. 2019 Sep 12;14(9):e0222381.

doi: 10.1371/journal.pone.0222381. eCollection 2019.

The epidemiological signature of influenza B virus and its B/Victoria and B/Yamagata lineages in the 21st century

Saverio Caini¹, Gabriela Kusznierz², Verònica Vera Garate², Sonam Wangchuk³, Binay Thapa³, Francisco José de Paula Júnior⁴, Walquiria Aparecida Ferreira de Almeida⁴, Richard Njouom⁵, Rodrigo A Fasce⁶, Patricia Bustos⁶, Luzhao Feng⁷, Zhibin Peng⁷, Jenny Lara Araya⁸, Alfredo Bruno^{9

10}, Doménica de Mora⁹, Mónica Jeannette Barahona de Gámez¹¹, Richard Pebody¹², Maria Zambon¹², Rocio Higueros¹³, Rudevelinda Rivera¹⁴, Herman Kosasih¹⁵, Maria Rita Castrucci¹⁶, Antonino Bella¹⁷, Hervé A Kadjo¹⁸, Coulibaly Daouda¹⁹, Ainash Makusheva²⁰, Olga Bessonova²¹, Sandra S Chaves^{22

23}, Gideon O Emukule²³, Jean-Michel Heraud²⁴, Norosoa H Razanajatovo²⁴, Amal Barakat²⁵, Fatima El Falaki²⁵, Adam Meijer²⁶, Gé A Donker¹, Q Sue Huang²⁷, Tim Wood²⁷, Angel Balmaseda²⁸, Rakhee Palekar²⁹, Brechla Moreno Arévalo³⁰, Ana Paula Rodrigues³¹, Raquel Guiomar³², Vernon Jian Ming Lee³³, Li Wei Ang³³, Cheryl Cohen^{34

35}, Florette Treurnicht³⁴, Alla Mironenko³⁶, Olha Holubka³⁶, Joseph Bresee³⁷, Lynnette Brammer²², Mai T Q Le³⁸, Phuong V M Hoang³⁸, Clotilde El Guerche-Séblain³⁹, John Paget¹; Global Influenza B Study team

Affiliations

¹ Netherlands Institute for Health Services Research (Nivel), Utrecht, The Netherlands.
² National Institute of Respiratory Diseases "Emilio Coni", Santa Fe, Argentina.
³ Royal Centre for Disease Control, Department of Public Health, Ministry of Health, Thimphu, Bhutan.
⁴ Ministry of Health, Department of Surveillance of Transmissible Diseases, Brasília/DF, Brazil.
⁵ Virology Department, Centre Pasteur of Cameroon, Yaoundé, Cameroon.
⁶ Sub-Department of Viral Diseases, Instituto de Salud Pública de Chile, Santiago, Chile.
⁷ Division of Infectious Diseases, Chinese Center for Disease Control and Prevention, Beijing, P.R. China.
⁸ National Influenza Center, Ministry of Health, San José, Costa Rica.
⁹ National Institute of Public Health Research (INSPI), National Reference Centre for Influenza and Other Respiratory Viruses, Guayaquil, Ecuador.
¹⁰ Agricultural University of Ecuador, Guayaquil, Ecuador.
¹¹ National Influenza Center, Ministry of Health, San Salvador, El Salvador.
¹² Public Health England, London, England, United Kingdom.
¹³ National Influenza Center, Ministry of Health, Guatemala City, Guatemala.
¹⁴ National Influenza Center, Ministry of Health, Tegucigalpa, Honduras.
¹⁵ US Naval Medical Research Unit No.2, Jakarta, Indonesia.
¹⁶ National Influenza Center, Department of Infectious Diseases, National Institute of Health, Rome, Italy.
¹⁷ Department of Infectious Diseases, National Institute of Health, Rome, Italy.
¹⁸ Department of Epidemic Virus, Institut Pasteur, Abidjan, Côte d'Ivoire.
¹⁹ Service of Epidemiological Diseases Surveillance, National Institute of Public Hygiene, Abidjan, Côte d'Ivoire.
²⁰ National Center of Expertise, Committee of Public Health Protection, Ministry of Health, Astana, Kazakhstan.
²¹ National Center of Expertise, Committee of Public Health Protection, Ministry of Health, Uralsk City, Kazakhstan.
²² Influenza Division, Centers for Disease Control and Prevention, Atlanta, Georgia, United States of America.
²³ Influenza Program, Centers for Disease Control and Prevention, Nairobi, Kenya.
²⁴ National Influenza Center, Virology Unit, Institut Pasteur de Madagascar, Antananarivo, Madagascar.
²⁵ National Influenza Center, Institut National d'Hygiène, Ministry of Health, Rabat, Morocco.
²⁶ National Institute for Public Health and the Environment, Centre for Infectious Diseases Research, Diagnostics and Laboratory Surveillance, Bilthoven, The Netherlands.
²⁷ Institute of Environmental Science and Research, Weillngton, New Zealand.
²⁸ National Influenza Center, Ministry of Health, Managua, Nicaragua.
²⁹ Pan American Health Organization, Washington, District of Columbia, United States of America.
³⁰ National Influenza Center, IC Gorgas, Panama City, Panama.
³¹ Department of epidemiology, National Institute of Health Doutor Ricardo Jorge, Lisbon, Portugal.
³² National Influenza Reference Laboratory, National Institute of Health Doutor Ricardo Jorge, Lisbon, Portugal.
³³ Public Health Group, Ministry of Health, Singapore, Singapore.
³⁴ Centre for Respiratory Diseases and Meningitis, National Institute for Communicable Diseases of the National Health Laboratory Service, Johannesburg, South Africa.
³⁵ School of Public Health, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa.
³⁶ L.V.Gromashevsky Institute of Epidemiology and Infectious Diseases, National Academy of Medical Science of Ukraine, Department of Respiratory and other Viral Infections, Kyiv, Ukraine.
³⁷ Influenza Division, National Center for Immunizations and Respiratory Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia, United States of America.
³⁸ National Institute of Hygiene and Epidemiology, Hanoi, Vietnam.
³⁹ Global Vaccine Epidemiology and Modeling Department (VEM), Franchise Epidemiologist, Sanofi Pasteur, Lyon, France.

PMID: 31513690
PMCID: PMC6742362
DOI: 10.1371/journal.pone.0222381

The epidemiological signature of influenza B virus and its B/Victoria and B/Yamagata lineages in the 21st century

Saverio Caini et al. PLoS One. 2019.

. 2019 Sep 12;14(9):e0222381.

doi: 10.1371/journal.pone.0222381. eCollection 2019.

Authors

Affiliations

¹ Netherlands Institute for Health Services Research (Nivel), Utrecht, The Netherlands.
² National Institute of Respiratory Diseases "Emilio Coni", Santa Fe, Argentina.
³ Royal Centre for Disease Control, Department of Public Health, Ministry of Health, Thimphu, Bhutan.
⁴ Ministry of Health, Department of Surveillance of Transmissible Diseases, Brasília/DF, Brazil.
⁵ Virology Department, Centre Pasteur of Cameroon, Yaoundé, Cameroon.
⁶ Sub-Department of Viral Diseases, Instituto de Salud Pública de Chile, Santiago, Chile.
⁷ Division of Infectious Diseases, Chinese Center for Disease Control and Prevention, Beijing, P.R. China.
⁸ National Influenza Center, Ministry of Health, San José, Costa Rica.
⁹ National Institute of Public Health Research (INSPI), National Reference Centre for Influenza and Other Respiratory Viruses, Guayaquil, Ecuador.
¹⁰ Agricultural University of Ecuador, Guayaquil, Ecuador.
¹¹ National Influenza Center, Ministry of Health, San Salvador, El Salvador.
¹² Public Health England, London, England, United Kingdom.
¹³ National Influenza Center, Ministry of Health, Guatemala City, Guatemala.
¹⁴ National Influenza Center, Ministry of Health, Tegucigalpa, Honduras.
¹⁵ US Naval Medical Research Unit No.2, Jakarta, Indonesia.
¹⁶ National Influenza Center, Department of Infectious Diseases, National Institute of Health, Rome, Italy.
¹⁷ Department of Infectious Diseases, National Institute of Health, Rome, Italy.
¹⁸ Department of Epidemic Virus, Institut Pasteur, Abidjan, Côte d'Ivoire.
¹⁹ Service of Epidemiological Diseases Surveillance, National Institute of Public Hygiene, Abidjan, Côte d'Ivoire.
²⁰ National Center of Expertise, Committee of Public Health Protection, Ministry of Health, Astana, Kazakhstan.
²¹ National Center of Expertise, Committee of Public Health Protection, Ministry of Health, Uralsk City, Kazakhstan.
²² Influenza Division, Centers for Disease Control and Prevention, Atlanta, Georgia, United States of America.
²³ Influenza Program, Centers for Disease Control and Prevention, Nairobi, Kenya.
²⁴ National Influenza Center, Virology Unit, Institut Pasteur de Madagascar, Antananarivo, Madagascar.
²⁵ National Influenza Center, Institut National d'Hygiène, Ministry of Health, Rabat, Morocco.
²⁶ National Institute for Public Health and the Environment, Centre for Infectious Diseases Research, Diagnostics and Laboratory Surveillance, Bilthoven, The Netherlands.
²⁷ Institute of Environmental Science and Research, Weillngton, New Zealand.
²⁸ National Influenza Center, Ministry of Health, Managua, Nicaragua.
²⁹ Pan American Health Organization, Washington, District of Columbia, United States of America.
³⁰ National Influenza Center, IC Gorgas, Panama City, Panama.
³¹ Department of epidemiology, National Institute of Health Doutor Ricardo Jorge, Lisbon, Portugal.
³² National Influenza Reference Laboratory, National Institute of Health Doutor Ricardo Jorge, Lisbon, Portugal.
³³ Public Health Group, Ministry of Health, Singapore, Singapore.
³⁴ Centre for Respiratory Diseases and Meningitis, National Institute for Communicable Diseases of the National Health Laboratory Service, Johannesburg, South Africa.
³⁵ School of Public Health, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa.
³⁶ L.V.Gromashevsky Institute of Epidemiology and Infectious Diseases, National Academy of Medical Science of Ukraine, Department of Respiratory and other Viral Infections, Kyiv, Ukraine.
³⁷ Influenza Division, National Center for Immunizations and Respiratory Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia, United States of America.
³⁸ National Institute of Hygiene and Epidemiology, Hanoi, Vietnam.
³⁹ Global Vaccine Epidemiology and Modeling Department (VEM), Franchise Epidemiologist, Sanofi Pasteur, Lyon, France.

PMID: 31513690
PMCID: PMC6742362
DOI: 10.1371/journal.pone.0222381

Abstract

We describe the epidemiological characteristics, pattern of circulation, and geographical distribution of influenza B viruses and its lineages using data from the Global Influenza B Study. We included over 1.8 million influenza cases occurred in thirty-one countries during 2000-2018. We calculated the proportion of cases caused by influenza B and its lineages; determined the timing of influenza A and B epidemics; compared the age distribution of B/Victoria and B/Yamagata cases; and evaluated the frequency of lineage-level mismatch for the trivalent vaccine. The median proportion of influenza cases caused by influenza B virus was 23.4%, with a tendency (borderline statistical significance, p = 0.060) to be higher in tropical vs. temperate countries. Influenza B was the dominant virus type in about one every seven seasons. In temperate countries, influenza B epidemics occurred on average three weeks later than influenza A epidemics; no consistent pattern emerged in the tropics. The two B lineages caused a comparable proportion of influenza B cases globally, however the B/Yamagata was more frequent in temperate countries, and the B/Victoria in the tropics (p = 0.048). B/Yamagata patients were significantly older than B/Victoria patients in almost all countries. A lineage-level vaccine mismatch was observed in over 40% of seasons in temperate countries and in 30% of seasons in the tropics. The type B virus caused a substantial proportion of influenza infections globally in the 21st century, and its two virus lineages differed in terms of age and geographical distribution of patients. These findings will help inform health policy decisions aiming to reduce disease burden associated with seasonal influenza.

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Conflict of interest statement

Clotilde El-Guerche Séblain is an employee of Sanofi Pasteur. She was the coordinator of the research project at Sanofi Pasteur, she helped define the study objectives, and critically revised the manuscript. When reviewing the manuscript, the revisions concerned the epidemiological findings of the study and not the public health findings or conclusions. This does not alter our adherence to PLOS ONE policies on sharing data and materials. Cheryl Cohen has received grant support from Sanofi Pasteur, Advanced Vaccine Initiative, US Centers for Disease Control and Prevention, and payment of travel costs from Parexel. All of the other authors declare that they have no conflict of interests to disclose.

Figures

**Fig 1. Countries participating in the Global Influenza B Study (GIBS), 2000–2018.**

**Fig 2. Distribution of influenza seasons by proportion of influenza B cases and geographical area (Inter-tropical belt, Northern hemisphere, Southern hemisphere).**
Red bars indicate 25^th, 50^th (median) and 75^th percentiles. The Global Influenza B Study, 2000–2018.

**Fig 3**
Proportion of influenza B cases in a season that were caused by the B/Victoria lineage viruses, according to countries median age (top) and geographical area (bottom). The Global Influenza B Study, 2000–2018.

See this image and copyright information in PMC

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The epidemiological signature of influenza B virus and its B/Victoria and B/Yamagata lineages in the 21st century

Affiliations

The epidemiological signature of influenza B virus and its B/Victoria and B/Yamagata lineages in the 21st century

Authors

Affiliations

Abstract

Conflict of interest statement

Figures

References

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LinkOut - more resources

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Medical