Abstract
Event-based biosurveillance is a recognized approach to early warning and situational awareness of emerging health threats. In this study, we build upon previous human and animal health work to develop a new approach to plant pest and pathogen surveillance. We show that monitoring public domain electronic media for indications and warning of epidemics and associated social disruption can provide information about the emergence and progression of plant pest infestation or disease outbreak. The approach is illustrated using a case study, which describes a plant pest and pathogen epidemic in China and Vietnam from February 2006 to December 2007, and the role of ducks in contributing to zoonotic virus spread in birds and humans. This approach could be used as a complementary method to traditional plant pest and pathogen surveillance to aid global and national plant protection officials and political leaders in early detection and timely response to significant biological threats to plant health, economic vitality, and social stability. This study documents the inter-relatedness of health in human, animal, and plant populations and emphasizes the importance of plant health surveillance.
Introduction
Plant pest and pathogen epidemics can profoundly impact society by affecting food security, human and animal health, and economic stability Citation1–Citation3. Besides causing natural epidemics, plant pests and pathogens can be used as weapons and for bio-crimes Citation4–Citation6. Timely information on emerging crop pests and pathogens is abundant and accessible through media and other Internet sources in the public domain Citation7. Many countries have agricultural extension systems for monitoring and reporting on crop pests and diseases, and outbreaks are increasingly reported by concerned populations as the events are unfolding. While such information does not typically undergo the rigor of (time-consuming) peer review, it has checks and balances. Online information is often subjected to widespread review and comment, which can identify and correct errors quickly Citation8.
Several biosurveillance systems detect indicators of emerging diseases using online sources Citation9 and monitor events to provide situational awareness. In this paper, we illustrate the application of one biosurveillance methodology. We illustrate this process with a case study documenting planthopper (Superfamily: Fulgoroidea) infestation and associated transmission of two viruses of rice in Vietnam between February 2006 and December 2007 and China from June to December 2007. The study also describes the role of ducks in managing plant pest and pathogen spread while contributing to zoonotic virus spread in birds and humans.
Background
Project Argus
Project Argus is a biosurveillance system designed to detect and track biological events that may threaten human, plant, and animal health globally Citation10. A taxonomy (hierarchical set of concepts) of infectious disease was created using direct, indirect, and enviroclimatic indicators Citation10–Citation13. Regional specialists fluent in 40 languages collectively utilize taxonomy-based keyword searching and Bayesian tools to identify relevant articles from collected articles. Articles are collected multiple times a day, 7 days a week, from several thousand publically available native-language text-based media sources Citation14. Event reports are generated from relevant articles and a stage is assessed according to a published heuristic model Citation12. The resulting reports are reviewed internally according to a documented quality control and assurance protocol. These reports are then posted to a secure Internet portal for Argus users, which can be accessed via http://www.opensource.gov. A complete report archive is maintained for retrospective analyses and refinement of the biosurveillance methodology.
The brown planthopper
The brown planthopper (BPH; Nilaparvata lugens (Stål) Family: Delphacidae) is a pest of rice in Asia that reduces rice yields at high infestation levels Citation15. The BPH is also a vector of rice grassy stunt virus (RGSV) and rice ragged stunt virus (RRSV) Citation16. Outbreaks of several planthopper species, but predominantly BPH, occurred in a number of East Asian countries in 2005–2008 Citation17 Citation18, reducing rice production by approximately 3.4M tons in China, Korea, Japan, and Vietnam in 2005–2007 Citation17. This is significant because rice is a staple food for the vast majority of people in the affected countries Citation19 Citation20. Moreover, China is the world's largest producer of rice, producing 29% of the world's rice in 2006 Citation21.
Among the methods used to control BPH in China and Vietnam, this study paid particular attention to the use of free-ranging ducks Citation22 Citation23, which feed on BPH, as Argus was also monitoring the spread of highly pathogenic avian influenza (HPAI H5N1).
Methods
Information in the public domain and available on the Internet was monitored prospectively between February 2006 and December 2007 to identify direct and indirect indicators of plant pest and pathogen threats to food crops. Native language sources in South-East Asia, as well as English sources were surveilled daily. Upon identification of the BPH outbreak in Vietnam and later China, surveillance was focused on Vietnamese and Chinese language sources in these countries. Public domain Internet sources included news media, university extension sites, blogs, business reports, other biosurveillance systems (e.g. ProMED Citation24), and official sources utilized for validation (e.g. Food and Agriculture Organization [FAO] of the United Nations [UN] alerts Citation25). Official sources are defined as government or international non-governmental organization [NGO] reports and peer-reviewed scientific journal articles. Previous experience suggests that the combination of English and native language sources is important for full coverage of an emerging event. Therefore, the study used over 180 Vietnamese and 580 Chinese language sources, respectively, and over 2,000 English language sources.
For plant biosurveillance, direct indicators include specific reports of plant pest or disease outbreaks. Indirect indicators are events resulting as a consequence of a plant pest or pathogen epidemic (e.g. pesticide shortage, farmer anxiety, food shortage). They are associated with progression, severity, or level of social disruption caused by an outbreak and may provide early warning of a new event or escalation of a known event Citation10 Citation11 Citation13. Table 1a and Table 1b show examples of direct and indirect indicators used in this study. Automated and predefined keyword combination searches based on the direct and indirect indicators Citation10 Citation11 Citation13 were performed in English, Chinese, and Vietnamese.
Table 1a. Examples of direct indicators used in the Project Argus Model for use of media and public domain Internet sources
Table 1b. Examples of indirect indicators used by the Project Argus Biosurveillance System for use of media and public domain Internet sources
A model representing the evolution of a plant pest or pathogen outbreak and associated societal disruption responses was employed to serve as a guide for analysis and interpretation (Table 2). In this model pre-event conditions (Stage A) may lead to a contained epidemic (Stage 1). Societal indirect indicators escalate in stages toward societal strain as an event progresses from unifocal (Stage 1) to multifocal (Stage 2) to multifocal with infrastructure strain (Stage 3) to eventual social instability or collapse (Stage 4). Recovery indicators (Stage R) reflect a return to normal conditions following a plant pest or pathogen epidemic. In this study, events at a given time are categorized at the highest stage present (e.g. if an event is multifocal, but demonstrates infrastructure collapse, then it would be considered to be stage 4). These stages and examples are summarized in Table 2. For the purposes of this study ‘epidemic’ is defined as an escalating plant pest or pathogen outbreak.
Table 2. Project Argus Plant Staging Model
Results
Case study: rice pest and pathogen epidemics in Vietnam and China summary of events and sources
Over 5,000 total articles and 239 unique articles (i.e. articles providing new information) on rice pest and pathogen epidemics were identified during the study period. Official government or international (NGO) reports and peer-reviewed scientific journal articles were used to verify information accuracy. Table 3 summarizes the article pool resulting from the searches. The specific sources cited and their indicators are provided in Tables Citation5–Citation7.
Table 3. Summary of the search results for a case study of brown planthopper and rice grassy stunt or rice ragged stunt in rice in Vietnam and China in 2006–2007
Table 4. Sources and indicators referenced in open source planthopper-virus case study in Vietnam, 2006–2007*
Internet media observations on planthoppers and virus diseases in Vietnam
Direct, indirect indicators, and associated stages concerning the BPH-virus epidemic in rice in Vietnam in 2006 are summarized in Table 4. In February 2006, as the ‘Winter-Spring’ crop approached harvest, BPH had infested nearly 65,000 ha in 16 of 58 provinces (Table 4_2006a). During the next crop rotation ‘Summer-Autumn’, BPH populations escalated between March and July (Table 4_2006b, c). Between October and late November 2006, government requests to implement a crop-free period to break the pest life cycle were ignored (Table 4_2006d). Devastation of the new ‘Winter-Spring’ crop lead to a state of emergency, triggering government assistance, export restrictions, and access to the national rice stockpile enabling the rice market to recover by December 2006 (Table 4_2006e–i).
In February 2007, public Internet media reported that the government urged farmers in the Mekong River Delta to destroy heavily infested rice fields and not plant the ‘Summer-Autumn’ rice crop to interrupt the pest life cycle (Table 4_2007a). By March, the Ministry of Agriculture and Rural Development (MARD), fearing that the BPH affected area could be 100 times larger than the previous year, reversed its earlier request to cancel the ‘Summer-Autumn’ rice crop (Table 4_2007b, c). The FAO funded a project to help Vietnamese farmers control BPH while other farmers sought off-farm employment due to drought (Table 4_2007d, e). The epidemic escalated to levels 10-fold higher than 2006 (Table 4_2007f). Local, state, and federal governments established mandates and assistance programs to control the BPH, curb speculation, profiteering, and absenteeism on farms (Table 4_2007g–i). Traffic, businesses, and homes were disrupted by massive flight clouds of BPH (Table 4_2007j). By October the Minister of Agriculture again restricted exports and accessed over 685 tons from the national rice stockpile to prevent societal strain (Table 4_2007k–m). This assistance and control protocol meetings led to stabilization and recovery of the rice supply and rice market (Table 4_2007n, o). During this year, RRSV and RGSV were confirmed in Vietnam by the International Rice Research Institute (IRRI) through the FAO assistance program Citation17 Citation26.
Planthoppers in China
During 2007, BPH migrated from Vietnam to China in large numbers. Direct, indirect indicators, and stages are summarized in Table 5. In June 2007, media reported that 1.2 million ha of rice fields in South China were infested with planthoppers (species unspecified)—a 40% increase over the previous season (Table 5_2007p). Media described BPH spreading from south to central to east China. By July 25, flooding, followed by BPH, caterpillars, and other pests affected 2.8 million hectares of paddy in Anhui province, Eastern China, causing US €800M damage, triggering authorities to activate emergency agricultural disaster plans (Table 5_2007q, r). The government allocated US €1.3M for BPH control operations (Table 5_2007r). Media reported that BPH invaded nearly 400,000 of the 1M hectares of rice in Sichuan province, Central China (Table 5_2007r). In Hubei, authorities reported that planthopper populations (mixed species) were higher in 2007 than in 2006, but due to early preventive measures (US €2.6M), crop losses would be less than in 2006 (Table 5_2007s). However, in Changsha, Hunan, southwest of Hubei, BPH populations were 60% higher than in 2006 despite planthopper control efforts (Table 5_2007t).
Table 5. Sources and indicators referenced in open source planthopper-virus case study in China, 2007*
In mid-October, reports of BPH continued from across southern China, but BPH populations were generally reported as lower than in 2006. From September to December, 115 local and regional articles focused on BPH control successes and on methods of preventing outbreaks stating that the epidemics were mitigated, leading to recovery. Chinese authorities promoted the use of light traps, fish, and ducks to control rice pests. One article on November 7, 2006 indicated that researchers were introducing a new ‘one rice [paddy] two ducks’ method, where at least two ducks are released into every quarter hectare of rice paddy (Table 5_2007u). The method reportedly controlled insect pests in the fields.
Avian Influenza in Vietnam
In Vietnam, media reports of sick, free-ranging ducks coincided with reports of avian influenza outbreaks. Direct, indirect indicators, and stages are summarized in Table 6. An article published on December 19 indicated that on December 6, 2006, southern Vietnam provincial officials detected Vietnam's first outbreak of Highly Pathogenic Avian Influenza Virus (HPAI) H5N1 of 2006. Over 7,000 chicks and ducklings were culled in Cau Mau and Bac Lieu provinces, southern Vietnam (Table 6_2007j). On December 27, 2006 the government declared the HPAI outbreak to be contained and banned free-ranging ducks in the Mekong Delta (southern Vietnam), but raised concerns over illegal poultry smuggling from China to Vietnam (Table 6_2007k).
Table 6. Summary of direct and indirect indicators obtained from public domain Internet sources for the relationship between ducks and Highly Pathogenic Avian Influenza (HPAI H5N1) epidemic in Vietnam, 2006–2007*
On February 28, 2007, media observed that Vietnam lifted a 2005 ban on hatching ducks and geese, even though a new outbreak of HPAI H5N1 in northern Vietnam (Hai Duong province) was reported that week (Table 5_2007v). However, movement of ducks was banned. Prior to lifting the ban on hatching ducks, farmers continued using free-range waterfowl to control insects in rice fields, with an estimated population of over 60M waterfowl in the country. Later, a peer-reviewed publication indicated that the ban on hatching ducks presented problems for vaccination crews because people were hesitant to present illegal waterfowl for vaccination Citation27. On February 28, media reported that 50 ducks were found dead on a farm in Tra On district (southern Vietnam). The birds had been taken there from Soc Trang, southern Vietnam to feed in recently harvested fields (Table 6_2007v). On March 12, 2007, Internet media reported that the HPAI H5N1 strain in Vietnam was found to be the same strain that was previously found only in China to the north of Vietnam (Table 6_2007w).
On June 29, 2007, it was reported that 435 H5N1-infected ducks from Mo Dao commune, in northern Vietnam, were destroyed by officials. In Que Vo district, Bac Ninh, in northern Vietnam, media reported that free-range ducks began dying; at least 100 duck carcasses were found in local rice paddies. Duck ownership was unclear. Concern was expressed by the locals about slow government response and unsafe water sanitation (Table 6_2007x). On October 15, 2007, it was observed that the Vietnamese government launched a campaign to fight avian influenza along with rice pests and pathogens (Table 6_2007y). Over the next few months, millions of ducks across Vietnam were vaccinated against avian influenza. In December, 2007, residents in Bac Lieu Province, southern Vietnam, expressed concern over the potential spread of avian influenza as unvaccinated ducks freely roamed paddies throughout the province, despite regulations requiring all unvaccinated ducks to be isolated and confined to farms. Local duck farmers complained that some officials were taking bribes and allowing unvaccinated ducks from other provinces to roam in their area.
Discussion
In this study, the severity of an epidemic was recognized as the epidemic unfolded by monitoring media on the Internet and by categorizing direct and indirect indicators into established stages of epidemic progression. The surveillance methodology utilized was adapted from animal and human disease biosurveillance and represents a novel approach to crop surveillance.
Validation sources
The estimates of crop losses and areas affected in the Internet news media were validated by official government or international NGO reports and peer-reviewed scientific journal articles (Table 7). It is important to note that often events appeared in the Internet media before the official publications (). Though official reports and peer-reviewed research papers may present highly accurate details and results at a highly technical level, the time required to conduct the research and publish it is months or years. For example, in Vietnam there were delays of one or more years after the case study was completed before official publications reported the estimates of the infestation or infection severity and crop loss Citation17. The power of the approach of using Internet sources for surveillance is that such information is available in hours to days following events. This is essential for early warning and situational awareness.
Fig. 1. Comparison of dates of Internet media reports and reports from official sources. Data above the diagonal line correspond to the case when a public domain source reports on an event before an official source reports on the same event. Below the line, an official source reports on an event before a public domain source.
Table 7. Validation of public domain Internet media reports by official reports
Indicators and staging
In this study, many of the sources reported direct indicators of outbreaks (e.g. number of hectares affected, percentage of yield reduction). However, indirect indicators were also reported. As the BPH-RRSV/RGSV epidemic emerged, indirect indicators included official acknowledgement of the outbreak; official action as government assistance with pesticides, training, food security, control strategies, and mandates; demand for countermeasures from the farmers in terms of public assistance; perception of threat (e.g. hoarding of pesticides, migration to cities for work); change of business practices (e.g. export restrictions, price gouging, profiteering); and strain on infrastructure integrity (e.g. rice stockpiles accessed, criminal activities such as rice, duck, and pesticide smuggling, and refusal to follow government pest control mandates).
Each report was staged based on the degree of pest or pathogen spread and associated social disruption (Table 2). Report staging over time is illustrated in a and a for Vietnam and China, respectively. In 2006, the BPH/RRSV-RGSV outbreak was first reported as a stage 2 on February 9, 2006 in Vietnam, and escalated to stage 3 on March 2, 2006 as food and societal infrastructure strain developed due to Vietnam's shortage of rice and food insecurity. Increased staging suggests escalating social pressure and infrastructure strain. Recovery was initially observed on November 22, 2006 when assistance arrived (e.g. training and pesticides provided, and rice stockpiles released by national government; FAO and IRRI scientists collaborating with Vietnam government scientists). In China, media reported events indicating that the epidemic escalated from stage 2 to stage 3 in less than a month (June 5 to June 25, 2007) and returned to stage 2 in mid-September 2007 when the government provided US €3.9M in aid, which may have facilitated the end of the epidemic and eventual recovery in November 2007. b and 3b demonstrate that multiple indicators are represented at each stage. Thus, both direct indicators, present throughout the study period (Tables 4 and 5), and indirect indicators are required to understand events such as those described in this case study.
Fig. 2. (a) Stage over time for the 2006–2007 case study of planthopper-virus in Vietnam. (b) Frequency of indirect indicators by stage for the 2006–2007 case study of planthopper-virus in Vietnam.
Fig. 3. (a) Stage over time for the 2007 case study of planthopper-virus in China. (b) Frequency of indirect indicators by stage for the 2007 case study of planthopper-virus in China.
Inter-relatedness of human, plant, and animal health
This case study documents the inter-relatedness of health in human, animal, and plant populations. The reporting described above suggests that BPH-vectored virus epidemics encouraged illicit movement and breeding of free-range ducks for the purpose of BPH control. In 2008, molecular sequence analysis indicated the China H5N1 strain was in northern Vietnam and the Cambodian strain was in southern Vietnam Citation28, suggesting that duck trade had introduced the virus from neighboring countries. Infected ducks excrete influenza viruses while living in paddies, providing a potential human and animal health concern to the public exposure to infectious water. Avian influenza virus is transmitted between ducks orally through water contaminated with feces Citation29 Citation30. In 2008, FAO announced that ducks, people, and rice paddies—rather than chickens—are the major factors driving outbreaks of HPAI H5N1 in Thailand and Vietnam Citation31–Citation33. Previous studies associate the spread of H5N1 with the movement of ducks at the end of the rice harvest Citation31 Citation32. That model, however, would not explain the spread of HPAI H5N1 during the rice cropping season as observed in the present study. Our working hypothesis is that ducks were herded into rice fields (while rice was still growing in the fields) to feed on BPH and other insects, such that the spread of HPAI H5N1 roughly followed the spread of BPH Citation31.
Significance of public media monitoring in identifying emerging epidemics
Plant pest and disease epidemiology has largely relied on field-collected direct measurements to assess the development and severity of outbreaks. This study demonstrates that Internet sources can provide important information for monitoring plant pest and pathogen epidemics at the local level. The methodology described here, employing staging of indirect as well as direct indicators, provides a focus on signatures in the media typical of emerging or escalating epidemics Citation13 Citation14. This approach can be utilized to detect outbreaks early, before official reports and studies are published and particularly where on-the-ground reporting is limited and where the media is available. We believe this study is the first to use Internet sources to document the impact of plant pest and pathogen epidemics on resource allocation and social stability.
Conflict of interest and funding
The authors have not received any funding or benefits from industry to conduct this study.
Acknowledgements
We appreciate Huong Luong's (Vietnamese Analyst, Project Argus, Georgetown University) contribution to this work by translating Vietnamese sources to English. Rishi Kapoor and Jeana Shoji (Chinese Analysts, Project Argus, Georgetown University) conducted the Chinese search and reporting. We acknowledge the financial support of the United States Government for this research.
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