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Mandell: Mandell, Douglas, and Bennett's Principles and Practice of Infectious

Diseases, 7th ed.
Copyright © 2009 Churchill Livingstone, An Imprint of Elsevier

14 – Outbreak Investigation
ANDRES G. LESCANO,
JOEL M. MONTGOMERY ,
DAVID L. BLAZES *
* All material in this chapter is in the public domain, with the exception of any borrowed figures or tables.

“Vulnerability is universal.” [1] Outbreaks of infectious disease can arise anywhere in the world and pose a
threat to local and global populations without respect for political borders, geographic separation, or cultural
differences. Many current conditions facilitate this potential for the rapid spread of infectious diseases,
including the globalization of the food supply, overuse of antibiotics, the growth of mega-cities with severe
crowding, our increasing proximity to animals and vectors of disease, and even climate change. [2] [3]

Recently, there have been numerous examples of outbreaks that have seized the public's attention. The
severe acute respiratory syndrome (SARS) epidemic of 2003, the recent resurgence of measles in North
America and Europe, and multiple outbreaks of imported food-borne gastroenteritis due to Cyclospora and
Salmonella are cases in point. [4] [5] The scope and potential impact of these outbreaks underscore the
importance of maintaining an informed cadre of astute clinicians who understand the dynamics of an
outbreak and how to investigate one. This chapter describes the key concepts involved in an outbreak
investigation, discusses basic transmission dynamics, and provides a short primer for conducting an outbreak
investigation.

Definitions

OUTBREAK, EPIDEMIC, AND PANDEMIC

An outbreak is an increase beyond expectation in the number of cases of a disease or condition occurring
among a specified population, in a well-defined geographic location and period of time. [6 ] Cases are
epidemiologically related, although this linkage is often not initially evident and may only be discovered after
thorough investigation. For example, in the 1981 multistate outbreak of Salmonella muenchen, the
epidemiologic link was discovered only when case patients reported smoking marijuana more frequently than
controls, and this rare Salmonella species was isolated from marijuana samples from the homes of cases. [7]

Outbreaks very often have an infectious origin, although some can be due to noninfectious agents, such as
food intoxication or even hysteria. It is often difficult to define how many cases beyond expectation
constitutes an outbreak, but even one case can indicate an outbreak if the disease has been eradicated
(smallpox) or eliminated (poliomyelitis in Europe), or is novel to humans (highly pathogenic [H5N1] avian
influenza in the Americas).

In the absence of timely control measures, outbreaks can spread and lead to epidemics or even pandemics.
Epidemics are conceptually identical to outbreaks but are more widely disseminated in time and space, such
as the cholera epidemic in London during the mid-1800s and SARS in southeast Asia. Pandemics, on the
other hand, spread globally and may persist through months, years, or decades; these include such historic
scourges as bubonic plague in the Middle Ages, influenza in 1918 and 1919, and acquired immunodeficiency
syndrome (AIDS) in the 20th and 21st centuries.

ENDEMIC VERSUS EPIDEMIC

Many infectious diseases are endemic in certain settings and occur regularly; malaria, dengue, and diarrheal
disease due to enteropathogens in the tropics are examples. Endemicity does not preclude the occurrence of
outbreaks, however, which may occur during point-source foodborne outbreaks when large pools of
susceptible individuals are exposed at a single time. Vibrio parahaemolyticus and norovirus, for example, are

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endemic causes of sporadic gastroenteritis but can also lead to outbreaks when contaminated seafood is
eaten raw. Often all that is required for an outbreak is a sufficiently large, naive population exposed to an
infectious inoculum of the agent.

Surveillance: Outbreak Detection

Outbreaks are typically identified through routine surveillance or by an astute clinician or laboratory.
Surveillance for infectious diseases can take many forms, but generally entails the continuous and systematic
collection and analysis of data, as well as the subsequent reporting of the significant findings—in this case,
the presence of an outbreak. Surveillance can be either active or passive and may collect data on incident or
prevalent cases, or both. Active surveillance is usually more sensitive for discovering an outbreak, but is
more costly and labor intensive. Passive surveillance is often less sensitive, but also less costly and thus can
be deployed on a broader scale.

Surveillance systems in the United States often follow a hierarchical reporting scheme, with local clinics,
hospitals, or laboratories tabulating cases and reporting to the local public health authorities. They then pass
collated data to the state-level public health officials, who in turn report to the Centers for Disease Control
and Prevention (CDC), and eventually to the World Health Organization (WHO), if necessary, for outbreaks of
potential global significance. Reports of outbreaks are updated by the CDC on EPi-X, a secure web-based
reporting system limited to public health officials, as well as in the Morbidity and Mortality Weekly Report
(MMWR ), available to the public electronically at http://www.cdc.gov/mmwr/ and in hard copy.

Some sentinel surveillance systems attempt to identify specific diseases using representative sites. For
example, the CDC's FoodNet monitors 7 sites for gastroenteritis, covering over 20 million people (about 8%)
in the United States. [8] This system has identified many outbreaks of gastrointestinal infections, such as the
2006 to 2007 multistate outbreak of Salmonella serotype Tennessee associated with peanut butter
consumption. [9]

Syndromic surveillance aims to identify unusual or novel diseases by monitoring for general clinical
syndromes, such as febrile pneumonia. In response to the intentional anthrax outbreak of 2001, syndromic
surveillance was intensified in the United States with the goal of rapidly identifying clusters of illness
compatible with a biowarfare attack to minimize loss of life. The BioSense system, among others, was thus
deployed and continues to be used around the country. [10]

Novel methods of outbreak surveillance are continuously being developed and refined. Some reporting
systems, like ProMED mail, have been functioning since the 1990s and rely on a network of health care
professionals and other interested parties (over 20,000 subscribers in 160 countries) to report outbreaks from
around the world. This e-mail- and web-based system covers outbreaks affecting humans, animals, and
plants, and is moderated by a panel of public health experts who screen each report before it is released.
Other new systems, like HealthMap (http://www.healthmap.org/en ), harness the broad reach of the
Internet by searching online news outlets and applying automated logic to sort “real” outbreaks from rumor.
[11] The CDC and the Infectious Diseases Society of America collaborate on the Emerging Infections

Network, an e-mail-based list-serv that connects practicing infectious diseases physicians from around the
world. The GeoSentinel Surveillance System (http://www.istm.org/geosentinel/main.html ) is a worldwide
network of travel medicine clinics that reports illnesses among travelers. [12]

Perhaps the most important type of surveillance for outbreaks remains the astute and vigilant clinician or
laboratorian. The first case of SARS was identified by a physician in Hanoi, Vietnam, who noticed an
unusually severe, atypical pneumonia. [13] [14] The first cases of AIDS were identified by a clinician who noted
unusual infections among a group of homosexual men. West Nile virus in New York City was also noted by
an astute clinician, in this case a veterinarian who noticed a die-off of birds. Furthermore, it is important for
clinicians to understand that they as individual providers may be seeing only the proverbial tip of the iceberg,
and that an outbreak may only be appreciated when cases are examined in aggregate.

Outbreak Epidemiology

GENERAL

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The methodology for conducting outbreak investigations [15] [16] and the study designs and methods used
have been well described in the literature. [17] [18] The scarcity of general descriptions of the epidemiology of
outbreaks is partially due to the heterogeneity of transmission mechanisms, the wide range of disease
agents, and the diverse situations that lead to outbreaks. Reviews of published outbreaks suggest that
foodborne transmission accounts for nearly half of all outbreaks reported. Myriad agents were identified as
potential causes, but none was predominant. [19] Most efforts to improve the standardized reporting of
outbreaks have been focused on either foodborne disease [20] or nosocomial infections. [21 ]

FOODBORNE OUTBREAKS

In the United States, 1247 foodborne outbreaks were reported to the CDC in 2006 and affected 25,659
people, for an incidence of 8.6 per 100,000 people. [22] As a reference, only 39 waterborne outbreaks were
detected in a similar time frame, 1999 to 2000. [23] The etiologic agent was identified in half of foodborne
outbreaks, and 91% of them were caused by an infectious agent, mainly viruses (54%) or bacteria (36%).
Nearly all outbreak-causing foodborne viruses were norovirus, and 52% of the bacterial causes were
Salmonella species. Between 1998 and 2002, Listeria monocytogenes accounted for most deaths, and the
proportion of outbreaks associated with viruses increased from 16% to 42%. [23] Surveillance of foodborne
outbreaks is currently conducted across Europe and in a few developing countries.

The primary factor leading to foodborne outbreaks is temperature mismanagement while preparing, cooking,
or storing food. [20] If food workers were involved, the outbreak was often associated with a single, nongloved
worker who handled the implicated food, or fecally contaminated foods that were improperly refrigerated. [24]

NOSOCOMIALLY TRANSMITTED OUTBREAKS

Outbreaks in hospital settings often benefit from better infrastructure for diagnosis and investigation.
Extensive work on infection control has led to the publication of the ORION guidelines for reporting
nosocomial outbreaks. [21] An analysis of an open-access database of nosocomial outbreaks published in
MEDLINE (www.outbreak -database.com ) demonstrated that outbreaks occurred mainly in hospitals
(83%) and more often in intensive care units (47%). [25 ] Surgical, neonatology, and internal medicine services
accounted for similar proportions of the outbreaks. A source was identified in only 63% of outbreaks, often an
index patient (40%), contaminated equipment or devices (21%), or the environment (19%). The mode of
transmission was unidentified in 28% of outbreaks, and in the rest it was primarily contact (60%). The three
most frequent pathogens were Staphylococcus (15%), Pseudomonas (8%), and Klebsiella (7%). Most of the
staphylococci outbreaks (71%) were caused by methicillin-resistant Staphylococcus aureus (MRSA) and 24%
of the Klebsiella outbreaks were due to extended-spectrum ß-lactamase-producing bacteria (ESBL). Many
smaller nosocomial outbreaks are likely excluded from this database because of publication bias in the
literature, and most of the published works are derived from developed countries. [25]

RESPIRATORY AND OTHER PERSON -TO -PERSON OUTBREAKS

The most typical outbreaks of respiratory illness are those caused by respiratory viruses with short incubation
periods and potential for rapid dissemination in a population. [26 ] Other viruses transmitted by droplet nuclei,
such as measles and mumps, also cause similar transmission patterns, although over extended periods
owing to their longer incubation periods. Tuberculosis, on the other hand, is less frequently observed in
outbreaks, probably because of its lengthy incubation period and difficulty in establishing a clear
epidemiologic link between index and secondary cases. Occasionally, this link can be established, such as a
common airline flight or workplace. [27]

SEXUALLY TRANSMITTED OUTBREAKS

Typically, sexually transmitted diseases are less efficiently transmitted because a personal relationship must
be established. AIDS has taught us that although sexual transmission may be inefficient, it certainly is
sufficient to establish a global pandemic. The Internet has been cited as one mechanism that increases the
probability of contact between cases and naive, susceptible individuals. [28]

ZOONOTIC AND VECTOR -BORNE OUTBREAKS

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Increased interactions between humans and their environment have recently led to a surge of emerging and
reemerging infections, most of them zoonotic or vector borne. No single common transmission pattern can
describe the breadth of these outbreaks. Point-source exposures are often observed, as in the case of
leptospirosis in the Eco-Challenge in Malaysia. [29 ] Continuous common-source exposures are also observed,
especially for vector-borne diseases such as dengue and malaria.

Key Epidemiologic Principles

INCUBATION PERIOD

Conventional models of disease transmission define the incubation period as the time elapsed from exposure
to a certain infectious agent to the presentation of symptomatic manifestations, and it is often expressed as a
range. In an outbreak investigation, the incubation period is a key parameter that may help to discern
between multiple potential etiologic causes. For example, symptoms of foodborne staphylococcal intoxication
often appear 30 minutes to 6 hours after exposure, whereas the incubation period for salmonellosis is 6 to 72
hours. So, abrupt gastroenteric illness in multiple subjects who recently shared a common meal is less likely
to be caused by an agent with a lengthy incubation period such as Salmonella. However, it should not be
mistakenly assumed that infectious agents with lengthy incubation periods cannot cause outbreaks, because
transmission of Mycobacterium tuberculosis during air travel has been demonstrated on several occasions.
[27] Cases from outbreaks caused by agents with long incubation periods typically appear over extended time

periods, such that their common origin is rarely obvious.

TRANSMISSION MODES

Point-source outbreaks can occur after the exposure of a group of people to an agent during a single, short
period of time. Cases often present in a single group during a short time, corresponding to the range of the
incubation period, unless there is secondary transmission. The epidemic curve demonstrates an abrupt onset
and gradual descent, with a single peak. Because the point source is commonly food or beverages, single-
source outbreaks very often present as gastroenteric illness.

Person-to-person outbreaks are characterized by the presence of two or more clusters of cases in time
separated by approximately one median of the incubation period, thus suggesting secondary transmission.
The distance between clusters of cases usually becomes less clear as the outbreak progresses because the
ranges of the incubation periods tend to blend into each other. Respiratory transmission is the most efficient
mechanism of person-to-person transmission and is most classically represented by respiratory viruses such
as influenza. Measles, adenovirus, and even pneumonic plague may also be transmitted in this manner.

In continuous-source outbreaks, exposure to the agent can occur over an extended time. Therefore, cases
appear over longer periods, often substantially beyond the range of the incubation period. Cases sometimes
present in several clusters, but the timing between clusters does not necessarily correspond closely to the
median incubation period. Vector-borne and zoonotic infections are typical of this transmission pattern, but
waterborne, respiratory, and nosocomial outbreaks have occasionally been described as well.

CHAIN OF TRANSMISSION

Exploring the connection between initial waves of cases and those occurring later often reveals important
interactions during propagated outbreaks with person-to-person transmission or a continuous common
source. Clearly identified transmission waves can be observed, such as those in Ebola outbreaks related to
cultural practices like burial traditions in Africa [30 ] or the transmission of Nipah virus in a Bangladeshi
community [31] ( Fig. 14-1 ). Transmission waves can also provide hints about the incubation period of the
agent, although these may be difficult to tease out of the data.

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Figure 14-1 Person-to-person chain of transmission of Nipah virus in a Bangladesh village with dates of onset of illness in
2004. Patients KK and II had no known contacts with any ill patients prior to onset of illness.

TEMPORAL AND GEOGRAPHIC CLUSTERING

Temporal case clustering can be demonstrated when there are common exposures over time, and may
reveal multiple transmission waves. Geographic clustering, on the other hand, is more often related to the
spatial proximity to a common source (point or continuous), or to the presence of more favorable conditions
for continuation of the chain of transmission. This occurs most commonly in zoonotic, vector-borne, and food-
or waterborne illness, but has also been observed in the transmission of tuberculosis on an airplane around
the seat of a patient with active disease. [27]

Epidemiologic Tools for Outbreak Investigation: Epidemic Curves

Epidemic curves are histograms depicting the number of cases of a disease over the duration of an outbreak
or epidemic. [6] If properly prepared, epidemic curves are key epidemiologic tools in the outbreak investigation
that may aid in determining the transmission mode of the outbreak, the incubation period, and possible period
of exposure. The three main modes of transmission can often be identified from epidemic curves —point
source, person to person, and continued common source ( Figs. 14-1 and 14-2 )—although occasionally two
of these modes can be seen at different stages in a single outbreak. The crucial step in preparing an
epidemic curve is choosing a time interval unit that corresponds to a fraction of the median incubation period
of the suspected agent (usually between one half to one fourth of the incubation period) so the epidemic
curve can demonstrate the details of the outbreak and clearly identify the onset, peak, and tail of the
outbreak.

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Figure 14-2 A, Single point source of outbreak of cyclosporiasis at a naval base in Peru. [32 ] B, Continuing source multistate
outbreak of Salmonella Tennessee associated with consumption of peanut butter, by week of symptoms onset—United States,
August 1, 2006, through April 23, 2007. [33]

Outbreak Investigation and Response

Why is it important to investigate an outbreak? First, and perhaps most important, conducting the
investigation may help us to understand the mode of transmission of the disease, identify the etiologic agent
and who may be at risk of infection, and ultimately prevent additional cases and reduce the overall morbidity
and mortality rates. Second, conducting the outbreak investigation may allow us to evaluate the sensitivity
and specificity of a surveillance system, evaluate or implement intervention strategies (i.e., vaccination, social
distancing, or removal of a point source), and contribute to the epidemiology and scientific knowledge of the
disease.

A systematic, step-by-step approach to conducting an outbreak investigation is imperative for identifying the
source of the outbreak and for controlling and preventing additional cases. This systematic approach can be
divided into 10 distinct steps [34 ] ( Table 14-1 ); these are not rigid in their order and several steps are often
accomplished simultaneously.

TABLE 14-1 -- Ten Steps for Conducting a Successful Outbreak Investigation

1. Determine whether an outbreak is occurring.

2. Verify the diagnosis.
3. Establish a case definition.
4. Enumerate cases.
5. Conduct descriptive analyses of the preliminary data.
6. Develop hypotheses about the cause of illness and source of infection.
7. Evaluate the hypotheses with analytic methods.
8. Conduct additional epidemiologic, environmental, or laboratory studies.
9. Develop and implement prevention and control measures.
10. Communicate the findings.

1.
Conducting an outbreak investigation can be resource intensive; therefore, before initiating the
investigation it is imperative to determine whether an outbreak is actually occurring. An outbreak or
an epidemic, with the latter generally implying a more serious situation, is an increase in the number
of cases of a disease or condition occurring in a well-defined geographic location and period of time,
beyond expectation. Several data sources may be available to help determine if the number of

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observed cases exceeds that of expected baseline number (e.g., notifiable disease registries, death
registries, hospital discharge summaries). It is important to recognize that new or improved
diagnostic tests, a new or enhanced surveillance system, or simply increased awareness of a
disease may artificially indicate that an outbreak is occurring.
2. Verifying the diagnosis often goes hand-in-hand with confirming the existence of an outbreak. It may
be necessary to collect additional biologic samples and, if possible, request specialized diagnostic
procedures or have the results confirmed at a secondary reference laboratory. However, in the
event of an outbreak of a new pathogen, it may be necessary to rely on clinical diagnosis alone, as
was the case in the early stages of the SARS pandemic. Furthermore, it is highly recommended to
interview patients to gather additional clinical and epidemiologic features.
3. Enumerating the number of cases during an outbreak is possible only once a standard case
definition has been established. This can be one of the most difficult and contentious components of
an outbreak investigation. The case definition is usually based on clinical features, such as sudden
onset of fever greater than 38° C, cough or sore throat, difficulty breathing, and the like. The case
definition is almost always restricted by person (e.g., children younger than 5 years of age, no
history of yellow fever vaccine), place (e.g., patients in a specific wing of a hospital, attendees of a
county fair), and time (e.g., persons with illness onset within the previous 24 hours). The initial case
definition is often quite broad so as to capture all possible cases; however, as the investigation
proceeds it usually becomes more refined and divided into subcategories, such as suspect (e.g.,
fever only), probable (e.g., fever with cough and shortness of breath, death with history of fever and
cough), and confirmed (e.g., fever and cough with laboratory confirmation of H5N1 infection).
4. Enumerating and tracking cases is most easily achieved by constructing a line-listing of cases. Data
in the line-listing should consist of a minimum of information such as symptom onset date, patient
identification data, clinical data, demographic data, laboratory data, and some risk factor or
epidemiologic data.
5. The next step, and often the most revealing, is descriptive analysis of the epidemiologic data. The
line-listing is converted to visual depiction of the data, referred to as the epidemic curve (as
described previously) and oriented by time on the x-axis (typically symptom onset date) and number
of cases on the y-axis (see Fig. 14-2 ). The epidemic curve can give us clues about trend (i.e.,
person-to-person transmission or point/common source exposure), size of the outbreak, and
incubation period. In addition to the epidemic curve, the data can be displayed in map form,
revealing potential information such as common-source exposure or clustering of cases. The Global
Positioning Systems (GPS) and Global Information Systems (GIS) are tools now commonly used in
modern epidemiologic outbreak investigations. [34]
6. The next step, albeit a process that likely begins from notification of the first case, is to begin to
develop hypotheses about the cause of illness and source of infection. In general, conducting the
initial descriptive epidemiologic analysis of the data will give us clues to better refine our
hypotheses. Furthermore, it is important that the investigator speak with an adequate representative
of the initial patients to understand potential links between cases. It is important to remember that
hypotheses must be testable with statistical methods (e.g., chi-square analysis, logistic regression,
etc.).
7. After careful consideration and development of initial hypotheses, these hypotheses must be
evaluated with analytic methods. Two methodologies are typically used for outbreak investigations:
cohort studies and case-control studies. [6] [35] Cohort studies are typically used for well-defined
populations, such as an outbreak of norovirus on a U.S. Navy ship. Cohort studies allow us to
calculate attack rates (number of exposed persons infected divided by the number of exposed
persons) and relative risk ratio (likelihood that someone with an exposure will develop the disease,
as opposed to someone compared without the exposure). [6] [36] In contrast, case-control studies are
usually used for outbreaks occurring in poorly defined populations. Case-control studies are the
most common and classic type of study conducted during an outbreak investigation, whereby cases
(individuals with the disease) are compared with controls (individuals without the disease) using a
measure of association known as the odds ratio. [6] [36] Similar to relative risk, odds ratios allow us to
quantify the relationship between disease and the exposure (e.g., consumption of potato salad at a

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church picnic or being located on a specific ward of a hospital).

8. Once the hypotheses have been tested using conventional analytic epidemiologic methods, it may
be necessary to refine the hypotheses by conducting additional studies (e.g., laboratory or
environmental testing) to further support the conclusions. For example, identifying Cyclospora
cayetanensis in the raspberry filling of a wedding cake would greatly support the epidemiologic
evidence that eating cake at the wedding was significantly associated with development of diarrheal
illness. [4] If no conclusive results were initially revealed, a new hypothesis may be proposed.
9. The primary purpose of conducting an outbreak investigation is not only to determine the source of
the infection but, first and foremost, to control and prevent additional cases. For example, during an
outbreak of yellow fever it may be necessary to vaccinate the population, apply insecticide, and
educate the community about ways to reduce mosquito breeding sites.
10. Finally, it is imperative to communicate the findings—unfortunately, this last step is often
overlooked. The results of the study should be presented to the stakeholders (i.e., hospital staff,
local health authorities, scientific community) so that others can learn from the investigation and
recommendations.

Although infectious diseases do not necessarily respect or recognize boundaries and jurisdictions of cities,
states, and countries, it is important to remember that local and state health departments, as well as national
and international authorities, have specific roles and responsibilities. [6] An investigation of a nosocomial
outbreak at a local hospital or a diarrheal disease outbreak at a daycare center, limited to one city or country,
would require only coordination at the local health department level. However, if it is determined in the course
of the outbreak investigation that the source of the nosocomial outbreak was in multiple states (e.g.,
contaminated blood products), the investigation would require coordination not only with state but perhaps
national authorities (i.e., CDC). Similarly, if an outbreak was occurring in multiple countries (i.e., a pandemic,
such as SARS or influenza), then it would be necessary to coordinate through the WHO and the Global
Outbreak Alert and Response Network. [37]

Consequences of an Outbreak

Outbreaks of infectious disease have the potential to be sensational and may at times lead to significant
public relations difficulties. The potential economic, social, or political disruptions that result from the public
learning about an outbreak may be a significant disincentive to reporting it in a timely fashion or, in some
cases, to cooperating with the investigation of an outbreak. This may occur on the local level, such as when a
restaurant does not desire to be associated with an outbreak of foodborne disease for fear of losing
customers, or on an international level, when a country does not report an epidemic for fear of decreased
tourism or limits on the export of goods. [38] These sensitivities must be considered when investigating an
outbreak, dealing with the media, and releasing public statements, with an effort made to minimize
sensationalism but still impart the correct information and secure the public's health.

Conclusion

The primary goal of any outbreak investigation is to control the disease within the affected population and to
prevent the disease from spreading to other populations. Outbreak investigations are arguably one of the
most exciting aspects of epidemiology and are frequently rewarding, in that a tangible, positive outcome often
results. However, outbreak investigations can be extremely stressful and are often conducted under severe
political and economic pressure, and their results are often demanded on a short timeline. In these days of
pandemic threats and the reemergence of old scourges, preparation and a good understanding of disease
outbreaks are essential for timely and adequate disease control.

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