• 1.

    Guan WJ et al.2020. Clinical characteristics of coronavirus disease 2019 in China. N Engl J Med 382: 17081720.

  • 2.

    Weaver SC, Charlier C, Vasilakis N, Lecuit M , 2018. Zika, chikungunya, and other emerging vector-borne viral diseases. Annu Rev Med 69: 395408.

  • 3.

    Laredo-Tiscareno SV et al., 2021. Detection of antibodies to Lokern, Main Drain, St. Louis Encephalitis, and West Nile viruses in vertebrate animals in Chihuahua, Guerrero, and Michoacan, Mexico. Vector Borne Zoonotic Dis 21: 884891.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4.

    Nunez-Avellaneda D et al.2021. Co-circulation of all four dengue viruses and Zika virus in Guerrero, Mexico, 2019. Vector Borne Zoonotic Dis 21: 458465.

  • 5.

    Nunez-Avellaneda D et al.2021. Chikungunya in Guerrero, Mexico, 2019 and evidence of gross underreporting in the region. Am J Trop Med Hyg.

  • 6.

    Laredo-Tiscareno SV et al.2018. Arbovirus surveillance near the Mexico-U.S. border: isolation and sequence analysis of chikungunya virus from patients with dengue-like symptoms in Reynosa, Tamaulipas. Am J Trop Med Hyg 99: 191194.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7.

    Beaty BJ, Calisher CH, Shope RE, Lennette EH, Lenette DA, Lennette ETDiagnostic Procedures for Viral, Rickettsial, and Chlamydial Infections. Washington, DC: American Public Health Association, 189212.

    • Search Google Scholar
    • Export Citation
  • 8.

    Tan LK et al.2019. Flavivirus cross-reactivity to dengue nonstructural protein 1 antigen detection assays. Diagnostics (Basel) 10: 11.

  • 9.

    Nasomsong W, Luvira V, Phiboonbanakit D , 2020. Case report: dengue and COVID-19 coinfection in Thailand. Am J Trop Med Hyg 104: 487489.

  • 10.

    Epelboin L, Blonde R, Nacher M, Combe P, Collet L , 2020. COVID-19 and dengue co-infection in a returning traveller. J Travel Med 27. doi: 10.1093/jtm/taaa114.

    • Search Google Scholar
    • Export Citation
  • 11.

    Verduyn M et al.2020. Co-infection of dengue and COVID-19: a case report. PLoS Negl Trop Dis 14: e0008476.

  • 12.

    Bicudo N, Bicudo E, Costa JD, Castro J, Barra GB , 2020. Co-infection of SARS-CoV-2 and dengue virus: a clinical challenge. Braz J Infect Dis 24: 452454.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13.

    Quental KN et al.2021. SARS-CoV-2 co-infection with dengue virus in Brazil: a potential case of viral transmission by a health care provider to household members. Travel Med Infect Dis 40: 101975.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    Villamil-Gomez WE et al.2021. SARS-CoV-2 and dengue virus co-infection: a case from north Caribbean Colombia. Travel Med Infect Dis 43: 102096.

  • 15.

    Masyeni S et al.2021. Serological cross-reaction and coinfection of dengue and COVID-19 in Asia: experience from Indonesia. Int J Infect Dis 102: 152154.

  • 16.

    Sebastião CS et al.2021. Coinfection between SARS-CoV-2 and vector-borne diseases in Luanda, Angola. J Med Virol. 94: 366371.

  • 17.

    Reyes-Ruiz JM et al.2021. Case report: extrapulmonary manifestations of COVID-19 and dengue coinfection. Am J Trop Med Hyg.

  • 18.

    Vicente CR, Silva T, Pereira LD, Miranda AE , 2021. Impact of concurrent epidemics of dengue, chikungunya, zika, and COVID-19. Rev Soc Bras Med Trop 54: e08372020.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19.

    Waggoner JJ et al.2016. Viremia and clinical presentation in Nicaraguan patients infected with zika virus, chikungunya virus, and dengue virus. Clin Infect Dis 63: 15841590.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20.

    Tsheten T, Clements ACA, Gray DJ, Adhikary RK, Wangdi K , 2021. Clinical features and outcomes of COVID-19 and dengue co-infection: a systematic review. BMC Infect Dis 21: 729.

    • PubMed
    • Search Google Scholar
    • Export Citation
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Evidence of Coinfections between SARS-CoV-2 and Select Arboviruses in Guerrero, Mexico, 2020–2021

Daniel Nunez-AvellanedaCollege of Veterinary Medicine, Iowa State University, Ames, Iowa;

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Fabian R. VillagómezLaboratorio de Microbiología Molecular, Escuela Nacional de Ciencias Biológicas del Instituto Politécnico Nacional, Ciudad de México, Mexico;

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Julio C. Villegas-PinedaDepartamento de Microbiología y Patología, Centro Universitario de Ciencias de la Salud, Universidad de Guadalajara, Guadalajara, Jalisco, México;

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Jacqueline Barrios-PalaciosNational Institute of Medical Sciences and Nutrition Salvador Zubirán, Experimental Pathology Section, Ciudad de México, Mexico;

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Ma. Isabel SalazarLaboratorio de Virología e Inmunovirología, Depto. Microbiología Escuela Nacional de Ciencias Biológicas Instituto Politécnico Nacional, Ciudad de Mexico, Mexico;

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Carlos Machain-WilliamsLaboratorio de Arbovirologia, Centro de Investigaciones Regionales “Dr. Hideyo Noguchi,” Universidad Autonoma de Yucatan, Merida, Yucatan, Mexico

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Bradley J. BlitvichCollege of Veterinary Medicine, Iowa State University, Ames, Iowa;

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ABSTRACT.

We provide evidence of concurrent and close sequential infections between SARS-CoV-2 and select arboviruses—namely, chikungunya virus (CHIKV); dengue viruses 1, 2, and 3 (DENV1–3), and Zika virus (ZIKV)—in patients in Guerrero, southwest Mexico, in 2020–2021. The study population consisted of 176 febrile patients with laboratory evidence of SARS-CoV-2 infection. Sera from all patients were serologically and antigenically tested for seven arboviruses known to occur in Guerrero. Eighteen patients contained CHIKV IgM, six of whom also contained CHIKV RNA. Another 16 patients contained flavivirus antigen. The flaviviruses responsible for the infections were identified by plaque reduction neutralization test as DENV1 (two patients), DENV2 (five patients), DENV3 (three patients), ZIKV (three patients), and an undetermined flavivirus (three patients). In summary, we identified patients in Guerrero, Mexico, with concurrent or recent sequential infections between SARS-CoV-2 and select arboviruses, exemplifying the importance of performing differential diagnosis in regions where these viruses cocirculate.

Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is the etiological agent of COVID-19, which is characterized by various clinical manifestations, including acute undifferentiated febrile illness, in humans.1 Others causes of acute undifferentiated febrile illness in humans include chikungunya virus (CHIKV), dengue viruses 1 to 4 (DENV1–4), West Nile (WNV), and Zika virus (ZIKV), all of which are arthropod-borne viruses (arboviruses) associated with fatal disease outcomes.2 CHIKV, DENV1-4, WNV, and ZIKV occur in Mexico and elsewhere in Latin America, complicating the diagnosis of COVID-19 in this region. The goal of this study was to assay febrile patients in Guerrero, a coastal state in southwest Mexico, for concurrent SARS-CoV-2 and arbovirus infections.

The study population consisted of 176 patients from Guerrero who had laboratory confirmed acute SARS-CoV-2 infections, probable acute or recent SARS-CoV-2 infections, or probable past SARS-CoV-2 infections. The patients presented with acute undifferentiated febrile illness in June 2020 to March 2021 at three participating sites in Guerrero: the Hospital General Adolfo Prieto in Taxco de Alarcón (HGAPTA), Laboratorio de Análisis Clínicos Avellaneda in Chilpancingo (LACAC), and Labymedic Laboratorios in Acapulco (LLA). As noted earlier, all patients presented with unspecified febrile illness, but the medical personnel at the participating performance sites were not willing to provide any other clinical information because of the time needed to compile these data. Nasopharyngeal swabs were collected from select patients and serum samples were collected from all patients. If a swab was collected, the patient was tested for SARS-CoV-2 RNA by quantitative reverse transcriptase polymerase chain reaction (qRT-PCR) using the DeCoV19 Kit Triplex kit (Genes2Life, Irapuato, Guanajuato, Mexico). If a swab was not collected, the patient was serologically assayed for SARS-CoV-2 using the Panbio COVID-19 IgG/IgM rapid test (Abbott Laboratories, Chicago, IL).- Serologic tests were performed at the participating sites and qRT-PCRs were performed at the Laboratorio MicroTec, a reference laboratory in Mexico City. Swabs were not taken from patients who considered the qRT-PCR testing to be cost-prohibitive. Patients with positive qRT-PCR results had confirmed acute SARS-CoV-2 infections. Patients that contained SARS-CoV-2 IgM, either in the presence or absence of SARS-CoV-2 IgG, were considered to have probable acute or recent SARS-CoV-2 infections. Patients with SARS-CoV-2 IgG in the absence of IgM had probable past SARS-CoV-2 infections.

An aliquot of each serum was transported to Iowa State University and serologically and antigenically tested for seven arboviruses known to occur in Guerrero (CHIKV, DENV1–4, WNV, and ZIKV).35 To identify patients with acute CHIKV infections, sera were assayed for CHIKV IgM using the CHIKjj Detect IgM ELISA Kit (InBios International Inc., Seattle, WA). The laboratory criteria for the diagnosis of chikungunya, as established by the WHO, is the isolation of CHIKV from acute serum, detection of CHIKV IgM or RNA in acute serum or a 4-fold increase in CHIKV IgG titer in sera collected at least 3 weeks apart.9 A patient has confirmed chikungunya if at least one of the aforementioned laboratory tests yields a positive result irrespective of the clinical presentation. Therefore, all patients with CHIKV IgM met the case definition for chikungunya.

All sera with CHIKV IgM were further assayed by RT-PCR. Complementary DNAs were generated using Superscript III reverse transcriptase (ThermoFisher, Waltham, MA), and PCRs were performed using high-fidelity Taq polymerase (ThermoFisher) in accordance to the manufacturer’s instructions. Primers specific to a 445-nt region of the CHIKV E1 gene were used (forward primer: 5′- GTACAGCAGAGTGTAAGGA-3′, reverse primer: 5′- TCTTCGCTCTCAGGCGTG-3′'). RT-PCR products were purified using the purelink gel extraction kit (ThermoFisher) and sequenced using a 3730 × 1 DNA sequencer (Applied Biosystems, Foster City, CA). All sera with CHIKV IgM were also assayed by plaque reduction neutralization test (PRNT) using an isolate of CHIKV (strain CH-R-1950) originally recovered from a patient in Tamaulipas, Mexico, in 2015.6 PRNTs were performed using African green monkey kidney (Vero) cells as previously described.7 Sera were tested at a starting dilution of 1:20, and titers were expressed as the reciprocal of highest serum dilutions yielding > 90% reduction in the number of plaques (PRNT90).

To identify patients with acute flavivirus infections, sera were assayed using the Human Dengue Virus NS1 Antigen ELISA Kit (MyBioSource Inc., San Diego, CA). The ELISA is not DENV-specific because the flavivirus nonstructural protein 1 contains group-reactive epitopes.8 If flavivirus antigen was detected, the patient was considered to have an acute flavivirus infection. All antigen-positive sera were titrated and tested by PRNT to identify the flavivirus(es) responsible for the infections. PRNTs were performed using DENV-1 (strain Hawaii), DENV-2 (strain NGC), DENV-3 (strain H-87), DENV-4 (strain 241), WNV (strain NY99-35261-11), and ZIKV (strain PRVABC59). Viruses were obtained from the WHO Center for Arbovirus Reference and Research, which is maintained at the Division of Vector-Borne Infectious Diseases, Centers for Disease Control and Prevention in Fort Collins, CO. For etiologic diagnosis, the PRNT90 antibody titer to the respective virus needed to be at least 4-fold greater than that to the other flaviviruses tested.

The ages of the patients in the study population ranged from 4 to 89 years, with mean of 45.7 years. There were 87 females and 89 males. Half of the patients presented at the LLA (88 patients) and the remainder at the HGAPTA and LACAC (55 and 33 patients, respectively). Twenty (11.4%) patients had laboratory-confirmed acute SARS-CoV-2 infections, 96 (54.5%) patients had probable acute or recent SARS-CoV-2 infections and 60 (34.1%) patients had probable past SARS-CoV-2 infections.

Eighteen patients with evidence of SARS-CoV-2 infection contained CHIKV IgM in their sera (Table 1). These patients had CHIKV PRNT90 titers ranging from 20 to 1280. Six of these patients also contained CHIKV RNA (Genbank Accession Nos. OL440054-OL440059). The number of CHIKV RNA-positive patients is likely an underestimate because the sera were transported to Iowa State University on ice packs instead of dry ice, which is not sold in Guerrero. Of the 18 CHIKV IgM-positive patients, two patients had confirmed acute SARS-CoV-2 infections, seven had probable acute or recent SARS-CoV-2 infections, and nine had probable past SARS-CoV-2 infections. The two CHIKV IgM-positive patients with confirmed acute SARS-CoV-2 infections were negative for CHIKV RNA. One patient was a 24-year-old man who developed symptoms in May 2020. The other patient was a 62-year-old man with illness onset in July 2020.

Table 1

Patients with concurrent and close sequential SARS-CoV-2 and chikungunya virus infections, Guerrero, 2020–2021

Patient ID Illness onset (month/year) Performance site Gender Age (years) SARS-CoV-2 diagnostic assay CHIKV IgM ELISA CHIKV RT-PCR CHIKV PRNT90 titer
RT-PCR IgM test IgG test
HG122 05/2020 HGAPTA M 24 + NT NT + 40
HG127 05/2020 HGAPTA F 27 NT + + + 20
LL005 07/2020 LLA M 62 + NT NT + 640
LL017 10/2020 LLA M 24 NT + + 640
LL018 10/2020 LLA F 57 NT + + 160
LL042 11/2020 LLA F 44 NT + + + 160
LA100 12/2020 LACAC M 38 NT + + + 20
LA101 12/2020 LACAC M 52 NT + + 320
LL057 01/2021 LLA M 74 NT + + + + 20
LL058 01/2021 LLA M 74 NT + + + + 1,280
LL059 01/2021 LLA M 80 NT + + + 20
HG172 02/2021 HGAPTA F 10 NT + + 40
LA120 02/2021 LACAC M 30 NT + + + 640
LL062 02/2021 LLA M 31 NT + + + + 320
LL064 02/2021 LLA F 43 NT + + 20
LL070 02/2021 LLA F 26 NT + + 160
LL078 03/2021 LLA M 44 NT + + + 640
LL084 03/2021 LLA M 27 NT + + 160

= positive; – = negative; CHIKV = chikungunya virus; F = female; HGAPTA = Hospital General Adolfo Prieto in Taxco de Alarcón; LACAC = Laboratorio de Análisis Clínicos Avellaneda in Chilpancingo; LLA = Labymedic Laboratorios in Acapulco; M = male; NT = not tested; PRNT = plaque reduction neutralization test; RT-PCR = reverse transcriptase polymerase chain reaction; SARS-CoV-2 = severe acute respiratory syndrome coronavirus 2.

Sera from 16 patients contained flavivirus antigen (Table 2). Of these, one patient had a confirmed acute SARS-CoV-2 infection, 10 had probable acute or recent SARS-CoV-2 infections, and five had probable past SARS-CoV-2 infections. The flaviviruses responsible for the infections were DENV1 (two patients), DENV2 (five patients), DENV3 (three patients), ZIKV (three patients), and an undetermined flavivirus (three patients). The patient that contained both SARS-CoV-2 RNA and flavivirus antigen was seropositive for DENV1. The patient was a 40-year-old woman who developed symptoms in June 2020. Of the 10 flavivirus antigen-positive patients with probable acute or recent SARS-CoV-2 infections, one patient was seropositive for DENV1, three were seropositive for DENV2, two were seropositive for DENV3, two were seropositive for ZIKV, and two had antibodies to an undetermined flavivirus.

Table 2

Patients with concurrent and close sequential SARS-CoV-2 and flavivirus infections, Guerrero, 2020–2021

Patient ID Illness onset (month/year) Performance site Gender Age (years) SARS-CoV-2 diagnostic assay Flavivirus NS1 ELISA PRNT outcome
RT-PCR IgM test IgG test
HG004 05/2020 HGAPTA M 68 NT + + + DENV3
HG005 05/2020 HGAPTA F 37 NT + + DENV3
HG011 05/2020 HGAPTA M 27 NT + + DENV1
HG012 06/2020 HGAPTA F 40 + NT NT + DENV1
HG013 06/2020 HGAPTA F 28 NT + + FLAVI
HG017 06/2020 HGAPTA M 35 NT + + DENV3
LL001 07/2020 LLA M 66 NT + + + DENV2
LL006 07/2020 LLA M 62 NT + + DENV2
LL007 07/2020 LLA M 61 NT + + ZIKV
LL012 08/2020 LLA F 52 NT + + DENV2
LL034 11/2020 LLA F 54 NT + + + DENV2
LL041 11/2020 LLA F 45 NT + + + ZIKV
LL048 11/2020 LLA F 44 NT + + + FLAVI
LL054 01/2021 LLA M 17 NT + + DENV2
LA016 01/2021 LACAC M 36 NT + + + FLAVI
LL080 03/2021 LLA M 72 NT + + + ZIKV

= positive; – = negative; DENV1 = dengue virus 1; DENV2 = dengue virus 2; DENV3 = dengue virus 3; F = female; FLAVI = undetermined flavivirus; HGAPTA = Hospital General Adolfo Prieto in Taxco de Alarcón; LACAC = Laboratorio de Análisis Clínicos Avellaneda in Chilpancingo; LLA = Labymedic Laboratorios in Acapulco; M = male; NT = not tested; PRNT = plaque reduction neutralization test; RT-PCR = reverse transcriptase polymerase chain reaction; SARS-CoV-2 = severe acute respiratory syndrome coronavirus 2; ZIKV = Zika virus.

Our data indicate that a subset of patients had concurrent or close sequential infections between SARS-CoV-2 and various arboviruses—namely CHIKV, DENV1, DENV2, DENV3, and ZIKV. Other studies have reported patients with concurrent SARS-CoV-2 and DENV infections.917 Most patients had DENV1 infections, but others had DENV2 or DENV3 infections. To the best of our knowledge, coinfections or close sequential infections between SARS-CoV-2 and CHIKV or ZIKV have not been reported. None of the patients with acute SARS-CoV-2 infections in Angola in 2021 had evidence of CHIKV or ZIKV infection.16 Coinfections were not reported during the concurrent outbreaks of SARS-CoV-2, CHIKV, DENV, and ZIKV in Espírito Santo State, Brazil, in 2020.18

In conclusion, we report apparent concurrent and close sequential infections between SARS-CoV-2 and select arboviruses in Guerrero, Mexico. SARS-CoV-2 and the arboviruses under investigation produce overlapping clinical manifestations (i.e., fever, headache, fatigue, and myalgia), complicating the diagnosis of coinfections.19,20 There is also considerable overlap in the laboratory characteristics associated with SARS-CoV-2 and DENV infections (i.e., thrombocytopenia, lymphopenia, leukopenia, and elevated liver enzymes).20 Failure to identify coinfections can adversely affect patient outcomes due to delays in the implementation of disease-specific treatments, such as the isolation of COVID-19 patients and the venous hydration of dengue patients. Our findings underscore the important need to perform differential diagnosis in regions where these viruses cocirculate. Prospective epidemiological studies are needed to determine whether SARS-CoV-2 potentiates infections with arboviruses or vice versa.

ACKNOWLEDGMENTS

We thank Gerardo Avellaneda-Juarez, Olivia Reyes-Ramos and Jonathan Cisneros-Pano for assisting with sera collections. The American Society of Tropical Medicine and Hygiene has waived the Open Access fee for this article due to the ongoing COVID-19 pandemic.

REFERENCES

  • 1.

    Guan WJ et al.2020. Clinical characteristics of coronavirus disease 2019 in China. N Engl J Med 382: 17081720.

  • 2.

    Weaver SC, Charlier C, Vasilakis N, Lecuit M , 2018. Zika, chikungunya, and other emerging vector-borne viral diseases. Annu Rev Med 69: 395408.

  • 3.

    Laredo-Tiscareno SV et al., 2021. Detection of antibodies to Lokern, Main Drain, St. Louis Encephalitis, and West Nile viruses in vertebrate animals in Chihuahua, Guerrero, and Michoacan, Mexico. Vector Borne Zoonotic Dis 21: 884891.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4.

    Nunez-Avellaneda D et al.2021. Co-circulation of all four dengue viruses and Zika virus in Guerrero, Mexico, 2019. Vector Borne Zoonotic Dis 21: 458465.

  • 5.

    Nunez-Avellaneda D et al.2021. Chikungunya in Guerrero, Mexico, 2019 and evidence of gross underreporting in the region. Am J Trop Med Hyg.

  • 6.

    Laredo-Tiscareno SV et al.2018. Arbovirus surveillance near the Mexico-U.S. border: isolation and sequence analysis of chikungunya virus from patients with dengue-like symptoms in Reynosa, Tamaulipas. Am J Trop Med Hyg 99: 191194.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7.

    Beaty BJ, Calisher CH, Shope RE, Lennette EH, Lenette DA, Lennette ETDiagnostic Procedures for Viral, Rickettsial, and Chlamydial Infections. Washington, DC: American Public Health Association, 189212.

    • Search Google Scholar
    • Export Citation
  • 8.

    Tan LK et al.2019. Flavivirus cross-reactivity to dengue nonstructural protein 1 antigen detection assays. Diagnostics (Basel) 10: 11.

  • 9.

    Nasomsong W, Luvira V, Phiboonbanakit D , 2020. Case report: dengue and COVID-19 coinfection in Thailand. Am J Trop Med Hyg 104: 487489.

  • 10.

    Epelboin L, Blonde R, Nacher M, Combe P, Collet L , 2020. COVID-19 and dengue co-infection in a returning traveller. J Travel Med 27. doi: 10.1093/jtm/taaa114.

    • Search Google Scholar
    • Export Citation
  • 11.

    Verduyn M et al.2020. Co-infection of dengue and COVID-19: a case report. PLoS Negl Trop Dis 14: e0008476.

  • 12.

    Bicudo N, Bicudo E, Costa JD, Castro J, Barra GB , 2020. Co-infection of SARS-CoV-2 and dengue virus: a clinical challenge. Braz J Infect Dis 24: 452454.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13.

    Quental KN et al.2021. SARS-CoV-2 co-infection with dengue virus in Brazil: a potential case of viral transmission by a health care provider to household members. Travel Med Infect Dis 40: 101975.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    Villamil-Gomez WE et al.2021. SARS-CoV-2 and dengue virus co-infection: a case from north Caribbean Colombia. Travel Med Infect Dis 43: 102096.

  • 15.

    Masyeni S et al.2021. Serological cross-reaction and coinfection of dengue and COVID-19 in Asia: experience from Indonesia. Int J Infect Dis 102: 152154.

  • 16.

    Sebastião CS et al.2021. Coinfection between SARS-CoV-2 and vector-borne diseases in Luanda, Angola. J Med Virol. 94: 366371.

  • 17.

    Reyes-Ruiz JM et al.2021. Case report: extrapulmonary manifestations of COVID-19 and dengue coinfection. Am J Trop Med Hyg.

  • 18.

    Vicente CR, Silva T, Pereira LD, Miranda AE , 2021. Impact of concurrent epidemics of dengue, chikungunya, zika, and COVID-19. Rev Soc Bras Med Trop 54: e08372020.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19.

    Waggoner JJ et al.2016. Viremia and clinical presentation in Nicaraguan patients infected with zika virus, chikungunya virus, and dengue virus. Clin Infect Dis 63: 15841590.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20.

    Tsheten T, Clements ACA, Gray DJ, Adhikary RK, Wangdi K , 2021. Clinical features and outcomes of COVID-19 and dengue co-infection: a systematic review. BMC Infect Dis 21: 729.

    • PubMed
    • Search Google Scholar
    • Export Citation

Author Notes

Address correspondence to Bradley J. Blitvich, Iowa State University, 2116 Veterinary Medicine Building, Ames, IA 50011. E-mail: blitvich@iastate.edu

Financial support: This study was supported by a postdoctoral scholarship from the from the Consejo Nacional de Ciencia y Tecnología of Mexico (scholarship no. 406531) and intramural funds provided by the College of Veterinary Medicine at Iowa State University.

Disclosure: This study was performed with the approval of the Institutional Review Boards at each of the participating institutions.

Authors’ addresses: Daniel Nunez-Avellaneda and Bradley J. Blitvich, Veterinary Microbiology & Preventive Medicine, Iowa State University, Ames, IA, E-mails: dnunez@iastate.edu and blitvich@iastate.edu. Fabian R. Villagómez, Laboratorio de Microbiología Molecular, Escuela Nacional de Ciencias Biológicas del Instituto Politécnico Nacional, Mexico City, Mexico, E-mail: fromerov1400@alumno.ipn.mx. Julio C. Villegas-Pineda, Departamento de Microbiología y Patología, Universidad de Guadalajara, Guadalajara, Mexico, E-mail: julio.villegas@academicos.udg.mx. Jacqueline Barrios-Palacios, Experimental Pathology Section, National Institute of Medical Sciences and Nutrition Salvador Zubirán, Mexico City, Mexico, E-mail: 18477@uagro.mx. Ma. Isabel Salazar, Department of Microbiology, Escuela Nacional de Ciencias Biológicas Instituto Politécnico Nacional, Mexico City, Mexico, E-mail: isalazarsan@yahoo.com. Carlos Machain-Williams, Hideo Noguchi Institute, Universidad Autonoma de Yucatan, Merida, Mexico, E-mail: carlos.machain@uady.mx.

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