.

Introduction

Dengue is a viral infectious disease that can present with a variety of symptoms, ranging from mild fever to severe hemorrhagic fever. Humans are the primary host for this virus, which spreads through a human-mosquito-human cycle, predominantly in tropical and subtropical regions worldwide. This flu-like illness has spread to about more than 100 countries, with an annual estimation of 390 million dengue virus infections, of which only 96 million people manifest clinically [1]. The recent surge in dengue incidence has shown significant year-to-year fluctuations in the timing and enormity of seasonal peaks, with a constantly increasing case fatality rate every year [2]. The four structurally similar but antigenically distinct dengue virus (DENV) serotypes (DENV1-DENV4) have been found to be circulating in various types of population [3, 4]. Research indicates that the shifting of these serotypes during an outbreak can serve as an underlying cause of changes in clinical characteristics. Additionally, individuals infected with one serotype exhibit long-term immunity to that specific serotype, but not to the other serotypes, which can lead to multiple infections (secondary and tertiary), potentially resulting in dengue shock syndrome. This type of serotype-specific clinical manifestation and the related disease severity can be explained by the antibody-dependent enhancement theory [5, 6]. Multiple dengue serotypes have also been co-detected in recent outbreaks, underscoring the severity of the situation. Bangladesh, a densely populated South Asian country with over 165 million people has been reported as a dengue-endemic country since the first recorded outbreak in 2000. Due to multiple risk factors, Bangladesh has been experiencing successive major dengue outbreaks in recent years [7]. Between 2000 and 2022, 788 dengue related fatalities have been found in Bangladesh; with 492 (more than 62%) of these deaths occurring between 2019 and 2022 [8]. Although dengue is endemic in Bangladesh, it has been reported as a public health issue in Bangladesh due to its recurrent outbreaks by the World Health Organization in 2014. The fatality rate due to dengue infection is significantly associated with dengue serotypes. Since the largest outbreak in 2019, DENV-3 has been found to be the most prevalent circulating serotype. The recent re-emergence of the DENV-4 serotype, absent for over 20 years, could pose a significant public health threat to Bangladesh due to the potential for secondary infections [7]. Given the severity of the 2023 dengue outbreak in Bangladesh, as well as the lack of data on the prevalence of circulating DENV serotypes and genotypes, in this study, we aimed to identify and determine the prevalence of the circulating variants of DENV and their association with demographics and clinical manifestations among the dengue-infected patients in the Chittagong region. Our study highlights the genetic variations of circulating DENV, which could have implications for diagnostic and prophylactic interventions for dengue in Bangladesh.

Materials and methods

Study participants and sample collection

A total of 711 participants from the One Stop Emergency and Casualty Unit and Paediatrics Departments of Chattogram Medical College Hospital, Chittagong General Hospital, Bangladesh Institute of Tropical and Infectious Diseases, Asperia Health Care Ltd., and Fatikchari Health complex were enrolled in the study. Briefly, all the participants presenting with an acute, undifferentiated fever within 3 days of onset who tested positive for dengue NS1 antigen (STANDARDTM Q Dengue NS1 Ag, SD Biosensor, Korea) were included in this study. In a recent study, the sensitivity of the STANDARDTM Q Dengue NS1 Ag test kit was found to be 99.1% in rapid diagnostic tests for the detection of dengue infections [9]. The patients were prospectively reviewed for detailed demographics, signs and symptoms, comorbid conditions, secondary dengue infection, and so on. 3 ml of venous blood were collected from each patient in ethylenediamine tetraacetic acid (EDTA) containing a vacutainer providing a unique ID, and the collected blood samples with DENV transported to the lab at a proper temperature (2–8 °C) and stored at −80 °C until analysis.

Viral RNA extraction and real-time reverse transcription-polymerase chain reaction (RT-PCR)

Viral RNA was extracted from the collected blood samples by using the High Pure Viral RNA Kit, (Roche Diagnostics, Indianapolis, USA) following the manufacturer's instructions. The concentration and purity of the extracted viral RNA were measured using NanoDropTM 2000 (Thermo Fisher Scientific, Waltham, MA, USA). Extracted viral RNA samples were used immediately for a multiplex real-time reverse transcription-polymerase chain reaction (RT-PCR) assay on Light Cycler 96 (Roche Diagnostics, Switzerland) to determine the dengue virus serotypes by using the RealStar Dengue Type RT-PCR Kit 1.0 (Altona Diagnostics, Hamburg, Germany), as per the manufacturer's instructions. This RT-PCR kit was chosen based on availability as well as the findings of a recent published study on the evaluation of sensitivity (100% for DENV-3 and DENV-4, 86.7% for DENV-1 and DENV-2) and specificity (97.9%–100% for all four serotypes) [10]. Briefly, the reaction was carried out with a reaction volume of 30 μL containing 20 μL master mix and 10 μL extracted viral RNA. The cycling conditions were 55 °C for 20 min for the reverse transcription, followed by 2 min at 95 °C for the initial denaturation, and 45 cycles of amplification with cycling conditions of 95 °C for 15 s, 60 °C for 45 s, and 72 °C for 15 s. In the case of PCR result interpretation, a cycle threshold (Ct) < 38 was evaluated as positive. 20% (n = 142) of the positive test results for DENV were further validated by using the STANDARDTM M10 Arbovirus Panel with the STANDARD M10 system (SD Biosensor, Suwon-si, Gyeonggi-do, Korea) according to the manufacturer's protocol. The STANDARDTM M10 Arbovirus Panel is a molecular in vitro diagnostic test that detects and differentiates arboviruses such as dengue virus, zika virus, chikungunya virus, yellow fever virus, and west Nile virus RNA by nucleic acid amplification using RT-PCR. As a result, this number of DENV samples was chosen at random, focusing on positive samples with a Ct value greater than 35, which covered all three identified DENV serotypes by the RealStar Dengue Type RT-PCR Kit, in order to assess the kit's detection ability at extremely low Ct values close to negative for DENV and the sensitivity and specificity as well.

Statistical analysis

Windows-based software (GraphPad Prism 9) was used to produce a statistical analysis of the variables. The chi-square test was used to compare the categorical variables, while the numerical data were expressed as the mean with a standard deviation (±SD). 95% confidence intervals were calculated for these values. A P value less than 0.05 was considered statistically significant.

Ethical approval and consent to participate

The Institutional Review Board of the Chittagong Medical College, Chattogram, Bangladesh approved the study. All participants of the study were informed of the purpose and methods of the investigation. Each patient provided written consent before participating in the study. Participation in the study was voluntary. The investigators collected personal information and other pertinent medical data using a semi-structured questionnaire. Blood samples from each patient were submitted to the lab after they were assigned a unique identification code (ID, anonymous or numerical). The principal investigator documented the test findings by decoding the IDs and adding them to the main dataset.

Results

Demographics and dengue virus serotypes

A total of 711 laboratory-confirmed (NS1 antigen) dengue patients were enrolled in the study between June and September 2024, of whom 503 (70.7%) were male. Among different age groups, most of the dengue-infected patients were 21–30 years old (n = 255, 35.9%), followed by 11–20 years old (n = 180, 25.3%), 31–40 years old (n = 123, 17.3%), 0–10 years old (n = 51, 7.2%), 41–50 years old (n = 48, 6.8%), 51–60 years old (n = 36, 5.1%), 61–70 years old (n = 15, 2.1%), and 71–80 years old (n = 3, 0.4%). Of the 711 dengue-infected patients, RT-PCR results showed that 84 (11.8%) of them were infected with DENV-1, 483 (67.9%) were DENV-2, and 144 (20.3%) were DENV-3. The DENV-4 serotype was not identified among the patients. Notably, 15 (2.1%) of the patients had a history of previous infection with dengue virus, but the serotypes were not confirmed, and the majority (n = 705, 99.2%) of the dengue-infected patients did not take any medication to recover from dengue infection. Additionally, 126 (17.7%) of the patients had comorbid conditions, in whom diabetes (21.4%) and hypertension (21.4%) were mostly found, followed by eye problems (14.3%), asthma/bronchitis (7.1%), cardiovascular diseases (7.1%), renal diseases (4.8%), and others (9.5%). Moreover, 579 (81.4%) of the patients felt less active or irritable during their illness (Table 1).

Table 1.

Characteristics of laboratory-confirmed dengue patients (N = 711)

CharacteristicsNo. of patients% of patients
Sex
Male50370.7
Female20829.3
Age group (years)
0–10517.2
11–2018025.3
21–3025535.9
31–4012317.3
41–50486.8
51–60365.1
61–70152.1
71–8030.4
>8000
Dengue virus serotype
DENV-18411.8
DENV-248367.9
DENV-314420.3
DENV-400
History of previous dengue infection
Yes152.1
No69697.9
History of previous medication for dengue infection
Yes60.8
No70599.2
Comorbid conditions
No58582.3
Yes12617.7
Allergy64.8
Asthma/Bronchitis97.1
Diabetes2721.4
Cardiovascular diseases97.1
Hypertension2721.4
Hypotension32.4
Jaundice32.4
Renal diseases64.8
Eye problem1814.3
Tuberculosis32.4
Urinary tract infection32.4
Others129.5
Activity level during illness
Normal13218.6
Less Active/Irritable57981.4

Significant correlation between age and infection with different serotypes was not found in the study (Fig. 1). Male patients had a greater proportion of infections with respective DENV serotypes compared with female patients. The gender distribution of DENV-1, DENV-2, and DENV-3 was 73.8% male and 26.2% female, 70.8% male and 29.2% female, and 68.8% male and 31.2% female, respectively (Fig. 2).

Fig. 1.
Fig. 1.

One-way ANOVA (mixed-effects analysis) for the comparison of ages among three dengue virus serotypes (DENV). P value less than 0.05 was considered as statistically significant

Citation: European Journal of Microbiology and Immunology 14, 3; 10.1556/1886.2024.00069

Fig. 2.
Fig. 2.

Distribution of gender infected with dengue virus serotypes DENV-1, DENV-2, and DENV-3

Citation: European Journal of Microbiology and Immunology 14, 3; 10.1556/1886.2024.00069

Comparative analysis between different age groups and infection with three dengue serotypes showed that the DENV-1 genotype was more prominent in the age groups of 0–10 years (10.7%), 41–50 years (10.7%), and 61–70 years (3.6%) compared with DENV-2 and DENV-3. The DENV-2 genotype was most prevalent in the age group of 21–30 years (37.3%) compared with other genotypes. In addition, the DENV-3 genotype was found mostly in the age group of 11–20 years (33.3%), followed by 31–40 years (22.9%), and 51–60 years (8.3%), compared with the DENV-2 and DENV-3 genotypes (Fig. 3).

Fig. 3.
Fig. 3.

Distribution of dengue virus serotypes DENV-1, DENV-2 and DENV-3 infected patients among different age groups

Citation: European Journal of Microbiology and Immunology 14, 3; 10.1556/1886.2024.00069

Dengue hotspots in Chittagong

Dengue risk zones in the Chittagong region were analyzed based on the detection of DENV serotypes among the study patients. 60% of dengue patients in Chittagong lived in five areas that are identified as hotspots, namely Bakalia, Chawkbazar, Kotwali, Double Mooring, and Baizid Bostami. Also, among the rural areas, the maximum number of patients were found in Sitakundu, Hathhazari, Patia, and Karnaphuli areas (Fig. 4).

Fig. 4.
Fig. 4.

Distribution of dengue hotspots in Chittagong region. A. Study area map of rural areas of Chattogram (outside City Corporation), B. Study map of urban areas of Chattogram (inside City Corporation)

Citation: European Journal of Microbiology and Immunology 14, 3; 10.1556/1886.2024.00069

Clinical manifestation

All the dengue cases (n = 711) infected with three different serotypes (DENV-1, DENV-2, and DENV-3) had fever (100%). Infected cases with DENV-3 were more likely to have headaches (75%), in contrast to DENV-2 and DENV-1, less likely to be observed. Instead, DENV-2 cases were more likely to present with muscle pain (54%), compared with DENV-1 (39.3%) and DENV-2 (47.9%). Anorexia was found mostly in cases with DENV-2 (73.9%), and cases with eye pain were mostly infected with DENV-3 (45.8%). Additionally, cases with DENV-1 infection had the highest proportion (28.6%) of abdominal pain, and 12.5% of the patients showed breathing difficulties who were infected with DENV-3. However, there were no significant differences in vomiting, watery stool, runny nose, rash, or bleeding among the three serotypes (Fig. 5).

Fig. 5.
Fig. 5.

Clinical manifestations by dengue virus serotypes DENV-1, DENV-2 and DENV-3 among the study patients

Citation: European Journal of Microbiology and Immunology 14, 3; 10.1556/1886.2024.00069

Table 2 shows the comparison of the duration of several clinical manifestations among the cases infected with three different dengue serotypes. Though DENV-2 (n = 483, 67.9%) was the most prevalent serotype among the cases, the duration of fever was highest in the patients infected with DENV-1 (mean ± SD, 4.79 ± 1.84 days) in contrast to DENV-3 (mean ± SD, 4.48 ± 1.68 days) and DENV-2 (mean ± SD, 4.33 ± 1.45 days) (P = 0.039). The duration of having a headache was higher in the cases with DENV-1 (mean ± SD, 4.60 ± 1.62 days) compared to the DENV-2 (mean ± SD, 3.93 ± 1.42 days) and DENV-3 (mean ± SD, 3.86 ± 1.60 days) (P = 0.0129). Cases with DENV-1 experienced eye pain for a longer period (mean ± SD, 4.89 ± 2.33 days) compared to DENV-2 (mean ± SD, 3.85 ± 1.39 days) and DENV-3 (mean ± SD, 3.64 ± 1.87 days) (P = 0.0032). In addition, the duration of having watery stool was highest in the patients infected with DENV-1 (mean ± SD, 3.22 ± 1.87 days) versus DENV-3 (mean ± SD, 3.18 ± 1.69 days) and DENV-2 (mean ± SD, 2.45 ± 1.01 days) (P = 0.0008). Moreover, cases with DENV-1 were longer compromised by runny noses (mean ± SD, 4.57 ± 1.18 days) compared to DENV-2 (mean ± SD, 3.73 ± 1.72 days) and DENV-3 infected patients (mean ± SD, 3.44 ± 1.84 days) (P = 0.0424). However, significant differences were not observed for the duration of having muscle pain, vomiting, or anorexia among the three dengue serotypes.

Table 2.

Comparison of duration of the clinical manifestations among the cases infected with three different dengue virus serotypes

Clinical manifestationsDENV-1 (N = 84)DENV-2 (N = 483)DENV-3 (N = 144)P value*
NDuration (days)NDuration (days)NDuration (days)
(mean ± SD)(mean ± SD)(mean ± SD)DENV-1 vs. DENV-2DENV-1 vs. DENV-3DENV-2 vs. DENV-3
Fever844.79 ± 1.844834.33 ± 1.451444.48 ± 1.680.0350.3220.566
Headache454.60 ± 1.623093.93 ± 1.421083.86 ± 1.600.0140.0150.905
Eye pain274.89 ± 2.331863.85 ± 1.39663.64 ± 1.870.0070.0030.620
Muscle pain334.73 ± 2.002614.07 ± 1.60694.26 ± 1.800.0850.8280.588
Vomiting453.27 ± 2.232552.69 ± 1.53812.74 ± 1.730.0940.2190.975
Watery stool273.22 ± 1.871322.45 ± 1.01513.18 ± 1.690.0200.9890.004
Runny nose274.57 ± 1.181323.73 ± 1.72483.44 ± 1.840.0940.0330.577
Anorexia334.81 ± 1.943574.29 ± 1.44874.34 ± 1.730.0430.1730.960

DENV = dengue virus serotype; N = no. of dengue virus infected patients; SD = standard deviation

*P value was calculated based on Tukey's multiple comparison test comparing each dengue virus serotype with the other two serotypes and P value less than 0.05 was considered statistically significant (marked bold).

Discussion

Bangladesh has been facing frequent dengue fever outbreaks since the dengue virus (DENV) emerged in 2000 [11]. In 2022, the nation faced the second-largest outbreak (62,382 cases and 281 deaths), followed by the most devastating dengue fever outbreak in the history of the nation in 2023, with the highest case fatality rate (321,179 cases and 1,705 deaths) [12].

Distribution of sex

Our study found a consistent disparity among the male and female patient numbers across all three serotypes, with male patients accounting for around 70% of the cases whereas females contributed nearly 30% (Table 1). This finding is consistent with previous studies reporting similar gender disparity patterns of dengue prevalence in Bangladesh and neighboring Asian countries [11, 13, 14]. It can be attributed to two main reasons: firstly, differences in behavioral patterns, outdoor activities, and work hours in the male population of South Asian countries contribute to increased exposure to dengue vectors, as men often spend more time outdoors at dawn and in the evening; secondly, disparity in seeking medical attention may also play a role, with men reportedly being more willing to seek medical care than women in both rural and urban areas [2].

Distribution of age groups

Throughout most of Southeast Asia, in the past, dengue was considered to be a disease that primarily affects children [15]. According to the current study, most dengue patients were adults (18–40 years old), consistent with several other recent studies carried out in South Asian countries, including Bangladesh, Singapore, Sri Lanka, India, and other nations [16–18]. Our study also found that the majority of dengue-infected patients were between the ages of 21 and 30, followed by other age groups (Table 1). Though adults are more prone to infections, there was no significant relationship between age and infection with different serotypes (Fig. 1).

Distribution of circulating DENV serotypes and comorbidities

Prior to 2018, DENV-2 was the predominant circulating serotype. In 2019, its prevalence was surpassed by DENV-3. However, in 2023, DENV-2 re-emerged as the primary circulating serotype (51%), with DENV-3 also remaining prevalent at 44%, which is consistent with our findings. According to our study, 67.9% of patients were infected with DENV-2, followed by DENV-3 (20.3%) and DENV-1 (11.8%) (Table 1). Additionally, distinct morbidities such as diabetes and hypertension were observed in the dengue classification group [16]. Among the patients who had comorbid conditions in our study sample, diabetes (21.4%) and hypertension (21.4%) had a higher prevalence, followed by the others (Table 1).

While DENV-2 was the most common serotype across all four age groups, comparative analysis of the age groups and serotypes revealed that the 21–30 years cohort was primarily infected with DENV-2, while the adjacent age groups were more susceptible to DENV-3. Children and older age groups were found to be predominantly infected with the DENV-1 serotypes (Fig. 3). Contrary to the current finding, earlier research on dengue outbreaks in Bangladesh has shown that DENV-3 was the most frequently circulating serotype from 2019 to 2024 across all age groups [19–21].

Distribution of dengue hotspots

This study represents the first comprehensive investigation into the identification and determination of DENV serotypes among patients with dengue infection, featuring a detailed map that delineates dengue hotspots within Chittagong, the second-largest city in Bangladesh, including its metropolitan areas (Fig. 4). We identified five metropolitan areas of Chittagong, including Bakalia, Chawkbazar, Kotwali, Double Mooring, and Baizid Bostami. These dengue hotspots are highly populated in comparison with other metropolitan areas (https://en.banglapedia.org/index.php/Chittagong_District). Additionally, among the rural areas, the maximum number of dengue patients were found in Sitakundu, Hathhazari, Patia, and Karnaphuli areas (Fig. 4).

Clinical features

In our study, fever was the most common clinical manifestation of DENV in all patients, regardless of the serotypes (100%); which has been observed among patients in previous dengue outbreaks as well [22]. While fever was the most prevalent clinical feature, other commonly associated symptoms, including headache, vomiting, muscle pain, anorexia, eye pain, watery stool, abdominal pain, and runny nose, were also observed in variable proportions based on different serotypes (Fig. 5). These are considered the general features of dengue fever [23] and demonstrate a strong correlation with related studies [24–26]. Although fever, pain, and rash are contemplated as triads of dengue fever, rash was observed with low frequency in recent outbreaks [16], including among all serotypes in our study sample. An increasing trend of anorexia was observed in most of the patients, with a high percentage in DENV-2 (73.9%), a very frequently reported gastrointestinal symptom of dengue fever along with vomiting in recent times [27]. Headache is the second most common symptom among dengue patients in all cases since its emergence [28]. Despite the highest number of patients having the DENV-2 serotype (N = 309), this study showed that headache as a symptom was more prevalent in the DENV-3 (75%) serotype compared to others. In addition, in many studies, respiratory distress is presented as being related to severe plasma leakage leading to serious complications [29]. However, this study observed a very low percentage of breathing difficulties in patients infected with three different serotypes (Fig. 5).

Although DENV2 was the most prevalent serotype in this study, the duration of clinical symptoms (fever, headache, watery stool, eye pain, anorexia) were significantly higher in patients carrying DENV1 (Table 2) which is consistent with a previous study conducted by Yung et al. [30].

This study investigates the demographic, epidemiological, and clinical characteristics of dengue patients infected with different circulating dengue virus serotypes during the 2023 outbreak in southern Bangladesh. However, the study recruited patients from hospitals or clinics, which may not reflect the full spectrum of dengue infection in the community, potentially underrepresenting milder or asymptomatic infections. This sampling bias may limit the generalizability of our findings to the broader population in southern Bangladesh. Future studies incorporating a more representative sample, including more outpatients and those with milder dengue, are crucial for a comprehensive understanding of serotype-specific disease characteristics.

Conclusion

Over the past 20 years, Bangladesh has experienced a noticeable change in the circulating DENV serotypes. Though recent major dengue outbreaks have been found to be associated with the prevalence of the serotype DENV-3, we found a higher prevalence of DENV-2 in the country's second-largest region. Variations in serotypes may have contributed to a rise in clinical presentation severity in recent times. Our results provide crucial insights into the patterns of dengue virus transmission and severity, thereby aiding in the development of targeted public health interventions and management strategies to combat future outbreaks.

Funding sources

This project was funded by Beximco Pharmaceuticals Ltd., Bangladesh (Dengue/Asperia/2023) and Asperia Healthcare Ltd (R&D/2023/001).

Author's contributions

Conceptualization: Adnan Mannan, Mohabbat Hossain, Abul Faisal Md. Nuruddin Chowdhury, H. M. Hamidullah Mehedi, Noor Mohammed, Mustafizur Rajman.

Data curation: Istiaq Uddin Ahmed, Kallyan Chakma, Mohabbat Hossain.

Methodology: Md. Abdur Rob, Mohabbat Hossain, Abul Faisal Md. Nuruddin Chowdhury, Mohammed Maruf ul Quader, Md. Zakir Hossain, Mustafizur Rahman, Adnan Mannan.

Formal analysis: Mohabbat Hossain.

Visualization: Mohabbat Hossain, Adnan Mannan.

Writing – original draft: Mohabbat Hossain, Susmita Barua, Silvia Naznin Etu, Uschash Sikder.

Writing – review & editing: Md. Abdur Rob, M. A. Sattar, Adnan Mannan.

Funding acquisition: Md. Abdur Rob, M. A. Sattar, Abul Faisal Md. Nuruddin Chowdhury, H. M. Hamidullah Mehedi, Noor Mohammed, Mohammed Maruf ul Quader, Adnan Mannan.

Investigation: Md. Abdur Rob, Mohabbat Hossain, Abul Faisal Md. Nuruddin Chowdhury, H. M. Hamidullah Mehedi, Noor Mohammed, Mohammed Maruf ul Quader, Md. Zakir Hossain, Susmita Barua, Silvia Naznin Etu, Uschash Sikder, Adnan Mannan.

Project administration: Md. Abdur Rob, Mohabbat Hossain, Abul Faisal Md. Nuruddin Chowdhury, H. M. Hamidullah Mehedi, Noor Mohammed, Mohammed Maruf ul Quader, Md. Zakir Hossain, Mustafizur Rahman, Adnan Mannan.

Supervision: Md. Abdur Rob, M. A. Sattar, Abul Faisal Md. Nuruddin Chowdhury, H. M. Hamidullah Mehedi, Noor Mohammed, Mohammed Maruf ul Quader, Md. Zakir Hossain, Adnan Mannan.

Conflict of interest

The authors declare that there is no conflict of interest.

Acknowledgements

The authors would like to thank Chittagong Medical College, 250 bedded General Hospital, Asperia Health Research & Development Foundation (ARF) and Disease Biology and Molecular Epidemiology Research Group (dBme), Chattogram for their help at different stages of this research.

References

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    Sharmin S, Viennet E, Glass K, Harley D. The emergence of dengue in Bangladesh: epidemiology, challenges and future disease risk. Trans Royal Soci Trop Medi Hyg. 2015;109(10):619627.

    • Search Google Scholar
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  • 3.

    Stanaway JD, Shepard DS, Undurraga EA, Halasa YA, Coffeng LE, Brady OJ, et al. The global burden of dengue: an analysis from the Global Burden of Disease Study 2013. Lancet Infec Dis. 2016;16(6):712723.

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    Siritt MEG, Halstead SB, Artsob H, Buchy P, Farrar J, Gubler DJ, et al. Dengue: a continuing global threat. Nat Revi Micro. 2016;8(12):S7S16.

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    Simmons CP, Farrar JJ, Van Vinh Chau N, Wills B. Dengue. New Eng J Med. 2012;366(15):14231432.

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    Moi ML, Takasaki T, Omatsu T, Nakamura S, Katakai Y, Ami Y, et al. Demonstration of marmosets (Callithrix jacchus) as a non-human primate model for secondary dengue virus infection: high levels of viraemia and serotype cross-reactive antibody responses consistent with secondary infection of humans. J Gen Viro. 2014;95(3):591600.

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    Hossain MS, Noman AA, Mamun SM, Mosabbir AA. Twenty-two years of dengue outbreaks in Bangladesh: epidemiology, clinical spectrum, serotypes, and future disease risks. Trop Medi Heal. 2023 Dec;51(1):14.

    • Search Google Scholar
    • Export Citation
  • 8.

    Bhowmik KK, Ferdous J, Baral PK, Islam MS. Recent outbreak of dengue in Bangladesh: a threat to public health. Heal Sci Rep. 2023;6(4):e1210.

    • Search Google Scholar
    • Export Citation
  • 9.

    Yow KS, Aik J, Tan EY, Ng LC, Lai YL. Rapid diagnostic tests for the detection of recent dengue infections: an evaluation of six kits on clinical specimens. PLoS One. 2021 Apr 1;16(4):e0249602.

    • Search Google Scholar
    • Export Citation
  • 10.

    Kann S, Blessmann J, Winkelmann Y, Hansen J, Maya Amaya LJ, Rivera Salcedo GE, et al. Dengue virus detection in Lao PDR and Colombia: comparative evaluation of PCR tests. Trop Med Intern Health. 2021 Oct;26(10):1296302.

    • Search Google Scholar
    • Export Citation
  • 11.

    Hasan MJ, Tabassum T, Sharif M, Khan MAS, Bipasha AR, Basher A, et al. Clinico-epidemiologic characteristics of the 2019 dengue outbreak in Bangladesh. Trans Royal Soci Trop Medi Hyg. 2021;115(7):733740.

    • Search Google Scholar
    • Export Citation
  • 12.

    Dengue - global situation. WHO; 2023 (https://www.who.int/emergencies/disease-outbreak-news/item/2023-DON498).

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    Anker M, Arima Y. Male–female differences in the number of reported incident dengue fever cases in six Asian countries. West Paci Surv Resp J. 2011;2(2):17.

    • Search Google Scholar
    • Export Citation
  • 14.

    Prattay KMR, Sarkar MR, Shafiullah AZM, Islam MS, Raihan SZ, Sharmin N. A retrospective study on the socio-demographic factors and clinical parameters of dengue disease and their effects on the clinical course and recovery of the patients in a tertiary care hospital of Bangladesh. PLoS Neg Trop Dis. 2022;16(4):e0010297.

    • Search Google Scholar
    • Export Citation
  • 15.

    Strengthening implementation of the global strategy for dengue fever/dengue haemorrhagic fever prevention and control. WHO; 1999 (https://www.who.int/publications/i/item/WHO-CDS-DEN-IC-2000.1).

    • Search Google Scholar
    • Export Citation
  • 16.

    Islam Q, Sagor H, Tuli T, Noor F, Islam M. Changing clinical pattern of dengue fever and its unusual manifestations-2019 outbreak in Dhaka, Bangladesh. J Bang Coll Phys Surg. 2021;39(1).

    • Search Google Scholar
    • Export Citation
  • 17.

    Jayadas T, Kumanan T, Arasaratnam V, Gajapathy K, Surendran SN. The clinical profile, hematological parameters and liver transaminases of dengue NS1 Ag positive patients admitted to Jaffna Teaching Hospital, Sri Lanka. BMC Res Notes. 2019;12:15.

    • Search Google Scholar
    • Export Citation
  • 18.

    Ooi EE, Goh KT, Gubler DJ. Dengue prevention and 35 years of vector control in Singapore. Emerg Infec Dis. 2006;12(6):887.

  • 19.

    Haider N, Hasan MN, Khalil I, Tonge D, Hegde S, Chowdhury MAB, et al. The 2022 dengue outbreak in Bangladesh: hypotheses for the late resurgence of cases and fatalities. J Med Ento. 2023;60(4):847852.

    • Search Google Scholar
    • Export Citation
  • 20.

    Rahim R, Hasan A, Hasan N, Nakayama EE, Shioda T, Rahman M. Diversity of dengue virus serotypes in Dhaka city: from 2017 to 2021. Bang J Med Microbiol. 2021;15(2):2329.

    • Search Google Scholar
    • Export Citation
  • 21.

    Shirin T, Akram A, Hasan S, Rahman A, Sultana S, Alam AN, et al. Analysis and identification of genomic and immunogenic features of dengue serotype 3 genomes obtained during the 2019 outbreak in Bangladesh. New Microb New Infec. 2002;48.

    • Search Google Scholar
    • Export Citation
  • 22.

    Azad D, Ferdousic D, Islam Q. National guideline for clinical management of dengue syndrome. Dhaka: Government of the People’s Republic of Bangladesh; 2018.

    • Search Google Scholar
    • Export Citation
  • 23.

    Rahman M, Rahman K, Siddque A, Shoma S, Kamal A, Ali K, et al. First outbreak of dengue hemorrhagic fever, Bangladesh. Emerg Infec Dis. 2002;8(7):738.

    • Search Google Scholar
    • Export Citation
  • 24.

    Deshwal R, Qureshi MI, Singh R. Clinical and laboratory profile of dengue fever. J Assoc Physicians India. 2015;63(12):3032.

  • 25.

    Chen CH, Huang YC, Kuo KC, Li CC. Clinical features and dynamic ordinary laboratory tests differentiating dengue fever from other febrile illnesses in children. J Micro Immun Infec. 2018;51(5):614620.

    • Search Google Scholar
    • Export Citation
  • 26.

    Halsey ES, Marks MA, Gotuzzo E, Fiestas V, Suarez L, Vargas J, et al. Correlation of serotype-specific dengue virus infection with clinical manifestations. PLoS Neg Trop Dis. 2012;6(5):e1638.

    • Search Google Scholar
    • Export Citation
  • 27.

    Hasan MJ, Tabassum T, Sharif M, Khan MAS, Bipasha AR, Basher A, et al. Comparison of clinical manifestation of dengue fever in Bangladesh: an observation over a decade. BMC Infec Dis. 2021;21:110.

    • Search Google Scholar
    • Export Citation
  • 28.

    Domingues R, Kuster G, de Castro FO, Souza V, Levi J, Pannuti C. Headache features in patients with dengue virus infection. Cephalalgia. 2006;26(7):879882.

    • Search Google Scholar
    • Export Citation
  • 29.

    Tamibmaniam J, Hussin N, Cheah WK, Ng KS, Muninathan P. Proposal of a clinical decision tree algorithm using factors associated with severe dengue infection. PLoS One. 2016;11(8):e0161696.

    • Search Google Scholar
    • Export Citation
  • 30.

    Yung CF, Lee KS, Thein TL, Tan LK, Gan VC, Wong JG, et al. Dengue serotype-specific differences in clinical manifestation, laboratory parameters and risk of severe disease in adults, Singapore. The Am J Trop Med Hyg. 2015 May 5;92(5):999.

    • Search Google Scholar
    • Export Citation
  • 1.

    Bhatt S, Gething PW, Brady OJ, Messina JP, Farlow AW, Moyes CL, et al. The global distribution and burden of dengue. Nature. 2013;496(7446):5047.

    • Search Google Scholar
    • Export Citation
  • 2.

    Sharmin S, Viennet E, Glass K, Harley D. The emergence of dengue in Bangladesh: epidemiology, challenges and future disease risk. Trans Royal Soci Trop Medi Hyg. 2015;109(10):619627.

    • Search Google Scholar
    • Export Citation
  • 3.

    Stanaway JD, Shepard DS, Undurraga EA, Halasa YA, Coffeng LE, Brady OJ, et al. The global burden of dengue: an analysis from the Global Burden of Disease Study 2013. Lancet Infec Dis. 2016;16(6):712723.

    • Search Google Scholar
    • Export Citation
  • 4.

    Siritt MEG, Halstead SB, Artsob H, Buchy P, Farrar J, Gubler DJ, et al. Dengue: a continuing global threat. Nat Revi Micro. 2016;8(12):S7S16.

    • Search Google Scholar
    • Export Citation
  • 5.

    Simmons CP, Farrar JJ, Van Vinh Chau N, Wills B. Dengue. New Eng J Med. 2012;366(15):14231432.

  • 6.

    Moi ML, Takasaki T, Omatsu T, Nakamura S, Katakai Y, Ami Y, et al. Demonstration of marmosets (Callithrix jacchus) as a non-human primate model for secondary dengue virus infection: high levels of viraemia and serotype cross-reactive antibody responses consistent with secondary infection of humans. J Gen Viro. 2014;95(3):591600.

    • Search Google Scholar
    • Export Citation
  • 7.

    Hossain MS, Noman AA, Mamun SM, Mosabbir AA. Twenty-two years of dengue outbreaks in Bangladesh: epidemiology, clinical spectrum, serotypes, and future disease risks. Trop Medi Heal. 2023 Dec;51(1):14.

    • Search Google Scholar
    • Export Citation
  • 8.

    Bhowmik KK, Ferdous J, Baral PK, Islam MS. Recent outbreak of dengue in Bangladesh: a threat to public health. Heal Sci Rep. 2023;6(4):e1210.

    • Search Google Scholar
    • Export Citation
  • 9.

    Yow KS, Aik J, Tan EY, Ng LC, Lai YL. Rapid diagnostic tests for the detection of recent dengue infections: an evaluation of six kits on clinical specimens. PLoS One. 2021 Apr 1;16(4):e0249602.

    • Search Google Scholar
    • Export Citation
  • 10.

    Kann S, Blessmann J, Winkelmann Y, Hansen J, Maya Amaya LJ, Rivera Salcedo GE, et al. Dengue virus detection in Lao PDR and Colombia: comparative evaluation of PCR tests. Trop Med Intern Health. 2021 Oct;26(10):1296302.

    • Search Google Scholar
    • Export Citation
  • 11.

    Hasan MJ, Tabassum T, Sharif M, Khan MAS, Bipasha AR, Basher A, et al. Clinico-epidemiologic characteristics of the 2019 dengue outbreak in Bangladesh. Trans Royal Soci Trop Medi Hyg. 2021;115(7):733740.

    • Search Google Scholar
    • Export Citation
  • 12.

    Dengue - global situation. WHO; 2023 (https://www.who.int/emergencies/disease-outbreak-news/item/2023-DON498).

  • 13.

    Anker M, Arima Y. Male–female differences in the number of reported incident dengue fever cases in six Asian countries. West Paci Surv Resp J. 2011;2(2):17.

    • Search Google Scholar
    • Export Citation
  • 14.

    Prattay KMR, Sarkar MR, Shafiullah AZM, Islam MS, Raihan SZ, Sharmin N. A retrospective study on the socio-demographic factors and clinical parameters of dengue disease and their effects on the clinical course and recovery of the patients in a tertiary care hospital of Bangladesh. PLoS Neg Trop Dis. 2022;16(4):e0010297.

    • Search Google Scholar
    • Export Citation
  • 15.

    Strengthening implementation of the global strategy for dengue fever/dengue haemorrhagic fever prevention and control. WHO; 1999 (https://www.who.int/publications/i/item/WHO-CDS-DEN-IC-2000.1).

    • Search Google Scholar
    • Export Citation
  • 16.

    Islam Q, Sagor H, Tuli T, Noor F, Islam M. Changing clinical pattern of dengue fever and its unusual manifestations-2019 outbreak in Dhaka, Bangladesh. J Bang Coll Phys Surg. 2021;39(1).

    • Search Google Scholar
    • Export Citation
  • 17.

    Jayadas T, Kumanan T, Arasaratnam V, Gajapathy K, Surendran SN. The clinical profile, hematological parameters and liver transaminases of dengue NS1 Ag positive patients admitted to Jaffna Teaching Hospital, Sri Lanka. BMC Res Notes. 2019;12:15.

    • Search Google Scholar
    • Export Citation
  • 18.

    Ooi EE, Goh KT, Gubler DJ. Dengue prevention and 35 years of vector control in Singapore. Emerg Infec Dis. 2006;12(6):887.

  • 19.

    Haider N, Hasan MN, Khalil I, Tonge D, Hegde S, Chowdhury MAB, et al. The 2022 dengue outbreak in Bangladesh: hypotheses for the late resurgence of cases and fatalities. J Med Ento. 2023;60(4):847852.

    • Search Google Scholar
    • Export Citation
  • 20.

    Rahim R, Hasan A, Hasan N, Nakayama EE, Shioda T, Rahman M. Diversity of dengue virus serotypes in Dhaka city: from 2017 to 2021. Bang J Med Microbiol. 2021;15(2):2329.

    • Search Google Scholar
    • Export Citation
  • 21.

    Shirin T, Akram A, Hasan S, Rahman A, Sultana S, Alam AN, et al. Analysis and identification of genomic and immunogenic features of dengue serotype 3 genomes obtained during the 2019 outbreak in Bangladesh. New Microb New Infec. 2002;48.

    • Search Google Scholar
    • Export Citation
  • 22.

    Azad D, Ferdousic D, Islam Q. National guideline for clinical management of dengue syndrome. Dhaka: Government of the People’s Republic of Bangladesh; 2018.

    • Search Google Scholar
    • Export Citation
  • 23.

    Rahman M, Rahman K, Siddque A, Shoma S, Kamal A, Ali K, et al. First outbreak of dengue hemorrhagic fever, Bangladesh. Emerg Infec Dis. 2002;8(7):738.

    • Search Google Scholar
    • Export Citation
  • 24.

    Deshwal R, Qureshi MI, Singh R. Clinical and laboratory profile of dengue fever. J Assoc Physicians India. 2015;63(12):3032.

  • 25.

    Chen CH, Huang YC, Kuo KC, Li CC. Clinical features and dynamic ordinary laboratory tests differentiating dengue fever from other febrile illnesses in children. J Micro Immun Infec. 2018;51(5):614620.

    • Search Google Scholar
    • Export Citation
  • 26.

    Halsey ES, Marks MA, Gotuzzo E, Fiestas V, Suarez L, Vargas J, et al. Correlation of serotype-specific dengue virus infection with clinical manifestations. PLoS Neg Trop Dis. 2012;6(5):e1638.

    • Search Google Scholar
    • Export Citation
  • 27.

    Hasan MJ, Tabassum T, Sharif M, Khan MAS, Bipasha AR, Basher A, et al. Comparison of clinical manifestation of dengue fever in Bangladesh: an observation over a decade. BMC Infec Dis. 2021;21:110.

    • Search Google Scholar
    • Export Citation
  • 28.

    Domingues R, Kuster G, de Castro FO, Souza V, Levi J, Pannuti C. Headache features in patients with dengue virus infection. Cephalalgia. 2006;26(7):879882.

    • Search Google Scholar
    • Export Citation
  • 29.

    Tamibmaniam J, Hussin N, Cheah WK, Ng KS, Muninathan P. Proposal of a clinical decision tree algorithm using factors associated with severe dengue infection. PLoS One. 2016;11(8):e0161696.

    • Search Google Scholar
    • Export Citation
  • 30.

    Yung CF, Lee KS, Thein TL, Tan LK, Gan VC, Wong JG, et al. Dengue serotype-specific differences in clinical manifestation, laboratory parameters and risk of severe disease in adults, Singapore. The Am J Trop Med Hyg. 2015 May 5;92(5):999.

    • Search Google Scholar
    • Export Citation
  • Collapse
  • Expand

Senior editors

Editor(s)-in-Chief: Dunay, Ildiko Rita, Prof. Dr. Pharm, Dr. rer. nat., University of Magdeburg, Germany

Editor(s)-in-Chief: Heimesaat, Markus M., Prof. Dr. med., Charité - University Medicine Berlin, Germany

Editorial Board

  • Berit Bangoura, Dr. DVM. PhD,  University of Wyoming, USA
  • Stefan Bereswill, Prof. Dr. rer. nat., Charité - University Medicine Berlin, Germany
  • Dunja Bruder, Prof. Dr. rer. nat., University of Magdeburg, Germany
  • Jan Buer, Prof. Dr. med., University of Duisburg, Germany
  • Edit Buzas, Prof. Dr. med., Semmelweis University, Hungary
  • Renato Damatta, Prof. PhD, UENF, Brazil
  • Maria Deli, MD, PhD, DSc, Biological Research Center, HAS, Hungary
  • Olgica Djurković-Djaković, Prof. Phd, University of Belgrade, Serbia
  • Jean-Dennis Docquier, Prof. Dr. med., University of Siena, Italy
  • Zsuzsanna Fabry, Prof. Phd, University of Washington, USA
  • Ralf Ignatius, Prof. Dr. med., Charité - University Medicine Berlin, Germany
  • Achim Kaasch, Prof. Dr. med., Otto von Guericke University Magdeburg, Germany
  • Oliver Liesenfeld, Prof. Dr. med., Inflammatix, USA
  • Matyas Sandor, Prof. PhD, University of Wisconsin, USA
  • Ulrich Steinhoff, Prof. PhD, University of Marburg, Germany
  • Michal Toborek, Prof. PhD, University of Miami, USA
  • Susanne A. Wolf, PhD, MDC-Berlin, Germany

 

Dr. Dunay, Ildiko Rita
Magdeburg, Germany
E-mail: ildiko.dunay@med.ovgu.de

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European Journal of Microbiology and Immunology
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