Using a One Health approach to prioritize zoonotic diseases in China, 2019.

BACKGROUND: China is vulnerable to zoonotic disease transmission due to a large agricultural work force, sizable domestic livestock population, and a highly biodiverse ecology. To better address this threat, representatives from the human, animal, and environmental health sectors in China held a One Health Zoonotic Disease Prioritization (OHZDP) workshop in May 2019 to develop a list of priority zoonotic diseases for multisectoral, One Health collaboration.
METHODS: Representatives used the OHZDP Process, developed by the US Centers for Disease Control and Prevention (US CDC), to prioritize zoonotic diseases for China. Representatives defined the criteria used for prioritization and determined questions and weights for each individual criterion. A review of English and Chinese literature was conducted prior to the workshop to collect disease specific information on prevalence, morbidity, mortality, and Disability-Adjusted Life Years (DALYs) from China and the Western Pacific Region for zoonotic diseases considered for prioritization.
RESULTS: Thirty zoonotic diseases were evaluated for prioritization. Criteria selected included: 1) disease hazard/severity (case fatality rate) in humans, 2) epidemic scale and intensity (in humans and animals) in China, 3) economic impact, 4) prevention and control, and 5) social impact. Disease specific information was obtained from 792 articles (637 in English and 155 in Chinese) and subject matter experts for the prioritization process. Following discussion of the OHZDP Tool output among disease experts, five priority zoonotic diseases were identified for China: avian influenza, echinococcosis, rabies, plague, and brucellosis.
CONCLUSION: Representatives agreed on a list of five priority zoonotic diseases that can serve as a foundation to strengthen One Health collaboration for disease prevention and control in China; this list was developed prior to the emergence of SARS-CoV-2 and the COVID-19 pandemic. Next steps focused on establishing a multisectoral, One Health coordination mechanism, improving multisectoral linkages in laboratory testing and surveillance platforms, creating multisectoral preparedness and response plans, and increasing workforce capacity.

Introduction

Zoonotic diseases are diseases that can spread between animals and people. Most known human infectious diseases and about three-quarters of newly emerging infections originate from animals. [1, 2] China is vulnerable to zoonotic disease transmission due to a large agricultural workforce, sizable domestic livestock population, and a highly biodiverse ecology, with more than 7,500 known vertebrate species [3]. The recent coronavirus disease 2019 (COVID-19) pandemic, resulting from the introduction of a novel coronavirus (SARS-CoV-2) to the human population, exemplifies challenges with emerging zoonotic diseases [4, 5]. Similarly, SARS-CoV, the virus that caused severe acute respiratory syndrome (SARS) in humans and spread worldwide in 2002–2003, is thought to have originated in bats before spreading to civets in a wildlife market in Guangdong Province, China [6]. COVID-19, SARS, and previous outbreaks of avian influenza highlight the potential global threat of zoonotic disease transmission and the need to use a multisectoral, One Health approach to address zoonotic diseases [7-9].

The population in China was approximately 1.4 billion in 2019 [10]. Most of this population resides in the temperate-monsoon and sub-tropical monsoon zones in Eastern China. The socio-economic level of development is also highest in eastern China. Western China, which borders Kazakhstan and Mongolia, is generally arid or semi-arid, less populated, relies on livestock production, and has a lower level of development. The tropical monsoon zone in the southern most regions of China experience zoonotic disease transmission risk similar to South East Asian countries, such as Laos, Myanmar and Vietnam, which border China to the south. Zoonotic disease transmission can impact society in many ways. This includes reducing the productivity of animals, threatening the livelihood of the population dependent on livestock as a major source of income, and causing unnecessary human illness and death [11].

Human and animal health and wildlife programs are implemented across 34 provinces, counties and prefectures, and autonomous regions under the authority and guidance of national level agencies. Chinese Centers for Disease Control (China CDC) and Animal Centers for Disease Control and Prevention (ACDC) conduct surveillance and investigations of zoonotic disease transmission among the human and livestock populations, respectively. The State Administration of Grasslands and Forestry and the Chinese Academy of Sciences monitor diseases among wildlife species, including occurrence of avian influenza in the wild bird population. To address the threat of zoonotic diseases in China, a One Health Zoonotic Disease Prioritization (OHZDP) workshop was held from in Beijing from May 15–17, 2019 [12, 13]. The goal of the workshop was to use a multisectoral, One Health approach to prioritize endemic and emerging zoonotic diseases of greatest concern in China that should be jointly addressed by sectors responsible for human, animal, and environmental health. The OHZDP workshop was supported by Chinese Center for Disease Control and Prevention (China CDC) and United States Centers for Disease Control and Prevention (US CDC). Representatives from the United Nations Food and Agriculture Organization (FAO) and the World Health Organization (WHO) also participated in the workshop. Outcomes from the workshop can be applied to all emerging and re-emerging zoonotic diseases in China.

Methods

Workshop representatives

A total of 53 representatives from national and eight provincial-level human, animal, and environmental health sectors in China and international organizations participated in the workshop. The eight provinces represent the primary ecological and socio-demographic regions in the east (Jiangsu and Shandong), northwest (Qinghai, Ningxia, and Gansu) and southwest (Guangxi, Sichuan and Yunnan) of China respectively. Not all provinces were able to participate. However, national managers participating in the workshop were able to provide input on behalf of the human, animal, and environmental health sector staff in the provinces unable to attend. The 53 participants included 28 voting members, nine facilitators, and 16 advisors. Twenty-two of the 28 voting members were from provincial human, animal, and environmental health agencies, and the remaining six voting members were from national agencies. All voting members were managers for their agency or for the infectious disease unit in the agency (). To support future OHZDP workshops at the provincial and regional levels, three US CDC staff trained six local partners from the human and animal health sectors to serve as workshop facilitators. Sixteen advisors from international organizations and China CDC were present to observe and participate in discussions.

Zoonotic disease list and literature review

The OHZDP process relies on a mixed methods prioritization approach based on a quantitative scoring tool developed by US CDC. The process has been previously described in detail [12, 13]. In brief, the OHZDP process allows participants to customize the ranking criteria and questions and weights to reflect the country-specific zoonotic disease situation and prevention and control goals across multiple sectors. In the three months before the OHZDP workshop, human and animal health staff in China developed an initial list of zoonotic diseases to be considered as potential zoonotic diseases of greatest concern to China for prioritization. The initial zoonotic disease list was developed from human and animal reportable disease lists from China and also incorporated expert opinion. Of the 40 diseases included on the national notifiable human disease list, 25 were zoonotic infections. Of the 157 diseases included on the national notifiable animal disease list, 17 could infect humans and were not notifiable human diseases. Combining these resulted in a list of 42 zoonotic diseases. This combined list of 42 diseases was shared with national human, animal, and environmental health experts for review and consideration. The experts could include additional zoonotic diseases to the list and remove diseases that were unlikely to pose potential threats in China. The final list included 30 zoonotic diseases for prioritization. The goal of the workshop was to identify zoonotic diseases of greatest concern to the country, and of those, prioritize the top five. For consistency with publications resulting from previous workshops, we use the term zoonotic diseases rather than zoonotic infections. The term highlights that these priority zoonotic infections are capable of causing disease.

We reviewed animal and human case reports and English and Chinese published and grey literature from the last five to 10 years to understand the occurrence and risks for each of the 30 diseases. Fourteen staff searched English and Chinese literature published to collect information on the prevalence, morbidity, mortality, and Disability-Adjusted Life Years (DALYs) for each of the 30 diseases from China and the WHO Western Pacific Region. Staff identified relevant articles by using Boolean logic and search terms that included country name (China), disease name (e.g., brucellosis), and one of the following terms: “morbidity”, “mortality”, “DALYs”, “cases”, “animals”, “vaccine”, and “wildlife”. If regional data were not available, global estimates on prevalence, incidence, morbidity, mortality, and DALYs were used instead. Regional and global data were obtained from websites of the WHO and FAO. All corresponding data were saved and shared with workshop participants for future reference.

Criteria selection

During the workshop, voting members jointly identified five criteria for ranking the 30 zoonotic diseases. Representatives also selected a single categorical question for each criterion. All questions required an ordinal or multinomial answer to be entered into the OHZDP Tool. Once the criteria and questions were identified, the nine voting groups separately decided on the relative importance of each criterion. Each group’s ranking was then entered in the OHZDP Tool by a facilitator and a group weight for each criterion was calculated to reflect this relative importance.

Disease weighting and final ranking

Facilitators and representatives answered each question for the 30 zoonotic diseases using country-specific, regional, and global data collected previously through the literature review. After scoring all the zoonotic diseases, the OHZDP Tool uses a decision tree analysis to generate the zoonotic disease ranking [12, 13]. Each criterion’s weight is multiplied by the score assigned for each disease and is weighted by the number of answer choices. The scores for all five questions for each disease were summed and then normalized such that the highest final score was 1. The ranked list of zoonotic diseases and corresponding normalized scores were presented to the representatives to discuss and decide on a final list of priority zoonotic diseases for China.

Results

The final list of 30 zoonotic diseases discussed at the One Health workshop in China included diseases caused by bacteria (n = 14), viruses (n = 9), parasites (n = 6), and a prion pathogen (n = 1) (). A total of 792 published articles were identified and reviewed for information on these 30 zoonotic diseases in China and the surrounding region. This included 637 and 155 articles from English and Chinese journals, respectively. Data from these articles, in addition to information obtained directly from WHO and FAO websites, were used to address the ordinal or multinomial question developed for each ranking criterion. These criteria and questions are described in .

When the workshop participants reviewed the initial list of 29 zoonotic diseases for prioritization, they discussed and decided to also include Japanese Encephalitis, making the final zoonotic disease list for prioritization 30 diseases. A rapid review of the literature and relevant data sources was conducted for Japanese encephalitis, a vector-transmitted virus. A list of zoonotic diseases and their normalized scores was generated from the OHZDP Tool (). The 28 voting members discussed the disease ranking and finalized a priority zoonotic disease list for China. Although the normalized final score for brucellosis was 0.690 (rank 8), the disease was added to the final list of the top five priority zoonotic diseases based on discussions among the voting members. The final priority zoonotic disease list for China included avian influenza, echinococcosis, rabies, plague, and brucellosis. Epidemiologic data for each of these diseases is included in the workshop report [13].

After finalizing the list of priority zoonotic diseases, workshop representatives were divided into four groups to discuss next steps, plans, and approaches to effectively address the top five priority zoonotic diseases for China. Topics discussed included strengthening One Health coordination, surveillance and laboratory, preparedness and response, and workforce capacity. Recommendations were aggregated and presented to all representatives ().

Discussion

The OHZDP workshop for China held in May 2019 provided a platform for establishing a One Health approach to emerging and re-emerging zoonotic diseases. Although the China disease experts developed country-specific ranking criteria and questions, the priority disease list (avian influenza, echinococcosis, rabies, plague, and brucellosis) and recommended next steps were consistent with outcomes from workshops conducted in other countries [13-18]. Coronaviruses were not included in the list of the top five priority zoonotic diseases in China at the time of the workshop. However, the COVID-19 pandemic has further demonstrated the importance of a One Health approach to emergency preparedness and response [19, 20]. Human, animal, and environmental health sectors have collaborated in China to investigate and respond to COVID-19 [21], SARS, and avian influenza disease transmission through information sharing, environmental cleaning, and case detection and management [22-24]. Workshop representatives supported efforts to strengthen multisectoral, One Health collaboration for preparing and responding to outbreaks caused by other emerging and re-emerging zoonotic diseases.

In China, One Health preparedness and planning collaboration could focus on identifying and assigning roles and responsibilities of staff from each sector as well as establishing mechanisms for human and animal case finding, standard laboratory testing and further information sharing, all in advance of an emergency. National and provincial level-led One Health offices could coordinate these activities to provide appropriate authority and resources as well as assist in conducting joint outbreak investigations, developing joint risk communication strategies to provide up-to-date and consistent messaging [24] and ensuring a stockpile of available vaccines and treatments for both humans and animals are available, if and when needed [25, 26].

Representatives also recommended regular multisectoral, One Health trainings, simulation exercises, and other preparedness and outbreak response educational opportunities to help strengthen the One Health workforce in China for responding to future zoonotic disease emergencies. Engagement of stakeholders across agencies in planning and preparedness activities can facilitate One Health collaboration, coordination, and communication before and during public health emergencies [26, 27]. China CDC has previously conducted pandemic influenza exercises. Expanding such exercises to include other sectors and address priority zoonotic diseases would likely be helpful.

All five of the top priority zoonotic diseases for China identified during the workshop have been included in the National Notifiable Disease Reporting System (NNDRS) maintained by National Health Commission and the China CDC for human infections [28]. China CDC also maintains surveillance for certain animal infections such as the plague. Human infections resulting from these five priority zoonotic diseases are typically identified, investigated, and reported to NNDRS by local and provincial level Centers for Disease Control (CDCs). Diseases in animals and wildlife are investigated through local level agencies and reported to separate national surveillance systems [29]. Laboratory diagnostic capacity and testing procedures vary by disease and sector, which can limit control and prevention efforts. Human and dog rabies, ranked third on the priority zoonotic disease list, are notifiable to human and animal health agencies in China. However, only 2% of all human cases of rabies are laboratory confirmed and the number of reported dog rabies was far below the number of human cases in 2017 (75 dog cases compared to 502 human cases) [29, 30]. During a Stepwise Approach to Rabies Elimination assessment in China in March 2019, human and animal health sector staff advocated for development of systems to jointly collect, view, and analyze human and animal data to inform provincial and national-level decision making related to rabies elimination program activities [31]. Similar One Health approaches would likely be beneficial for preventing and controlling the other priority zoonotic diseases for China.

OHZDP workshop participants from other countries made similar recommendations for developing systems or mechanisms to organize and harmonize data collection (including standardization) across the relevant different sectors for the priority zoonoses [32]. Such systems could be implemented at the national and provincial level in China and include feedback tools (e.g., dashboards for visualization) for key decision makers in each sector [33, 34]. Animal disease surveillance, including at animal farms, breeding sites, and market locations are critical for early detection of zoonotic diseases and limiting transmission or ‘spill-over’ to the human population. Animal disease surveillance could be highly beneficial for all five priority zoonotic diseases, including brucellosis where the transmission between animal and human cases may be through direct exposures, or indirect, through consumption of unpasteurized milk. Pilot programs using mobile phones and tablets to collect and transmit information for geographically disparate locations to monitor and visualize disease and risk factor data in close to real-time for both human and animal populations can improve the efficiency of identifying and responding to zoonotic disease transmission [35-37].

Several provinces have implemented multi-sector trainings prior to the OHZDP workshop. Provinces along the Tibetan Plateau in western China (e.g., Qinghai, Tibet, and Xinjiang), for example, have conducted multisectoral annual meetings and trainings on echinococcosis prevention and control due to the endemicity of the infection among herding dogs and potential for debilitating health effects for the human population [38, 39]. Other provinces (e.g., Inner Mongolia) have provided targeted multisectoral, One Health training through the National Field Epidemiology Training Program for specific diseases, such as brucellosis (unpublished data). However, these multisectoral training opportunities are limited and do not yet exist in all provinces or for all priority zoonotic diseases. OHZDP workshop representatives in China supported the development of additional opportunities during pre-service medical and veterinary school programs that can encourage future professional collaboration through the One Health approach to zoonotic disease control and prevention. National and provincial level programs can also expand knowledge of biosecurity and biosafety concepts for priority zoonotic diseases during pre-service and in-service programs and multisectoral training through implementation of professional development projects that require engagement of staff from other health sectors. These One Health training programs can support future work for all emerging and re-emerging infectious diseases.

The OHZDP process is flexible and adaptable to address zoonotic diseases at subnational, national, and regional levels. The main outcome of this workshop was to identify a list of priority zoonotic diseases for China that could be addressed using a multisectoral, One Health approach. The priority zoonotic disease list was developed prior to the emergence of SARS-CoV-2 and the COVID-19 pandemic. We hypothesize that COVID-19 would likely score among the top five zoonotic diseases if we conducted this workshop during 2020, primarily due to significant transmission of SARS-CoV-2 and COVID-19 disease. We argue that regardless of individual disease scores, the next steps outlined by representatives from this workshop can be applied to COVID-19. Proposed work on surveillance, multisector training, and preparedness and response capacity can be applied to any emerging or re-emerging zoonotic disease. Future One Health workshops can be conducted to review and update the priority zoonotic disease list by including assessments of SARS-COV2 and other coronaviruses, as warranted. Such workshops can provide additional opportunities to further strengthen and institutionalize multisectoral, One Health collaboration on human, animal, and environmental health priorities.

The OHZDP workshop has been conducted in more than 25 locations [13]. Each of the countries, including China, developed country-specific criteria and corresponding weights for ranking the zoonotic diseases of greatest national concern. In China, these country-specific criteria included the use of a ‘social impact’ criterion to reflect public interest and concern based on Baidu (internet) search analytic results. The one-year Baidu search timeframe could have influenced the score of this criterion. The index score of certain diseases could have reflected possible mentions from other news sources and/or international events as well as zoonotic diseases present during the year proceeding the workshop. However, the weight for this criterion was relatively lower compared to the other four criteria. Using ‘social impact’ to reflect public interest and concern was unique and an informative criterion that incorporated public perspectives in ranking the relative importance of zoonotic diseases in China. Utilizing a prioritization method that can be adapted to meet country level concerns promoted engagement and contribution from workshop participants [12, 13]. Representatives in China also decided to score zoonotic diseases without preventable measures (such as treatment or a vaccine) higher compared to vaccine preventable diseases or those with a known or accessible treatment. This differed from other workshops [13-18] and was based on the perceived need to rapidly respond to zoonotic diseases having the potential for uncontrolled epidemic spread. Despite having different criteria and questions, two zoonotic diseases, rabies and avian influenza, were among the top five prioritized zoonotic diseases in 25 and 24 of the workshops conducted to date, respectively. The national level workshop did not aim to address all possible zoonotic disease prioritization criteria since the OHZDP methods focus on the top five criteria of greatest concern. Participants discussed many different criteria during the workshop and agreed on the five criteria most likely associated the potential zoonotic disease threat in the country. Future workshops–including those conducted at the regional or provincial level—could develop and apply more targeted and specific criteria for identifying a local list of priority zoonotic diseases. The outcomes of this first OHZDP workshop in China support opportunities for international engagement, regional collaborations, and sharing of lessons learned to develop and implement multisectoral, One Health programs to prevent and control these prioritized zoonotic diseases.

Conclusion

Representatives from Chinese national and provincial level human, animal and environment health sectors participated in an OHZDP workshop in May 2019. Workshop representatives successfully developed a list of priority zoonotic diseases that can be jointly addressed through a multisectoral, One Health approach. Voting members agreed upon criteria and questions specific to China for ranking 30 zoonotic diseases. Combining results from the OHZDP Tool and subject matter expert discussions, representatives agreed on five priority zoonotic diseases for China: avian influenza, echinococcus, rabies, plague, and brucellosis. The OHZDP workshop provided an opportunity for multisectoral, One Health discussion and collaboration. As a product of this collaboration, representatives suggested the establishment of a One Health coordinating office to help facilitate information sharing among One Health sectors. Approaches for improving One Health surveillance and laboratory capacity for the priority zoonotic diseases, particularly in responding to outbreaks were also identified. To respond to the priority zoonotic diseases, opportunities to strengthen One Health workforce capacity should be considered at the local and provincial levels. One Health collaboration in these areas and others can help reduce unnecessary morbidity and mortality and potential economic burden due to emerging and re-emerging zoonotic diseases in China. Future workshops can be conducted to review and update the list of priority zoonotic diseases and further strengthen multisectoral, One Health collaboration in China.

25 Feb 2021

PONE-D-20-41070

Using a One Health Approach to Prioritize Zoonotic Diseases in China, 2019

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Reviewer #1: “Using a One Health Approach to Prioritize Zoonotic Diseases in China, 2019”

PLOS ONE

This article describes findings from a May 2019 One Health Zoonotic Disease Prioritization (OHZDP) workshop in China. Representatives were identified from eight provinces, national agencies, and international agencies, and voting members selected from thirty zoonotic diseases to create a zoonotic disease prioritization list consisting of five diseases: avian influenza, echinococcosis, rabies, plague, and brucellosis. The authors emphasize a One Health, multi-sectoral approach throughout the document. The importance of the workshop and its applicability for zoonotic disease preparedness is evident.

The workshop organization, process of disease evaluation and prioritization, and recommendations were poorly outlined. The workshop’s country-specific use for China was described, but as described by the authors had a bias towards the richer more populous southeastern region and had very limited representation from the West, Northeast or central regions. Despite this, echinococcosis made the final list, an issue that was addressed in a zoonoses workshop held in the Western provinces. How was information from other regional provinces weighed into this process? This is largely unclear.

Overall, this article was written with broad brush strokes and lacks the granularity needed to understand the actual process, biases, concerns of methods and results.

• Methods: How were the 53 representatives chosen? How were the 8 provinces chosen to be represented? How were the 29 voting members chosen?

• Methods: The authors explain how 30 zoonotic diseases were researched for finding DALYs, morbidity, mortality, and prevalence; however, it is unclear how the 30 zoonotic diseases were originally picked. Lines 136-137 could be more specific explaining the initial zoonotic disease list development. Why wasn’t a more general literature review used that might help catch emerging infections that are not reportable but could be greater problems in the future?

• Throughout the paper the term “zoonotic diseases” is used although the actual transmissible agent(s) are zoonotic infections. More care should be taken to describe infection vs. disease. This includes presenting causative agents in table 2 so that the other 27 countries that have also gone through this process can determine areas of overlap based on the actual microbes vs. the generalized disease.

• Lines 176-177: There is a complete lack of explanation how the criteria were determined and very limited justification of them, despite the fact that this is described as a discussion. For instance why was human mortality the final determinant for disease hazard/burden vs. DALY or something that also included agricultural impact? Why was vaccination the only control/prevention measure listed in the literature review and as the determining criteria? What is the evidence behind internet hits (Baidu index) as a measure of “societal impact” particularly in a society that does not have free internet access to all sites and data? What are the inherent biases of these choices?

• Expand upon weights, and questions/answers within the text- how did the answers determined using the criteria in Table 3 lead to the raw scores in table 2? This must be explained so that these numbers make sense.

• Since the focus is on zoonotic diseases, it would be helpful to show the morbidity/mortality numbers for animals affected by the diseases chosen in addition to the human data.

Minor points:

• Update the population of China stated in line 84.

• Add international agencies that participated in the workshop among those listed in Table 1.

• Why is Xinjiang hemorrhagic fever highlighted in Table 2?

Reviewer #2: The authors report on the results of a One Health meeting to prioritize zoonotic disease control measures in China. The meeting was sponsored by Chinese agencies responsible for human, animal and environmental health, with assistance from the US CDC. The meeting was held in 2019, prior to the start of the COVID-19 pandemic. As such COVID was not subject to this prioritization effort. However, the authors comment that “outcomes from the workshop can be applied to all emerging and re-emerging zoonotic diseases in China. (line 181). They also note in the discussion that the COVID-19 pandemic has further demonstrated the importance of a One Health approach to emergency preparedness and response (lines 207-208). I think it would be useful for the authors to demonstrate how the scaling system could be used to compare SARS-CoV2 to the other zoonotic diseases they evaluated. By my reckoning it comes out ahead of avian influenza, although the balance of the assessment would shift from early in the pandemic (no vaccine or therapies, little awareness) to later in the pandemic (vaccine and therapies and huge public interest). This would take a fairly dry assessment of an important exercise and turn it into a model for how this approach can help reprioritize public health actions.

Specific comments:

Lines 47-48 “Disease severity” would be more understandable than “disease hazard” in describing this measure.

Line 76 “resulting from spillover… which might be from an animal source.” The concept of spillover implies an animal source. Why is it necessary to qualify the statement?

Line 109 As noted above, why not demonstrate how to apply the outcomes to the COVID-19 pandemic?

Line 120 Note at the time of the meeting.

181 What is the point of a 6-decimal place “normalized final score”? The ranking is based on categorical values from 0-4. The decimals imply a level of precision that are not reasonable distinctions. Particularly when the final choice was made based on “discussions among the voting members”.

Lines 194-197 This part of the discussion is a restatement of methods.

Lines 198-199 This is a restatement of results.

Lines 200-204 This appears to be a restatement of the premise behind the meeting.

Lines 315-317 This should be part of an acknowledgement and not part of the conclusions.

In looking at the scoring system, it is not clear why the prevention and control measures are expressed as a negative relation, when all of the others are positive. I can understand that if a disease emerges for which there is no vaccine or therapy available (see COVID-19) then prioritizing their development is important. However, if (such as with rabies) vaccines and therapies are available, and the disease is not being effectively controlled, that demonstrates a critical need to better coordinate measures across One Health platforms. For the diseases that were ranked these are important considerations.

Reviewer #3: Overall, this is a nicely done paper and illustrates the utility of systematic prioritization of known zoonotic disease threats.

Methods: In the methods section the workshop representatives are a bit confusing. I would suggest modifying the Table 1 to include columns where they can check off if it is human, animal or environment. And possibly to indicate if they had a voting member. The 9 groups were also unclear – how were they divided and why?

Also the totals don’t seem to add up - there were 53 participants but then there were 28 voting members but 16 observers. This is 56. Just a bit more clarity here would be very helpful as to the relative roles and who was involved in the decision making.

The lit review and data gathering process is critical. It is great that they did this. I would suggest that they include a bit more detail on the databases they searched, time frames searched, etc. While not necessarily a systematic review, it would be great to have as much detail reported about the search as possible. Also, were things like Promed databases used, etc.

There are nine groups with 28 voting members – but the groups had to come to consensus so does this really mean there are only 9 votes?

This is a very nice discussion and systematic method of prioritizing current identified threats. However, as was pointed out SARS-CoV-2 and coronaviruses were not included at the time of the workshop but emerged as a significant threat. Some discussion around how to increase the capacity and response for unknown threats would also be useful.

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12 Jul 2021

Responses to Editor and Reviewers

Editor’s comments

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Reviewers' comments

Reviewer #1

1. The workshop’s country-specific use for China was described, but as described by the authors had a bias towards the richer more populous southeastern region and had very limited representation from the West, Northeast or central regions. Despite this, echinococcosis made the final list, an issue that was addressed in a zoonoses workshop held in the Western provinces. How was information from other regional provinces weighed into this process? This is largely unclear.

We appreciate the reviewer’s question. From our perspective, the selection of provinces may have biased slightly away from the populated and highly developed Eastern Provinces. We selected provinces to represent the epidemiology of zoonotic infections in each of the major regions in China. Animal and human health sector staff from Qinghai, Ningxia, Gansu, Guangxi and Yunnan Provinces where are in the western region of China participated in the workshop. Qinghai, Ningxia, and Gansu provinces have lower population density and socio-economic development compared to provinces in the Eastern Region, and experience zoonotic disease transmission similar to other provinces in the Northwest Region, including Inner Mongolia, Xinjiang, and Tibet. Qinghai Province, for example, is located on the northeastern part of the Tibetan plateau with an average elevation of 3,000 meters. Guangxi Yunnan Provinces both have significantly lower GDP compared to the populated Eastern Provinces.

Information about zoonotic disease transmission from provinces in the central (e.g., Hubei, Hunan) and northeastern (e.g., Jilin and Heilongjiang) region were obtained from review of the published and grey literature, official reports, and input from National Animal, Human, and Environmental sector staff in Beijing. For example, Yin Wenwu and his team from China CDC worked closely with Heilongjiang and Hunan Province, the high-risk province for rabies and anthrax respectively.

Although not all provinces were able to participate, the pre-workshop review and discussions during the workshop provided the opportunity to review existing animal, human, and environmental data and information from all regions in China. In future workshops, we will request participation from these other provinces.

2. Methods: How were the 53 representatives chosen? How were the 8 provinces chosen to be represented? How were the 29 voting members chosen?

The total of 53 participants included 28 voting members, 16 advisors, and 9 facilitators. Twenty-two of the voting members were from provincial human, animal, and environmental health agencies in the east, northwest and southwest of China and the remaining six voting members were from national agencies. All voting members were the managers responsible for their agency or for the infectious disease unit in the agency. Nine advisors were from international agencies in China and the other seven were from China CDC. Three of the 9 facilitators were from US CDC and served as trainers. The other six facilitators were from China CDC and other agencies in China. Agency representatives presented in Table 1. We have included this additional information to the Methods section of the revised manuscript. Please see lines 101-108. Table 1 was also revised to add agencies not included as voting members.

3. Methods: The authors explain how 30 zoonotic diseases were researched for finding DALYs, morbidity, mortality, and prevalence; however, it is unclear how the 30 zoonotic diseases were originally picked. Lines 136-137 could be more specific explaining the initial zoonotic disease list development.

We initiated the selection of the 30 important zoonotic infections with a review of China’s national list of notifiable human and animal diseases. We identified the zoonotic infections from the notifiable list of human diseases and cross-referenced this with the list of reportable animal diseases that could cause human infections. Of the 40 diseases included on the national notifiable human disease list, 25 were zoonotic infections. Of the 157 diseases included on the national notifiable animal disease list, 17 could infect humans and were not notifiable human diseases. Combining these resulted in a list of 42 zoonotic diseases. This combined list of 42 diseases was shared with human, animal, and environmental health experts at the national offices in Beijing. The experts could also include zoonotic diseases that could be a concern in China but were not notifiable disease in the country. The final list included 30 zoonotic diseases for prioritization. The goal of the workshop was to identify zoonotic diseases of greatest concern to the country, and of those, prioritize the top five. We reviewed animal and human case reports from the last 5 to 10 years, reviewed the English and Chinese literature to understand the occurrence and risks for each of these 30 diseases. Additional zoonotic diseases could be added to the list during the workshop if the participants determined that another disease should be considered. With this approach, Japanese encephalitis (JE) was added to the list of the diseases during the workshop. We conducted a rapid review of the literature on JE and provided this information to workshop participants for discussion. The workshop was not intended to provide an exhaustive list of every possible zoonotic infection in China or the WHO Western Pacific Region. We have provided additional information to paper to better describe the process as outlined above. Please see lines 119-129 (methods) and lines 166-169 (results).

4. Why wasn’t a more general literature review used that might help catch emerging infections that are not reportable but could be greater problems in the future?

We developed the initial list of important zoonotic infections in China using the lists of national notifiable diseases and expert opinion. After developing the initial list of important zoonotic diseases in China, human health, animal health, and environmental health ministries reviewed the list and had the opportunity to add other zoonotic infections to the list is warranted (by expert opinion and/or other unpublished or published literature). During the workshop, additional zoonotic infections could be added to the list if requested by the participants. This is the standard approach used in the One Health Zoonotic Disease Prioritization workshop and has been determined to the be an efficient approach for the host countries. Because we also included feedback from experts on the list of important zoonotic diseases, we do not envision a larger literature search would have resulted in a different list of priority zoonotic diseases.

5. Throughout the paper the term “zoonotic diseases” is used although the actual transmissible agent(s) are zoonotic infections. More care should be taken to describe infection vs. disease. This includes presenting causative agents in table 2 so that the other 27 countries that have also gone through this process can determine areas of overlap based on the actual microbes vs. the generalized disease.

Thank you for comment. We appreciate the distinction. As with the other One Health Zoonotic Disease Prioritization workshops, we refer to the zoonotic infections as diseases. This highlights that these priority zoonotic infections as capable of causing diseases; zoonotic infections unlikely to cause disease, were unlikely to be included as a priority zoonoses for the country. For consistency with the publications resulting from similar workshops, we would like to continue to use the term zoonotic diseases.

6. Lines 176-177: There is a complete lack of explanation how the criteria were determined and very limited justification of them, despite the fact that this is described as a discussion. For instance, why was human mortality the final determinant for disease hazard/burden vs. DALY or something that also included agricultural impact?

All workshop voting members were involved in the development of the criteria that were most important to their ministries and agencies/units for addressing zoonotic diseases in China. All voting members and workshop participants discussed and agreed on using these criteria to prioritize the top five zoonotic diseases in China. Following this discussion, workshop participants decided that the “Disease hazard/severity” criterion would solely focus on the human case fatality rate, which would help measure disease severity. They also decided that the “Economic impact” criterion would focus solely on animal burden in relation to production losses. Components for the other two criteria (“Epidemic scale and intensity” and “Prevention and control”) focused on both human and animal health. For the OHZDP process, not every criteria and question needs to incorporate components of each sector.

7. Why was vaccination the only control/prevention measure listed in the literature review and as the determining criteria?

While vaccine was one of the key search terms used during the literature review, additional resources outside of the literature review for prevention and control measures for the zoonotic diseases were also available to the workshop participants. For the prevention and control criteria, workshop participants identified that this criterion should be measured by availability of human and animal vaccination and human treatment and medication. The focus was on prevention for humans and animals and then treatment for human if infected.

8. What is the evidence behind internet hits (Baidu index) as a measure of “societal impact” particularly in a society that does not have free internet access to all sites and data? What are the inherent biases of these choices?

Workshop participants thought it was important to include “Social Impact” as a criterion for the zoonotic disease prioritization. To measure “Societal Impact”, workshop participants used the Baidu index as a proxy to assess public interest and social impact of the disease. The Baidu index is the most used online search engine in China and provides various automatically generated indexes. Most the of the population has access to the internet via mobile devices, particularly Smart phones. In 2018, approximately 73.02% of the population in China conducted an internet search using Baidu. These searches included health and disease specific search information. The Baidu search index is based on the search volume of users in Baidu, using keywords as the statistical objects, and the result represents the weighted sum of the search frequency of each keyword in Baidu web search. Diseases that received a lot of public attention (>700 ‘hit’ value) in the past year (1 year) were given the highest score of 4. Diseases that received little to no public attention (<100 ‘hit’ value) were given a score of 0. The index represents the weighted sum of the search frequency in a certain time period. Higher index values reflect a larger search volume, suggesting greater public interest and social impact. The one-year search timeframe could have influenced the score of this criterion. Certain diseases and their index score could be based on possible mentions from other news sources and/or international events as well as zoonotic diseases present during the year proceeding the workshop. Nevertheless, utilizing the Baidu index was a creative and unique way to measure societal interest and impact from these diseases. This approach can be used to monitor changes and emerging societal concerns over time. Please see lines 285-289.

9. Expand upon weights, and questions/answers within the text- how did the answers determined using the criteria in Table 3 lead to the raw scores in table 2? This must be explained so that these numbers make sense.

Thank you for your comment. In the methods section under “Disease weighting and final ranking”, a brief explanation of how the answers for each zoonotic disease and the criteria weighting are applied using decision tree analysis built into the OHZDP Tool. The full detailed methods for how the raw scores are attained are described in the original OHZDP publication (https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0109986). To determine the ranked zoonotic disease list, we utilized a decision tree analysis built into the OHZDP Tool. Each criterion’s weight is multiplied by the score assigned for each disease and is weighted by the number of answer choices. The weighted scores for all 5 criteria for each disease are summed and normalized in relation to the zoonotic disease with the highest raw score. The OHZDP Tool then generated the ranked zoonotic disease list in order of the normalized final scores. These normalized final scores were calculated based on the inputs from the workshop participants. We have added in additional information on the methods into the revised manuscript in lines 152-156.

10. Since the focus is on zoonotic diseases, it would be helpful to show the morbidity/mortality numbers for animals affected by the diseases chosen in addition to the human data.

Thank you for your comment. After much discussion, workshop participants agreed that the “Disease hazard/severity” criterion would solely focus on the human case fatality rate. Participants also decided that the “Economic impact” criterion would focus solely on animal burden in relation to production losses. Components of the other two criteria (“Epidemic scale and intensity” and “Prevention and control”) focused on both human and animal. For the OHZDP process not every criteria and question need to incorporate components of each sector.

11. Minor points:

• Update the population of China stated in line 84.

China's population is still estimated to be 1.4 billion in 2019.

• Add international agencies that participated in the workshop among those listed in Table 1.

Thank you for this suggestion. All international agencies participating in the workshop have been added to Table 1 in revised manuscript.

• Why is Xinjiang Hemorrhagic Fever highlighted in Table 2?

Xinjiang Hemorrhagic Fever was not highlight in Table 2 (as following picture shows). There was no special reference for XHF during the workshop.

Reviewer #2:

1. I think it would be useful for the authors to demonstrate how the scaling system could be used to compare SARS-CoV2 to the other zoonotic diseases they evaluated. By my reckoning it comes out ahead of avian influenza, although the balance of the assessment would shift from early in the pandemic (no vaccine or therapies, little awareness) to later in the pandemic (vaccine and therapies and huge public interest). This would take a fairly dry assessment of an important exercise and turn it into a model for how this approach can help reprioritize public health actions.

Thank you for your suggestion. The process is flexible and adaptable to additional situations and can be applied to emerging infectious diseases as well. While the prioritization process focuses on endemic and emerging zoonotic diseases, countries are able to build and strengthen capacity for the priority zoonoses regardless if they are endemic or emerging. Having all relevant sectors work together using a One Health approach to develop a shared priority list as well as an action plan to address those priorities is helping to advance One Health, and this in turn helps to better prepare partners from multiple sectors to address an unknown pathogen or reemerging infectious diseases. We agree that a follow-up workshop – or analysis of COVID-19 as a priority zoonotic disease - should be conducted but recommend that this is developed as a separate project. We have provided additional comments in the discussion section of the revised manuscript to describe such a possible follow-up workshop. Please see lines 266-279.

2. Lines 47-48 “Disease severity” would be more understandable than “disease hazard” in describing this measure.

We appreciate this comment and have revised to “disease hazard” to “disease hazard/severity” in Lines 39 (as well as Table 3) in revised manuscript. We completely agree “disease severity” is more understandable to clarify the measure. Considering the language decided and agreed upon by the voting members during the workshop and the word using in workshop report, “hazard” is kept in this form.

3. Line 76 “resulting from spillover… which might be from an animal source.” The concept of spillover implies an animal source. Why is it necessary to qualify the statement?

Thank you for your comment. We have revised the statement to read: “The recent coronavirus disease 2019 (COVID-19) pandemic, resulting from the introduction of a novel coronavirus (SARS-CoV-2) to the human population, exemplifies challenges with emerging zoonotic diseases.”. Please see line 57-59 of revised manuscript.

4. Line 109 As noted above, why not demonstrate how to apply the outcomes to the COVID-19 pandemic?

We appreciate this comment and agree that demonstrating the flexibility and adaptability of the tool is important. The main outcome of this initial workshop was to identify a list of priority zoonotic diseases that could be addressed using a One Health Approach. The list of 5 prioritized zoonotic diseases is a tangible outcome of the workshop. However, proposed work on surveillance, cross-sector training, and preparedness and response capacity should be applied to any new (or old) zoonotic disease. While the prioritization process focuses on endemic and emerging zoonotic diseases, countries are able to build and strengthen capacity for the priority zoonosis regardless of if they are endemic or emerging. Rather than generating a new score for COVID-19, we agree that the One Health approach could be applied to other emerging diseases not identified at the time of the workshop. We propose conducting follow-up workshop or separate project for this analysis. We have provided additional comments in the discussion section of the revised manuscript to describe such a possible follow-up workshop or analysis. Please see lines 194-196, 266-279.

5. Line 120 Note at the time of the meeting.

We add the date of meeting in Line 85 of revised manuscript.

6. What is the point of a 6-decimal place “normalized final score”? The ranking is based on categorical values from 0-4. The decimals imply a level of precision that are not reasonable distinctions. Particularly when the final choice was made based on “discussions among the voting members”.

Thank you for your comment. We have updated the content and Table 2 to reflect only 3-decimal place for the raw and normalized final scores. Please see line 172 and Table 2 in the revised manuscript.

7. Lines 194-197 This part of the discussion is a restatement of methods.

Thank you for this comment. We have deleted the these lines from the discussion section of the manuscript.

8. Lines 198-199 This is a restatement of results.

Thank you for this comment. We have deleted these lines from the discussion section of the manuscript.

9. Lines 200-204 This appears to be a restatement of the premise behind the meeting.

Thank you for this comment. We have deleted these lines from the discussion section of the manuscript.

10. Lines 315-317 - This should be part of an acknowledgement and not part of the conclusions.

Thank you for this comment. We moved these lines to the acknowledgement section in the revised manuscript.

11. In looking at the scoring system, it is not clear why the prevention and control measures are expressed as a negative relation, when all of the others are positive. I can understand that if a disease emerges for which there is no vaccine or therapy available (see COVID-19) then prioritizing their development is important. However, if (such as with rabies) vaccines and therapies are available, and the disease is not being effectively controlled, that demonstrates a critical need to better coordinate measures across One Health platforms. For the diseases that were ranked these are important considerations.

Thank you for your comment. Workshop participants decided it was most important to have zoonotic diseases without any prevention or control measure (vaccination or treatment/medicine) be ranked higher than zoonoses that have at least some prevention and control measures. However, after the priority zoonotic diseases were identified, participants also discussed One Health coordination and strengthening in China. During this discussion, participants recommended that there was a need to develop and implement multisectoral plans for disease control and prevention (including for outbreak control and response) for the priority zoonotic diseases.

Reviewer #3:

1.Methods: I would suggest modifying the Table 1 to include columns where they can check off if it is human, animal or environment, and possibly to indicate if they had a voting member.

Thank you for your comment. We have updated the Table 1 to include each organization and corresponding role in the workshop. The table now includes voting members and advisors. Below is Table 1 that has included in the revised version of the manuscript.

Table 1. Agencies participating in the One Health Zoonotic Disease Prioritization workshop, Beijing, China, May 15-17, 2019.

Voting Members

National Level

National Institute for Communicable Diseases Control and Prevention, China CDC

National Institute of Parasitic Diseases (NIPD), China CDC

Division of Infectious Disease, China CDC

China Animal Disease Control Centre

National Research Center for Wildlife Diseases

Eastern Region

Jiangsu Provincial CDC

Shandong Provincial CDC

Jiangsu Academy of Agricultural Sciences, Jiangsu Society of Animal Husbandry and Veterinary Medicine

Shandong Provincial Animal CDC

Northwestern Region

Qinghai Provincial CDC

Gansu Provincial CDC

Ningxia Hui Autonomous Region CDC

Qinghai Animal CDC

Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences

Qinghai Academy of Animal Science and Veterinary Medicine

Southwestern Region

Yunnan Provincial CDC

Guangxi University of Chinese Medicine, School of Public Health and Management

Sichuan Provincial CDC

Guangxi Zhuang Autonomous Region Animal CDC

Yunnan Provincial Institute of Endemic Disease Prevention and Control

Sichuan Provincial Animal CDC

Facilitators

US Centers for Disease Control and Prevention (Trainer)

National Institute for Communicable Diseases Control and Prevention, China CDC

Center for Global Public Health, China CDC

Jiangsu Provincial CDC

National Research Center for Wildlife Diseases

Yinchuan Animal CDC

Advisors and Other Participants

US Department of Health and Human Services China Office

US Department of Agriculture (USDA) China Office

US National Institutes of Health

US Centers for Disease Control and Prevention

Food and Agriculture Organization (FAO) China Office

WHO China Office

Center for Global Public Health, China CDC

National Institute for Communicable Diseases Control and Prevention, China CDC

1. The 9 groups were also unclear – how were they divided and why?

Thank you for your comment. The 28 voting members were divided into nine groups. Participating provinces were categorized into three regions. Each region (East, Northwest, and Southwest) had two voting groups (one for the human sector and one for the animal sector), making six voting groups. There were also three additional voting groups for the national level (one for the human health sector, one for the animal health sector, and one for the environmental sector). Please see lines 101 to 104, where we have provided additional detail in the establishing the nine voting groups.

3. Also the totals don’t seem to add up - there were 53 participants but then there were 28 voting members but 16 observers. This is 56. Just a bit more clarity here would be very helpful as to the relative roles and who was involved in the decision making.

Thank you for your comment. There were 53 participants at the workshop. This included 28 voting members, 16 advisors, and 9 facilitators. National and regional representatives involved in the organization of the workshop were identified as decision makers during the workshop. We have also updated Table 1 in the manuscript to better highlight the organizations participating in the workshop and their roles (voting members, advisors, facilitators).

4. I would suggest that they include a bit more detail on the databases they searched, time frames searched, etc. While not necessarily a systematic review, it would be great to have as much detail reported about the search as possible. Also, were things like Promed databases used, etc.

Thank you for your comment. The literature review process incorporates information from the published and gray literature. Additional zoonotic disease information was obtained from informal reports, summary documents, or input from technical experts in country, and data provided by government and partner organizations, and other data sources such as ProMed, Global Incident Map, HealthMap, and news articles.

We used the CNKI literature search engine database for our search of Chinese literature on the 30 important zoonotic diseases in China. We followed the same process that was used to search the English literature. For both the English and Chinese review, we focused on literature published within the last ten years.

5. There are nine groups with 28 voting members – but the groups had to come to consensus so does this really mean there are only 9 votes?

Thank you for the comment. Yes, there were only 9 votes casted for the 28 voting members. The 28 voting members were divided into nine groups. Participating provinces were categorized into three regions. Each region (East, Northwest, and Southwest) had two voting groups (one for the human sector and one for the animal sector), making six voting groups. There were also three additional voting groups for the national level (one for the human health sector, one for the animal health sector, and one for the environmental sector).We have added this information to the Methods section of the of revised manuscript. Please see lines 101-104.

6. This is a very nice discussion and systematic method of prioritizing current identified threats. However, as was pointed out SARS-CoV-2 and coronaviruses were not included at the time of the workshop but emerged as a significant threat. Some discussion around how to increase the capacity and response for unknown threats would also be useful.

Thank you for your comment. While the prioritization process focuses on endemic and emerging zoonotic diseases, countries are able to build and strengthen capacity for the priority zoonoses regardless of whether they are endemic or emerging. Having all relevant sectors work together using a One Health approach to develop a shared priority list as well as an action plan to address those priorities is helping to advance One Health, and this in turn helps to better prepare partners from multiple sectors to address an unknown pathogen or reemerging infectious diseases. We agree that a follow-up workshop – or analysis of COVID-19 as a zoonotic disease - should be conducted but recommend that this developed as a separate project. We have provided additional comments in the discussion section of the revised manuscript to describe such a possible follow-up workshop. Please see lines 266-279.

While the prioritization process focuses on endemic and emerging zoonotic diseases, when countries are able to build and strengthen capacity for the priority zoonoses regardless of if they are endemic or emerging, countries are building better capacity to address whatever the next new pathogen is. Having all relevant sectors work together using a One Health approach to develop a shared priority list as well as an action plan to address those priorities is helping to advance One Health, and this in turn helps to better prepare partners from multiple sectors to address an unknown pathogens or reemerging infectious diseases. Some comments were added in the discussion of Line 195-196 of revised manuscript.

Submitted filename: response to editor and reviewers.docx

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3 Aug 2021

PONE-D-20-41070R1

Using a One Health Approach to Prioritize Zoonotic Diseases in China, 2019

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Reviewer #1: The authors addressed most of our comments. Explanations were added for the categories and inclusions of workshop participants as well as the formation of the initial zoonotic disease list. Statements were added for expanding upon weighting and ranking methods. These additions improved the methods section.

An explanation was added concerning COVID-19, the timing of the 2019 workshop, and considerations for the future. This addition helps readers understand the lower ranking of SARS.

Minor edits:

An explanation of the Baidu index was added, although more language regarding the bias of this approach would be useful to readers.

The authors’ reply to comment 1 could be incorporated into the manuscript text regarding participation of certain provinces and geographic locations. Including an explanation about provincial participation and potential biases would strengthen the methods section.

Table 1: The number of agencies is less than the number of participants. Could you add the number of participants per agency?

The previous comment concerning terminology of diseases versus infections was only partially addressed. The authors replied that the terminology was used for consistency with previous OHZDP workshops. Changing the terminology to correctly identify infections or diseases should be implemented. At the very least, a statement regarding this ‘consistency’ of terminology should be included.

In the discussion, limitations or implications of use of the chosen criteria (not just social impact) should be added.

Reviewer #2: (No Response)

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25 Sep 2021

Response to Journal and Reviewers

Journal Requirements

Please review your reference list to ensure that it is complete and correct. If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text, or remove these references and replace them with relevant current references. Any changes to the reference list should be mentioned in the rebuttal letter that accompanies your revised manuscript. If you need to cite a retracted article, indicate the article’s retracted status in the References list and also include a citation and full reference for the retraction notice.

Response to Journal

Thanks for providing the requirements. Accordingly, the reference list has been reviewed and revised as follows:

1.Reference [3] is revised to include complete information on line 346-347.

2.Reference [30] is provided with updated URL on line 417, to replace formerly invalid URL.

3.All URL of the reference has been checked for validity, and ‘Last accessed MMMDD,YYYY’ was updated for references [3][10][13][18][25][28][29][30] .

4.No reference has been found retracted, by searching references in https://pubmed.ncbi.nlm.nih.gov/.

Reviewer 1

The authors addressed most of our comments. Explanations were added for the categories and inclusions of workshop participants as well as the formation of the initial zoonotic disease list. Statements were added for expanding upon weighting and ranking methods. These additions improved the methods section. An explanation was added concerning COVID-19, the timing of the 2019 workshop, and considerations for the future. This addition helps readers understand the lower ranking of SARS.

Response to Reviewer 1

Thanks for reviewer’s comment. We deeply appreciate your review on the paper. We have studied the comments carefully and revised the manuscript that takes all the points into account. The following addresses each of the comments item by item. We would like to express our appreciation for your professional comments during each revision, which have really helped the paper improved much.

Minor edits

Q1:

An explanation of the Baidu index was added, although more language regarding the bias of this approach would be useful to readers.

The authors’ reply to comment 1 could be incorporated into the manuscript text regarding participation of certain provinces and geographic locations. Including an explanation about provincial participation and potential biases would strengthen the methods section.

A1:

Thanks for your comments. Certain provinces were added to geographic locations on line 100-101,

“The eight provinces represent the primary ecological and socio-demographic regions in the east (Jiangsu and Shandong), northwest (Qinghai, Ningxia, and Gansu ) and southwest (Guangxi, Sichuan and Yunnan) of China respectively. ”

Thanks for your suggestion of incorporating our reply to previous comment 1 into this revision about provincial participation and potential biases . As the example of our previous reply, though staffs from Heilongjiang and Hunan Province were unnable to attend the workshop, Yin Wenwu (who attended) and his team from China CDC worked closely with these provinces, the high-risk province for rabies and anthrax respectively.

Accordingly, it is revised on line 101-103:

“Not all provinces were able to participate. However, national managers participating in the workshop were able to provide input on behalf of the human, animal, and environmental health sector staff in the provinces unable to attend. ”

Q2:

Table 1: The number of agencies is less than the number of participants. Could you add the number of participants per agency?

A2:

Thanks for your comments. Accordingly to the comments, the number of participants has been added to each agency in table 1.

Voting Members (No. participants)

National Level

National Institute for Communicable Diseases Control and Prevention, China CDC (2)

National Institute of Parasitic Diseases (NIPD), China CDC (1)

Division of Infectious Disease, China CDC (1)

China Animal Disease Control Centre (1)

National Research Center for Wildlife Diseases (1)

Eastern Region

Jiangsu Provincial CDC (2)

Shandong Provincial CDC (1)

Jiangsu Academy of Agricultural Sciences, Jiangsu Society of Animal Husbandry and Veterinary Medicine (1)

Shandong Provincial Animal CDC (1)

Northwestern Region

Qinghai Provincial CDC (3)

Gansu Provincial CDC (1)

Ningxia Hui Autonomous Region CDC (1)

Qinghai Animal CDC (2)

Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences (1)

Qinghai Academy of Animal Science and Veterinary Medicine (3)

Southwestern Region

Yunnan Provincial CDC (1)

Guangxi University of Chinese Medicine, School of Public Health and Management (1)

Sichuan Provincial CDC (1)

Guangxi Zhuang Autonomous Region Animal CDC (1)

Yunnan Provincial Institute of Endemic Disease Prevention and Control (1)

Sichuan Provincial Animal CDC (1)

Q3:

The previous comment concerning terminology of diseases versus infections was only partially addressed. The authors replied that the terminology was used for consistency with previous OHZDP workshops. Changing the terminology to correctly identify infections or diseases should be implemented. At the very least, a statement regarding this ‘consistency’ of terminology should be included.

A3:

Your understanding for the consistency with previous OHZDP workshops is much appreciated. A statement regarding this ‘consistency’ is included in method section on line 129-131 as,

“For consistency with publications resulting from previous workshops, we use the term zoonotic diseases rather than zoonotic infections. The term highlights that these priority zoonotic infections are capable of causing disease.”

Q4:

In the discussion, limitations or implications of use of the chosen criteria (not just social impact) should be added.

A4:

Thanks for reviewer’s comments, the limitations of using chosen criteria is important and should be added. The method of One Health Zoonotic Disease Prioritization has been utilized in more than 25 locations, including USA, Uganda, Kenya, Kenya, etc [13-17]. Much experiences have been accumulated by the workshop and are inherited by the workshop advisor. The national level workshop did not aim to address all possible zoonotic disease prioritization criteria since the OHZDP methods focus on the top five criteria of greatest concern.Participants discussed many different criteria during the workshop and agreed on the five criteria most likely associated the potential zoonotic disease threat in the country.

Each criteria has a corresponding question, which is required an ordinal or multinomial answer to measure the diseases. When deciding criteria, the participants bear in mind to cover as much diseases as possible, but still a few disease has no answer to certain criteria’s question. Taking criteria “Economic impact” as example, livestock production loss is the question used for measurement. If livestock production loss is not available, case fatality rate and mortality were used as proxies; if China-specific data is not available, global data is used instead (see line 454-456, footnote * of Table 3). Future workshops – including those conducted at the regional or provincial level - could develop and apply more targeted and specific criteria for identifying a local list of priority zoonotic diseases.

According revision is added on line 304-310.

Submitted filename: Response to Reviewers.doc

Click here for additional data file.

26 Oct 2021

Using a One Health Approach to Prioritize Zoonotic Diseases in China, 2019

PONE-D-20-41070R2

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11 Nov 2021

PONE-D-20-41070R2

Using a One Health Approach to Prioritize Zoonotic Diseases in China, 2019

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Table 1

Agencies participating in the one health zoonotic disease prioritization workshop, Beijing, China, May 15–17, 2019.

Voting Members (No. participants)

National Level

National Institute for Communicable Diseases Control and Prevention, China CDC (2)

National Institute of Parasitic Diseases (NIPD), China CDC (1)

Division of Infectious Disease, China CDC (1)

China Animal Disease Control Centre (1)

National Research Center for Wildlife Diseases (1)

Eastern Region

Jiangsu Provincial CDC (2)

Shandong Provincial CDC (1)

Jiangsu Academy of Agricultural Sciences, Jiangsu Society of Animal Husbandry and Veterinary Medicine (1)

Shandong Provincial Animal CDC (1)

Northwestern Region

Qinghai Provincial CDC (3)

Gansu Provincial CDC (1)

Ningxia Hui Autonomous Region CDC (1)

Qinghai Animal CDC (2)

Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences (1)

Qinghai Academy of Animal Science and Veterinary Medicine (3)

Southwestern Region

Yunnan Provincial CDC (1)

Guangxi University of Chinese Medicine, School of Public Health and Management (1)

Sichuan Provincial CDC (1)

Guangxi Zhuang Autonomous Region Animal CDC (1)

Yunnan Provincial Institute of Endemic Disease Prevention and Control (1)

Sichuan Provincial Animal CDC (1)

Facilitators

US Centers for Disease Control and Prevention (Trainer)

National Institute for Communicable Diseases Control and Prevention, China CDC

Center for Global Public Health, China CDC

Jiangsu Provincial CDC

National Research Center for Wildlife Diseases

Yinchuan Animal CDC

Advisors and Other Participants

US Department of Health and Human Services China Office

US Department of Agriculture (USDA) China Office

US National Institutes of Health

US Centers for Disease Control and Prevention

Food and Agriculture Organization (FAO) China Office

WHO China Office

Center for Global Public Health, China CDC

National Institute for Communicable Diseases Control and Prevention, China CDC

Table 2

Raw and normalized scores for 30 zoonotic diseases generated from the One Health Zoonotic Disease Prioritization (OHZDP) tool during the OHZDP workshop, Beijing, China, May 15–17, 2019.

The top five priority zoonotic diseases selected by voting members are highlighted in grey and bolded.

Rank	Disease	Raw Score	Normalized Final Score
1	Zoonotic avian influenza	0.975	1.000
2	Echinococcosis/hydatid diseases	0.927	0.951
3	Rabies	0.925	0.949
4	Plague	0.777	0.797
5	Zoonotic tuberculosis	0.754	0.773
6	Streptococcus suis	0.720	0.739
7	Japanese Encephalitis	0.677	0.694
8	Brucellosis	0.672	0.690
9	Schistosomiasis	0.667	0.684
10	Scrub typhus	0.664	0.681
11	Creutzfeldt-Jakob disease	0.651	0.667
12	Anthrax	0.597	0.613
13	Severe fever with thrombocytopenia syndrome (SFTS)	0.588	0.603
14	Cysticercosis	0.578	0.593
15	Hepatitis E	0.556	0.570
16	Q fever	0.508	0.521
17	Salmonellosis	0.476	0.488
18	Cryptosporidiosis	0.476	0.488
19	Colibacillosis	0.454	0.465
20	Listeriosis	0.431	0.442
21	Severe Acute Respiratory Syndrome (SARS)	0.397	0.407
22	Tularemia	0.378	0.387
23	Xinjiang hemorrhagic fever (XHF) Crimean Congo hemorrhagic fever (CCHF)	0.378	0.387
24	Clonorchiasis	0.377	0.386
25	Yersiniosis	0.353	0.362
26	Leptospirosis	0.323	0.331
27	Intestinal amebiasis	0.308	0.316
28	Epidemic hemorrhagic fever	0.307	0.315
29	Zoonotic swine influenza	0.246	0.252
30	Campylobacteriosis	0.198	0.203

Table 3

Criteria, criterion weights, questions, and answer choices selected by workshop participants, Beijing, China, May 15–17, 2019.

Criteria	Criterion Weight	Question	Answer Choices
Disease hazard/severity	.403	What is the case fatality rate (CFR) in humans?	i. ≤ 1% CFR (0)ii. 1% < x ≤ 5% CFR (1)iii. 5% < x ≤ 10% CFR (2)iv. 10% < x ≤ 50% CFR (3)v. > 50% CFR (4)
Epidemic scale and intensity	.277	In the past 5 years, has the disease caused outbreaks or sporadic cases in China?	i. Yes–both animals and humans (3)ii. Yes–no animals, just humans (2)iii. Yes–just animals, no humans (1)iv. No–neither animals nor humans (0)
Economic impact	.123	What is the livestock production loss*?	i. Less than or equal to 5% production loss (0)ii. > 5% to 10% production loss (1)iii. > 10% to 20% production loss (2)iv. >20% production loss (3)
Prevention & control	.099	Are prevention and control measures readily available?	i. None (4)ii. Human vaccine, or human treatment/medicine, or animal vaccine (3)iii. Human vaccine, and human treatment/medicine, no animal vaccine (2)iv. Human vaccine, and animal vaccine, no human treatment/medicine (1)v. Human vaccine, and human treatment/medicine, and animal vaccine (0)
Social impact	.095	How much public attention has the disease received in the past 1 year according to the Baidu index†?	i. < 100 hits+ (0)ii. 101–300 hits+ (1)iii. 301–500 hits+ (2)iv. 501–700 hits+ (3)v. > 700 hits+ (4)

*Case fatality rate and mortality were used as proxies in cases where livestock production loss numbers were not available; global data were used due to limited China-specific data. For diseases where no data were available, a score of 0 was applied.

†http://index.baidu.com/v2/index.html#/ The Baidu index represents the weighted sum of the search frequency in a certain time period. Higher index values reflect a larger search volume, suggesting greater public interest and social impact

+ A hit is a request to a web server for a file (e.g. image, pdf, etc.) or an HTML page that contains specific content being searched.

Table 4

Recommendations and next steps identified by workshop participants for improving the control and prevention of the top five priority zoonotic diseases in China.

The priority zoonotic diseases for China include avian influenza, echinococcus, rabies, plague, and brucellosis.

Recommendation	Proposed Activities
Strengthen One Health Coordination	Develop framework (above Health Commission and Department of Agriculture) to coordinate multisectoral work on priority zoonotic diseases.
	Develop and implement multisectoral plans for disease control and prevention (including for outbreak control and response).
	Establish platform for multisectoral information sharing
Support Multisectoral, One Health Surveillance and Laboratory System Development	Identify and standardize common data elements/variables to facilitate multisectoral data sharing.
	Develop systems/platforms for routine multisectoral data sharing.
	Establish collaborative multisectoral process for sharing and discussing lessons learned on priority zoonotic disease prevention and control strategies.
	Identify resources to support training/capacity building on One Health surveillance approaches and laboratory testing.
Collaborate in outbreak preparedness and response	Ensure a joint stockpile of drugs, vaccine, personal protective equipment (PPE), and laboratory supplies are available to all sectors for the priority zoonotic diseases. This potential cost-savings approach can help strengthen and standardize response capacity.
	Develop joint One Health trainings, simulation exercises, and other laboratory and response staff across sectors for outbreak/pandemic preparedness for the priority zoonotic diseases.
	Develop and pilot mechanism to rapidly share outbreak related information and data across relevant sectors to improve response capacity for priority zoonotic diseases.
	Create and disseminate One Health education material and information sharing sessions to general public on potential zoonotic disease threats.
Strengthen Workforce Capacity	Develop One Health training opportunities during pre-service medical and veterinary school programs, including training on One Health concepts to encourage future professional collaboration.
	Include information on biosecurity and biosafety concepts on the five priority zoonotic diseases in pre-service and in-service programs.
	Organize in-service One Health seminars, presentations, and trainings on the five priority zoonotic diseases, including exposure risks to human and animal health workers.