#Global #trends in #antimicrobial #resistance in #animals in low- and middle-income countries (Science, abstract)

[Source: Science, full page: (LINK). Abstract, edited.]

Global trends in antimicrobial resistance in animals in low- and middle-income countries

Thomas P. Van Boeckel1,2,6,*,†,  João Pires1,6,†, Reshma Silvester2, Cheng Zhao1, Julia Song3,4, Nicola G. Criscuolo1, Marius Gilbert5, Sebastian Bonhoeffer6,‡, Ramanan Laxminarayan1,2,4,‡

1 Institute for Environmental Decisions, ETH Zurich, Zurich, Switzerland. 2 Center for  Disease Dynamics, Economics and Policy, New Delhi, India. 3 Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ, USA. 4 Princeton Environmental Institute, Princeton University, Princeton, NJ, USA. 5 Université Libre de Bruxelles (ULB), Brussels, Belgium. 6 Institute for Integrative Biology, ETH Zurich, Zurich, Switzerland.

*Corresponding author. Email: thomas.vanboeckel@env.ethz.ch

† These authors contributed equally to this work.

‡ These authors contributed equally to this work.

Science  20 Sep 2019: Vol. 365, Issue 6459, eaaw1944 / DOI: 10.1126/science.aaw1944


Livestock antibiotic resistance

Most antibiotic use is for livestock, and it is growing with the increase in global demand for meat. It is unclear what the increase in demand for antibiotics means for the occurrence of drug resistance in animals and risk to humans. Van Boeckel et al. describe the global burden of antimicrobial resistance in animals on the basis of systematic reviews over the past 20 years (see the Perspective by Moore). There is a clear increase in the number of resistant bacterial strains occurring in chickens and pigs. The current study provides a much-needed baseline model for low- and middle-income countries and provides a “one health” perspective to which future data can be added.

Science, this issue p. eaaw1944; see also p. 1251


Structured Abstract


The global scale-up in demand for animal protein is the most notable dietary trend of our time. Since 2000, meat production has plateaued in high-income countries but has grown by 68%, 64%, and 40% in Asia, Africa, and South America, respectively. The transition to high-protein diets in low- and middle-income countries (LMICs) has been facilitated by the global expansion of intensive animal production systems in which antimicrobials are used routinely to maintain health and productivity. Globally, 73% of all antimicrobials sold on Earth are used in animals raised for food. A growing body of evidence has linked this practice with the rise of antimicrobial-resistant infections, not just in animals but also in humans. Beyond potentially serious consequences for public health, the reliance on antimicrobials to meet demand for animal protein is a likely threat to the sustainability of the livestock industry, and thus to the livelihood of farmers around the world.


In LMICs, trends in antimicrobial resistance (AMR) in animals are poorly documented. In the absence of systematic surveillance systems, point prevalence surveys represent a largely untapped source of information to map trends in AMR in animals. We use geospatial models to produce global maps of AMR in LMICs and give policy-makers—or a future international panel—a baseline for monitoring AMR levels in animals and target interventions in the regions most affected by the rise of resistance.


We identified 901 point prevalence surveys from LMICs reporting AMR rates in animals for common indicator pathogens: Escherichia coli, Campylobacter spp., nontyphoidal Salmonella spp., and Staphylococcus aureus. From 2000 to 2018, the proportion of antimicrobial compounds with resistance higher than 50% (P50) increased from 0.15 to 0.41 in chickens and from 0.13 to 0.34 in pigs and plateaued between 0.12 and 0.23 in cattle. Global maps of AMR (available at resistancebank.org) show hotspots of resistance in northeastern India, northeastern China, northern Pakistan, Iran, eastern Turkey, the south coast of Brazil, Egypt, the Red River delta in Vietnam, and the areas surrounding Mexico City and Johannesburg. Areas where resistance is just starting to emerge are Kenya, Morocco, Uruguay, southern Brazil, central India, and southern China. Uncertainty in our predictions was greatest in the Andes, the Amazon region, West and Central Africa, the Tibetan plateau, Myanmar, and Indonesia. Dense geographical coverage of point prevalence surveys did not systematically correlate with the presence of hotspots of AMR, such as in Ethiopia, Thailand, Chhattisgarh (India), and Rio Grande do Sul (Brazil). The highest resistance rates were observed with the most commonly used classes of antimicrobials in animal production: tetracyclines, sulfonamides, and penicillins.


The portfolio of antimicrobials used to raise animals for food is rapidly getting depleted, with important consequences for animal health, farmers’ livelihoods, and potentially for human health. Regions affected by the highest levels of AMR should take immediate actions to preserve the efficacy of antimicrobials that are essential in human medicine by restricting their use in animal production. In some middle-income countries, particularly in South America, surveillance must be scaled up to match that of low-income African countries that are currently outperforming them despite more limited resources. Policy-makers coordinating the international response to AMR may consider sparing African countries from the most aggressive measures to restrict access to veterinary drugs, which may undermine livestock-based economic development and rightfully be perceived as unfair. However, in regions where resistance is starting to emerge, there is a window of opportunity to limit the rise of resistance by encouraging a transition to sustainable animal farming practices. High-income countries, where antimicrobials have been used on farms since the 1950s, should support this transition—for example, through a global fund to subsidize improvement in farm-level biosafety and biosecurity.



The global scale-up in demand for animal protein is the most notable dietary trend of our time. Antimicrobial consumption in animals is threefold that of humans and has enabled large-scale animal protein production. The consequences for the development of antimicrobial resistance in animals have received comparatively less attention than in humans. We analyzed 901 point prevalence surveys of pathogens in developing countries to map resistance in animals. China and India represented the largest hotspots of resistance, with new hotspots emerging in Brazil and Kenya. From 2000 to 2018, the proportion of antimicrobials showing resistance above 50% increased from 0.15 to 0.41 in chickens and from 0.13 to 0.34 in pigs. Escalating resistance in animals is anticipated to have important consequences for animal health and, eventually, for human health.

Keywords: Antibiotics; Drugs Resistance; Worldwide; Cattle; Poultry; Pigs.



Effect of #closure of live #poultry #markets in #China on #prevention and control of #human #infection with #H7N9 #avian #influenza: a case study of four cities in #Jiangsu Province (J Public Health Policy, abstract)

[Source: US National Library of Medicine, full page: (LINK). Abstract, edited.]

J Public Health Policy. 2019 Sep 16. doi: 10.1057/s41271-019-00185-2. [Epub ahead of print]

Effect of closure of live poultry markets in China on prevention and control of human infection with H7N9 avian influenza: a case study of four cities in Jiangsu Province.

Ma J1, Yang N1, Gu H2, Bai L1, Sun J1, Gu S1, Gu J3.

Author information: 1 Center for Health Policy and Management Studies, School of Government, Nanjing University, Nanjing, 210093, China. 2 Center for Health Policy and Management Studies, School of Government, Nanjing University, Nanjing, 210093, China. ghai1008@nju.edu.cn. 3 Nanjing Foreign Language School Xianlin Campus, Nanjing, China.



As of August 2017, China had encountered five seasonal epidemics of H7N9 avian influenza. To prevent people from contracting H7N9 avian influenza, most cities closed live poultry markets (LPMs) to cut off the source of H7N9 virus. The objective of this study is to assess the impact of LPMs closure on reducing zoonotic transmission of avian influenza A (H7N9) virus and to make specific recommendations on the duration of closing the LPMs. Results show that the closure of LPMs can effectively control the spread of H7N9 avian influenza and reduce the incidence of human infection with H7N9. If cases of H7N9 avian influenza continue to occur, LPMs should close for at least 3-4 weeks in susceptible areas to control the spread of infection.

KEYWORDS: Avian influenza; H7N9; Incidence; Live poultry market; Zoonotic transmission

PMID: 31527787 DOI: 10.1057/s41271-019-00185-2

Keywords: Avian Influenza; H7N9; Human; Poultry; Live Poultry Markets; Jiangsu; China.


Where #backyard #poultry raisers seek care for sick poultry: implications for #avian #influenza #prevention in #Bangladesh (BMC Public Health, abstract)

[Source: US National Library of Medicine, full page: (LINK). Abstract, edited.]

BMC Public Health. 2018 Aug 3;18(1):969. doi: 10.1186/s12889-018-5819-5.

Where backyard poultry raisers seek care for sick poultry: implications for avian influenza prevention in Bangladesh.

Rimi NA1, Sultana R2,3, Ishtiak-Ahmed K2,4, Haider N2,5, Azziz-Baumgartner E6, Nahar N2, Luby SP2,6,7.

Author information: 1 Program for Emerging Infections (PEI), Infectious Diseases Division (IDD), icddr, b, 68, Shaheed Tajuddin Ahmed Sharani, Mohakhali, Dhaka, 1212, Bangladesh. nadiarimi@icddrb.org. 2 Program for Emerging Infections (PEI), Infectious Diseases Division (IDD), icddr, b, 68, Shaheed Tajuddin Ahmed Sharani, Mohakhali, Dhaka, 1212, Bangladesh. 3 Department of Public Health, University of Copenhagen, Copenhagen, Denmark. 4 University of Copenhagen, Copenhagen, Denmark. 5 Technical University of Denmark, Copenhagen, Denmark. 6 Centers for Disease Control and Prevention (CDC), Atlanta, GA, USA. 7 Stanford University, Stanford, California, USA.




In Bangladesh, backyard poultry raisers lack awareness of avian influenza and infrequently follow government recommendations for its prevention. Identifying where poultry raisers seek care for their ill poultry might help the government better plan how to disseminate avian influenza prevention and control recommendations.


In order to identify where backyard poultry raisers seek care for their ill poultry, we conducted in-depth and informal interviews: 70 with backyard poultry raisers and six with local poultry healthcare providers in two villages, and five with government veterinary professionals at the sub-district and union levels in two districts during June-August 2009.


Most (86% [60/70]) raisers sought care for their backyard poultry locally, 14% used home remedies only and none sought care from government veterinary professionals. The local poultry care providers provided advice and medications (n = 6). Four local care providers had shops in the village market where raisers sought healthcare for their poultry and the remaining two visited rural households to provide poultry healthcare services. Five of the six local care providers did not have formal training in veterinary medicine. Local care providers either did not know about avian influenza or considered avian influenza to be a disease common among commercial but not backyard poultry. The government professionals had degrees in veterinary medicine and experience with avian influenza and its prevention. They had their offices at the sub-district or union level and lacked staffing to reach the backyard raisers at the village level.


The local poultry care providers provided front line healthcare to backyard poultry in villages and were a potential source of information for the rural raisers. Integration of these local poultry care providers in the government’s avian influenza control programs is a potentially useful approach to increase poultry raisers’ and local poultry care providers’ awareness about avian influenza.

KEYWORDS: Avian influenza; Backyard poultry raiser; Bangladesh; Informal care provider, poultry care provider, poultry disease; Perception

PMID: 30075714 PMCID: PMC6090748 DOI: 10.1186/s12889-018-5819-5 [Indexed for MEDLINE] Free PMC Article

Keywords: Avian Influenza; Poultry; Human; Public Health; Bangladesh.


#Rapid #evolution of #Mexican #H7N3 highly pathogenic #avian #influenza viruses in #poultry (PLoS One, abstract)

[Source: PLoS One, full page: (LINK). Abstract, edited.]


Rapid evolution of Mexican H7N3 highly pathogenic avian influenza viruses in poultry

Sungsu Youk , Dong-Hun Lee , Helena L. Ferreira, Claudio L. Afonso, Angel E. Absalon, David E. Swayne, David L. Suarez, Mary J. Pantin-Jackwood

Published: September 12, 2019 / DOI: https://doi.org/10.1371/journal.pone.0222457



Highly pathogenic avian influenza (HPAI) virus subtype H7N3 has been circulating in poultry in Mexico since 2012 and vaccination has been used to control the disease. In this study, eight Mexican H7N3 HPAI viruses from 2015–2017 were isolated and fully sequenced. No evidence of reassortment was detected with other avian influenza (AI) viruses, but phylogenetic analyses show divergence of all eight gene segments into three genetic clusters by 2015, with 94.94 to 98.78 percent nucleotide homology of the HA genes when compared to the index virus from 2012. The HA protein of viruses from each cluster showed a different number of basic amino acids (n = 5–7) in the cleavage site, and six different patterns at the predicted N-glycosylation sites. Comparison of the sequences of the Mexican lineage H7N3 HPAI viruses and American ancestral wild bird AI viruses to characterize the virus evolutionary dynamics showed that the nucleotide substitution rates in PB2, PB1, PA, HA, NP, and NS genes greatly increased once the virus was introduced into poultry. The global nonsynonymous and synonymous ratios imply strong purifying selection driving the evolution of the virus. Forty-nine positively selected sites out of 171 nonsynonymous mutations were identified in the Mexican H7N3 HPAI viruses, including 7 amino acid changes observed in higher proportion in North American poultry origin AI viruses isolates than in wild bird-origin viruses. Continuous monitoring and molecular characterization of the H7N3 HPAI virus is important for better understanding of the virus evolutionary dynamics and further improving control measures including vaccination.


Citation: Youk S, Lee D-H, Ferreira HL, Afonso CL, Absalon AE, Swayne DE, et al. (2019) Rapid evolution of Mexican H7N3 highly pathogenic avian influenza viruses in poultry. PLoS ONE 14(9): e0222457. https://doi.org/10.1371/journal.pone.0222457

Editor: Maria Serena Beato, Istituto Zooprofilattico Sperimentale delle Venezie, ITALY

Received: April 24, 2019; Accepted: August 29, 2019; Published: September 12, 2019

This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

Data Availability: All relevant data are within the manuscript and its Supporting Information files.

Funding: This research was supported by the ARS Project 6040-32000-066-00D, 6040-32000-072-00D and CRIP (Center of Research in Influenza Pathogenesis) an NIAID funded Center of Excellence in Influenza Research and Surveillance (CEIRS, contract HHSN272201400008C). D-H. Lee is partially supported by the U.S. Department of Agriculture, Agricultural Research Service CRIS project no. 6040-32000-066-51S. Its contents are solely the responsibility of the authors and do not necessarily represent the official views of the USDA or NIH. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the USDA. USDA is an equal opportunity provider and employer. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Competing interests: The authors have declared that no competing interests exist.

Keywords: Avian Influenza; H7N3; Poultry; Mexico.


#H3N2 #avian #influenza viruses detected in live #poultry #markets in #China bind to #human-type #receptors and transmit in guinea pigs and ferrets (Emerg Microbes Infect., abstract)

[Source: US National Library of Medicine, full page: (LINK). Abstract, edited.]

Emerg Microbes Infect. 2019;8(1):1280-1290. doi: 10.1080/22221751.2019.1660590.

H3N2 avian influenza viruses detected in live poultry markets in China bind to human-type receptors and transmit in guinea pigs and ferrets.

Guan L1, Shi J1, Kong X1, Ma S1, Zhang Y1, Yin X1, He X1, Liu L1, Suzuki Y2, Li C1, Deng G1, Chen H1.

Author information: 1 State Key Laboratory of Veterinary Biotechnology, Harbin Veterinary Research Institute, CAAS , Harbin , People’s Republic of China. 2 College of Life and Health Sciences, Chubu University , Aichi , Japan.



The H3N2 influenza viruses became widespread in humans during the 1968 H3N2 pandemic and have been a major cause of influenza epidemics ever since. Different lineages of H3N2 influenza viruses are also commonly found in animals. If a different lineage of H3N2 virus jumps to humans, a human influenza pandemic could occur with devastating consequences. Here, we studied the genetics, receptor-binding properties, and replication and transmission in mammals of 15 H3N2 avian influenza viruses detected in live poultry markets in China. We found that the H3N2 avian influenza viruses are complicated reassortants with distinct replication phenotypes in mice. Five viruses replicated efficiently in mice and bound to both human-type and avian-type receptors. These viruses transmitted efficiently to direct-contact guinea pigs, and three of them also transmitted among guinea pigs and ferrets via respiratory droplets. Moreover, ferret antiserum induced by human H3N2 viruses did not react with any of the H3N2 avian influenza viruses. Our study demonstrates that the H3N2 avian influenza viruses pose a clear threat to human health and emphasizes the need for continued surveillance and evaluation of the H3N2 influenza viruses circulating in nature.

KEYWORDS: Avian influenza virus; H3N2; ferret; guinea pig; transmission

PMID: 31495283 DOI: 10.1080/22221751.2019.1660590

Keywords: Avian Influenza; H3N2; Reassortant strain; Poultry; Live poultry markets; China.


Protective efficacy of an inactivated chimeric #H5 #avian #influenza #vaccine against H5 highly pathogenic avian influenza virus clades and (J Gen Virol., abstract)

[Source: US National Library of Medicine, full page: (LINK). Abstract, edited.]

J Gen Virol. 2018 Dec;99(12):1600-1607. doi: 10.1099/jgv.0.001140. Epub 2018 Oct 25.

Protective efficacy of an inactivated chimeric H5 avian influenza vaccine against H5 highly pathogenic avian influenza virus clades and

Li J1, Hou G1, Wang Y2, Wang S1, Cheng S1, Peng C1, Jiang W1.

Author information: 1 ​China Animal Health and Epidemiology Center, Qingdao, PR China. 2 ​Shanghai Entry-Exit Inspection and Quarantine Bureau, Shanghai, PR China.



The H5 subtype of highly pathogenic avian influenza (HPAI) viruses pose a serious challenge to public health and the poultry industry in China. In this study, we generated a chimeric QH/KJ recombinant virus expressing the entire haemagglutinin (HA)-1 region of the HPAI virus A/chicken/China/QH/2017(H5N6) (clade and the HA2 region of the HPAI virus A/chicken/China/KJ/2017(H5N1) (clade The resulting chimeric PR8-QH/KJ virus exhibited similar in vitro growth kinetics as the parental PR8-QH and PR8-KJ viruses. The chimeric PR8-QH/KJ virus induced specific, cross-reactive haemagglutination-inhibition and serum-neutralizing antibodies against both QH and KJ viruses, although PR8-QH and PR8-KJ exhibited no cross-reactivity with each other. Furthermore, the chimeric PR8-QH/KJ vaccine significantly reduced virus shedding and completely protected chickens from challenge with HPAI H5N6 and H5N1 viruses. However, the Re-8 vaccine against clade viruses provided specific-pathogen-free chickens only partial protection when challenged with QH virus. Our results suggest that the antigenic variation of these epidemic viruses occurred and they can escape the current vaccine immunization. The Re-8 vaccine needs an update. The chimeric PR8-QH/KJ vaccine is effective against H5 HPAI virus clades and in chickens.

KEYWORDS: Avian influenza virus; H5N1; H5N6; chimeric vaccine

PMID: 30358528 DOI: 10.1099/jgv.0.001140 [Indexed for MEDLINE]

Keywords: Avian Influenza; H5N6; H5N1; Poultry; Vaccines.


#Antigenic Variation of #Avian #Influenza A(#H5N6) Viruses, #Guangdong Province, #China, 2014–2018 (Emerg Infect Dis., abstract)

[Source: US Centers for Disease Control and Prevention (CDC), Emerging Infectious Diseases Journal, full page: (LINK). Abstract, edited.]

Volume 25, Number 10—October 2019 / Dispatch

Antigenic Variation of Avian Influenza A(H5N6) Viruses, Guangdong Province, China, 2014–2018

Ru Bai1, Reina S. Sikkema1, Cong rong Li, Bas B. Oude Munnink, Jie Wu, Lirong Zou, Yi Jing, Jing Lu, Runyu Yuan, Ming Liao, Marion P.G. Koopmans1  , and Chang-wen Ke1

Author affiliations: Guangdong Provincial Center for Disease Control and Prevention, Guangzhou, China (R. Bai, C. Li, J. Wu, L. Zou, Y. Jing, J. Lu, R. Yuan, C. Ke); Erasmus Medical Centre, Rotterdam, the Netherlands (R.S. Sikkema, B.B. Oude Munnink, M.P.G. Koopmans); Southern Medical University (C. Li, Y. Jing, C. Ke); South China Agricultural University, Guangzhou (M. Liao)



Market surveillance showed continuing circulation of avian influenza A(H5N6) virus in live poultry markets in Guangdong Province in 2017, despite compulsory vaccination for avian influenza A(H5Nx) and A(H7N9). We analyzed H5N6 viruses from 2014–2018 from Guangdong Province, revealing antigenic drift and decreased antibody response against the vaccine strain in vaccinated chickens.

Keywords: Avian Influenza; H5N6; Poultry; Guangdong; China.