Viral Coinfections
Abstract
:1. Introduction
2. Virus–Virus Interaction in Coinfections
2.1. Viral Interference
2.2. Viral Synergy
2.3. Viral Noninterference
3. Outcome of Viral Coinfections on Host
3.1. Effects on Virus Transmission
3.2. Effects on Viral Pathogenicity
4. Study of Viral Coinfection
4.1. Identification
- (i)
- (ii)
- Application of digital droplet PCR (ddPCR) makes it possible to identify two highly similar viruses [153]. This method improves the accuracy and sensitivity of coinfection detection.
- (iii)
- The transmission electron microscopy detection method of a gold nanoparticle gene probe also has applications in coinfection detection [154]. This method makes detection more convenient, which is conducive to clinical detection.
- (iv)
- Fayyadh et al. used multicolor imaging with self-assembled quantum dot probes to image and successfully detect H1N1, H3N2, and H9N2 influenza viruses in coinfected cells [155]. This method provides a basis for in vitro detection of coinfection, which is more direct and easier to operate than traditional detection.
- (v)
4.2. Viral Separation and Purification
- (i)
- The purification of viruses by CPE is a mainstream method for virus isolation in coinfection, but it requires the selection of suitable cell lines, where one virus can produce obvious CPE while the other virus does not produce obvious CPE. The disadvantage of this method is whether or not some traditional virus isolation cell lines are sensitive to another virus, and coinfection may affect the formation of CPE. At present, it is feasible to separate snakehead retrovirus (SnRV) from grouper nervous necrosis virus (GNNV) by SGF-1 [165]; FMDV from PPRV [130] or single serotype FMDV from multiple serotypes ofFMDV [142] by BHK21; IAV from respiratory viruses by suspended MDCK cells (MDCK-S) and adherent MDCK cells (MDCK-A) [166]; porcine epidemic diarrhea (PEDV) from porcine kobuvirus 1 (PKV) by Vero cells [157]; Hepatitis E virus (HEV) from porcine sapelovirus (PSV) by N1380 cells [167]; and porcine circovirus 2 (PCV2) from porcine parvovirus (PPV) by PK-15 [168].
- (ii)
- An endpoint dilution assay is used to isolate two viruses with a highly similar host range/orientation but different replication rates. However, the separation success rate is usually low. It needs subsequent molecular-level detection and multi-generation blind passages for verification. Beperet et al. successfully isolated two different subtypes of alphabaculoviruses from coinfection samples by an endpoint dilution assay [162]. Dormitorio et al. successfully detected avian influenza virus (AIV) from suspicious allantoine fluid samples using this method [169].
- (iii)
- The Ab neutralization method is suitable for different serotype viruses or two viruses with a distant genetic relationship. This method has a high success rate, but it needs to be verified by subsequent multi-generation blind passages. For the coinfection of multiple serotypes of the same virus, the serotype is generally determined first, and then the 2-dimensional microneutralization test (2D-MNT) corresponding to the serotype is carried out. Mahajan used 2D-MNT to isolate and purify multiple serotype viruses from coinfection samples of FMDV [142].
- (iv)
- The organic solvent treatment method has certain limitations. Whether an organic solvent can kill one virus without affecting another virus needs to be verified. The choice of organic solvent is crucial. At present, it is feasible to remove PPRV with an organic solvent in coinfection of FMDV and PPRV [130]. The use of 5% H2O2 can completely inactivate the infectious laryngotracheitis virus, while the infectivity of NDV, infectious bronchitis virus, and AIV is reduced without being fully inactivated [172].
- (v)
- Hemadsorption is suitable for virus isolation from non-hemagglutinating viruses. The integrity of this method for virus isolation is uncertain and the virus needs to be transferred to susceptible cell lines for amplification. At present, it is feasible to remove PPRV in coinfections of FMDV and PPRV [130]. Hemadsorption is useful for viruses such as IAV, parainfluenza virus, and mumps virus, which express their hemagglutinin proteins on the plasma membrane of infected cells [161].
- (vi)
- Acid/alkali treatment is suitable for the separation of one PH-sensitive virus and another non-PH-sensitive virus. However, due to the difference in PH sensitivity of the isolated virus and the misdetection of molecular detection methods, this method has some notable limitations. Acidic environments (PH < 6.6) can effectively inhibit AIV replication [173]. The optimum survival range of the plague virus is from pH 6 to pH 11, while that of NDV is from pH 2 to pH 11 [174]. Thus, we can isolate viruses from coinfection samples by acid/alkali treatment.
- (vii)
- Reverse genetic system rescues viruses. Some viruses have a mature reverse genetics system. We can isolate the complete genome fragments of the virus from the positive samples and then obtain complete or defective viruses. The disadvantage of this method is that constructing the system necessitates a considerable workload, and it is not suitable for the separation of two related viruses.
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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Coinfecting Viruses | Outcome | Method(s) of Detection | Method(s) of Purification | Cause Mechanisms | Effect on Host | Reference (Published Year) |
---|---|---|---|---|---|---|
HIV and HBV | NA | liver biopsies | NA | NA | Occurrence of complications and increased incidence of nonalcoholic fatty liver disease (NALFD) | [189] (2021) |
COVID-19 and CoV 229E/OC43, AdV, HRV, FluA | Independence | MRT-qPCR | NA | NA | No obvious trend change | [190] (2021) |
HPIV and HRV, RSV, AdV, HCoV, HboV, FluB, HMPV, FluA | NA | multiplex PCR | NA | NA | Alleviation of clinical symptoms in coinfection hosts | [191] (2019) |
HBV and HCV | Noninterference (in vitro) coinfection interfered HBV (in vivo) | PCR, serologic profiles | NA | MiRNA 122 mediated by HCV core protein inhibits HBV replication. | A faster progression and high incidence of hepatocellular carcinoma | [192] (2018) |
DENV, CHIKV, and ZIKV | NA | MRT-qPCR | NA | NA | Mean viraemia was significantly lower in coinfections compared to monoinfections. ZIKV- DENV coinfection did not significantly differ from reported ZIKV monoinfections. Coinfection by ZIKV–CHIKV could affect foetal death | [141] (2019) |
FluA and hPIV2 | coinfection enhanced FluA | Virus titration and Immunofluorescent staining | Cell fusion induced by hPIV2 infection promotes FluA replication. | NA | [9] (2016) | |
FluA and FluB | Noninterference | RT-PCR | Using Embryonating Chicken Eggs | NA | Patients presented typical influenza-like disease symptoms including fever > 39°C, myalgia, pharyngitis, and cough. | [193] (2013) |
HBV, HCV, and HDV | Interference (HCV to HBV) Noninterference (HDV to HBV) | hepatitis B surface antigen loss rates | NA | NA | NA | [194] (2011) |
RV and FluA | coinfection interfered FluA | Virus titration | NA | RV inhibits FluA replication by activating innate immune defense. | Reduced mortality in mice | [22] (2018) |
SARS-CoV-2 and FluA | NA | Virus titration | NA | Coinfections caused severe lymphopenia in peripheral blood, resulting in reduced total IgG, neutralizing antibody titers, and CD4+ T cell responses against each virus. | The coinfection of SARS-CoV-2 with IAV enhanced disease severity. | [195] (2022) |
Leprosy virus and HIV | Noninterference | clinical form and type of leprosy reaction | NA | HIV coinfected patients and patients with leprosy alone expressed similar levels of IL-1β and IL-6. | No change in tissue immunological behavior in patients coinfected with HIV and leprosy. | [196] (2017) |
MDV and REV | Synergy | Confocal imaging, Western blotting, and qRT-PCR | Using the pfu and TCID50 methods | Two virus synergistic replication in vitro is related to innate immune pathway, Akt pathway, and cell adhesion and migration pathway. | Coinfection with Marek’s disease virus (MDV) and reticuloendotheliosis virus (REV) causes synergistic pathogenic effects and serious losses to the poultry industry. | [112] (2022) |
DNV and CHIKV | Noninterference | RT-qPCR | NA | NA | The viruses could stably co-exist both in the cell lines and adult mosquitoes. | [100] (2010) |
DNV and DENV | Interference (DNV to DENV) | Immunostaining for flow cytometry | Cell inoculated virus | NA | NA | [102] (2004) |
DENV, DNV and JEV | Noninterference | Flow cytometry and IFA | Cell inoculated virus | NA | Triple co-infections of viruses can be easily established without signs of disease in C6/36 mosquito cells by sequential viral challenge followed by serial split passage of whole cells. | [197] (2010) |
IBV and APV | Interference (IBV to APV) | RT-PCR | NA | NA | NA | [198] (2001) |
IBV and NDV | Interference (IBV to NDV) | qRT-PCR | NA | NA | NA | [199] (2007) |
HPAIV and NDV | Interference (NDV to HPAIV) | Virus titration | NA | This viral interference is titer dependent. | HPAIV replication was affected and an increase in survival was found in all coinfected groups when compared to the HPAIV single-inoculated group. | [148] (2016) |
SINV and LACV | BHK cell: Enhancement(both SINV and LACV) C6/36 cell: coinfection don’t affect LACV; enhanced SINV | qRT-PCR | CPE | NA | NA | [149] (2014) |
Sindbis Virus and other alphaviruses | Interference | Plaque assays | NA | This interference depends on a central role for the alphavirus trans-acting protease that processes the nonstructural proteins. | Mosquito cells persistently infected with Sindbis virus are broadly able to exclude other alphaviruses | [40] (1997) |
WNV and CxFV | Noninterference (in vitro) Coinfection enhanced WNV (in vivo) | Plaque assays, qRT-PCR, and IFA | NA | The WNV titer in CxFV Izabal (+) C6/36 cells did not reach the maximum titer observed in CxFV Izabal (−) cells due to death of cells caused by CxFV Izabal. | NA | [10] (2010) |
AIV and NDV | Interference | RT-PCR and serology | NA | NA | Coinfection with LPAIV had no impact on clinical signs; ducks coinfected with HPAIV survived for shorter duration. | [200] (2015) |
HSV and VZV | Interference (superinfection exclusion, SE) | Laser confocal | Fluorescent virus rescue | The downregulation of heparan sulfate proteoglycan 2 (HSPG2) that alphaherpesvirus receptor may partially account for the exclusion. | NA | [201] (2014) |
HMPV and HRSV | NA | ELISA and RT-PCR | NA | NA | Increased hospitalization rates | [144] (2005) |
HCV and TTV | NA | PCR-HMA | NA | A generic method based upon PCR and heteroduplex mobility analysis (HMA) can be used to rapidly determine coinfection with two strains of the homologous virus. | NA | [202] (2000) |
GaHV-1 and FWPV | NA | PCR | Using Embryonating Chicken Eggs and CPE | NA | NA | [203] (2010) |
WSSV and IHHNV | NA | PCR and histopathology | NA | NA | Except for typical clinical symptoms of WSSV infection, coinfected shrimps did not have any other external deformities. | [204] (2014) |
lvCIAV and iIBDV | Synergy | PCR, RT-PCR and ELISA | NA | LvCIAV infection attenuated subsequent iIBDV infection-induced T cell recruitment and subsequent B cell depletion in the bursa. | Without occurrence of clinical signs | [205] (2013) |
Multiple coronaviruses | Noninterference | RT-PCR | NA | Bats are natural hosts of coronavirus and potential zoonotic sources of viral pathogens. | NA | [206] (2016) |
HAdV, HEV, RSV and HRV | Noninterference | xTAG RVP Fast v2 and qRT-PCR | NA | NA | Lower frequency of lower respiratory tract infections, lower wheezing rates and higher hospitalization rates | [207] (2016) |
HIV and FluA | Synergy | NA | NA | NA | Higher risk of influenza infection | [208] (2016) |
PCV2 and CSFV | NA | proteomic profiling | NA | Mitochondrial dysfunction, nuclear factor erythroid 2-related factor 2 (Nrf2)-mediated oxidative stress response and apoptosis signaling pathways might be the specifical targets during PCV2-CSFV coinfection. | NA | [209] (2017) |
PPRV and FMDV | Interference | qPT-PCR | Plaque assays, neutralization with antibodies and Viral RNA transfection | NA | NA | [130] (2016) |
RSV and FluA | Interference | Virus titration and IFA | NA | FluA blocks the growth of RSV by competing with RSV for protein synthesis and selective budding. | NA | [210] (2000) |
Two different FluA | Interference | Virus titration, RT-PCR and qRT-PCR | Plaque assays | H3N2 and H1N1 have different abilities to inhibit the replication and transmission of their respective drug-resistant virus mutants. | NA | [211] (2010) |
PRRSV and SIV | Interference | IFA and qRT-PCR | Plaque assays and cell inoculated virus | PRRSV and SIV demonstrate additive effects on the expression of several types of virally induced transcripts. | NA | [212] (2014) |
Two different VACV | Synergy (lung) Interference (spleen) | qPCR | NA | NA | NA | [136] (2018) |
Two different WNV | Interference | Virus titration | NA | This interference depends on blocking the transmission of superinfecting virus. | NA | [213] (1969) |
SLEV and WNV | Interference | qRT-PCR | NA | This interference depends on blocking the transmission of superinfecting virus. | NA | [214] (2009) |
DENV1 and DENV3 | Interference | IFA | NA | This interference depends on blocking the transmission of superinfecting virus. | NA | [215] (1982) |
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Du, Y.; Wang, C.; Zhang, Y. Viral Coinfections. Viruses 2022, 14, 2645. https://doi.org/10.3390/v14122645
Du Y, Wang C, Zhang Y. Viral Coinfections. Viruses. 2022; 14(12):2645. https://doi.org/10.3390/v14122645
Chicago/Turabian StyleDu, Yanting, Chen Wang, and Ying Zhang. 2022. "Viral Coinfections" Viruses 14, no. 12: 2645. https://doi.org/10.3390/v14122645
APA StyleDu, Y., Wang, C., & Zhang, Y. (2022). Viral Coinfections. Viruses, 14(12), 2645. https://doi.org/10.3390/v14122645