Viruses Associated with Acute Conjunctivitis in Vanuatu

Kasso Johnson Ministry of Health Eye Program, Vanuatu;

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Fasihah Taleo Vanuatu Country Office, World Health Organization, Port Vila, Vanuatu;

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Kalbule Willie Ministry of Health Eye Program, Vanuatu;

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Edwin Amel Ministry of Health Eye Program, Vanuatu;

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Madopule Nanu Ministry of Health Eye Program, Vanuatu;

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Marie Alguet Ministry of Health Eye Program, Vanuatu;

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Jose Wass Ministry of Health Eye Program, Vanuatu;

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Prudence Rymill Ministry of Health Eye Program, Vanuatu;

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Anthony Solomon Department of Control of Neglected Tropical Diseases, World Health Organization, Geneva, Switzerland;

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Kevin Ruder Francis I. Proctor Foundation, University of California San Francisco, San Francisco, California;

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Cindi Chen Francis I. Proctor Foundation, University of California San Francisco, San Francisco, California;

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Lina Zhong Francis I. Proctor Foundation, University of California San Francisco, San Francisco, California;

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Armin Hinterwirth Francis I. Proctor Foundation, University of California San Francisco, San Francisco, California;

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David Liu Francis I. Proctor Foundation, University of California San Francisco, San Francisco, California;

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Thomas Abraham Francis I. Proctor Foundation, University of California San Francisco, San Francisco, California;

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Gerami Seitzman Francis I. Proctor Foundation, University of California San Francisco, San Francisco, California;
Department of Ophthalmology, University of California San Francisco, San Francisco, California

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Thomas Lietman Francis I. Proctor Foundation, University of California San Francisco, San Francisco, California;
Department of Ophthalmology, University of California San Francisco, San Francisco, California

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Thuy Doan Francis I. Proctor Foundation, University of California San Francisco, San Francisco, California;
Department of Ophthalmology, University of California San Francisco, San Francisco, California

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for the SCORPIO Study Group

ABSTRACT.

The first manifestation of a viral infection may be conjunctivitis. There are limited data on the etiology of viral conjunctivitis in Vanuatu, a country in the South Pacific Ocean. Patients presenting to one of two Vanuatu health centers with presumed infectious conjunctivitis were eligible if symptom onset was within 14 days of screening. Conjunctival and anterior nasal swabs were obtained and subjected to unbiased RNA deep sequencing (RNA-seq) to identify DNA and RNA viruses. For samples collected from May to November 2021, RNA-seq identified a viral etiology in 12/48 patients. Human adenovirus species were the most common viruses (58%) detected, followed by human herpes viruses (cytomegalovirus, varicella zoster virus, and human herpes 7 virus). Rhinovirus C, Epstein-Barr virus, and bocavirus were also detected. In summary, the etiology for viral conjunctivitis in Vanuatu appears broad. Unbiased testing may be useful for disease surveillance.

Infectious conjunctivitis can be acute, new, and sudden in onset (less than 3 months) or chronic (3 months or more) and may result in significant ocular morbidity. Chronic infectious conjunctivitis secondary to the ocular strains of Chlamydia trachomatis (“trachoma”) disproportionally affects low-resource countries.1,2 Although Vanuatu has recently been declared the first Pacific Island nation to eliminate trachoma, very little is known about causes of acute conjunctivitis in this country, and there is a paucity of previously published data on the molecular or microbiological diagnosis of acute conjunctivitis in the Pacific Islands.3 Acute infectious conjunctivitis is generally heterogeneous and dependent on region, and affects all populations.4 Viral etiology, such as human adenovirus (HAdV), can be highly transmissible and has important public health implications, including lost wages due to time off work and the overprescription of topical antibiotics.5,6 SCORPIO (Seasonal Conjunctivitis Outbreak Reporting for Prevention and Improved Outcomes) is a collaborative study including over 20 international sites that leverages unbiased RNA deep sequencing (RNA-seq) to interrogate the global etiology of acute infectious conjunctivitis.7,8

This article focuses on the viral etiology of acute conjunctivitis in Vanuatu. SCORPIO was approved by the University of California San Francisco (UCSF) institutional review boards and the Vanuatu Ministry of Health. This study adhered to the tenets of the Declaration of Helsinki. The local study team consisted of Vanuatu’s practicing ophthalmologists, nurses, and healthcare workers who are trained in the identification of conjunctivitis. The entire study team participated in acute conjunctivitis study protocol training. Patients of any age with presumed infectious conjunctivitis of up to 14 days’ duration were prospectively enrolled, on the day of presentation, at two sites, Santo and Port Vila, in Vanuatu. Informed consent was obtained from all patients or guardians for children under 18 years of age. Sterile polyester applicators (Puritan, Guilford, ME) were used to swab the lower fornix of each eye and each anterior nasal passage. Swabs were placed in DNA/RNA-Shield media (Zymo Research, Irvine, CA) to inactive pathogens and preserve nucleic acids, and then stored in a −20°C freezer prior to shipping to UCSF for processing. Sample processing, library preparation, and sequencing have been previously described.7,9 The prespecified criteria for presumed pathogen identification were, in brief: 1) virus known to be a human pathogen and representing the most abundant matched reads after water background subtraction; 2) two or more unique reads covering separate regions in DNA virus genomes; or 3) one or more unique reads matching RNA virus genomes. All confidence intervals (CIs) were calculated using the adjusted Wald method.

From May to November 2021, we enrolled 48 patients. Of those 48 patients, samples from 12 (25%) tested positive for viral RNA fragments on unbiased RNA-seq. Patient demographics and clinical symptoms and signs from the 12 patients with viral conjunctivitis pathogens are shown in Table 1. Patients’ ages ranged from 1 month to 68 years; 42% (95% CI: 19–68%) were female. The mean time of symptom onset to presentation was 5 days (range: 1–14 days). Bilateral eye involvement occurred in 33% (95% CI: 14–61%). The most common systemic symptom was coughing (42%; 95% CI: 19–68%), followed by rhinorrhea (33%; 95% CI: 14–61%) and sore throat (9%; 95% CI: 0–40%). Forty-two percent (95% CI: 19–68%) of patients reported affected contacts or family members. On examination of the eyes, 91% (95% CI: 60–100%) presented with purulent discharge, 50% (95% CI: 25–75%) with tearing, 36% (95% CI: 15–65%) with subepithelial infiltrates, and 20% (95% CI: 5–52%) with membranes or pseudomembranes. No patients reported vomiting, although one patient reported diarrhea. No patients had preauricular lymphadenopathy on examination. Forty-five percent (95% CI: 21–72%) of patients presented on topical antibiotics.

Table 1

Patient demographics, clinical symptoms and signs, and associated viruses

Demographics Clinical symptoms and signs Medications and sequencing
Patient no. Age Sex Contact affected Symptom duration (d) Eye (s) affected Sore throat Runny nose Coughing Diarrhea Itching Preauricular lymphadenopathy Tearing Purulent discharge Subepithelial infiltrates Membrane or pseudomembrane Topical medications Results Sites*
1   8 mo M No 1 Right No No No No No No No Yes No Unknown No CMV N, OS
2 2 yr M No 7 Left No Yes Yes No No No Yes Yes No No No HAdV-B N, OD, OS
3 7 yr F Yes 6 Both No No No No No No No Yes No No Tetracycline HAdV-B OS
4 5 yr M Yes 5 Left No Yes Yes No No Unknown Yes Yes Yes Yes No HAdV-C N
5 68 yr F No 7 Left No Yes Yes No No No No Yes No No Tetracycline VZV N
6 47 yr F No 2 Right No No No No No No Yes Yes Yes Yes Tetracycline HAdV-B N, OD, OS
7 7 yr M Yes 3 Right Yes Yes Yes No Yes No Yes Yes No No Tetracycline HAdV-B OS
8 11 yr F Yes 14 Both No No No No No No No Yes No No Ciprofloxacin EBV OS
9 3 yr F No 7 Both No No No No No No Yes Yes Yes No No Bocavirus OD
10 3 yr M Yes 1 Left Unknown Yes Yes Yes No No No Yes No No No Rhinovirus C N
11   1 mo M No 3 Both No No No No No No Yes No Unknown Both No HAdV-D N, OD, OS
12 22 yr M No 3 Left No No No No No No No Unknown Yes Unknown No HAdV-B, HHV-7 OD

CMV = cytomegalovirus; EBV = Epstein-Barr virus; F = female; HAdV = human adenovirus; HHV-7 = human herpes virus 7; M = male; N = nasal; OD = right eye; OS = left eye; VZV = varicella zoster virus.

Sample collection site in which the identified virus(es) met the pathogen call criteria.

Of the viruses identified as associated with conjunctivitis, RNA-seq demonstrated that DNA viruses were the most common pathogens (Figure 1). Of the DNA viruses, seven patients had detectable HAdV RNA in one of their samples taken from either the conjunctiva or nose. Other DNA viruses included cytomegalovirus (CMV), varicella zoster virus (VZV), Epstein-Barr virus (EBV), and bocavirus (Table 1, Figure 1). One patient had codetection of HAdV-B and human herpes virus 7 (HHV-7). Rhinovirus C, a nonenveloped, positive-strand RNA virus, was detected in a 3-year-old boy who had presented with coughing and diarrhea (Figure 2).

Figure 1.
Figure 1.

Stacked bar graph of DNA and RNA viruses detected with RNA-seq. CMV = cytomegalovirus; EBV = Epstein-Barr virus; HAdV = human adenovirus; HHV-7 = human herpes virus 7; VZV = varicella zoster virus.

Citation: The American Journal of Tropical Medicine and Hygiene 108, 3; 10.4269/ajtmh.22-0600

Figure 2.
Figure 2.

Representative external photos of affected patients. Top panel: 2-year-old boy with left eye involvement, purulent discharge, and eyelid crustiness associated with human adenovirus B. Second panel: 3-year-old girl with bilateral eye involvement associated with bocavirus. The left eye was more injected than the right eye with associated tearing and discharge. Third panel: 3-year-old boy with associated rhinovirus C infection. Bottom panel: 68-year-old man with left eye involvement associated with varicella zoster virus. Scabbing of vesicles (red arrows) can be seen in the V1 distribution.

Citation: The American Journal of Tropical Medicine and Hygiene 108, 3; 10.4269/ajtmh.22-0600

In this cohort of patients from Vanuatu, we found that viral-associated conjunctivitis was identified in 25% (12/48) of patients who presented acutely to two health centers. Of those patients, HAdV species accounted for 58%. Although the majority of adenovirus cases were associated with species B, species D and C were also detected. The HAdV types included 5, 7, and 8, indicating that multiple strains were circulating in this population. Human herpes viruses (VZV, CMV, and HHV-7) comprised the second-largest group of pathogens detected.

The patient enrollment period corresponded to various waves of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) transmission worldwide. However, Vanuatu did not experience any large outbreaks until January 2022. During the time of sample collection, Vanuatu had fewer than seven cases of SARS-CoV-2 infection documented.10 It was not surprising that no SARS-CoV-2 RNA was detected in any of the samples we collected.

Bocavirus was detected in a conjunctival sample of a 3-year-old girl with bilateral eye involvement. She was noted to have rhinorrhea, suggesting upper respiratory involvement. Bocaviruses belong to the family Parvoviridae, and are small, icosahedral, nonenveloped, single-stranded DNA viruses. They are frequently detected in the upper airways of children with respiratory symptoms and had been documented in children with conjunctivitis.11,12 Longitudinal serology analysis suggested that the majority of children had acquired bocavirus infection by 6 years of age and that primary infections are strongly associated with respiratory symptoms.11 It remains a debate whether bocaviruses are truly pathogenic, because they are frequently coidentified with other bacteria and viruses.11,12 Antibody testing for IgM was not assessed in this patient. However, RNA-seq detected bocavirus RNA and, given that this is a DNA virus, this indicated that actively replicating viral particles were present on the conjunctiva of this patient.

The only RNA virus detected in our cohort was rhinovirus C. Rhinoviruses are positive-strand RNA viruses in the Enterovirus genus. Rhinoviruses can be detected in the conjunctiva and upper and lower airways of patients with respiratory tract infections and in fecal samples of children with gastroenteritis.13,14 Our patient was a 3-year-old boy who presented with coughing, diarrhea, and conjunctivitis of the left eye. He had been exposed to a sick contact. He had an ocular purulent discharge, but was not noted to have corneal involvement.

The unbiased nature of RNA-seq allowed for the identification of multiple viruses in the same host. In a 22-year-old man, both HAdV-B and HHV-7 RNA fragments were detected in the conjunctival sample. Subepithelial infiltrates were noted in the affected eye, but visual acuity remained 20/20. Although HHV-7 can be associated with conjunctivitis, it is highly prevalent in persons older than 6 years of age and can be found to shed intermittently in saliva.15,16 Thus, we suggest that the patient’s ocular symptoms were likely secondary to HAdV-B infection. It was unclear whether detection of HHV-7 in this setting represented coinfection, reactivation, or colonization.17,18

Viral conjunctivitis has generally been attributed to human adenoviruses.19,20 Here, viral conjunctivitis represented only a quarter of all patients tested. However, HAdV infection accounted for the majority of viral pathogens identified, with HAdV-B7 predominant. HAdV-B7 is known to cause severe respiratory disease, epidemic keratoconjunctivitis, and acute hemorrhagic conjunctivitis.21,22 None of the patients reported severe respiratory disease, although some presented with mild upper respiratory symptoms such as coughing. Two patients with HAdV-B7 presented with corneal involvement. No hemorrhagic conjunctivitis was documented.

The main limitations of the study include the small sample size collected at the two health centers in Vanuatu and the lack of traditional microbiological testing. Worldwide, however, testing of any type for the etiology of conjunctivitis is rarely performed in the ambulatory setting. Additional limitations include the possibility that the patient cleared the pathogen prior to swabbing and that topical medications used at the time of swabbing limited pathogen detection. Finally, although there were only a few confirmed cases of SARS-CoV-2 in Vanuatu during the enrollment period, patients were anecdotally less likely to seek care than prior to the pandemic, and health centers were not operating at full capacity. Thus, the results reported in the study are likely to be an underestimation of the circulating viruses associated with infectious conjunctivitis in the population.

In summary, this study suggests that DNA viruses are commonly associated with acute conjunctivitis in Vanuatu. Multiple human adenovirus types can circulate at the same time and affect children and adults alike. It is unclear whether this pattern has evolved over time, because there exists limited literature on the viral etiology of conjunctivitis in Vanuatu. As SCORPIO continues to characterize pathogens causing acute conjunctivitis in Vanuatu and around the world, regional priorities for treatment pathways, surveillance, and diagnostic and therapeutic research may become clearer.

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Author Notes

Address correspondence to Thuy Doan, Francis I. Proctor Foundation, University of California San Francisco, 490 Illinois St., Fl. 2, San Francisco, CA 94158. E-mail: thuy.doan@ucsf.edu

Financial support: Research reported in this manuscript was supported by the National Eye Institute of the National Institutes of Health under Award Number R01EY032041 (T. D.), a Research to Prevent Blindness Unrestricted Grant, and the Peierls Foundation. F. T. and A. S. are staff members of the World Health Organization. The authors alone are responsible for the views expressed in this article and they do not necessarily represent the views, decisions, or policies of the institutions with which they are affiliated, or of the National Institutes of Health.

Seasonal Conjunctivitis Outbreak Reporting for Prevention and Improved Outcomes (SCORPIO) Study Group: Aravind Eye Hospital, Madurai, India: Lalitha Prajna, N. Venkatesh Prajna, Ramesh Gunasekaran, Sankalp Singh Sharma, and Vishnu Teja; B. P. Koirala Lions Center for Ophthalmic Studies, Kathmandu, Nepal: Meenu Chaudhary and Sanjeeta Sitaula; Centre de Recherche en Sante de Nouna, Nouna, Burkina Faso: Ali Sié, Boubacar Coulibaly, and Mamadou Bountogo; Chulalongkorn University, Bangkok, Thailand: Thanapong Somkijrungroj and Vannarut Satitpitakul; Hai Yen Vision Institute, Ho Chi Minh City, Vietnam: Huy Tran, Linh Hoàng Mai, Thảo Hạ Xuân, and Yen Tran; Hospital Clinico Universidad de Chile, Santiago, Chile: Cristhian A. Urzua, Fabian Vega, Felipe Salgado, and Loreto Cuitino; Instituto Mexicano de Oftalmología, Santiago de Querétaro, Mexico: Fernando Pérez Pérez, Jaime Macías Martínez, and Van Charles Lansingh; Khon Kaen University, Khon Kaen, Thailand: Sukhumal Thanapaisal and Wipada Laovirojjanakul; National Eye Institute, Bethesda, MD: George McKie (Program Officer); Oregon Health and Science University, Portland, Oregon: Kenia Chavez, Travis Redd, and Winston Chamberlain; Pacific Vision Institute of Hawaii, Honolulu, Hawaii: Angel Cheng and Vivien Tham; Phramongkutklao Hospital, Bangkok, Thailand: Wiwan Sansanayudh; Programme National de Santé Oculaire, Niamey, Niger: Abba Kaka Hajia Yakoura, Abdou Amza, Abdoul Salam Youssoufou Souley, Adam Nouhou Diori, Beido Nassirou, Boubacar Kadri, Boubacar Mariama, Cissé Mamadou Ibrahim, Lamyne Aboubacar Roufaye, Ramatou Boulhassane, Saley Ali, and Zakou Abdou; Rabin Medical Center, Petah Tikva, Israel: Lee Goren and Ruti Sella; Sinai Hospital, Baltimore, Maryland: Clare Kelliher and Laura Green; Singapore Eye Research Institute, Singapore: Hon Shing Ong, Jod Mehta, and Yu-Chi Liu; Stanford University School of Medicine, Stanford, California: Benjamin A. Pinsky; Taipei Veterans General Hospital, Taipei, Taiwan: De-Kuang Hwang and Nai-Wen Fan; The University of Sydney Save Sight Institute, Sydney, Australia: Hong Sheng Chiong, Javier Lacorzana, Maria Cabrera-Aguas, and Stephanie Watson; University of California Los Angeles Stein Eye Institute, Los Angeles, California: Edmund Tsui, Joana Ramirez, Nina M. Cherian, Rachel Feit-Leichman, Reginald E. Hughes Jr., and Tania Onclinx; University of California San Diego Shiley Eye Institute, La Jolla, California: Carol Yu, Esmeralda McClean, and Iliana Molina; University of California San Francisco Francis I. Proctor Foundation, San Francisco, California: Armin Hinterwirth, Cindi Chen, Danny Yu, David Liu, Elodie Lebas, Emily Colby, Gerami Seitzman, Kevin Ruder, Lina Zhong, Michael Deiner, Thomas Abraham, Thomas Lietman, Thuy Doan (Principal Investigator), Travis Porco, and Stephen McLeod; University of California Berkeley School of Optometry, Berkeley, California: Kuniyoshi Kanai and Meredith Whiteside; University of Nebraska Medical Center Truhlsen Eye Institute, Omaha, Nebraska: Steven Yeh and Tolulope Fashina; University of New Mexico, Albuquerque, New Mexico: James Chodosh; University of Papua New Guinea School of Medicine and Health Sciences, Port Moresby, Papua New Guinea: Bridgit Tarkap, Jambi N. Garap, and Magdalene Mangot; Vanuatu Eye Program, Ministry of Health, Port Vila, Vanuatu: Edwin Amel, Fasihah Taleo, Kasso Johnson, Kalbule Willie, Madopule Nanu, and Prudence Rymill; World Health Organization, Geneva, Switzerland: Anthony Solomon.

Authors’ addresses: Kasso Johnson, Kalbule Willie, Edwin Amel, Madopule Nanu, Marie Alguet, Jose Wass, and Prudence Rymill, Ministry of Health Eye Program, Vanuatu, E-mails: kassojohnson@vanuatu.gov.vu, wkalbule@vanuatu.gov.vu, edamel74@gmail.com, madopule@gmail.com, and prymill@vanuatu.gov.vu. Fasihah Taleo, Vanuatu Country Office, World Health Organization, Port Vila, Vanuatu, E-mail: taleof@who.int. Anthony Solomon, Department of Control of Neglected Tropical Diseases, World Health Organization, Geneva, Switzerland, E-mail: solomona@who.int. Kevin Ruder, Cindi Chen, Lina Zhong, Armin Hinterwirth, David Liu, and Thomas Abraham, Francis I. Proctor Foundation, University of California San Francisco, San Francisco, California, E-mails: kevin.ruder@ucsf.edu, cindi.chen@ucsf.edu, lina.zhong@ucsf.edu, armin.hinterwirth@ucsf.edu, david.liu5@ucsf.edu, and thomas.abraham@ucsf.edu. Gerami Seitzman, Thomas Lietman, and Thuy Doan, Francis I. Proctor Foundation, University of California San Francisco, San Francisco, California, and Department of Ophthalmology, University of California San Francisco, San Francisco, California, E-mails: gerami.seitzman@ucsf.edu, tom.lietman@ucsf.edu, and thuy.doan@ucsf.edu.

  • Figure 1.

    Stacked bar graph of DNA and RNA viruses detected with RNA-seq. CMV = cytomegalovirus; EBV = Epstein-Barr virus; HAdV = human adenovirus; HHV-7 = human herpes virus 7; VZV = varicella zoster virus.

  • Figure 2.

    Representative external photos of affected patients. Top panel: 2-year-old boy with left eye involvement, purulent discharge, and eyelid crustiness associated with human adenovirus B. Second panel: 3-year-old girl with bilateral eye involvement associated with bocavirus. The left eye was more injected than the right eye with associated tearing and discharge. Third panel: 3-year-old boy with associated rhinovirus C infection. Bottom panel: 68-year-old man with left eye involvement associated with varicella zoster virus. Scabbing of vesicles (red arrows) can be seen in the V1 distribution.

  • 1.

    Solomon AW , Burton MJ , Gower EW , Harding-Esch EM , Oldenburg CE , Taylor HR , Traoré L , 2022. Trachoma. Nat Rev Dis Primers 8: 32.

  • 2.

    Lietman TM , Oldenburg CE , Keenan JD , 2020. Trachoma: time to talk eradication. Ophthalmology 127: 1113.

  • 3.

    Butcher R et al., 2020. Ocular Chlamydia trachomatis infection, anti-Pgp3 antibodies and conjunctival scarring in Vanuatu and Tarawa, Kiribati before antibiotic treatment for trachoma. J Infect 80: 454461.

    • Search Google Scholar
    • Export Citation
  • 4.

    Kaur G , Seitzman GD , Lietman TM , McLeod SD , Porco TC , Doan T , Deiner MS , 2022. Keeping an eye on pink eye: a global conjunctivitis outbreak expert survey. Int Health 14: 542544.

    • Search Google Scholar
    • Export Citation
  • 5.

    Garcia-Zalisnak D , Rapuano C , Sheppard JD , Davis AR , 2018. Adenovirus ocular infections: prevalence, pathology, pitfalls, and practical pointers. Eye Contact Lens 44: S1S7.

    • Search Google Scholar
    • Export Citation
  • 6.

    Ghebremedhin B , 2014. Human adenovirus: viral pathogen with increasing importance. Eur J Microbiol Immunol (Bp) 4: 2633.

  • 7.

    Prajna NV et al., 2022. Outpatient human coronavirus associated conjunctivitis in India. J Clin Virol 157: 105300.

  • 8.

    Lalitha P et al., 2022. Deep sequencing analysis of clinical samples from patients with acute infectious conjunctivitis during the COVID-19 delta surge in Madurai, India. J Clin Virol 157: 105318.

    • Search Google Scholar
    • Export Citation
  • 9.

    Lalitha P et al., 2019. Unbiased pathogen detection and host gene profiling for conjunctivitis. Ophthalmology 126: 10901094.

  • 10.

    Johns Hopkins Database, 2022. Available at: https://coronavirus.jhu.edu. Accessed August 5, 2022.

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    Meriluoto M et al., 2012. Association of human bocavirus 1 infection with respiratory disease in childhood follow-up study, Finland. Emerg Infect Dis 18: 264271.

    • Search Google Scholar
    • Export Citation
  • 12.

    Guido M , Tumolo MR , Verri T , Romano A , Serio F , De Giorgi M , De Donno A , Bagordo F , Zizza A , 2016. Human bocavirus: current knowledge and future challenges. World J Gastroenterol 22: 86848697.

    • Search Google Scholar
    • Export Citation
  • 13.

    Bochkov YA , Gern JE , 2012. Clinical and molecular features of human rhinovirus C. Microbes Infect 14: 485494.

  • 14.

    Lau SK , Yip CC , Lung DC , Lee P , Que TL , Lau YL , Chan KH , Woo PC , Yuen KY , 2012. Detection of human rhinovirus C in fecal samples of children with gastroenteritis. J Clin Virol 53: 290296.

    • Search Google Scholar
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