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Dynamics of dengue and SARS-COV-2 co-infection in an endemic area of Colombia

Dynamics of dengue and SARS-COV-2 co-infection in an endemic area of Colombia Since the COVID‑19 outbreak, millions of people have been infected with SARS‑ CoV‑2 around the world. An area of epidemiological relevance is Latin America, tropical regions, due to the distribution of endemic diseases such as chi‑ kungunya, dengue (DENV ), malaria, Zika virus, where febrile disease abounds. The early signs and symptoms of DENV and COVID‑19 could be similar, making it a risk that patients may be wrongly diagnosed early during the disease. The problem increases since COVID‑19 infection can lead to false positives in DENV screening tests. We present two cases of acute undifferentiated febrile syndrome that were diagnosed with SARS‑ CoV‑2 and DENV co ‑infection, confirmed by ELISA and RT‑PCR for both viral pathogens. The occurrence of simultaneous or overlapped infections can alter the usual clinical course, severity, or outcome of each infection. Therefore, epidemiological surveillance and intensified preparation for those scenarios must be considered, as well as further studies should be done to address cases of co‑infection promptly to avoid major complications and fatal outcomes during the current pandemic. Other endemic tropical diseases should not be neglected. Keywords: COVID‑19, SARS‑ CoV‑2, Coinfection, Dengue, Colombia, Overlap disease Introduction thrombocytopenia, abnormal liver function tests and Severe acute respiratory syndrome coronavirus-2 (SARS- other laboratory findings [4]. CoV-2) causing coronavirus disease 2019 (COVID-19) In tropical countries, COVID-19 can easily be misdi- has spread rapidly throughout Latin America. In Colom- agnosed with dengue or other more common infectious bia and other tropical countries, the pandemic poten- diseases, leading to a delay in the diagnosis of COVID- tially coincides with another epidemic already in the 19 infection and further spread of the virus [3]. Failure region, dengue (DENV) [1]. DENV is an arboviral infec- to consider COVID-19 in such cases has serious impli- tion transmitted by the Aedes aegypti mosquito char- cations for the patient, as well as public health. Public acterized by acute onset of high fever [2], meanwhile, health concerns are generated due to the possibility that COVID-19 is a viral infection that usually begins with the presence of both viruses and the development of co- respiratory symptoms. There are similarities in the ini - infections harm mortality and other clinical outcomes tial presentation of patients with COVID-19 and dengue [5]. Co-infection can be defined as the simultaneous [3], headache, myalgia, fever, associated with leukopenia, presence of two or more infections, which can increase the severity and duration of one or both diseases [3]. Information about DENV and COVID-19 co-infec- tion is scarce, and the dynamics of the disease and out- *Correspondence: cristina.martinezavila@gmail.com comes may be altered in this scenario. Rapid serological Department of Epidemiology and Clinical Research, BIOTOXAM GROUP, testing for dengue sometimes gives a false positive in Universidad de los Andes, Cartagena, Colombia acute undifferentiated febrile disease in the COVID-19 Full list of author information is available at the end of the article © The Author(s) 2022. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Acosta‑Pérez et al. Tropical Diseases, Travel Medicine and Vaccines (2022) 8:12 Page 2 of 6 infection setting [4]. This situation complicates things nonstructural protein 1 (NS1) with positive immuno- further, thus, it can be difficult to distinguish early infec - globulin (Ig) M and IgG and a nasopharyngeal swab for tions vs. co-infection, generating a significant risk for the SARS-CoV-2 real-time reverse transcriptase (RT-PCR) population and demanding greater attention for health- was taken. care systems. This treatment did not improve her symptoms and has In this paper, we describe 2 patients with co-infection gradually worsened. ABG tests were performed which of SARS-CoV-2 and DENV, confirmed by ELISA and showed severe hypoxemia (partial pressure of oxygen RT-PCR for both viral pathogens in Colombia, to dis- [PaO2]: 36 mmHg, PaO2/fraction of inspired oxygen close important details of this emerging overlapping [FiO2] 68 mmHg. A repeat of the complete blood count coinfection. This study has important implications for showed a sudden drop in the platelet count to 20,000/ distinguishing and determining co-infection from mono- mm without any visible bleeding. Therefore, dengue RT- infection, as well as the clinical picture in such cases of PCR was requested due to doubtful diagnosis and DENV co-infection between DENV and SARS-CoV-2. serotype 2 (DENV2) was detected. RT–PCR for SARS- CoV-2 was positive, confirming the diagnosis of dengue Methods with warning signs associated with severe COVID-19. This study included two cases of COVID-19 co-infection She was transferred to the ICU, for ventilatory support with DENV admitted in an intensive care unit (ICU) of due to progression to acute respiratory distress syndrome a third level hospital of an endemic country (Cartagena, and refractory hypoxemia that requires invasive mechan- Colombia) during COVID-19 pandemic. Clinical and ical ventilation. Clinical characteristics were attributed laboratory investigations that were undertaken to deter- to SARS-CoV-2 infection. On subsequent days, increas- mine the diagnosis included: images: x-ray or CT, serum ing trends in the number of platelets and leukocytes were chemistry, inflammatory biomarkers, molecular test. observed, and clinical symptoms improved. However, extubation was not achieved; she required a tracheos- Results: cases presentations tomy and was discharged to a chronic care unit for pul- Case 1 monary rehabilitation. A 65-year-old Colombian woman with a history of hypertension, presented with 8 days of asthenia, ret- Case 2 roorbital pain, frontoparietal headache in location, rated 58-year-old Colombian male, without known medical 6/10, joint and muscle pain. 2 days before admission, he history, complained of persistent fever of 39 °C, diarrhea, added dry cough, sore throat, and sensation of dyspnea dyspnea, asthenia, myalgias, and dry cough that lasted without any other associated symptoms. She was observ- 3 days; he had tested positive for SARS-COV 19 by RT- ing quarantine and denied contact with cases suspicious PCR. Due to the worsening of cough, dyspnea, and short- or confirmed of COVID-19 infection as well as mosquito ness of breath, he consulted an online clinic where he was bites. The patient had self-medicated with paracetamol, referred to the hospital for evaluation. On examination, which provided temporary relief; however, her condition he appeared dehydrated, with peripheral cyanosis, som- was persistent, prompting consultation. nolent but arousable with marked respiratory effort and Her vital signs revealed a body temperature of 38.9 °C, bibasilar crackles. Vital signs with a pulse rate of 108/ a respiratory rate of 26 breaths/minute, a pulse rate of minute, respiratory rate of 32 breaths/minute, blood 110/minute, and a blood pressure of 130/80 mmHg. pressure of 100/70 mmHg. Oxygen saturation at presen- Oxygen saturation at presentation was 90% in room air. tation was 84% in room air, without any other findings on Physical examination only showed bibasilar crackles physical examination. and a petechial rash. Analysis revealed leukopenia with Immediately, a portable chest radiograph was per- lymphopenia, thrombocytopenia, moderate D-Dimer, formed showing multiple radiopacities of interstitial transaminases, C-reactive protein (CRP), and elevation of occupation and peripheral distribution (Fig.  2). Con- LDH (Table 1). sidering that he has acute respiratory failure supported A chest CT scan was performed, and scattered ground by clinical findings (tachypnea, tachycardia, cyanosis, glass images were shown in both lung fields, compromis - altered levels of consciousness, diffuse crackles and res - ing 50–60% of the lung parenchyma due to probable viral piratory effort), he was intubated (pressure control ven - pneumonia (Fig. 1). tilation [PCV] mode, inspiratory oxygen fraction [F iO ], She was hospitalized with supportive treatment, dexa- 0.5, positive end-expiratory pressure [PEEP], 10 c mH O; methasone (after the recovery trial), IV fluids, paraceta - inspiratory pressure [Pi], 15 cmH O; inspiratory time mol, additional oxygen with nasal cannula, and close [Ti], 1.5 s; frequency [f ], 12 per minute) and transferred monitoring. The rapid dengue test revealed a positive to the ICU. A costa‑Pérez et al. Tropical Diseases, Travel Medicine and Vaccines (2022) 8:12 Page 3 of 6 Table 1 Timeline events of DENV and SARS‑ CoV‑2 coinfection cases Case 1 Case 2 Reference value Days of symptoms on admission 8 3 Admission diagnosis COVID‑19 COVID‑19 Comorbidities Arterial Hypertension None known Day 1 symptoms Headache, myalgia, altralgia, fever Fever, dry cough, asthenia, adynamia Respiratory symptoms 48 hours after initial symptoms From the 1st day of the onset of symptoms Day 1 hospitalization Suspicion and sampling NS1/IgM DENV Suspicion and sampling RT‑PCR COVID ‑19 Leukocytes/mm 3100 2180 4000–11,000 Lymphocytes/mm 410 (10%) 296.48 (13,6%) 20–40% Hemoglobin (mg/dL) 13 11.8 13–15 Hematocrit (%) 48 45 30–45 Platelet/mm 47,000 70,000 150,000–450,000 AST (U/L) 48 64 < 40 ALT (U/L) 25 33 < 40 D‑Dimer (ng/mL) 639 1475 < 500 CRP (mg/dL) 9 49.8 < 1 LDH (U/L) 494 989 < 150 Serum creatinine (mg/dL) 0.75 1.9 0.5–1 Day 3 NS1/IgM positive (9 days of symptoms) RT‑PCR positive for COVID 19 Day 4 RT‑PCR positive for COVID 19 Persistent thrombocytopenia suspected DENV ELISA and collection of RT‑PCR sample collec‑ tion Day 5 RT–PCR DENV positive for DENV serotype 2 ELISA positive for DENV. RT–PCR DENV positive for DENV serotype 3 Clinical course and outcome Patient progressed to ventilatory failure requir‑ Patient with acute ventilatory failure, requiring ing prolonged invasive mechanical ventilation, invasive mechanical ventilation, with progres‑ needed for tracheostomy, transferred to a sive clinical deterioration and multiple organ chronic care center failure, that eventually led to death Final diagnosis DENV2 and SARS‑ CoV‑2 co ‑infection DENV3 and SARS‑ CoV‑2 co ‑infection Fig. 1 Axial CT scan view showing scattered ground glass in both Fig. 2 Portable chest radiograph showing multiple radiopacities of lung fields, with 50% lung involvement (red arrows) interstitial occupation and peripheral distribution (red arrows) Acosta‑Pérez et al. Tropical Diseases, Travel Medicine and Vaccines (2022) 8:12 Page 4 of 6 Arterial blood gas analysis revealed a pH of 7.45, an patients affected in isolation by COVID-19 [10]. Cases of oxygen pressure of 48 mmHg, a carbon dioxide pressure coinfection of SARS-CoV-2 with microorganisms such as of 30 mmHg, and a bicarbonate of 21.1 mmol/L, a PaO2/ Mycoplasma pneumoniae, influenza virus, cytomegalo - fraction of inspired oxygen [FiO2] 96 mmHg. Laboratory virus, HIV, Legionella, Pneumocystis jirovecii, and even tests had leukopenia with lymphocytopenia and throm- with multiple respiratory viruses have been reported bocytopenia. Renal function, liver enzymes, CRP, serum [11]. In endemic areas such as Colombia, establishing LDH, and D-dimer were elevated (Table 1). Due to severe the presence of multiple agents is essential to carry out thrombocytopenia in an endemic area, dengue serology an adequate therapeutic approach to avoid complications was positive for NS1 antigen. To confirm the diagnosis, and fatal outcomes. an anti-dengue IgM/IgG ELISA, serology test and RT- Recent studies suggest that COVID-19 and DENV PCR were requested and DENV serotype 3 (DENV3) coinfection presents less severe symptoms compared to was detected. Therefore, the patient was diagnosed with isolated monoinfection, probably associated with oppo- severe COVID-19 with dengue fever with signs of red site pro-and anticoagulant states triggered by SARS- flags. CoV-2 and DENV respectively [12]. Furthermore, the During his hospitalization, the patient’s acute hypoxic possible improvement of DENV has been considered respiratory failure did not recover, his oxygenation was when there is a second infection with different viruses poor, despite the tracheal intubation connected to the has been considered [13]. In this article, we present two ventilator. Renal and liver function continued to decline. cases of severe coinfection with hematocrit and ventila- Subsequently, he became hypotensive and started nor- tory compromise, one of which had a fatal outcome. epinephrine for suspected cardiogenic vs septic shock. The clinical and laboratory manifestations of each Empiric treatment with broad-spectrum antibiotics, entity can have considerable overlap, presenting with dexamethasone (after recovery trial), and IV fluids was fever, myalgia, asthenia, adynamia, diarrheal episodes, started. During this time, the ICU-prone ventilation pro- and dermatological lesions (Table  2) that make the dif- tocol was initiated to improve oxygenation to his lungs. ferential diagnosis difficult [5]. Studies in Latin America The patient’s condition deteriorated sharply, developing have revealed that both viral diseases can trigger second- multiorgan failure, characterized by pulmonary, renal, ary hemophagocytic lymphohistiocytosis [6]. liver, and possible neurologic compromise. The patient In relation to laboratory tests, when having a patient remained on life-sustaining support. After 17 days in the with AFI, at least a complete blood count should be ICU, Extracorporeal membrane oxygenation (ECMO) performed, liver enzymes, CRP, and kidney function was performed. Despite the best efforts of the medical should be performed [6]. In COVID-19, the most com- staff, the patient eventually died. mon hematologic abnormality is lymphopenia, present in approximately 80% of individuals, neutrophils are Discussion often elevated, and white blood cell count may be normal The causes of acute febrile illness (AFI) in Colombia are [14]. In DENV, the hematological parameter of interest diverse [6], including multiple arboviral infections such is hemoconcentration, which represents an alarm sign as: chikungunya, zika, and DENV, which is the most fre- [2, 15]; also, unlike COVID-19, thrombocytopenia and quently reported [2]. However, in the epidemiological neutropenia can occur. The association between leukope - context of the COVID-19 pandemic, the possibility of nia and thrombocytopenia occurs in both entities, being the occurrence of these diseases should not be underes- more frequent in DENV than in COVID-19, occurring timated. In the cases described, it was pertinent to rule in 60–80% of cases [5, 15]. Liver function is also usually out infection by DENV and COVID-19. COVID-19 and affected, with an increase in aminotransferases (AST and DENV infections are difficult to distinguish, as they share ALT) by 25 and 33%, respectively; as well as an increase clinical and laboratory characteristics, which can lead to in CRP in up to 60% of individuals [2, 15]. misdiagnosis or delayed treatment and patient isolation It is important to know and properly interpret the [3, 7]. laboratory analysis, as according to the chronology and Different studies have raised the possible cross-reac - clinical course of the infection, alterations that represent tion between DENV and SARS-CoV-2 antibodies, which some alarm sign (hemoconcentration in DENV), severity, generates a risk of false positives and diagnostic doubts or prognosis (D-dimer in COVID-19) may occur. Like- [7, 8]. Information related to infection by one or another wise, there are tests, such as ferritin, which are biomark- agent is available; to date, the effects of coinfection ers of interest in COVID-19; but even though it can also remain unknown [9]. The cases of co-infection by SARS- be increased in DENV, they are not clinically important CoV-2 and influenza do not appear to have a more severe [9]. In our case, both patients presented thrombocytope- course, but they showed similar clinical characteristics to nia, elevated transaminases, and increased CRP, making A costa‑Pérez et al. Tropical Diseases, Travel Medicine and Vaccines (2022) 8:12 Page 5 of 6 Table 2 Comparisons and differences of COVID ‑19 and DENV performance of adequate confirmatory tests, since rapid serological tests for DENV can cross-react with SARS- Symptoms and laboratory findings COVID-19 DENV CoV-2 antigens and give false positives [12]. A system- Fever +++ +++ atic review of 15,976 samples indicates that the use of Headache ++ +++ antibody tests for COVID-19, in particular rapid test Retro‑ orbital pain ++ employing lateral flow immunoassays, have limited ben - Asthenia + ++ efits in the point-of-care testing [16], particularly in the Rash + ++ early phase of SARS-CoV-2 infection leading to a signifi - Purpura ++ cant hurdle to rely on the laboratory diagnosis [17]. It is Myalgia/Arthralgia + ++ worth to mention that a Peruvian cohort, the largest in Dyspnea ++ + Latin America, affirms that possible cross-reactions of Anorexy + + IgM/IgG-DENV rapid test results concerning antibod- Cough +++ + ies developed after infection with SARS-CoV-2 are not Chest pain ++ + ruled out when describing cases of false positives in rapid Pharyngitis ++ ++ tests DENV [18]. However, in this cohort they stated that Anosmia, eugesia +++ + there would be no cross-reaction between the rapid test Diarrhea + + of the NS1-DENV antigen and the IgM and IgG anti- Nausea, emesis + + bodies of SARS-CoV-2 since the patients hospitalized Abdominal pain ++ with COVID-19 days later presented an unfavorable and Neurological Agitation/Alteration + + unusual evolution after detecting the presence of the CRP ++ viral agent of the vector Aedes aegypti [18]. Furthermore, Lymphocytes ↓↓ ↓ according to the Colombian consensus on the care, diag- Neutrophils ↑ ↓ nosis, and treatment of SARS-CoV-2 infection, positivity Platelets ↓ ↓ in ELISA and molecular tests such as RT-PCR confirmed Ferritin ↑ ↑ co-infection with SARS-CoV-2 and DENV. Taking into Transaminases ↑ ↑ account the following information, our cases coincide D‑Dimer ↑ with what is stated in the literature. Legend: + stands for frequency of findings, more than 1 (+) corresponds to frequently. ↑ elevated levels, decreased levels. Adapted from: [5] Conclusions The medical challenge of co-infection of SARS-CoV-2 and DENV lies in the similarity of the clinical and labo- differentiation difficult from the clinical approach point ratory characteristics of the two infections. The shared of view. pathophysiology and endotheliotropic nature of both Within the differential diagnoses, oriented by respira - viruses could condition an amplified immune response tory symptoms, common respiratory pathogens such as in the host, causing the clinical presentation to overlap. Streptococcus spp. and Mycoplasma pneumoniae, influ - It is necessary to carry out adequate clinical reasoning, enza, emerging diseases such as leptospirosis or toxo- remembering the possibility of COVID-19 in patients plasmosis are included. Up to 25% of patients with DENV DENV positive and vice versa, since there could be cross present with respiratory symptoms [1, 3, 4]. The clinical reactions in laboratory tests. To avoid misdiagnosis or presentations similar to DENV can be caused by other delayed treatment and patient isolation, we recommend arboviruses such as chikungunya virus presented in early asking for confirmatory tests when there are doubts; con - 2016 and Zika virus in 2017, malaria, Q fever, leptospi- sidering the result will affect treatment, prognosis, and rosis, salmonellosis, and primary HIV infection depend- outcome. Prospective studies are needed to allow us to ing on the prevailing clinical context [6]. Considering the understand the behavior and dynamics of this associa- current pandemic, in the cases described, no viral panel tion and to identify the impact in terms of morbidity and was carried out for other respiratory viruses or arbovi- mortality during co-infection. ruses, as the certainty of clinical evidence leaned toward COVID-19. Acknowledgments In fact, in an Argentine retrospective study, they sug- Not applicable. gest that the existence of prolonged fevers longer than Authors’ contributions 10 days, headache, rash, whether there are respiratory MCMA supervised the study and wrote the manuscript; TAP collected the symptoms, should lead to the suspicion of a concomi- clinical data; AAH and TRY analyzed the data and images; and CDC reviewed the manuscript. The author(s) read and approved the final manuscript. tant COVID-19 and DENV infection; respecting the Acosta‑Pérez et al. Tropical Diseases, Travel Medicine and Vaccines (2022) 8:12 Page 6 of 6 Funding 12. Carosella LM, Pryluka D, Maranzana A, Barcan L, Cuini R, Freuler C, et al. The author(s) received no financial support for the research, authorship, and/ Characteristics of patients co‑ infected with severe acute respiratory or publication of this article. syndrome coronavirus 2 and dengue virus, Buenos Aires, Argentina, march‑ June 2020. Emerg Infect Dis. 2021;27:348–51. Availability of data and materials 13. Ulrich H, Pillat MM, Tárnok A. Dengue Fever, COVID‑19 (SARS‑ CoV‑2), and We have presented the data of the patients in the manuscript as tables and Antibody‑Dependent Enhancement (ADE): A Perspective. Cytometry A. have submitted the figures separately as figures. 2020;97. Epub ahead of print. https:// doi. org/ 10. 1002/ cyto.a. 24047. 14. Terpos E, Ntanasis‑Stathopoulos IEI. Hematological findings and compli‑ cations of COVID‑19. Am J Hematol. 2020;95:834–47. Declarations 15. Oliveira ÉCLD, Pontes ERJC, Cunha RVD, Fróes ÍBNDD. Alterações hematológicas em pacientes com dengue. Rev Soc Bras Med Trop. Ethics approval and consent to participate 2009;42:682–5. This research has been confirmed by the Research Center of Gestión Salud 16. Deeks JJ, Dinnes J, Takwoingi Y, et al. Antibody tests for identification of and Ethics Committee. current and past infection with SARS‑ CoV‑2. Cochrane Database Syst Rev. 2020;6. Epub ahead of print. https:// doi. org/ 10. 1002/ 14651 858. CD013 Consent for publication Written informed consent was obtained from a legally authorized 17. Masyeni S, Santoso MS, Widyaningsih PD, et al. Serological cross‑reaction representative(s) for anonymized patient information to be published in this and coinfection of dengue and COVID‑19 in Asia: experience from Indo ‑ article which was approved by the Research Center. nesia. Int J Infect Dis. 2021;102:152. 18. Mejía‑Parra JL, Aguilar ‑Martinez S, Fernández‑Mogollón JL, et al. Charac‑ Competing interests teristics of patients coinfected with Severe Acute Respiratory Syndrome The author(s) declared no potential conflicts of interest with respect to the Coronavirus 2 and dengue virus, Lambayeque, Peru, May–August 2020: A research, authorship, and/or publication of this article. retrospective analysis. Travel Med Infect Dis. 2021;43. Epub ahead of print. https:// doi. org/ 10. 1016/j. tmaid. 2021. 102132. Author details 1 2 Internal Medicine, Universidad Libre, Cali, Colombia. Intensive Care Unit, Gestión Salud IPS, Cartagena, Colombia. Department of Epidemiology Publisher’s Note and Clinical Research, BIOTOXAM GROUP, Universidad de los Andes, Carta‑ Springer Nature remains neutral with regard to jurisdictional claims in pub‑ gena, Colombia. lished maps and institutional affiliations. Received: 13 February 2022 Accepted: 9 May 2022 References 1. Cardona‑ Ospina JA, Arteaga‑Livias K, Villamil‑ Gómez WE, Pérez‑Díaz CE, Bonilla‑Aldana D, Mondragon‑ Cardona Á, et al. Dengue and COVID‑ 19, overlapping epidemics? An analysis from Colombia. J Med Virol. 2021;93:522–7. 2. Kumar RP, Sunith R, Karthikeyan A, et al. Dengue Fever: A Review Article. Int J Curr Microbiol App Sci. 2020;9. Epub ahead of print. https:// doi. org/ 10. 20546/ ijcmas. 2020. 901. 168. 3. Lorenz C, Azevedo TSC‑NF. COVID ‑19 and dengue fever: a danger ‑ ous combination for the health system in Brazil. Travel Med Infect Dis. 2020;35:101659. 4. Henrina J, Putra ICS, Lawrensia S, et al. Coronavirus disease of 2019: a mimicker of dengue infection. SN Compr Clin Med. 2020;2. Epub ahead of print. https:// doi. org/ 10. 1007/ s42399‑ 020‑ 00364‑3. 5. Nacher M, Douine M, Gaillet M, Flamand C, Rousset DRC. Simultaneous dengue and COVID‑19 epidemics: difficult days ahead? PLoS Negl Trop Dis. 2020;14:1–8. 6. Moreira J, Bressan CS, Brasil P, et al. Epidemiology of acute febrile illness in Latin America. Clin Microbiol Infect. 2018;24. Epub ahead of print. https:// doi. org/ 10. 1016/j. cmi. 2018. 05. 001. 7. Santoso MS, Masyeni S, Haryanto S, et al. Assessment of dengue and COVID‑19 antibody rapid diagnostic tests cross‑reactivity in Indonesia. Re Read ady y to to submit y submit your our re researc search h ? Choose BMC and benefit fr ? Choose BMC and benefit from om: : Virol J. 2021;18:1–5. 8. Lustig Y, Keler S, Kolodny R, Ben‑ Tal N, Atias‑ Varon D, Shlush E, et al. Poten‑ fast, convenient online submission tial antigenic cross‑reactivity between SARS‑ CoV‑2 and dengue viruses. Clin Infect Dis Epub ahead of print. 2020. https:// doi. org/ 10. 1093/ cid/ thorough peer review by experienced researchers in your field ciaa1 207. rapid publication on acceptance 9. Milby KM, Atallah AN, Rocha‑Filho CR, Pinto ACPN, Rocha APD, Reis FSA, support for research data, including large and complex data types et al. SARS‑ CoV‑2 and arbovirus infection: a rapid systematic review. Sao Paulo Med J. 2020;138:498–504. • gold Open Access which fosters wider collaboration and increased citations 10. Ding Q, Lu P, Fan Y, Xia YLM. The clinical characteristics of pneumonia maximum visibility for your research: over 100M website views per year patients coinfected with 2019 novel coronavirus and influenza virus in Wuhan, China. J Med Virol. 2020;92:1549–55. At BMC, research is always in progress. 11. Fu Y, Cheng YWY. Understanding SARS‑ CoV‑2‑mediated inflammatory responses: from mechanisms to potential therapeutic tools. Virol Sin. Learn more biomedcentral.com/submissions 2020;35:266–71. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png "Tropical Diseases, Travel Medicine and Vaccines" Springer Journals

Dynamics of dengue and SARS-COV-2 co-infection in an endemic area of Colombia

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Abstract

Since the COVID‑19 outbreak, millions of people have been infected with SARS‑ CoV‑2 around the world. An area of epidemiological relevance is Latin America, tropical regions, due to the distribution of endemic diseases such as chi‑ kungunya, dengue (DENV ), malaria, Zika virus, where febrile disease abounds. The early signs and symptoms of DENV and COVID‑19 could be similar, making it a risk that patients may be wrongly diagnosed early during the disease. The problem increases since COVID‑19 infection can lead to false positives in DENV screening tests. We present two cases of acute undifferentiated febrile syndrome that were diagnosed with SARS‑ CoV‑2 and DENV co ‑infection, confirmed by ELISA and RT‑PCR for both viral pathogens. The occurrence of simultaneous or overlapped infections can alter the usual clinical course, severity, or outcome of each infection. Therefore, epidemiological surveillance and intensified preparation for those scenarios must be considered, as well as further studies should be done to address cases of co‑infection promptly to avoid major complications and fatal outcomes during the current pandemic. Other endemic tropical diseases should not be neglected. Keywords: COVID‑19, SARS‑ CoV‑2, Coinfection, Dengue, Colombia, Overlap disease Introduction thrombocytopenia, abnormal liver function tests and Severe acute respiratory syndrome coronavirus-2 (SARS- other laboratory findings [4]. CoV-2) causing coronavirus disease 2019 (COVID-19) In tropical countries, COVID-19 can easily be misdi- has spread rapidly throughout Latin America. In Colom- agnosed with dengue or other more common infectious bia and other tropical countries, the pandemic poten- diseases, leading to a delay in the diagnosis of COVID- tially coincides with another epidemic already in the 19 infection and further spread of the virus [3]. Failure region, dengue (DENV) [1]. DENV is an arboviral infec- to consider COVID-19 in such cases has serious impli- tion transmitted by the Aedes aegypti mosquito char- cations for the patient, as well as public health. Public acterized by acute onset of high fever [2], meanwhile, health concerns are generated due to the possibility that COVID-19 is a viral infection that usually begins with the presence of both viruses and the development of co- respiratory symptoms. There are similarities in the ini - infections harm mortality and other clinical outcomes tial presentation of patients with COVID-19 and dengue [5]. Co-infection can be defined as the simultaneous [3], headache, myalgia, fever, associated with leukopenia, presence of two or more infections, which can increase the severity and duration of one or both diseases [3]. Information about DENV and COVID-19 co-infec- tion is scarce, and the dynamics of the disease and out- *Correspondence: cristina.martinezavila@gmail.com comes may be altered in this scenario. Rapid serological Department of Epidemiology and Clinical Research, BIOTOXAM GROUP, testing for dengue sometimes gives a false positive in Universidad de los Andes, Cartagena, Colombia acute undifferentiated febrile disease in the COVID-19 Full list of author information is available at the end of the article © The Author(s) 2022. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Acosta‑Pérez et al. Tropical Diseases, Travel Medicine and Vaccines (2022) 8:12 Page 2 of 6 infection setting [4]. This situation complicates things nonstructural protein 1 (NS1) with positive immuno- further, thus, it can be difficult to distinguish early infec - globulin (Ig) M and IgG and a nasopharyngeal swab for tions vs. co-infection, generating a significant risk for the SARS-CoV-2 real-time reverse transcriptase (RT-PCR) population and demanding greater attention for health- was taken. care systems. This treatment did not improve her symptoms and has In this paper, we describe 2 patients with co-infection gradually worsened. ABG tests were performed which of SARS-CoV-2 and DENV, confirmed by ELISA and showed severe hypoxemia (partial pressure of oxygen RT-PCR for both viral pathogens in Colombia, to dis- [PaO2]: 36 mmHg, PaO2/fraction of inspired oxygen close important details of this emerging overlapping [FiO2] 68 mmHg. A repeat of the complete blood count coinfection. This study has important implications for showed a sudden drop in the platelet count to 20,000/ distinguishing and determining co-infection from mono- mm without any visible bleeding. Therefore, dengue RT- infection, as well as the clinical picture in such cases of PCR was requested due to doubtful diagnosis and DENV co-infection between DENV and SARS-CoV-2. serotype 2 (DENV2) was detected. RT–PCR for SARS- CoV-2 was positive, confirming the diagnosis of dengue Methods with warning signs associated with severe COVID-19. This study included two cases of COVID-19 co-infection She was transferred to the ICU, for ventilatory support with DENV admitted in an intensive care unit (ICU) of due to progression to acute respiratory distress syndrome a third level hospital of an endemic country (Cartagena, and refractory hypoxemia that requires invasive mechan- Colombia) during COVID-19 pandemic. Clinical and ical ventilation. Clinical characteristics were attributed laboratory investigations that were undertaken to deter- to SARS-CoV-2 infection. On subsequent days, increas- mine the diagnosis included: images: x-ray or CT, serum ing trends in the number of platelets and leukocytes were chemistry, inflammatory biomarkers, molecular test. observed, and clinical symptoms improved. However, extubation was not achieved; she required a tracheos- Results: cases presentations tomy and was discharged to a chronic care unit for pul- Case 1 monary rehabilitation. A 65-year-old Colombian woman with a history of hypertension, presented with 8 days of asthenia, ret- Case 2 roorbital pain, frontoparietal headache in location, rated 58-year-old Colombian male, without known medical 6/10, joint and muscle pain. 2 days before admission, he history, complained of persistent fever of 39 °C, diarrhea, added dry cough, sore throat, and sensation of dyspnea dyspnea, asthenia, myalgias, and dry cough that lasted without any other associated symptoms. She was observ- 3 days; he had tested positive for SARS-COV 19 by RT- ing quarantine and denied contact with cases suspicious PCR. Due to the worsening of cough, dyspnea, and short- or confirmed of COVID-19 infection as well as mosquito ness of breath, he consulted an online clinic where he was bites. The patient had self-medicated with paracetamol, referred to the hospital for evaluation. On examination, which provided temporary relief; however, her condition he appeared dehydrated, with peripheral cyanosis, som- was persistent, prompting consultation. nolent but arousable with marked respiratory effort and Her vital signs revealed a body temperature of 38.9 °C, bibasilar crackles. Vital signs with a pulse rate of 108/ a respiratory rate of 26 breaths/minute, a pulse rate of minute, respiratory rate of 32 breaths/minute, blood 110/minute, and a blood pressure of 130/80 mmHg. pressure of 100/70 mmHg. Oxygen saturation at presen- Oxygen saturation at presentation was 90% in room air. tation was 84% in room air, without any other findings on Physical examination only showed bibasilar crackles physical examination. and a petechial rash. Analysis revealed leukopenia with Immediately, a portable chest radiograph was per- lymphopenia, thrombocytopenia, moderate D-Dimer, formed showing multiple radiopacities of interstitial transaminases, C-reactive protein (CRP), and elevation of occupation and peripheral distribution (Fig.  2). Con- LDH (Table 1). sidering that he has acute respiratory failure supported A chest CT scan was performed, and scattered ground by clinical findings (tachypnea, tachycardia, cyanosis, glass images were shown in both lung fields, compromis - altered levels of consciousness, diffuse crackles and res - ing 50–60% of the lung parenchyma due to probable viral piratory effort), he was intubated (pressure control ven - pneumonia (Fig. 1). tilation [PCV] mode, inspiratory oxygen fraction [F iO ], She was hospitalized with supportive treatment, dexa- 0.5, positive end-expiratory pressure [PEEP], 10 c mH O; methasone (after the recovery trial), IV fluids, paraceta - inspiratory pressure [Pi], 15 cmH O; inspiratory time mol, additional oxygen with nasal cannula, and close [Ti], 1.5 s; frequency [f ], 12 per minute) and transferred monitoring. The rapid dengue test revealed a positive to the ICU. A costa‑Pérez et al. Tropical Diseases, Travel Medicine and Vaccines (2022) 8:12 Page 3 of 6 Table 1 Timeline events of DENV and SARS‑ CoV‑2 coinfection cases Case 1 Case 2 Reference value Days of symptoms on admission 8 3 Admission diagnosis COVID‑19 COVID‑19 Comorbidities Arterial Hypertension None known Day 1 symptoms Headache, myalgia, altralgia, fever Fever, dry cough, asthenia, adynamia Respiratory symptoms 48 hours after initial symptoms From the 1st day of the onset of symptoms Day 1 hospitalization Suspicion and sampling NS1/IgM DENV Suspicion and sampling RT‑PCR COVID ‑19 Leukocytes/mm 3100 2180 4000–11,000 Lymphocytes/mm 410 (10%) 296.48 (13,6%) 20–40% Hemoglobin (mg/dL) 13 11.8 13–15 Hematocrit (%) 48 45 30–45 Platelet/mm 47,000 70,000 150,000–450,000 AST (U/L) 48 64 < 40 ALT (U/L) 25 33 < 40 D‑Dimer (ng/mL) 639 1475 < 500 CRP (mg/dL) 9 49.8 < 1 LDH (U/L) 494 989 < 150 Serum creatinine (mg/dL) 0.75 1.9 0.5–1 Day 3 NS1/IgM positive (9 days of symptoms) RT‑PCR positive for COVID 19 Day 4 RT‑PCR positive for COVID 19 Persistent thrombocytopenia suspected DENV ELISA and collection of RT‑PCR sample collec‑ tion Day 5 RT–PCR DENV positive for DENV serotype 2 ELISA positive for DENV. RT–PCR DENV positive for DENV serotype 3 Clinical course and outcome Patient progressed to ventilatory failure requir‑ Patient with acute ventilatory failure, requiring ing prolonged invasive mechanical ventilation, invasive mechanical ventilation, with progres‑ needed for tracheostomy, transferred to a sive clinical deterioration and multiple organ chronic care center failure, that eventually led to death Final diagnosis DENV2 and SARS‑ CoV‑2 co ‑infection DENV3 and SARS‑ CoV‑2 co ‑infection Fig. 1 Axial CT scan view showing scattered ground glass in both Fig. 2 Portable chest radiograph showing multiple radiopacities of lung fields, with 50% lung involvement (red arrows) interstitial occupation and peripheral distribution (red arrows) Acosta‑Pérez et al. Tropical Diseases, Travel Medicine and Vaccines (2022) 8:12 Page 4 of 6 Arterial blood gas analysis revealed a pH of 7.45, an patients affected in isolation by COVID-19 [10]. Cases of oxygen pressure of 48 mmHg, a carbon dioxide pressure coinfection of SARS-CoV-2 with microorganisms such as of 30 mmHg, and a bicarbonate of 21.1 mmol/L, a PaO2/ Mycoplasma pneumoniae, influenza virus, cytomegalo - fraction of inspired oxygen [FiO2] 96 mmHg. Laboratory virus, HIV, Legionella, Pneumocystis jirovecii, and even tests had leukopenia with lymphocytopenia and throm- with multiple respiratory viruses have been reported bocytopenia. Renal function, liver enzymes, CRP, serum [11]. In endemic areas such as Colombia, establishing LDH, and D-dimer were elevated (Table 1). Due to severe the presence of multiple agents is essential to carry out thrombocytopenia in an endemic area, dengue serology an adequate therapeutic approach to avoid complications was positive for NS1 antigen. To confirm the diagnosis, and fatal outcomes. an anti-dengue IgM/IgG ELISA, serology test and RT- Recent studies suggest that COVID-19 and DENV PCR were requested and DENV serotype 3 (DENV3) coinfection presents less severe symptoms compared to was detected. Therefore, the patient was diagnosed with isolated monoinfection, probably associated with oppo- severe COVID-19 with dengue fever with signs of red site pro-and anticoagulant states triggered by SARS- flags. CoV-2 and DENV respectively [12]. Furthermore, the During his hospitalization, the patient’s acute hypoxic possible improvement of DENV has been considered respiratory failure did not recover, his oxygenation was when there is a second infection with different viruses poor, despite the tracheal intubation connected to the has been considered [13]. In this article, we present two ventilator. Renal and liver function continued to decline. cases of severe coinfection with hematocrit and ventila- Subsequently, he became hypotensive and started nor- tory compromise, one of which had a fatal outcome. epinephrine for suspected cardiogenic vs septic shock. The clinical and laboratory manifestations of each Empiric treatment with broad-spectrum antibiotics, entity can have considerable overlap, presenting with dexamethasone (after recovery trial), and IV fluids was fever, myalgia, asthenia, adynamia, diarrheal episodes, started. During this time, the ICU-prone ventilation pro- and dermatological lesions (Table  2) that make the dif- tocol was initiated to improve oxygenation to his lungs. ferential diagnosis difficult [5]. Studies in Latin America The patient’s condition deteriorated sharply, developing have revealed that both viral diseases can trigger second- multiorgan failure, characterized by pulmonary, renal, ary hemophagocytic lymphohistiocytosis [6]. liver, and possible neurologic compromise. The patient In relation to laboratory tests, when having a patient remained on life-sustaining support. After 17 days in the with AFI, at least a complete blood count should be ICU, Extracorporeal membrane oxygenation (ECMO) performed, liver enzymes, CRP, and kidney function was performed. Despite the best efforts of the medical should be performed [6]. In COVID-19, the most com- staff, the patient eventually died. mon hematologic abnormality is lymphopenia, present in approximately 80% of individuals, neutrophils are Discussion often elevated, and white blood cell count may be normal The causes of acute febrile illness (AFI) in Colombia are [14]. In DENV, the hematological parameter of interest diverse [6], including multiple arboviral infections such is hemoconcentration, which represents an alarm sign as: chikungunya, zika, and DENV, which is the most fre- [2, 15]; also, unlike COVID-19, thrombocytopenia and quently reported [2]. However, in the epidemiological neutropenia can occur. The association between leukope - context of the COVID-19 pandemic, the possibility of nia and thrombocytopenia occurs in both entities, being the occurrence of these diseases should not be underes- more frequent in DENV than in COVID-19, occurring timated. In the cases described, it was pertinent to rule in 60–80% of cases [5, 15]. Liver function is also usually out infection by DENV and COVID-19. COVID-19 and affected, with an increase in aminotransferases (AST and DENV infections are difficult to distinguish, as they share ALT) by 25 and 33%, respectively; as well as an increase clinical and laboratory characteristics, which can lead to in CRP in up to 60% of individuals [2, 15]. misdiagnosis or delayed treatment and patient isolation It is important to know and properly interpret the [3, 7]. laboratory analysis, as according to the chronology and Different studies have raised the possible cross-reac - clinical course of the infection, alterations that represent tion between DENV and SARS-CoV-2 antibodies, which some alarm sign (hemoconcentration in DENV), severity, generates a risk of false positives and diagnostic doubts or prognosis (D-dimer in COVID-19) may occur. Like- [7, 8]. Information related to infection by one or another wise, there are tests, such as ferritin, which are biomark- agent is available; to date, the effects of coinfection ers of interest in COVID-19; but even though it can also remain unknown [9]. The cases of co-infection by SARS- be increased in DENV, they are not clinically important CoV-2 and influenza do not appear to have a more severe [9]. In our case, both patients presented thrombocytope- course, but they showed similar clinical characteristics to nia, elevated transaminases, and increased CRP, making A costa‑Pérez et al. Tropical Diseases, Travel Medicine and Vaccines (2022) 8:12 Page 5 of 6 Table 2 Comparisons and differences of COVID ‑19 and DENV performance of adequate confirmatory tests, since rapid serological tests for DENV can cross-react with SARS- Symptoms and laboratory findings COVID-19 DENV CoV-2 antigens and give false positives [12]. A system- Fever +++ +++ atic review of 15,976 samples indicates that the use of Headache ++ +++ antibody tests for COVID-19, in particular rapid test Retro‑ orbital pain ++ employing lateral flow immunoassays, have limited ben - Asthenia + ++ efits in the point-of-care testing [16], particularly in the Rash + ++ early phase of SARS-CoV-2 infection leading to a signifi - Purpura ++ cant hurdle to rely on the laboratory diagnosis [17]. It is Myalgia/Arthralgia + ++ worth to mention that a Peruvian cohort, the largest in Dyspnea ++ + Latin America, affirms that possible cross-reactions of Anorexy + + IgM/IgG-DENV rapid test results concerning antibod- Cough +++ + ies developed after infection with SARS-CoV-2 are not Chest pain ++ + ruled out when describing cases of false positives in rapid Pharyngitis ++ ++ tests DENV [18]. However, in this cohort they stated that Anosmia, eugesia +++ + there would be no cross-reaction between the rapid test Diarrhea + + of the NS1-DENV antigen and the IgM and IgG anti- Nausea, emesis + + bodies of SARS-CoV-2 since the patients hospitalized Abdominal pain ++ with COVID-19 days later presented an unfavorable and Neurological Agitation/Alteration + + unusual evolution after detecting the presence of the CRP ++ viral agent of the vector Aedes aegypti [18]. Furthermore, Lymphocytes ↓↓ ↓ according to the Colombian consensus on the care, diag- Neutrophils ↑ ↓ nosis, and treatment of SARS-CoV-2 infection, positivity Platelets ↓ ↓ in ELISA and molecular tests such as RT-PCR confirmed Ferritin ↑ ↑ co-infection with SARS-CoV-2 and DENV. Taking into Transaminases ↑ ↑ account the following information, our cases coincide D‑Dimer ↑ with what is stated in the literature. Legend: + stands for frequency of findings, more than 1 (+) corresponds to frequently. ↑ elevated levels, decreased levels. Adapted from: [5] Conclusions The medical challenge of co-infection of SARS-CoV-2 and DENV lies in the similarity of the clinical and labo- differentiation difficult from the clinical approach point ratory characteristics of the two infections. The shared of view. pathophysiology and endotheliotropic nature of both Within the differential diagnoses, oriented by respira - viruses could condition an amplified immune response tory symptoms, common respiratory pathogens such as in the host, causing the clinical presentation to overlap. Streptococcus spp. and Mycoplasma pneumoniae, influ - It is necessary to carry out adequate clinical reasoning, enza, emerging diseases such as leptospirosis or toxo- remembering the possibility of COVID-19 in patients plasmosis are included. Up to 25% of patients with DENV DENV positive and vice versa, since there could be cross present with respiratory symptoms [1, 3, 4]. The clinical reactions in laboratory tests. To avoid misdiagnosis or presentations similar to DENV can be caused by other delayed treatment and patient isolation, we recommend arboviruses such as chikungunya virus presented in early asking for confirmatory tests when there are doubts; con - 2016 and Zika virus in 2017, malaria, Q fever, leptospi- sidering the result will affect treatment, prognosis, and rosis, salmonellosis, and primary HIV infection depend- outcome. Prospective studies are needed to allow us to ing on the prevailing clinical context [6]. Considering the understand the behavior and dynamics of this associa- current pandemic, in the cases described, no viral panel tion and to identify the impact in terms of morbidity and was carried out for other respiratory viruses or arbovi- mortality during co-infection. ruses, as the certainty of clinical evidence leaned toward COVID-19. Acknowledgments In fact, in an Argentine retrospective study, they sug- Not applicable. gest that the existence of prolonged fevers longer than Authors’ contributions 10 days, headache, rash, whether there are respiratory MCMA supervised the study and wrote the manuscript; TAP collected the symptoms, should lead to the suspicion of a concomi- clinical data; AAH and TRY analyzed the data and images; and CDC reviewed the manuscript. The author(s) read and approved the final manuscript. tant COVID-19 and DENV infection; respecting the Acosta‑Pérez et al. Tropical Diseases, Travel Medicine and Vaccines (2022) 8:12 Page 6 of 6 Funding 12. Carosella LM, Pryluka D, Maranzana A, Barcan L, Cuini R, Freuler C, et al. The author(s) received no financial support for the research, authorship, and/ Characteristics of patients co‑ infected with severe acute respiratory or publication of this article. syndrome coronavirus 2 and dengue virus, Buenos Aires, Argentina, march‑ June 2020. Emerg Infect Dis. 2021;27:348–51. Availability of data and materials 13. Ulrich H, Pillat MM, Tárnok A. Dengue Fever, COVID‑19 (SARS‑ CoV‑2), and We have presented the data of the patients in the manuscript as tables and Antibody‑Dependent Enhancement (ADE): A Perspective. Cytometry A. have submitted the figures separately as figures. 2020;97. Epub ahead of print. https:// doi. org/ 10. 1002/ cyto.a. 24047. 14. Terpos E, Ntanasis‑Stathopoulos IEI. Hematological findings and compli‑ cations of COVID‑19. Am J Hematol. 2020;95:834–47. Declarations 15. Oliveira ÉCLD, Pontes ERJC, Cunha RVD, Fróes ÍBNDD. Alterações hematológicas em pacientes com dengue. Rev Soc Bras Med Trop. Ethics approval and consent to participate 2009;42:682–5. This research has been confirmed by the Research Center of Gestión Salud 16. Deeks JJ, Dinnes J, Takwoingi Y, et al. Antibody tests for identification of and Ethics Committee. current and past infection with SARS‑ CoV‑2. Cochrane Database Syst Rev. 2020;6. Epub ahead of print. https:// doi. org/ 10. 1002/ 14651 858. CD013 Consent for publication Written informed consent was obtained from a legally authorized 17. Masyeni S, Santoso MS, Widyaningsih PD, et al. Serological cross‑reaction representative(s) for anonymized patient information to be published in this and coinfection of dengue and COVID‑19 in Asia: experience from Indo ‑ article which was approved by the Research Center. nesia. Int J Infect Dis. 2021;102:152. 18. Mejía‑Parra JL, Aguilar ‑Martinez S, Fernández‑Mogollón JL, et al. Charac‑ Competing interests teristics of patients coinfected with Severe Acute Respiratory Syndrome The author(s) declared no potential conflicts of interest with respect to the Coronavirus 2 and dengue virus, Lambayeque, Peru, May–August 2020: A research, authorship, and/or publication of this article. retrospective analysis. Travel Med Infect Dis. 2021;43. Epub ahead of print. https:// doi. org/ 10. 1016/j. tmaid. 2021. 102132. Author details 1 2 Internal Medicine, Universidad Libre, Cali, Colombia. Intensive Care Unit, Gestión Salud IPS, Cartagena, Colombia. Department of Epidemiology Publisher’s Note and Clinical Research, BIOTOXAM GROUP, Universidad de los Andes, Carta‑ Springer Nature remains neutral with regard to jurisdictional claims in pub‑ gena, Colombia. lished maps and institutional affiliations. Received: 13 February 2022 Accepted: 9 May 2022 References 1. 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Journal

"Tropical Diseases, Travel Medicine and Vaccines" – Springer Journals

Published: May 15, 2022

Keywords: COVID-19; SARS-CoV-2; Coinfection; Dengue; Colombia; Overlap disease

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