BW-ch01.pdf

History of Biological Weapons: From Poisoned Darts to Intentional Epidemics

Chapter 1

HISTORY OF BIOLOGICAL WEAPONS:

FROM POISONED DARTS TO

INTENTIONAL EPIDEMICS

JAMES W. MARTIN, MD, FACP * ; GEORGE W. CHRISTOPHER, MD, FACP † ; and EDWARD M. EITZEN, JR, MD, MPH ‡

INTRODUCTION

EARLY ATTEMPTS

THE EARLY ERA OF MODERN MICROBIOLOGY AND THE WORLD WARS

THE US PROGRAM

KOREAN WAR AND COLD WAR ALLEGATIONS

DISARMAMENT

THE SOVIET PROGRAM

SOUTH AFRICA

THE SPECIAL CASE OF IRAQ

BIOLOGICAL TERRORISM

BIOCRIMES

SUMMARY

* Colonel, Medical Corps, US Army; Chief, Operational Medicine Department, US Army Medical Research Institute of Infectious Diseases, 1425 Porter

Street, Fort Detrick, Maryland 21702

† Lieutenant Colonel, Medical Corps, US Air Force; Discovery Biology Team Leader, Transformational Medical Technologies Initiative, Chemical-Biologi-

cal Medical Defense Division, Defense Threat Reduction Agency, 8725 John J. Kingman Road Stop 6201, Fort Belvoir, Virginia 22060; formerly, Chief,

Containment Care Department, US Army Medical Research Institute of Infectious Diseases, 1425 Porter Street, Fort Detrick, Maryland

‡ Senior Partner, Biodefense Programs, Edward Martin and Associates Consulting, 5309 North 1st Place, Arlington, Virginia 22203; formerly, Com-

mander, US Army Medical Research Institute of Infectious Diseases, 1425 Porter Street, Fort Detrick, Maryland

Medical Aspects of Biological Warfare

INTRODUCTION

Since prehistoric times, humans have used available

technologies for destructive and beneficial purposes.

Aboriginal use of curare and amphibian-derived tox-

ins as arrow poisons anticipated modern attempts to

weaponize biological toxins such as botulinum and

ricin. The derivation of the modern term “toxin” from

the ancient Greek term for arrow poison, τωξικον

φαρµακον (toxicon pharmicon; toxon = bow, arrow) ,

underscores the historical link between weaponry and

biological agents.

Multiple factors confound the study of the history

of biological weapons, including secrecy surrounding

biological weapons programs, difficulties confirming

allegations of biological attack, the lack of reliable

microbiological and epidemiological data regarding

alleged or attempted attacks, and the use of allegations

of biological attack for propaganda and hoaxes. How-

ever, a review of historical sources and recent events in

Iraq, Afghanistan, Great Britain, and the United States

demonstrates that interest in biological weapons by

state-sponsored programs, terrorist organizations, and

criminal elements is likely to continue.

EARLY ATTEMPTS

The early use of biological weapons included the

contamination of water with animal carcasses and filth.

Another ancient tactic was to allow an enemy to take

sanctuary in an area endemic for an infectious agent

in anticipation that the enemy force would become

infected, for example, allowing unimpeded access of

opposing forces to areas where transmission of malaria

was highly likely.

The Carthaginian leader, Hannibal, used early bio-

logical weapons (serpent toxins) in the naval battle of

the Eurymedon against King Eumenes of Pergamum

in 84 bce . Hannibal ordered earthen pots filled with

serpents to be hurled onto the decks of the Pergamene

ships. The pots shattered on impact, releasing live

serpents among the enemy sailors. The Carthagin-

ians exploited the ensuing panic and chaos to win

the battle. 3

One of the most notorious early biological war-

fare methods was the hurling of cadavers over the

walls of besieged cities, primarily as a terror tactic.

De Mussis provided a dramatic record of the use

of plague victims in biological warfare. 4,5 After war

broke out between the Genoese and the Mongols in

343 for control of the lucrative caravan trade route

from the Black Sea to the Orient, the Mongols laid

siege to Caffa, a Genoese colony in the Crimea. The

plague, later known as the Black Death, was spread-

ing from the Far East and reached the Crimea in 346.

The Mongols were severely afflicted and forced to lift

their siege. As a parting shot, they hurled “mountains

of dead” over the city wall, probably with the use of

a trebuchet, in the hope that “the intolerable stench

would kill everyone inside.” An outbreak of plague in

the city followed. A review of the incident by Wheelis 5

suggests that the introduction of plague into the city

by the cadavers—as a result of a tactically successful

biological attack—is the most biologically plausible

of several competing hypotheses on the source of the

outbreak. Although historically the predominant mode

of human plague transmission has been attributed to

bites from infected fleas, modern experience (United

States 970–995) 6 has implicated direct transmission

from contact with infected (animal) carcasses in 0%

of instances in which the source of the infection could

be attributed epidemiologically. Contact with tissue

and blood would have been inevitable during the

disposal of hundreds or possibly thousands of cadav-

ers that had been smashed on impact. Typically, rats

are sedentary and rarely venture far from their nests;

it is unlikely that they would have traversed an open

distance of several hundred meters between the Mon-

gol front line and the city walls. 5 Transmission from

sylvatic to urban rodents is infrequent, at least under

current ecological conditions. 7 Alternatively, plague

could have been introduced by imported human cases

or infected rodents brought into the city through the

maritime trade, which was maintained during the

siege. Regardless of the portal of entry, the epidemic

was likely amplified by an increase in the population

of rats and fleas under siege conditions.

Smallpox was particularly devastating to Native

Americans. The unintentional yet catastrophic in-

troduction of smallpox to the Aztec empire during

the Narváez expedition of 50, and its subsequent

spread to Peru in advance of Pizarro’s invasion of

the Inca empire, played a major role in the conquest

of both empires. 8 At the conclusion of the French and

Indian War in 763, the Native Americans conducted a

series of attacks against British forts along the western

frontier in what is known as Pontiac’s Rebellion. An

outbreak of smallpox at Fort Pitt presented an op-

portunity to take advantage of the Native Americans’

unique susceptibility to this disease. 9 On May 4, 763,

William Trent, the local militia leader, wrote of the

actions of Captain Ecuyer, the Fort Pitt commander:

“We gave them two Blankets and a Handkerchief from

History of Biological Weapons: From Poisoned Darts to Intentional Epidemics

the Smallpox Hospital. I hope it will have the desired

effect.” 0, Subsequently (in July 763), Sir Jeffrey Am-

herst, British commander of forces in the American

colonies, conceptualized a similar plan with Colonel

Henry Bouquet, apparently unaware of the actions

at Fort Pitt, thus sanctioning the concept of use of

smallpox as a biological weapon. ,3 An epidemic of

smallpox occurred among the Native Americans of the

Ohio River Valley that year. In retrospect, it is difficult

to evaluate the tactical success of Captain Ecuyer’s

biological attack because smallpox may have been

transmitted after other contacts with colonists, as had

previously happened in New England and the South.

Although scabs from smallpox patients are thought

to be of low infectivity as a result of binding of the

virus in fibrin matrix, and transmission by fomites has

been considered inefficient compared with respiratory

droplet transmission. 8

THE EARLY ERA OF MODERN MICROBIOLOGY AND THE WORLD WARS

The birth of scientific bacteriology during the 9th

century provided the scientific and technical basis for

modern biological weapons programs. The Hague

Conventions of 899 and 904 outlawed the use of

“poison or poisoned arms,” although the possible

use of bacteriological weapons was not specifically

identified or addressed. 4,5 Germany started the first

known scientific, state-sponsored biological weapons

program during World War I. 6 German espionage

agents reportedly undertook a covert biological cam-

paign in the United States before the United States

entered the war. The Allies had purchased US draft

animals for military use, and German operatives in-

fected these animals with glanders and anthrax while

they were awaiting shipment overseas. 7 The Germans

also conducted similar operations in Romania, Russia,

Norway, Mesopotamia, and Argentina, with varying

levels of success. Attempts were also made to cripple

grain production in Spain with wheat fungus, but

without success. 8

The German biowarfare program of World War I is

of special interest for several reasons: it was the first

national offensive program, the first program to have

a scientific foundation, and the first confirmed instance

of actual wartime use of biological agents. The German

program was a large-scale (strategic) biological attack,

which targeted neutrals rather than belligerents and

targeted crops and animals as opposed to humans.

It is impossible to determine the effectiveness of this

program; although the German operatives involved

thought it was a success, no documentary evidence

supports this conclusion.

In response to chemical warfare during World War

I, the 95 Geneva Protocol, an international protocol

(for the Prohibition of the Use in War of Asphyxiat-

ing, Poisonous or Other Gases, and of Bacteriological

Methods of Warfare), was formulated. The protocol,

developed by the League of Nations’ Conference for

the Supervision of the International Trade in Arms

and Ammunition, addressed warfare methods of na-

tion-states only. It had no verification mechanism and

relied on voluntary compliance. Many of the original

signatory states reserved the right to retaliatory use,

making it effectively a no first-use protocol. Signatories

that began basic research programs to develop bio-

logical weapons between World War I and II included

Belgium, Canada, France, Great Britain, Italy, The

Netherlands, Poland, and the Soviet Union. 9

After the Japanese defeat of Russia in the 905

Russo-Japanese War, Japan became the dominant

foreign power in Manchuria. The Kwantung Army

was created to maintain Japanese economic interests

in the region. During the 5 months from September

93 to the end of 93, the Japanese military seized

full control of Manchuria. In 93 Major Shiro Ishii, a

Japanese army physician with an established interest

in biological agents, came to Harbin to conduct hu-

man research. He established his initial laboratory in

the industrial sector of Harbin known as the Nangang

District, but soon realized that his controversial invol-

untary human research could not be conducted freely

there. Ishii moved to a secret facility at Beiyinhe, 00

km south of Harbin, and began experimenting on a

more dramatic scale. No research study subjects sur-

vived; all died of either experimental infection or live

vivisection. These studies continued until a prisoner

riot and escape occurred, which resulted in the clos-

ing of the facility in 937. However, larger and more

extensive facilities were subsequently built. 9

In August 936 Ishii, now promoted to Lieutenant

Colonel, was made chief of the Kwantung Army water

purification bureau. That autumn the Japanese ap-

propriated 6 km of farmland 4 km south of Harbin,

which encompassed 0 villages and displaced 600

families from their ancestral homes. There Ishii built

the massive research facility known as Unit 73, where

a census of 00 prisoners was kept as expendable sub-

jects of experimentation. Ultimately, more than 3,000

Chinese prisoners were killed and cremated after these

experiments. Most of the evidence was destroyed at the

end of the war, and in all likelihood the actual number

was much greater. 9

Major Wakamatsu Yujiro, a less flamboyant but

equally ruthless veterinary officer, ran the Unit 00

Medical Aspects of Biological Warfare

facility at Changchun. In 936 Japan appropriated

0 km of land near Mokotan, a small village just

6 km south of Changchun, the capital of Japanese-

occupied Manchuria. Predominantly a veterinary and

agricultural biowarfare research unit (independent

from Ishii’s Unit 73), Unit 00 focused on developing

biological weapons for sabotage operations. Although

animals and crops were the focus of most of the re-

search, numerous human studies were also conducted,

similar to those conducted by Unit 73. 9

In April 939 a third major research facility, Unit Ei

644, was established in an existing Chinese hospital

in Nanking, under the command of one of Ishii’s

lieutenants, Lieutenant Colonel Masuda. Prisoners,

including women and children, became the subjects of

grisly experimentation, and were cremated in the camp

incinerator usually late at night. Chemical warfare

experiments were conducted in a gas chamber with

an observation window. Unit Ei 644 supported Unit

73’s research efforts with bacterial agent production

and flea cultivation. 9

Eleven Chinese cities were allegedly attacked dur-

ing “field trials” using infectious agents including

Yersinia pestis , Vibrio cholerae , and Shigella . These attacks

may have backfired because up to 0,000 Japanese sol-

diers reportedly contracted cholera after a biological

attack on Changde in 94. 0 As a result of the Japanese

biowarfare program, 580,000 people are estimated to

have died in China. The field trials were terminated in

943, yet basic research and human experimentation

at Unit 73 and elsewhere continued until the end of

the war. 9,

Vaccine research and development was conducted

at both Tokyo University and Unit 73. By the end of

the war, the Japanese biowarfare program claimed to

have effective vaccines for anthrax, cholera, dysentery,

typhoid, and typhus. Unit 73 reportedly produced 0

million doses of vaccine per year, with millions more

doses produced at satellite facilities in Manchuria and

other parts of China. Use of biological warfare agents

by Japanese forces may have given them an advantage

over the Chinese, but results were erratic and prone to

backfire. Despite the enormously expensive program

(both in terms of national treasure and human lives)

and the weaponization of many agents, Japan never

developed a credible biowarfare capability, mainly

because of the failure to develop an effective delivery

system.

In contrast to Japanese efforts during World War II,

a German offensive biological weapons program never

materialized. Studies of experimental infections using

prisoners were done primarily to study pathogenesis

and develop vaccines and sulfonamide antibiotics,

rather than to develop biological weapons. Hitler re-

portedly issued orders prohibiting biological weapons

development. With the support of high-ranking Nazi

party officials, however, German scientists began bio-

logical weapons research, but their results lagged far

behind those of other countries.

Polish physicians used a vaccine and a serologic

test during World War II in a brilliant example of

“biological defense.” Knowing that inoculation with

killed Proteus OX-9 would cause a false-positive

Weil-Felix typhus test, Polish physicians inoculated the

local population with a preparation of formalin-killed

Proteus OX-9 to create a serologic pseudoepidemic

of typhus. Using serologic surveillance, the German

army avoided areas that appeared to contain epidemic

typhus; consequently, residents of these areas were

spared deportation to concentration camps. 3 Several

reported but unconfirmed allegations indicate that

Polish resistance fighters conducted biological warfare

against Nazi occupation forces, including using letters

contaminated with Bacillus anthracis to cause cases of

cutaneous anthrax among Gestapo officials 8,4 and

using typhus against German soldiers. 8,5 Czechoslo-

vakian agents reportedly used a grenade contaminated

with botulinum toxin, supplied by British Special

Operations, to assassinate Reinhard Heydrich, the

Nazi governor of occupied Czechoslovakia 6 ; how-

ever, the veracity of this reported incident has been

challenged. 8

The perceived threat of biological warfare before

World War II prompted Great Britain to stockpile

vaccines and antisera, establish an emergency public

health laboratory system, and develop offensive bio-

logical weapons. “Cattle cakes” consisting of cattle feed

contaminated with B anthracis spores were designed to

be dropped from aircraft into Axis-occupied Europe

to cause epizootic anthrax among livestock, 7,8 which

would in turn induce famine. The cattle cakes were

intended as a strategic economic weapon rather than

as a direct cause of human anthrax. In addition, ex-

plosive munitions designed to aerosolize and disperse

B anthracis spores as an antipersonnel weapon were

tested on Gruinard Island near the coast of Scotland

in 94. These experiments successfully produced

anthrax among targeted sheep. 9 The island was

quarantined because of focal soil contamination by

B anthracis spores. The antipersonnel weapons were

not mass produced, and neither the cattle cakes nor

the explosive munitions were used. 6 Great Britain

continued research and development after the war in

conjunction with the United States and Canada and

performed secret open-air tests using pathogens in

open ocean near the Bahamas and Scotland in 948,

95, 953, 954, and 955. Simulant studies were

performed off the coast of the United Kingdom in

History of Biological Weapons: From Poisoned Darts to Intentional Epidemics

957, 958, 964, and 965. 6 Great Britain’s offensive

program was ultimately terminated between 955

and 956 30 because of budgetary constraints and reli-

ance on nuclear deterrence. 7,8 Gruinard Island was

decontaminated in 986 using ,000 tons of seawater

and 80 tons of formaldehyde. 3

THE US PROGRAM

The US military recognized biological warfare as

a potential threat after World War I. Major Leon Fox

of the Army Medical Corps wrote an extensive report

concluding that improvements in health and sanitation

made biological weapons unfeasible and ineffective. In

the fall of 94, before the US entry into World War II,

opinions differed about the threat of biological warfare.

Consequently, the secretary of war asked the National

Academy of Sciences to appoint a committee to study

the issue. The committee concluded in February 94

that biowarfare was feasible and that the United States

should reduce its vulnerability.

President Roosevelt established the War Reserve

Service (with George W Merck as director) to de-

velop defensive measures against a biological attack.

By November 94 the War Reserve Service asked

the Army’s Chemical Warfare Service to assume

responsibility for a secret large-scale research and

development program, including the construction

and operation of laboratories and pilot plants. The

Army selected a small National Guard airfield at

Camp Detrick in Frederick, Maryland, for the new

facilities in April 943. By summer of 944, the Army

had testing facilities in Horn Island, Mississippi (later

moved to Dugway, Utah), and a production facility in

Terre Haute, Indiana. Cattle cakes using B anthracis

spores were produced at Camp Detrick and shipped

to Great Britain but were never used. No agents were

produced at the Terre Haute plant because of safety

concerns; simulant tests had disclosed contamination

after trial runs. The War Reserve Service was dis-

banded after the war, and the Terre Haute plant was

leased for commercial pharmaceutical production. 6

In January 946 Merck reported to the secretary of

war that although the focus of the program was to

defend against a biological threat, the United States

clearly needed a credible capability to retaliate if at-

tacked with biological weapons. Basic research and

development continued at Camp Detrick.

The United States learned of the extent of Japanese

biological weapons research after World War II. At

the end of the war, in a move that has now become

controversial, Ishii, then a lieutenant general, and his

fellow scientists were given amnesty for providing

information derived from years of biological warfare

research. 9

When war broke out on the Korean peninsula in

June 950, concerns about Soviet biological weapons

development and the possibility that the North Kore-

ans, Chinese, or the Soviets might resort to biological

warfare resulted in expansion of the US program. A

large-scale production facility in Pine Bluff, Arkansas,

was established. The new plant featured advanced

laboratory safety and engineering measures enabling

large-scale fermentation, concentration, storage, and

weaponization of microorganisms. In 95, the first

biological weapons, anticrop bombs, were produced.

The first antipersonnel munitions were produced in

954, using Brucella suis . The United States weapon-

ized seven antipersonnel agents and stockpiled three

anticrop agents (see Table -) in 6 years. 3 However,

the US military has never used biological weapons. The

Central Intelligence Agency developed weapons using

toxins including cobra venom and saxitoxin for covert

operations; all records regarding their development

and deployment were destroyed in 97. 33

Field tests were done in the United States between

949 and 968, in which the general public and test sub-

jects were uninformed. At least 39 open-air tests were

conducted at several locations including the Dugway

TABLE 1-1

BIOLOGICAL AGENTS PRODUCED BY THE US MILITARY (DESTROYED 1971–1973) *

Lethal Agents

Incapacitating Agents

Anticrop Agents

Bacillus anthracis

Brucella suis

Rice blast

Francisella tularensis

Coxiella burnetii

Rye stem rust

Botulinum toxin

Venezuelan equine encephalitis virus

Wheat stem rust

Staphylococcal enterotoxin B

* Lethal and incapacitating agents were produced and weaponized. Anticrop agents were produced but not weaponized.

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