Common cold viruses circulating in children threaten wild chimpanzees through asymptomatic adult carriers
Williams, J. M. et al. Causes of death in the Kasekela chimpanzees of Gombe National Park, Tanzania. Am. J. Primatol. 70(8), 766–777 (2008).
Google Scholar
Emery Thompson, M. et al. Risk factors for respiratory illness in a community of wild chimpanzees (Pan troglodytes schweinfurthii). R. Soc. Open Sci. 5(9), 18484 (2018).
Google Scholar
Wallis, J. & Rick Lee, D. Primate conservation: The prevention of disease transmission. Int. J. Primatol. 20(6), 803–826 (1999).
Google Scholar
Goodall, J. The Chimpanzees of Gombe: Patterns of Behavior (Belknap Press, 1986).
Hastings, B., Kenny, D., Lowenstine, L. J. & Foster, J. W. Mountain gorillas and measles: Ontogeny of a wildlife vaccination program, in Proceedings of the American Association of Zoo Veterinarians Annual Meeting, 1991, no. Table 1, pp. 198–205.
Köndgen, S. et al. Pandemic human viruses cause decline of endangered great apes. Curr. Biol. 18(4), 260–264 (2008).
Google Scholar
Humle, T. The 2003 Epidemic of a Flu-Like Respiratory Disease at Bossou. In The Chimpanzees of Bossou and Nimba (eds Matsuzawa, T. et al.) 325–333 (Springer, 2011).
Google Scholar
Kaur, T. et al. Descriptive epidemiology of fatal respiratory outbreaks and detection of a human-related metapneumovirus in wild chimpanzees (Pan troglodytes) at Mahale Mountains National Park, Western Tanzania. Am. J. Primatol. 70(8), 755–765 (2008).
Google Scholar
Palacios, G. et al. Human metapneumovirus infection in wild mountain Gorillas, Rwanda. Emerg. Infect. Dis. 17(4), 711–713 (2011).
Google Scholar
Grützmacher, K. S. et al. Codetection of respiratory syncytial virus in habituated wild western lowland gorillas and humans during a respiratory disease outbreak. Ecohealth 13(3), 499–510 (2016).
Google Scholar
Mazet, J. A. K. et al. Human respiratory syncytial virus detected in mountain gorilla respiratory outbreaks. Ecohealth 17(4), 449 (2020).
Google Scholar
Patrono, L. V. et al. Human coronavirus OC43 outbreak in wild chimpanzees, Côte d´Ivoire, 2016. Emerg. Microbes Infect. 7(1), 1–4 (2018).
Google Scholar
Grützmacher, K. S. et al. Human respiratory syncytial virus and Streptococcus pneumoniae Infection in Wild Bonobos. Ecohealth 15(2), 462 (2018).
Google Scholar
Köndgen, S. et al. Evidence for human Streptococcus pneumoniae in wild and captive chimpanzees: A potential threat to wild populations. Sci. Rep. 7(1), 1–8 (2017).
Google Scholar
Scully, E. J. et al. Lethal respiratory disease associated with human rhinovirus C in Wild Chimpanzees, Uganda, 2013. Emerg. Infect. Dis. 24(2), 267–274 (2018).
Google Scholar
Negrey, J. D. et al. Simultaneous outbreaks of respiratory disease in wild chimpanzees caused by distinct viruses of human origin. Emerg. Microbes Infect. 8(1), 139–149 (2019).
Google Scholar
Hosaka, K. Mahale: A single flu epidemic killed at least 11 chimps. Pan Afr. News 2(2), 3–4 (1995).
Google Scholar
Szentiks, C. A., Köndgen, S., Silinski, S., Speck, S. & Leendertz, F. H. Lethal pneumonia in a captive juvenile chimpanzee (Pan troglodytes) due to human-transmitted human respiratory syncytial virus (HRSV) and infection with Streptococcus pneumoniae. J. Med. Primatol. 38(4), 236–240 (2009).
Google Scholar
Carne, C., Semple, S., Morrogh-Bernard, H., Zuberbühler, K. & Lehmann, J. The risk of disease to great Apes: Simulating disease spread in Orang-Utan (Pongo pygmaeus wurmbii) and Chimpanzee (Pan troglodytes schweinfurthii) Association Networks. PLoS ONE 9(4), e95039 (2014).
Google Scholar
Hanamura, S. et al. Chimpanzee deaths at Mahale caused by a flu-like disease. Primates 49(1), 77–80 (2008).
Google Scholar
Patrono, L. V. et al. Monkeypox virus emergence in wild chimpanzees reveals distinct clinical outcomes and viral diversity. Nat. Microbiol. 5(7), 955–965 (2020).
Google Scholar
Heikkinen, T. & Järvinen, A. The common cold. Lancet 361(9351), 51 (2003).
Google Scholar
Pappas, D. E. The Common Cold,” in Principles and Practice of Pediatric Infectious Diseases, Elsevier, 2018, pp. 199–202.e1.
Ball, T. M., Holberg, C. J., Aldous, M. B., Martinez, F. D. & Wright, A. L. Influence of attendance at day care on the common cold from birth through 13 years of age. Arch. Pediatr. Adolesc. Med. 156(2), 121–126 (2002).
Google Scholar
Byington, C. L. et al. Community surveillance of respiratory viruses among families in the Utah better identification of germs-longitudinal viral epidemiology (BIG-LoVE) study. Clin. Infect. Dis. 61(8), 1217–1224 (2015).
Google Scholar
Monto, A. S. & Ullman, B. M. Acute respiratory illness in an american community: The Tecumseh study. JAMA 227(2), 164–169 (1974).
Google Scholar
Birger, R. et al. Asymptomatic shedding of respiratory virus among an ambulatory population across seasons. mSphere 3(4), e00249-18 (2018).
Google Scholar
Shaman, J. et al. Asymptomatic summertime shedding of respiratory viruses. J. Infect. Dis. 217(7), 1074–1077 (2018).
Google Scholar
Monto, A. S. & Sullivan, K. M. Acute respiratory illness in the community. Frequency of illness and the agents involved. Epidemiol. Infect. 110(1), 145 (1993).
Google Scholar
O’Neill, M. B., Laval, G., Teixeira, J. C., Palmenberg, A. C. & Pepperell, C. S. Genetic susceptibility to severe childhood asthma and rhinovirus-C maintained by balancing selection in humans for 150 000 years. Hum. Mol. Genet. 29(5), 736 (2020).
Google Scholar
Bianchini, S. et al. Role of respiratory syncytial virus in pediatric pneumonia. Microorganisms 8(12), 1–14 (2020).
Google Scholar
Gern, J. E. et al. Relationships among specific viral pathogens, virus-induced interleukin-8, and respiratory symptoms in infancy. Pediatr. Allergy Immunol. 13(6), 386–393 (2002).
Google Scholar
Coverstone, A. M. et al. Recurrent wheezing in children following human metapneumovirus infection. J. Allergy Clin. Immunol. 142(1), 297 (2018).
Google Scholar
Kermani-Alghoraishi, M., Pouramini, A., Kafi, F. & Khosravi, A. Coronavirus disease 2019 (COVID-19) and severe pericardial effusion: From pathogenesis to management: A case report based systematic review. Curr. Probl. Cardiol. 47(2), 100933 (2022).
Google Scholar
Sidhu, R. S., Sharma, A., Paterson, I. D. & Bainey, K. R. Influenza H1N1 infection leading to cardiac tamponade in a previously healthy patient: A case report. Res. Cardiovasc. Med. 5(3), 1–4 (2016).
Keshavarz Valian, N., Pourakbari, B., Asna Ashari, K., Hosseinpour Sadeghi, R. & Mahmoudi, S. Evaluation of human coronavirus OC43 and SARS-COV-2 in children with respiratory tract infection during the COVID-19 pandemic. J. Med. Virol. 94(4), 1450 (2022).
Google Scholar
Kloepfer, K. M. et al. Detection of pathogenic bacteria during rhinovirus infection is associated with increased respiratory symptoms and asthma exacerbations. J. Allergy Clin. Immunol. 133(5), 1301-1307.e3 (2014).
Google Scholar
Demuri, G. P., Gern, J. E., Eickhoff, J. C., Lynch, S. V. & Wald, E. R. Dynamics of bacterial colonization with Streptococcus pneumoniae, Haemophilus influenzae, and Moraxella catarrhalis during symptomatic and asymptomatic viral upper respiratory tract infection. Clin. Infect. Dis. 66(7), 1045 (2018).
Google Scholar
Köster, P. C., Lapuente, J., Cruz, I., Carmena, D. & Ponce-Gordo, F. Human-borne pathogens: Are they threatening wild great ape populations?. Vet. Sci. 9(7), 356 (2022).
Google Scholar
Dunay, E., Apakupakul, K., Leard, S., Palmer, J. L. & Deem, S. L. Pathogen transmission from humans to great apes is a growing threat to primate conservation. Ecohealth 15(1), 148–162 (2018).
Google Scholar
Chatterjee, A., Mavunda, K. & Krilov, L. R. Current state of respiratory syncytial virus disease and management. Infect. Dis. Ther. 10(Suppl 1), 5 (2021).
Google Scholar
Esneau, C., Duff, A. C. & Bartlett, N. W. Understanding rhinovirus circulation and impact on illness. Viruses 14(1), 141 (2022).
Google Scholar
Simon, A., Manoha, C., Müller, A. & Schildgen, O. Human metapneumovirus and its role in childhood respiratory infections. Curr. Pediatr. Rep. 2(3), 156–165 (2014).
Google Scholar
Morrison, R. E., Mushimiyimana, Y., Stoinski, T. S. & Eckardt, W. Rapid transmission of respiratory infections within but not between mountain gorilla groups. Sci. Rep. 11(1), 19622 (2021).
Google Scholar
Gilardi, K., et al. Best Practice Guidelines for Health Monitoring and Disease Control in Great Ape Populations. (2015).
Granados, A., Goodall, E. C., Luinstra, K., Smieja, M. & Mahony, J. Comparison of asymptomatic and symptomatic rhinovirus infections in university students: incidence, species diversity, and viral load. Diagn. Microbiol. Infect. Dis. 82(4), 292 (2015).
Google Scholar
IUCN SSC Primate Specialist Group, “Great apes, COVID-19 and the SARS CoV-2,” Apr-2021. [Online]. Available: [Accessed: 19-Apr-2023].
Macfie, E. J. & Williamson, E. A. Best Practice Guidelines for Great Ape Tourism. Gland, Switzerland: IUCN SSC Primate Specialist Group (2010).
Sundell, N. et al. PCR detection of respiratory pathogens in asymptomatic and symptomatic adults. J. Clin. Microbiol. 57(1), 10–1128 (2019).
Google Scholar
Nuno, A. et al. Protecting great apes from disease: Compliance with measures to reduce anthroponotic disease transmission. People Nat. 4, 1387–1400 (2022).
Google Scholar
Hartter, J. & Goldman, A. Local responses to a forest park in western Uganda: Alternate narratives on fortress conservation. Oryx 45(1), 60–68 (2011).
Google Scholar
Jin, X. et al. Global burden of upper respiratory infections in 204 countries and territories, from 1990 to 2019. EClin. Med. 37, 100986 (2021).
Chow, E. J., Uyeki, T. M. & Chu, H. Y. The effects of the COVID-19 pandemic on community respiratory virus activity. Nat. Rev. Microbiol. 21, 195–210 (2022).
Google Scholar
Bonilla, F. A. & Oettgen, H. C. Adaptive immunity. J. Allergy Clin. Immunol. 125(2), S33–S40 (2010).
Google Scholar
Alper, C. M., Winther, B., Mandel, E. M. & Doyle, W. J. Temporal relationships for cold-like illnesses and otitis media in sibling pairs. Pediatr. Infect. Dis. J. 26(9), 778–781 (2007).
Google Scholar
Lutwama, J. J. et al. Clinic- and hospital-based sentinel influenza surveillance, Uganda 2007–2010. J. Infect. Dis. 206, S87–S93 (2012).
Google Scholar
Ramesh, A. et al. Metagenomic next-generation sequencing of samples from pediatric febrile illness in Tororo, Uganda. PLoS ONE 14(6), e0218318 (2019).
Google Scholar
L’Huillier, A. G. et al. Survival of rhinoviruses on human fingers. Clin. Microbiol. Infect. 21(4), 381 (2015).
Google Scholar
Kuehl, H. S., Elzner, C., Moebius, Y., Boesch, C. & Walsh, P. D. The price of play: Self-organized infant mortality cycles in chimpanzees. PLoS ONE 3(6), e2440 (2008).
Google Scholar
Turner, R. B. & Lee, W.-M. Rhinovirus, in Clinical Virology, pp. 1063–1082 (2009).
Mäkelä, M. J. et al. Viruses and bacteria in the etiology of the common cold. J. Clin. Microbiol. 36(2), 539 (1998).
Google Scholar
Jacobs, S. E., Lamson, D. M., Kirsten, S. & Walsh, T. J. Human rhinoviruses. Clin. Microbiol. Rev. 26(1), 135–162 (2013).
Google Scholar
Royston, L. & Tapparel, C. Rhinoviruses and respiratory enteroviruses: not as simple as ABC. Viruses 8(1), 16 (2016).
Google Scholar
Firquet, S. et al. Survival of enveloped and non-enveloped viruses on inanimate surfaces. Microbes Environ. 30(2), 140 (2015).
Google Scholar
Jackson, D. J. & Gern, J. E. Rhinovirus infections and their roles in asthma: Etiology and exacerbations. J. Allergy Clin. Immunol. Pract. 10(3), 673–681 (2022).
Google Scholar
Calvo, C. et al. Respiratory syncytial virus coinfections with rhinovirus and human bocavirus in hospitalized children. Medicine (Baltimore) 94(42), e1788 (2015).
Google Scholar
Teo, S. M. et al. The infant nasopharyngeal microbiome impacts severity of lower respiratory infection and risk of asthma development. Cell Host Microbe 17(5), 704–715 (2015).
Google Scholar
Mysore, V. et al. Protective heterologous T cell immunity in COVID-19 induced by the trivalent MMR and Tdap vaccine antigens. Medicine 2(9), 1050-1071.e7 (2021).
Google Scholar
Comunale, B. A. et al. Poliovirus vaccination induces a humoral immune response that cross reacts with SARS-CoV-2. Front. Med. 8, 710010 (2021).
Google Scholar
Brooks, N. A. et al. The association of Coronavirus Disease-19 mortality and prior bacille Calmette–Guerin vaccination: a robust ecological analysis using unsupervised machine learning. Sci. Rep. 11(1), 774 (2021).
Google Scholar
Winkley, K. et al. Immune cell residency in the nasal mucosa may partially explain respiratory disease severity across the age range. Sci. Rep. 11(1), 15927 (2021).
Google Scholar
Zhu, Y. et al. Ancestral SARS-CoV-2, but not Omicron, replicates less efficiently in primary pediatric nasal epithelial cells. PLoS Biol. 20(8), e3001728 (2022).
Google Scholar
Price, R. H. M., Graham, C. & Ramalingam, S. Association between viral seasonality and meteorological factors. Sci. Rep. 9(1), 1–11 (2019).
Google Scholar
Clarke, K., Rivas, A. C., Milletich, S., Sabo-Attwood, T. & Coker, E. S. Prenatal exposure to ambient PM2.5 and early childhood growth impairment risk in east Africa. Toxics 10(11), 705 (2022).
Google Scholar
Weary, T. E. et al. Respiratory disease patterns in rural Western Uganda, 2019–2022. Front. Pediatr. 12, 1336009 (2024).
Google Scholar
ECMWF, Fort Portal Weather & Climate | Temperature & Weather By Month—Climate-Data.org,” 2022. [Online]. Available: [Accessed: 27-Oct-2022].
Okure, D. et al. Characterization of ambient air quality in selected urban areas in Uganda using low-cost sensing and measurement technologies. Environ. Sci. Technol. 56(6), 3324–3339 (2022).
Google Scholar
Drewe, J., O’Riain, M. J., Beamish, E., Currie, H. & Parsons, S. Survey of infections transmissible between baboons and humans, Cape Town, South Africa. Emerg. Infect. Dis. J. 18(2), 298 (2012).
Google Scholar
Naughton-Treves, L., Treves, A., Chapman, C. A. & Wrangham, R. W. Temporal patterns of crop-raiding by primates: linking food availability in croplands and adjacent forest. J. Appl. Ecol. 35(4), 596–606 (1998).
Google Scholar
Sarkar, D. et al. Exploring multiple dimensions of conservation success: Long-term wildlife trends, anti-poaching efforts and revenue sharing in Kibale National Park, Uganda. Anim. Conserv. 25(4), 532–549 (2022).
Google Scholar
Wrangham, R. & Ross, E. Science and Conservation in African Forests: The Benefits of Longterm Research (Cambridge University Press, 2008).
Google Scholar
Narat, V. et al. Higher convergence of human-great ape enteric eukaryotic viromes in central African forest than in a European zoo: A One Health analysis. Nat. Commun. 14(1), 1–13 (2023).
Google Scholar
Negrey, J. D. et al. Viruses associated with ill health in wild chimpanzees. Am. J. Primatol. 84(2), e23358 (2022).
Google Scholar
Teo, K. W. et al. Rhinovirus persistence during the COVID-19 pandemic—Impact on pediatric acute wheezing presentations. J. Med. Virol. 94(11), 5547–5552 (2022).
Google Scholar
Diesner-Treiber, S. C. et al. Respiratory infections in children during a covid-19 pandemic winter. Front. Pediatr. 9, 1132 (2021).
Google Scholar
Be’er, M. et al. Unforeseen changes in seasonality of pediatric respiratory illnesses during the first COVID-19 pandemic year. Pediatr. Pulmonol. 57(6), 1425–1431 (2022).
Google Scholar
Kraay, A. N. M. et al. Fomite-mediated transmission as a sufficient pathway: a comparative analysis across three viral pathogens. BMC Infect. Dis. 18(1), 1–13 (2018).
Google Scholar
Leung, N. H. L. et al. Respiratory virus shedding in exhaled breath and efficacy of face masks. Nat. Med. 26(5), 676–680 (2020).
Google Scholar
Reagan, K. J., McGeady, M. L. & Crowell, R. L. Persistence of human rhinovirus infectivity under diverse environmental conditions. Appl. Environ. Microbiol. 41(3), 618–620 (1981).
Google Scholar
Nuwer, R. Chimpanzees are dying from our colds—These scientists are trying to save them. Nature 625(7995), 442–446 (2024).
Google Scholar
Cook, R. A., Karesh, W. B. & Osofsky, S. A. One world, One health: Building Interdisciplinary bridges to health in a globalized world. in One World, One Health (2004).
Mackenzie, J. S. & Jeggo, M. The one health approach—Why is it so important?. Trop. Med. Infect. Dis. 4(2), 88 (2019).
Google Scholar
Köndgen, S., Schenk, S., Pauli, G., Boesch, C. & Leendertz, F. H. Noninvasive monitoring of respiratory viruses in wild chimpanzees. Ecohealth 7(3), 332–341 (2010).
Google Scholar
Forno, E. et al. Effect of vitamin D3 supplementation on severe asthma exacerbations in children with asthma and low vitamin D levels: The VDKA randomized clinical trial. JAMA 324(8), 1 (2020).
Google Scholar
Bochkov, Y. A., Grindle, K., Vang, F., Evans, M. D. & Gern, J. E. Improved molecular typing assay for rhinovirus species A, B, and C. J. Clin. Microbiol. 52(7), 2461–2471 (2014).
Google Scholar
Wessels, E., Schelfaut, J. J. G., Bernards, A. T. & Claas, E. C. J. Evaluation of several biochemical and molecular techniques for identification of Streptococcus pneumoniae and Streptococcus pseudopneumoniae and their detection in respiratory samples. J. Clin. Microbiol. 50(4), 1171–1177 (2012).
Google Scholar
Kaida, A. et al. Seasonal distribution and phylogenetic analysis of human metapneumovirus among children in Osaka City, Japan. J. Clin. Virol. 35(4), 394–399 (2006).
Google Scholar
Edgar, R. C. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32(5), 1792 (2004).
Google Scholar
Guindon, S. et al. New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0. Syst. Biol. 59(3), 307–321 (2010).
Google Scholar
Lefort, V., Longueville, J.-E. & Gascuel, O. SMS: Smart model selection in PhyML. Mol. Biol. Evol. 34(9), 2422–2424 (2017).
Google Scholar
Rambaut, A. FigTree, version 1.4.4 (2018).
Tamura, K., Stecher, G. & Kumar, S. MEGA11: Molecular evolutionary genetics analysis version 11. Mol. Biol. Evol. 38(7), 3022 (2021).
Google Scholar
Kuznetsova, A., Brockhoff, P. B. & Christensen, R. H. B. lmerTest package: Tests in linear mixed effects models. J. Stat. Softw. 82(13), 1–26 (2017).
Google Scholar
Burnham, K. P., Anderson, D. R. & Huyvaert, K. P. AIC model selection and multimodel inference in behavioral ecology: Some background, observations, and comparisons. Behav. Ecol. Sociobiol. 65(1), 23–35 (2011).
Google Scholar
Breiman, L. Random forests. Mach. Learn. 45(1), 5–32 (2001).
Google Scholar
Liaw, A. & Wiener, M. Classification and regression by randomForest. R. News 2(3), 18–22 (2002).
link
:max_bytes(150000):strip_icc()/iStock-638362340-5927164b3df78cbe7ef56a87.jpg "Top 20 Vaccines You Should Know About")
-1733903826621.jpg "Why Harry Styles Chooses a Pescatarian Diet: Exploring The Benefits Of Nutrition And Sustainability")