2024 Volume 12 Pages 237-248
Tomato brown rugose fruit (ToBRF) disease is an emerging disease of tomato worldwide. It has been reported that the virus causing the disease has overcome the resistance gene commonly used by breeders against other tobamoviruses. Due to the aforementioned concern, this disease has been designated by European and Mediterranean Plant Protection Organization (EPPO) as a high-priority addition to its ‘Alert List’. While no official reports of the disease currently exist within the Philippines, the significant import and movement of plant materials within and into the country necessitates continued vigilance. The absence of a formal regulatory framework in the Philippines for this disease elevates the risk of its emergence and subsequent establishment within the country. Consequently, proactive measures to identify potential sources and mitigate the spread of the disease are of paramount importance. In this review, a management strategy has been proposed that can reduce the initial amount of inoculum (Xo), rate of infection (r), and length of time of infection (t) if the virus causing the disease enters the country.
Tomato (Solanum lycopersicum) is one of the major crops cultivated worldwide and has a total trade worth of $9.08 billion in 2019. Globally, the top producer of tomato includes Mexico, The Netherlands, Spain, Morocco, and Canada [1]. Tomatoes occupy a significant position among commonly used ingredients in Filipino cuisine. This widespread culinary application underscores its status as a vital agricultural commodity within the Philippines. Tomato in the Philippines are also used in processed products such as sauces, soups, and pastes/ketchups. In the country, tomato production increases annually despite the decrease in size of areas planted with the crop. In 2019, Ilocos Region registered the biggest portion of production amounting to 73.32 thousand metric tons or 32.8% of the total output followed by Northern Mindanao (21.7%), Central Luzon (14.1%), Calabarzon (7.2%), and Western Visayas (5.1%) [2].
Unfortunately, tomato is a crop susceptible to several infectious agents with virus being the most destructive especially those that belongs to genus Tobamovirus, genus Virgoviridae. Tobacco mosaic virus (TMV), tomato mosaic virus (ToMV), and the emerging tomato brown rugose fruit virus (ToBRFV) are the most destructive species that belong to this group. As a tobamovirus, ToBRFV can either be transmitted through external seed contamination, mechanically by common cultural practices, or by circulating water [3]. ToBRF disease was first observed at Israel in 2014 but it was only in 2016 that the causal virus was recognized as a novel virus. Concern about the disease is increasing as it is continuously spreading in Africa, Asia, Northern America, and other countries in Europe and Mediterranean [4]. The scope of ToBRF disease spread is likely more severe than has been previously reported given the worldwide nature of seed manufacturing, distribution chain, and seed transmissibility of the disease [5]. In line with this, the European and Mediterranean Plant Protection Organization (EPPO) added the ToBRF disease in ‘Alert List’ of viruses and marked it with the highest priority for pest risk analysis [4]. The serious threat posed by this disease necessitates immediate attention, as tomato growers could face significant crop losses if it establishes itself in fields. Data gathered in Florida (USA) fortifies this claim. In 2019, the virus caused an estimated yield loss of 30–70% in the tomato production of the state, resulting in economic losses of $262 million a year [6].
Today, importation of seeds or susceptible Solanaceous plant are the main sources of ToBRFV when introduced to another area. Based on a report, there is a difficulty in tracing the geographical origin of the seed lots [4]. Individual consignments of hybrid seeds are frequently made up of mixed lots of seed from various countries of origin. This practice increases the risk of the seeds carrying and introducing the virus to new areas. The following increases the risk of introduction and spread of the virus: (1) entry of infected tomato fruit or planting materials, (2) use of containers or other equipment previously used in contaminated tomato production, and (3) the presence of insect vectors. As a tobamovirus, the successful introduction and establishment of the ToBRFV in a tomato production area would result in a faster and easier spread of the disease.
The Philippines has yet to report any cases of ToBRF disease. However, the ongoing import of tomato seeds and planting materials poses a potential risk of introduction. This concern is heightened by confirmed reports of the disease in neighboring countries such as China, along with unsubstantiated reports in Thailand, Vietnam, and India [4]. The potential establishment of the ToBRFV within the Philippine tomato-growing regions poses a significant threat to the industry. To proactively mitigate this risk, a comprehensive risk assessment is essential. The risk assessment would entail identification of potential sources of the ToBRFV and evaluation of the likelihood of its introduction and establishment within the Philippines. This information would then serve as the basis for the development of appropriate management strategies should ToBRFV emerges in the country. Hence, this review can serve as a valuable foundation for such an initiative.
Given that the ToBRFV can be transmitted both through seeds and mechanically to another tomato plant, contaminated seeds and transplants pose the primary risk factors for its spread and subsequent introduction into new planting areas [7]. The introduction of the virus into crop production area can occur via contaminated seeds in both screenhouse and open-field tomato cultivation. While the frequency of this transmission route might be low, its impact on high-intensity screenhouse tomato production can be significant. To add, there is a report that mentioned that fruits also aid in long distance spread of the virus although the risk for spread is considered low [8]. Agricultural commodities such as tomato fruit or seeds move through different steps in international trade. Figure 1 illustrates the potential pathways for the entry of infected seed or planting materials. The movement of materials showed in the illustration is crucial to visually depicts the routes through which the ToBRFV can spread and ultimately establish itself in new geographic regions, even those previously unaffected by the disease. Figure 1 also showed that ToBRFV infection can occur at any point within the depicted pathway. This contamination can persist until the final consumer receives the tomatoes.
Understanding the potential pathways of entry for the ToBRFV is critical. This knowledge empowers regulatory bodies to identify the origin of the virus and implement restrictions on the movement of materials originating from these sources. In Mexico, imported tomato and pepper seeds from 14 different countries in Asia, Africa, and America tested positive for ToBRFV [4, 9]. The same issue was encountered in Egypt where the importation of seeds from The Netherlands, a country that also has cases of the disease, is thought to be a possible contributor to the spread of ToBRFV [4]. This demonstrates how crucial the entry point of ToBRFV-contaminated planting material for it to proliferate, emerge, and establish in remote areas.
It is interesting to note that individual consignments of hybrid seeds frequently consist of mixed lots of seeds produced from several countries, increasing the association of the virus with the seed. Major international seed corporations such as Monsanto, Syngenta, East-West Seed, and Bayer CropScience often carry out operations in multiple nations to produce some hybrid tomato seed lots [4, 10]. Plant lines may be exposed to a higher risk of ToBRFV infection by being grown in various locations. For instance, two parental lines were bred in The Netherlands, then larger quantities of these seeds were produced in France or Spain, and these seeds were then planted in Thailand or China where the hybrid tomato was bred through the cross-pollination of two parental lines [11, 12]. These countries where the hybrid seeds were grown have cases and are at high risk for establishment of ToBRF disease. In line with this, the International Seed Federation (ISF) admitted that phytosanitary certification of seed is challenging as there are cases of failure to retain seed lot number which makes phytosanitary certification difficult and unreliable sometimes [11]. In addition, during seed production, some cultivation practices may become a source of mechanical transmission of the disease that may later pass to the seeds of tomato. In connection to this, some farm practices involve inoculating plants with a weaker strain of ToBRFV in an attempt to achieve cross-protection. However, this practice is not allowed in the European Union as it further increases the spread of the viral disease. This led to a criminal investigation by the Dutch Intelligence and Inspection Services [13]. In the scenario where a portion of the mass-produced seeds intended for international distribution originates from farms employing the unauthorized cross-protection technique, this practice has the potential to facilitate the dissemination of the disease to new geographic regions.
In Figure 1, it is subdivided into import and disease exposure pathway. The import pathway includes the country of origin of seed, re-export of planting materials, and the National Plant Quarantine Services Division (NPQSD) of the Philippines that is responsible for inspection and quarantine of imported commodity entering the country. During the quarantine, imported seeds must be tested or diagnosed as it may carry the infectious agent like the ToBRFV. In line with this, the Philippines has yet to report any cases of ToBRF disease. However, the current regulatory framework lacks protocols specifically designed to prevent the introduction of this virus into the country. This regulatory gap exposes the Philippines to the potential emergence and establishment of the ToBRFV, particularly through importations from countries with confirmed cases, such as China. Furthermore, the disease exposure pathway in Figure 1 shows the pathway of seeds from the quarantine regulatory body to seed companies, commercial growers, nursery, and indoor and open-field tomato growers. This contribute to the local spread of ToBRFV if and only if the virus is already present in the country. In regard to contributors to the biosecurity risks, some key aspects of the pathway shown in Figure 1 are the country of seed origin and the way in which the plant derived from imported seed is grown (e.g., open-field or screenhouse; crop and disease management practices) [14].
The mechanical spread of the virus can occur within greenhouses or open-fields through contaminated tomato packaging materials or the introduction of tomatoes brought on-site for consumption. To date, outbreaks of ToBRFV have predominately been reported on tomatoes cultivated in protected environments and this is due to the intensive cultural practices such as thinning of seedlings, pruning, and trellising that may cause wounds or microlesions [5,15]. In the Philippines, the Department of Agriculture recommended that transplanted tomato must be pruned 10–20 days after transplanting [3]. The use of the same equipment for pruning both infected and healthy tomato plants, either within greenhouses or open fields, poses a significant risk of mechanically transmitting the ToBRFV. In this context, it is important to recognize that the aforementioned risk of mechanical transmission is only relevant if the ToBRFV is already established within the locality. Similarly, inoculum from infected plants can persist on wires, glass, concrete surfaces, and soil within greenhouses after harvest, potentially harboring the ToBRFV. Because cultivated tomato is subjected to more intensive handling in screenhouse, the risk of association of the virus with the seed varieties intended for screenhouse is much likely to be higher than in open-field.
2.3 Presence of alternate hostField-grown tomato is susceptible to infection as weed reservoirs act as source of inoculum, potentially facilitating mechanical transmission by contaminated clothing, farm equipment, or pollinators. Notably, the ToBRFV has been detected in weeds such as Chaenopodium murale and Solanum nigrum [16]. Species of Nicotiana (N. bentamiana, N, celvelandi, N. glutinosa, and N. tabacum), and other solanaceous crops (S. lycopersici, S. melongena, S. tuberosum cv. Kexin 1, C. annum, C. amaranticolor, and C. quinoa) also serve as reservoir of the virus [17]. The Philippines presents an interesting case where its top tomato-producing regions, Ilocos Region and Northern Mindanao, also hold the distinction of being a major tobacco-growing areas. This geographic overlap raises concerns, since tobacco emerges as a potential secondary host for ToBRFV, alongside the primary host, tomato. This co-occurrence of both hosts within the same regions could heighten the vulnerability of these areas to the establishment and spread of the ToBRFV.
2.4 Presence of insect vectorsTomato grown in open-field are adversely affected by virus acquired by pollinating insects such as bumblebees (Bombus terrestris) and the pest like the South American tomato pinworm (Tuta absoluta). In fact, a study reported that B. terrestris are the primary carriers of ToBRFV inoculum, contributing to the spread of the disease in tomatoes. The bees transfer the virus by carrying crude sap on their mandibles or mechanically through their vibrating bodies [18]. Furthermore, recent findings reported that the lepidopteran T. absoluta can also transmit the ToBRFV to a healthy tomato [19]. On the positive note, there have been no reports of B. terrestris and T. absoluta in the Philippines [20,21]. However, due to the limited research on potential insect vectors of ToBRFV, maintaining vigilance is crucial [18,19]. Therefore, investigating the potential for transmission by other tomato pollinators in the Philippines is essential.
This section outlines various strategies for controlling or managing potential ToBRFV outbreaks. These strategies can be categorized into five main approaches: (1) avoidance, (2) exclusion, (3) eradication, (4) protection of the plant, and (5) development of resistant host. The first three strategies focus on the control of ToBRFV while the last two strategies are directed towards the host. Each management strategies may influence the amount of initial inoculum (Xo), infection rate (r), and length of time for infection (t). Because viruses can have secondary disease cycles, a polycyclic model can likely be used to determine the amount of disease. In relation to this, the polycyclic disease model that is typically represented by the equation X=Xoert will be the basis for the critical analysis of the effects of each control methods. While this review won’t delve into calculating the exact amount of disease, it will explore how factors like Xo (initial inoculum), r (infection rate), and t (infection duration) influence the effectiveness of various management strategies. Reducing any of these factors (Xo, r, or t) will consequently reduce the amount of disease.
3.1 Avoidance of the ToBRFV or diseased-tomatoChoosing a geographic area or planting site strategically can affect Xo (initial inoculum), r (infection rate), and/or t (infection duration). As shown in Table 3, avoidance methods that prevent ToBRFV introduction delay the onset of infection, thereby reducing the number of infected plants throughout the tomato growing season.
As a foundational principle for disease prevention, prioritizing the use of clean and virus-free seeds and other planting materials is crucial [22]. To ensure this, implementing a robust surveillance or quarantine protocol for imported planting materials and seeds entering the Philippines through designated ports is essential. While diagnosing viral contamination in planting materials can be challenging, international research groups have already developed various diagnostic tools, including DAS-ELISA, RT-PCR, RT-LAMP, and CRISPR-Cas12a [23, 24, 25]. However, these diagnostic tools developed in other countries are not currently available for, or integrated into, the quarantine protocol of the Philippines specific for this disease. Implementation of these diagnostic tools within the Philippines would significantly enhance the capacity of the country to intercept potential introduction of ToBRFV. Early diagnosis of the planting materials will guarantee that the tomatoes grown are ToBRFV-free. Therefore, implementing effective diagnostic procedures for imported planting materials and seeds can ensure its cleanliness and absence of ToBRFV contamination. This, in turn helps minimize the amount of initial inoculum (Xo).
However, if some infected planting materials by-pass the inspection due to possible smuggling, avoidance of ToBRFV is still possible by modifying cultural practices. It was suggested in a report that growing of a non-host crop in the field or greenhouse previously infected with ToBRFV should be considered [4]. The duration of the non-host crop period should be determined by the severity of the ToBRFV outbreak. A one-year gap without host plants and alternate weed hosts has been suggested [4]. In Israel, a minimum crop-free period of 1.5 months was implemented [4]. This fallow period is expected to reduce the initial inoculum (Xo) of ToBRFV in previously infested tomato open-field growing areas.
3.2 Exclusion of the ToBRFV or diseased-tomatoThe Philippines currently lacks both rapid detection methods for ToBRFV and widespread awareness amongst tomato cultivators regarding this emerging disease. This deficiency presents a challenge in preventing the introduction of ToBRFV via contaminated seeds. However, should seeds harboring the virus be identified, exclusionary measures can be implemented through chemical or physical treatment of seeds or seedlings. It is important to recognize that seeds are the primary mode for the long-distance dispersal of ToBRFV [26]. ToBRFV can reside either on testa (seed coat) or the endosperm (nutrient-rich tissue) of seeds. Microscopic lesions formed during germination create entry points for the virus to infect young plants emerging from the seeds. Because of this, it is important to disinfect the contaminated surface of the seeds either by using disinfecting solutions such as 10% trisodium phosphate for three hours, 4% hydrogen peroxide for 30 minutes, or in 2.5% sodium hypochlorite for 15 minutes [27]. Furthermore, physical control strategies can also be employed to decontaminate suspected planting materials without affecting the germination of tomato. This strategy includes thermal-based seed treatment either at 80 °C for 24 hours, 75 °C for 48 hours, or 70 °C for 96 hours [26].
3.3 Eradication of the ToBRFV or diseased-tomatoEradication should be done whenever the virus or disease is already present in the growing areas before it passes the economic threshold level. Several countries in Europe which includes Germany, Italy, The Netherlands, and Spain have implemented successful strategies for eradicating ToBRFV outbreaks in greenhouses cultivating tomatoes [28]. Early intervention through a practice known as roguing, which involves systematically removing and destroying tomato plants that exhibit initial symptoms of tobamovirus infection, can effectively eliminate potential sources of initial inoculum (Xo). This helps prevent the establishment and spread of the disease within a localized area. However, this approach becomes progressively less efficient and ineffective as disease incidence increases throughout a farm [29]. Additionally, the removal of alternate host (solanaceous crops, Chaenopodium morale, C. amaranticolor, C. quinoa, and Petunia hybrida) along with infected plant and plant parts is crucial to minimize potential reservoirs and sources of infection. Following the removal of any alternate host or symptomatic plants, composting of tomato debris infected with ToBRFV is not recommended due to its inadequacy in ensuring complete viral inactivation [30]. Instead, destroy the ToBRFV-infected plant by incineration [31].
Sanitizing farm implements is another crucial method to control ToBRFV spread. The virus can rapidly spread through human handling of infected plants. Furthermore, ToBRFV can persist on surfaces such as farm tools, protective clothing, and containers, acting as potential vectors for mechanical transmission by humans. To address this challenge, recommendations include disinfection of pots and cutting tools, along with the implementation of virucidal handwashing practices [28]. Disinfection of non-metallic equipment with a household bleach solution is necessary due to the extended viability of viral particles on surfaces such as clothing, plant debris, growing media, and tools [32]. Another study had recommended the use of either 0.5% Lactoferrin, 2% Virocid, or a combination of 10% sodium hypochlorite and 3% Virkon as effective disinfectants against ToBRFV [33]. Implementing this management strategy in a screenhouse environment can potentially reduce the initial inoculum (Xo) of the virus.
3.4 Protection of healthy tomato cropDisease-free tomato can be protected by modifying the plant spacing and by using protected structures like the screenhouse. These methods could either reduce the rate of infection (r) or the amount of initial inoculum (Xo). Protection of plants can be done by planting tomatoes in a screenhouse to protect the tomato from the vectors of the virus such as bumblebee (B. terrestris) or South American tomato pinworm (T. absoluta). This may seem very unconventional for large tomato production as large production area uses open field for cultivation. Therefore, exploring modified plant spacing strategies as an alternative approach is worthwhile. However, it's important to consider that strong winds in open fields can damage tomato plants, potentially creating wounds that facilitate mechanical transmission of the virus. In line with this, a report showed that increased plant spacing is effective in mitigating the spread of viral diseases such as beet mosaic, beet yellows, cauliflower mosaic, and groundnut rosette [34]. Therefore, implementing wider plant spacing may result to a minimal reduction in disease spread and severity within the field. This strategy can be particularly beneficial for tomatoes cultivated in open-fields.
3.5 Development of resistant/tolerant tomato cultivarTomato brown rugose fruit virus overcomes the Tm-22 gene normally used by breeders against tobamoviruses [35]. Therefore, screening indigenous tomato varieties offers a promising avenue for discovering novel sources of resistance to ToBRFV. Following this approach, some private breeding companies have already initiated efforts to identify novel sources of resistance to ToBRFV by utilizing wild tomato accessions. Table 1 presents some of the known patents submitted for the development of new ToBRFV-resistant varieties. One promising source of resistance has been identified in S. habrochaites LYC4943 that has a dominant resistant trait conferred by CC-NBS-LRR gene. The F1 plant was created by crossing the S. habrochaites and S. lycopersicum to create two populations for mapping [36]. Meanwhile, S. pimpinellifolium PI79532 confers only a recessive resistance trait [37]. Intriguingly, three additional accessions of Solanum pimpinellifolium (GNL.3919, GNL.3920, and GNL.3951) exhibiting high levels of resistance to ToBRFV were identified. Moreover, crosses made between these particular accessions demonstrated polygenic resistance, suggesting a more intricate genetic architecture underlying this trait [38].
Patent No. | Source | Accessions | Description | Reference |
---|---|---|---|---|
US11168336B2 | S. habrochaites | LYC4943 | The CC-NBS-LRR gene on chromosome 8 confers a dominant resistant characteristic | [36] |
US20230276763A1 | S. pimpinellifolium | PI79532 (LA2348) | ToBRFV resistance is a recessive trait | [37] |
WO2019110130A1 | S. pimpinellifolium | GNL.3919, GNL.3920, GNL.3951 | A polygenic ToBRFV resistance trait based on three loci from three distinct accessions. | [38] |
Since there are known sources of resistance available, several seed companies have responded to the challenge of this emerging ToBRF disease by developing resistant varieties. Table 2 shows the commercially available varieties from other countries and the companies that developed these. Syngenta offers five commercially available varieties (Lansor, Barosor, Ibeth, Ouri, and Waqu beefsteak tomatoes) [39]. Rijk Zwaan had also released three varieties with intermediate to high resistance (Cuarzyta RZ, Sylvyta RZ, and Vivalto RZ) [40]. Similarly, Bayer had also developed three varieties with intermediate resistance (Strabini, Ferreira, and Novero) [41]. Enza Zaden presents a number of high-yielding tomatoes resistant to ToBRFV (Table 2) [42]. While these resistant varieties are available mostly in the western countries, their availability in the Philippines remains unconfirmed due to lack of documentation. Therefore, raising awareness among tomato growers is crucial to prioritize their cultivation and mitigate the threat posed by ToBRFV.
Company | Varieties | Reference |
---|---|---|
Syngenta | Lansor, Barosor, Ibeth, Quri, Waqu | [39] |
Rijk Zwaan | Cuarzyta RZ, Sylvyta RZ, Vivalto RZ | [40] |
Bayer | Strabini, Ferreira, Novero | [41] |
Enza Zaden | Ponza, Help, Annico Cove, Ardile, Reina, Bronski, Corsica, Dunk, Falkland, Icaria, Macapule, Saint Anna, Sunstream Keys, Sunstream Lau, Tobinaro, Tamagino, Ustica | [42] |
Pepper is also known as a host of ToBRFV but the impact of the virus is only minor as most hybrid pepper cultivar carries L resistance genes against tobamoviruses. Reports revealed that ToBRFV has not yet overcome this R gene [43]. Once resistant/tolerant cultivar has been selected or developed, it may be recommended in the future as the first line of defense for ToBRF disease as it may help in decreasing the amount of initial inoculum (Xo) and rate of infection (r). Table 3 shows the summary of the effects brought by the different strategies for the management of ToBRF disease in tomato growing areas that may either affect the amount of initial inoculum (Xo) and rate of infection (r), and/or length of time for infection (t).
Methods/strategies for control | Major effect by reduction in | ||
---|---|---|---|
Amount of initial inoculum (Xo) | Rate of infection (r) | Length of time for infection (t) | |
A. Avoidance of the pathogen | |||
Use of disease-free seeds | ✓ | ✓ | |
Modification of cultural practices | ✓ | ✓ | |
B. Exclusion of the pathogen | |||
Treatment of seeds | ✓ | ✓ | |
C. Eradication of the pathogen | |||
Roguing | ✓ | ✓ | ✓ |
Elimination of alternate host | ✓ | ✓ | |
Sanitation | ✓ | ✓ | |
D. Protection of the plant | |||
Increase plant spacing | ✓ | ✓ | |
Modification of nutrition | ✓ | ✓ | |
Use of protected structures | ✓ | ✓ | ✓ |
E. Development of resistant host | |||
Selection and breeding for resistance | ✓ | ✓ | ✓ |
There is no single strategy better than the other in controlling and managing the ToBRF disease. The most appropriate to use in managing the disease is the use of holistic approach like the Integrated Pest Management (IPM) that will help in preventing further large-scale damage to crops. This management approach is an effective, environmentally sensitive approach in disease management that relies in the combination of common-sense practices. This approach uses the current, comprehensive information about the disease and its interaction with the environment. This information combines with the known management strategies (avoidance, exclusion, eradication, protection, and use of resistant varieties) can be used to manage the disease below the economic threshold level by the most economical means with least possible hazards to people, property, and the environment. Based on the epidemiological effects on amount of initial inoculum (Xo), rate of infection (r), and length of time of infection (t), a proposed flowchart of possible management strategy was produced. Figure 2 shows different scenarios or conditions and the recommended management for the control of ToBRF disease.
Since there is still no report of ToBRF disease in the Philippines, it is thus important for the regulatory bodies responsible for overseeing the entry of imported commodity to keep an eye to this disease. If possible, researchers in the Philippines must start the detection of the virus causing the disease in the ports of entry. Gathering of tomato plant samples from farms within the Philippines must also be done to ensure that the disease is not yet established in the country. Researchers in the Philippines must also consider detecting the virus in other possible alternate hosts especially those plants belonging to Solanaceae family as well as those pollinators of tomato in the country. Once the virus causing the disease is found in the country, breeding institutions must also consider looking for indigenous tomato cultivars or varieties in the country that may possess considerable degree of resistance to this emerging disease.
This review examines the potential factors that may increase the risk for the emergence and establishment of ToBRF disease in the Philippines. This includes the movement of planting materials via importation, cultural practices being employed in the tomato fields, and presence of insect vector and alternate host. With this regard, ToBRF disease management was formulated based on the possible scenarios or conditions that may be faced by the tomato growers. This review encompasses scenarios across the entire spectrum, from the period preceding the introduction of the virus into the country to the point at which the virus establishes itself within the tomato-growing regions. Most of these management strategies are preventive measures to ensure that there is little to no initial inoculum (Xo) that will be present in the tomato growing area. Stringent regulatory controls, implemented at point of entry through quarantine operations, exemplify this approach. Take note that this is only possible if there are diagnostic tools available for the detection of the virus. Furthermore, if the virus had already entered the country through illegal importation, there are also available cultural and chemical methods for the management of the disease.
This work was supported by the Department of Science and Technology – Accelerated Science and Technology Human Resource Development Program (DOST-ASTHRDP).