Possible Bioterrorism by North Korea and South Korea’s Preparedness

Abstract

This paper reviews the elements and infection mechanisms of bioterrorism, assess North Korea's capability for biological warfare, and propose strategies for South Korea to counter potential bioterrorist threats from the North. The four critical elements of bioterrorism include the biological agent, the weaponization of the agent, the delivery system, and the impact of weather conditions on the attack. The infection routes for biological agents in bioterrorism include inhalation, ingestion, dermal exposure, and injection. The potential agents under development could include anthrax, smallpox, plague, and botulinum toxin, which might be deployed using missiles, artillery shells, or through covert operations. Proximity to North Korea significantly increases vulnerability to biological attacks. Possible methods include contaminating water supplies, food sources, or densely populated areas. Anthrax, smallpox, plague, and botulinum toxin could theoretically be delivered using packages attached to balloons. Minimizing the impact of a bioterrorism event requires strategy that includes four key actions: detection, decision-making, distribution, and dispensation. By integrating these steps, authorities can effectively manage and mitigate the effects of a bioterrorism event. Civilian doctors play a role in the early detection, diagnosis, treatment, and management of biological agents. Educating medical professionals is crucial for preparing against potential biological warfare or bioterrorism threats.

Introduction

Recent reports about North Korea sending balloons filled with trash and other waste materials into South Korea have raised concerns regarding potential bioterrorism risks (Fig. 1). Although the current payloads consist of rubbish, used toilet paper, and cigarette butts—primarily intended for psychological harassment and propaganda—the possibility that these actions could escalate to bioterrorism should not be entirely dismissed [1,2].

Figure 1. North Korea drops trash balloons across the border. https://media.cnn.com/api/v1/images/stellar/prod/2024-06-02t065626z-1688605478-rc2u28af5s6w-rtrmadp-3-southkorea-northkorea-balloons.JPG?c=original. Accessed June 7, 2024.

While the current use of trash balloons does not constitute bioterrorism, the situation highlights the importance of maintaining vigilance and preparedness for potential escalations. Therefore, it is crucial to have effective mechanisms for detection, decision-making, distribution, and dispensation in place to mitigate any future threats that may emerge from such activities.

The aim of this paper is to review the elements and infection mechanisms of bioterrorism, assess North Korea's capability for biological warfare, and propose strategies for South Korea to counter potential bioterrorist threats from the North.

Methods

In PubMed search, “bioterrorism and Korea” showed 60 articles. In Research Information Sharing Service (https://www-riss-kr-ssl.openlink.inha.ac.kr/index.do), “bioterrorism” showed 92 domestic papers. The title and abstracts were reviewed and papers about the basics or principles of bioterrorism or related to ‘Korea’ were selected.

Critical elements of bioterrorism

The four critical elements of bioterrorism include the biological agent, the weaponization of the agent, the delivery system, and the impact of weather conditions on the attack.

• 1. Biological agents: Biological agents used in bioterrorism include bacteria, viruses, or toxins that can lead to severe illness or death. Examples include anthrax (Bacillus anthracis), smallpox (variola virus), and botulinum toxin. These agents are selected for their lethality, ease of production, and potential to spread.

• 2. Weaponizing a biological agent: Weaponizing a biological agent involves processing it to enhance its delivery and effectiveness. Techniques may include increasing the agent's environmental stability, creating fine particles for aerosolization, or incorporating it into devices designed for efficient dispersion. For instance, converting a liquid culture into a dry powder can improve the dispersibility of the agent, facilitating its delivery over a wider area.

• 3. The delivery system of a biological agent: The delivery system refers to the method by which the agent is dispersed to the target population. There are two primary strategies: point source and line source attacks. Point source attacks involve releasing the agent from a single location, such as through a building's ventilation system. In contrast, line source attacks distribute the agent along a trajectory, such as from a moving vehicle. The selection of the delivery method is influenced by various factors, including the target environment and the desired area of impact.

• 4. Weather conditions for biological attack: Weather conditions significantly influence the effectiveness of a biological attack. Factors such as wind speed and direction, temperature, and humidity can affect the spread and potency of the biological agent. For example, high winds might disperse the agent over a broader area but could also dilute its concentration. Conversely, stable, low-wind conditions might retain the agent in the target area for an extended period. Understanding these weather conditions is essential for both planning an effective attack and developing defenses to mitigate its impact [3,4].

Infection mechanisms in bioterrorism

Bioterrorism involves the intentional release of biological agents such as bacteria, viruses, or toxins, aiming to cause illness or death in humans, animals, or plants. These agents utilize natural infection mechanisms to propagate and inflict damage. The infection routes for biological agents in bioterrorism include inhalation, ingestion, dermal exposure, and injection. Understanding how these agents can be weaponized underscores the necessity for comprehensive public health and safety strategies to identify and counter potential bioterrorism threats.

• 1. Inhalation: Numerous biological agents, including B. anthracis, the bacterium responsible for anthrax, are highly effective when aerosolized. When these aerosols are inhaled, the pathogens can enter the respiratory tract and then disseminate to other body parts, leading to severe respiratory problems or systemic infections.

• 2. Ingestion: Another method involves contaminating food and water supplies with biological agents. For instance, ingesting Salmonella or Escherichia coli can lead to foodborne illnesses, causing gastrointestinal distress and potentially severe systemic infections.

• 3. Dermal exposure: Certain biological agents can infect individuals through skin contact. This may happen through direct contact with contaminated surfaces or via vectors such as insects. For example, agents such as smallpox can be transmitted through skin contact with infectious lesions.

• 4. Injection: While less common, biological agents can be directly introduced into the bloodstream through injection, bypassing other bodily defenses. This introduction can occur via contaminated needles or through insect vectors [5].

Capability of North Korea’s biological warfare and threats

Decades of open source information affirm that North Korea has held an interest in developing a bioweapons program. Although the lack of recent and reliable public information prevents a comprehensive assessment of its current capability, threats posed by North Korea’s biological weapons (BW) program must be considered a realistic proposition and addressed by the international community. Several reports have construed the types of biological agents North Korea may possess, the state of weaponization of these agents, and the means through which North Korea might deliver them [6].

The potential agents under development could include anthrax, smallpox, plague, and botulinum toxin, which might be deployed using missiles, artillery shells, or through covert operations. Intelligence reports from the United States (US) and South Korea have periodically indicated the presence of a BW program in North Korea. However, these assessments often rely on limited and indirect evidence. Occasionally, accounts from North Korean defectors have shed light on the existence of BW research facilities and the possible weaponization of biological agents [7].

Potential threat to South Korea: South Korea's proximity to North Korea significantly increases its vulnerability to biological attacks. North Korea has the capability to deploy biological agents through missiles, drones, or covert operatives. Possible methods include contaminating water supplies, food sources, or densely populated areas. Such attacks could target both military bases and civilian populations in South Korea, causing widespread disruption and high casualty rates. Additionally, the mere threat of biological attacks can instill fear and panic, adversely affecting public morale and the economy. A biological attack could result in substantial economic losses, disrupt trade, and overburden public health systems. Furthermore, any deployment of BW by North Korea could destabilize the region, potentially leading to increased military conflicts and international interventions.

History of weaponized balloons; "Balloon bomb" by Japanese during the World War II

During the World War II, Japanese unit 731 looked into using balloons to spread germs. This was especially significant, because large balloons were developed and used to attack the US. During 1944–45 the Japanese launched paper balloons carrying incendiary bombs to set fires in US forests. The balloons were blown eastward from Japan at altitudes of 30,000 to 50,000 feet at speeds of 20 to 150 knots, and reached the US and Canada from three to five days after launching. A total of around 9,300 of these incendiary balloons were launched, although only a few successfully made the 6,200-mile Pacific crossing to the northwestern US. US Army specialists were concerned that the balloons were in fact carrying germs, but none of Ishii’s biological agents was used [8].

Shiro Ishii’s (Japanese biologist) biological warfare agents were used against China. On 4 October 1940, a lone Japanese plane circled over the town of Chuhsien in Chekiang Province and scattered rice and wheat grains believed to be flea-infected. A number of townspeople took ill, and 23 died of a plague-type illness. Three weeks later, there was another release of infected wheat grain over the port of Ningpo, and 99 persons succumbed to plague. In a third incident, on 4 November 1941, a lone plane over Changteh in Hunan Province released wheat and rice grains, as well as pieces of paper and cotton that, upon scientific examination, appeared to have been infected [9].

Possible BW deliverable using packages attached to balloons and their antidotes

Anthrax, smallpox, plague, and botulinum toxin could theoretically be delivered using packages attached to balloons. However, there are significant technical and logistical challenges associated with this delivery method.

Anthrax (B. anthracis): Anthrax spores are relatively hardy and can be dispersed as an aerosol. Balloons could potentially carry packages that release anthrax spores into the air. Ensuring effective dispersion and achieving a concentration sufficient to cause infection over a target area would be technically challenging. Weather conditions such as wind and humidity would also affect the distribution and viability of the spores.

Effective antibiotics for treating anthrax include ciprofloxacin, doxycycline, and penicillin. It is critical to initiate treatment early to ensure its effectiveness. For cases of inhalational anthrax, antitoxins such as raxibacumab and obiltoxaximab may be administered in conjunction with antibiotics to neutralize the bacteria's toxins. The anthrax vaccine, known as Anthrax Vaccine Adsorbed, is primarily used for pre-exposure prophylaxis among military personnel and other high-risk groups.

Smallpox (variola virus): The smallpox virus can be aerosolized, though it is less stable in the environment than anthrax spores. Smallpox is both highly infectious and lethal; however, the virus is sensitive to environmental factors such as UV light, temperature, and humidity. Any balloon delivery system would need to maintain the viability of the virus during transport and release.

Tecovirimat and cidofovir are antiviral medications used to treat smallpox. Brincidofovir is another potential treatment option. The vaccinia virus vaccine is effective in preventing smallpox when administered before exposure or within a few days following exposure. Additionally, the vaccine can reduce the severity of the disease if administered shortly after exposure.

Plague (Yersinia pestis): The bacterium responsible for plague can be weaponized in its pneumonic form, which is both highly contagious and deadly. Y. pestis is sensitive to environmental conditions, making it difficult to ensure the bacterium remains viable during transport and release. Additionally, effectively dispersing it as an aerosol from a balloon package would be challenging and may not achieve the desired infection rate.

Streptomycin, gentamicin, doxycycline, and ciprofloxacin are effective antibiotics for treating plague. It is critical to administer these drugs promptly, particularly in cases of pneumonic plague. In severe instances, patients may require respiratory support along with other supportive measures. Although there is currently no widely available vaccine for plague, research efforts continue. Prophylactic antibiotics may be administered to individuals exposed to Y. pestis.

Botulinum toxin: Botulinum toxin is among the most potent toxins known and can be administered as an aerosol. Although the toxin itself is highly potent, delivering it effectively would necessitate precise control over both dosage and dispersion to impact a large area. Additionally, environmental conditions could significantly influence its stability and effectiveness.

Botulinum antitoxin, derived from equine sources, can neutralize circulating toxins in the body if administered early. The heptavalent botulinum antitoxin is effective against all known serotypes of botulinum neurotoxin. Intensive care support, including mechanical ventilation, may be necessary for patients experiencing severe respiratory muscle paralysis. In cases of wound botulism, surgical removal of the source of toxin production and antibiotic therapy are crucial [10].

The effective delivery of agents would necessitate sophisticated mechanisms to aerosolize them and ensure their dispersion over the target area. This requirement would increase the complexity of the balloon packages. Given their slow movement, balloons can be easily detected and intercepted by contemporary air defense systems. Therefore, employing balloons for delivery might be perceived as a low-tech approach, diminishing its appeal for advanced biological warfare. Additionally, balloons do not offer the precise control provided by other delivery methods such as missiles or drones, making the achievement of a desired impact on a specific target area uncertain.

While it is theoretically possible to deliver biological agents like anthrax, smallpox, plague, and botulinum toxin using packages attached to balloons, this method presents significant technical and logistical challenges. Factors including environmental conditions, dispersion mechanisms, detection, and interception must all be considered. More sophisticated and reliable delivery methods would likely be preferred for the deployment of BW.

Minimizing the impact of a bioterrorism event

Minimizing the impact of a bioterrorism event requires a coordinated response strategy that includes four key actions: detection, decision-making, distribution, and dispensation. By integrating these steps, authorities can effectively manage and mitigate the effects of a bioterrorism event, thereby protecting public health and safety.

• 1. Detection: Early detection of a bioterrorism event is crucial for minimizing its impact. This involves utilizing advanced biosurveillance systems and technologies to monitor unusual disease patterns or outbreaks. Rapid identification of biological agents through laboratory testing and field detection devices is essential for recognizing an attack.

• 2. Decision-making: Once a potential bioterrorism event is detected, swift and informed decision-making is crucial. This process involves analyzing the detected data to confirm the presence of a biological agent, assessing the potential spread and impact, and determining the appropriate response. Decision-making frameworks and models, supported by real-time data and expert consultation, assist in planning the response actions. It is vital to maintain clear communication channels between public health officials, government agencies, and emergency responders to ensure coordinated efforts.

• 3. Distribution: Effective distribution of resources and information is critical during a bioterrorism response. This involves distributing medical supplies, vaccines, and antidotes to affected areas. Effective logistics planning ensures that these resources are available where and when they are needed. Distribution strategies also include deploying response teams and establishing communication networks to disseminate information to the public and healthcare providers. Additionally, the use of technology, such as Geographic Information Systems, aids in mapping the spread of the threat and optimizing resource allocation.

• 4. Dispensation: Dispensing medical countermeasures to the affected population represents the final step in the process. This requires the establishment of mass vaccination or medication dispensing sites, proper administration of treatments, and monitoring of intervention effectiveness. Public health campaigns and community engagement play vital roles in ensuring adherence to prescribed medical advice. Additionally, training and drills for healthcare providers and volunteers are essential for efficient dispensing operations.

Preparedness of South Korea against possible bioterrorism by North Korea

Efforts to counter and neutralize North Korea’s BW threats should be led by South Korea and the US. Strategies for counter-measures should include military and “dual-response” public health preparations, as well as formal and informal efforts to engage North Korea in biological fields. Overall, the goal of the international community should be to simultaneously gather more information about North Korea’s BW capability and reduce this threat posed by North Korea [6].

Following the Anthrax bioterrorism attacks in the US in 2001, the Korean government established comprehensive countermeasures against bioterrorism. These measures included the government assuming management of all infectious agents that cause diseases, including smallpox, anthrax, plaque, botulism, and the causative agents of viral hemorrhagic fevers (ebola fever, marburg fever, and lassa fever) for national security. In addition, the South Korean government is reinforcing the ability to prepare and respond to bioterrorism [11].

The South Korean government is actively preparing for the possibility of biological terrorism, including potential threats from North Korea. This preparation involves multiple strategies and measures aimed at ensuring the country is equipped to detect, respond to, and mitigate the effects of biological attacks. Below are some of the key aspects of South Korea's preparedness:

For the detection of bioterrorism, South Korea has developed and implemented advanced surveillance systems to quickly identify biological threats. These systems monitor disease outbreaks and unusual health patterns that could signal a biological attack. They integrate nationwide networks, connecting hospitals, laboratories, and public health agencies to facilitate rapid reporting and information sharing.

Regarding medical countermeasures, the South Korean government maintains strategic stockpiles of antibiotics, antivirals, antitoxins, and vaccines. These stockpiles are regularly updated to ensure they are sufficient and effective against potential biological agents such as anthrax, smallpox, plague, and botulinum toxin. Additionally, prophylactic vaccinations are provided for military personnel and first responders against certain biological threats. For instance, vaccines for anthrax and smallpox may be administered to high-risk groups.

Role of civilian medical doctors and the need for education

Civilian doctors play a vital role in the early detection, diagnosis, treatment, and management of biological agents. Consequently, educating these medical professionals is crucial for preparing against potential biological warfare or bioterrorism threats from North Korea. Their responsibilities include early detection and diagnosis, effective treatment and management, prevention of secondary transmission, and collaboration with public health authorities.

• 1. Early detection and diagnosis: Many biological agents initially manifest with nonspecific symptoms that resemble those of common illnesses. It is crucial to educate doctors about the specific clinical presentations of agents such as anthrax, smallpox, plague, and botulinum toxin.

• 2. Effective treatment and management: Knowledge of appropriate treatments— such as antibiotics for anthrax and plague, antivirals for smallpox, and antitoxins for botulinum toxin—is crucial for effective patient care. Additionally, training in necessary supportive care is essential, including providing respiratory support for botulism and implementing isolation procedures for highly contagious diseases.

• 3. Preventing secondary transmission: The prevention of secondary transmission involves education on proper infection control measures to prevent the spread of infectious agents. It is also crucial to understand protocols for isolating (quarantine) patients and managing contacts to effectively contain outbreaks.

• 4. Public health collaboration: Civilian doctors must be aware of their roles in the broader public health response, including communication with public health officials and participating in surveillance efforts. Additionally, engaging in simulation exercises to practice responses to biological incidents is necessary.

Because the emergency department represents the front line of defense for the recognition of agents of bioterrorism, it is essential that emergency physicians have the ability to quickly diagnose victims of bioterrorism [10]. When South Korean clinicians happen to meet patients suspected as bioterrorism casualties, contact points are as follows:

• 1. Korea Disease Control and Prevention Agency. Tel: 1339 or +82-43-719-7997, E-mail: capitalkdca@korea.kr

• 2. National Disaster and Safety Status Control Center. Tel: +82-2-2100-5500 (5503), E-mail: mpss@korea.kr.

Discussion

Biological warfare involves the use of pathogens—bacteria, viruses, or other disease-causing organisms—or toxins produced by living organisms as weapons. These agents can be used to harm or kill humans, animals, or plants. While there are some early examples of biological warfare, it was first used for sabotage by Germany during World War I. The development of BW on a militarily significant scale began in several countries between the world wars. During World War II, countries including the US, United Kingdom (UK), Canada, Germany, Japan, and the Soviet Union had active BW programs. Of these, only Japan used biological warfare on a fairly large scale. Following the collapse of the Soviet Union, and under pressure from the US and UK, President Yeltsin issued a decree in 1992 that banned continued offensive biological warfare activities. Many questions about the biological warfare program remain unanswered [12]. Currently, more than a dozen nations, including Iraq, Iran, Libya, Syria, and North Korea, are either actively pursuing or already possess BW for use against their enemies [13].

South Korea has experienced over 30 suspected terrorism-related events since 1958, including attacks on its citizens in foreign countries. The most prevalent forms of terrorism have involved bombings, shootings, hijackings, and kidnappings. Before 1990, North Korea was responsible for nearly all terrorism-related incidents within South Korea, including multiple assassination attempts on its presidents, frequent kidnappings of South Korean fishermen, and several high-profile bombings. Since 1990, the majority of terrorist attacks targeting South Korean citizens have occurred overseas, aligning with the global rise of terrorism by international terrorist organizations or deranged individuals [14].

While the current use of trash balloons does not constitute bioterrorism, the situation underscores the need for continued vigilance and preparedness against potential escalations.

When biological agents such as B. anthracis (anthrax), Y. pestis (plague), or Francisella tularensis (tularemia) are employed in bioterrorism, stockpiled oral antibiotics are distributed. In the case of a smallpox virus attack, vaccines are deployed. These resources are collectively known as national strategic stockpiles. The high dispersal capability of BW means that a bioterrorism event could lead to a widespread distribution of patients and exposed individuals across various cities and provinces [15].

To ensure the survival of individuals who may have been exposed, it is crucial to implement pre-symptomatic preventive measures. Effective resource management strategies are necessary to ensure the safe transportation of medical supplies from storage facilities to regional health agencies and to administer these supplies efficiently to the affected populations. Establishing mass medication (vaccination) centers is vital. Although there are no stringent requirements for the location of these centers, ideal facilities should enable large numbers of people to quickly receive preventive measures. This involves setting up vaccine (antibiotic) storage rooms, educational consultation rooms, screening rooms, and vaccination (medication) rooms within the facility, as well as providing ample parking space. Schools and large gymnasiums often fulfill these requirements.

Once an appropriate facility has been designated, a diverse team of personnel is necessary to effectively carry out large-scale vaccinations or antibiotic distributions. This team should include healthcare providers such as doctors, nurses, and nursing assistants, as well as administrative staff responsible for managing and reporting on medications. Additionally, security personnel are needed to maintain facility security and manage parking, along with volunteers. Given the challenges of mobilizing personnel following a bioterrorism event, it is crucial to preemptively secure idle medical staff and volunteers.

From the perspective of a medical doctor, training civilian medical professionals is essential for preparing for potential biological warfare or bioterrorism threats from North Korea. By improving their knowledge and skills through specialized education and training programs, these doctors become pivotal in the early detection, effective treatment, and containment of biological threats. Such preparedness not only safeguards individual patients but also enhances the overall public health response, thereby reducing the effects of a possible bioterrorism incident.