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2
Infectious Diseases
Waterborne Diseases
Introduction
Societies depend heavily on the ocean for food, transportation,
recreation, waste disposal, and minerals. Clearly, some of these
uses are in conflict, and four of these five major uses provide a
vehicle for transmission of disease agents to humans. The primary
source of marine-borne illness is seafood (Czachor, 1992; Lipp and
Rose, 1997). Currently seafood is in high demand, both in
industrialized and emerging nations, and it continues to be a
source of infectious diseases in humans throughout the world
(Garrett et al., 1997; IOM, 1991). In the United States, the demand
for seafood is so high that fish and fish products were the third
leading contributor to the U.S. international trade deficit,
reaching a staggering $4.2 billion in 1997 (McCarthy, 1996; NMFS,
1998).
Transportation has also contributed to waterborne infectious
diseases through the consumption of contaminated water and/or
seafood by ship passengers and crew. There is also evidence that
ships are responsible for the dissemination of exotic species,
including human pathogens, through the discharge of bilge water
into coastal waters (NRC, 1996). Recreation is another source of
exposure through ingestion of seawater or contact of skin and/or
mucous membranes with seawater. Finally, disposal of human wastes
in the ocean can lead to diseases of plants and animals, including
humans.
In the final decade of the 20th century it appears that
waterborne diseases of humans are as prevalent as they were at the
start of century. For example, waterborne illnesses continue to be
a major killer of children throughout the world
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(ICDDR,B, 1998). It is estimated that 60% of the world's
population lives in coastal zones, the area within a few kilometers
of the shoreline. Disease incidence is increasing worldwide,
promoted by both natural phenomena such as El Niño and human
activities, including sewage disposal. Ancient diseases like
cholera still cause epidemics (Plate V) while new agents of disease
(e.g., hepatitis E and Vibrio vulnificus) continue to be
discovered. Although the pathogenesis of diseases such as cholera
and dysentery is well understood, the cause of outbreaks of these
diseases is unresolved. Experts still debate how cholera epidemics
arise despite a detailed understanding of the genetics, chemical
structure, and mode of action of the cholera toxin. Cholera is
known to reside in human hosts and spread by the oral fecal route,
however, epidemics may be seeded by vibrios that reside in
estuaries and other saline waters and infect people through
contaminated drinking water and seafood. The molecular structure of
recently discovered disease agents has confirmed their existence on
Earth for thousands of years. The apparent emergence of these
pathogens could be the result of anthropogenic influences or may
reflect more sensitive modern detection technologies. Whatever the
cause, it is clear that infectious diseases, including waterborne
diseases conveyed by the ocean, still plague humankind.
The Agents of Waterborne Disease
The principal agents of diseases that derive from seawater and
seafood are viruses and bacteria. Most disease appears to result
from ingestion of contaminated seafood (IOM, 1991), although
accidental ingestion of seawater (e.g., recreational exposure or
contamination of potable water with seawater) is another important
route of infection. Some agents enter the human body through wounds
(e.g., puncture wounds from sea urchins and cuts from fishing gear)
others—Leptospira—although rarely contracted from
seawater, enter through broken skin, or penetrate mucous membranes,
and a few—avian schistosomes—penetrate unbroken skin.
Viruses are obligate parasites and require living cells for
reproduction. Certain viruses, however, can survive in seawater for
long periods of time (e.g., hepatitis A, poliovirus) and are
concentrated by marine bivalve mollusks, such as oysters and clams.
Human waterborne viral infections result from contamination of
seawater or seafood by sewage.
Unlike viruses, most of the pathogenic bacteria do not require
human hosts for replication. Indeed, some are naturally occurring
in estuaries and the coastal ocean, and can grow on, or within,
many animals, ranging from zooplankton to fish, and on marine
plants, ranging from phytoplankton to macrophytes. In general,
bacteria that cause seawater- and seafood-borne diseases in humans
come from two different sources. The foreign or allochthonous
bacteria come from humans and other animals by means of fecal
contamination: sewage outfalls, septic tanks, and land surface
runoff. One exception to this generalization for
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Representative terms from entire chapter:
coastal ocean
Page 45
allochthonous bacteria is Leptospira interrogans; it
lives in the urinary tract of mammals, especially rodents, and
enters water by means of contaminated urine. The indigenous or
autochthonous bacteria are usually commensals of marine plants
and animals, although some may be free-living in the water. For
example, the vibrios are indigenous to estuaries and the ocean, and
several species are human pathogens. Vibrio cholerae causes
human cholera and V. parahaemolyticus causes gastroenteritis
and wound infections. Because of the popularity of seafood in
Japan, V. parahaemolyticus is one of the most common causes
of gastroenteritis there (IASR, 1996). Examples of the more common
microorganisms that cause human disease and are conveyed by
seawater are listed in Table 2-1. Detailed discussion of these
common microbial agents of disease can be found in most textbooks
of microbiology, including Howard et al. (1994). Grimes (1991) has
reviewed the literature on estuarine bacteria capable of causing
human disease.
TABLE 2-1 Selected List of Major Agents of
Waterborne Disease Conveyed by the Coastal Ocean and Their Usual
Routes of Transmission to Humans
Agent
Disease
Usual Transmission Route
Viruses
Hepatitis A virus
Infectious hepatitis
Seafoodb,
waterc
Hepatitis E virus
Hepatitis
Waterc
Caliciviruses
Gastroenteritis
Seafoodb,
waterc
Rotaviruses
Infantile gastroenteritis
Waterc
Astroviruses
Gastroenteritis
Seafoodb,
waterc
Enteroviruses
Varied
Waterb
Autochthonous Bacteriaa
Mycobacterium marinum
Granuloma
Waterd
Vibrio alginolyticus
Wound infections
Waterd
Vibrio cholerae
Cholera
Seafoodb,
waterc
Vibrio parahaemolyticus
Gastroenteritis, wound inf.
Seafoodb,
waterd
Allochthonous Bacteriaa
Escherichia coli
Dysentery, gastroenteritis
Waterd
Leptospira interrogans
Leptospirosis
Waterd
Listeria monocytogenes
Listeriosis
Seafoodb
Morganella morganii
Scromboid food poisoning
Seafood
Salmonella species
Typhoid, gastroenteritis
Waterc
Shigella species
Bacillary dysentery
Waterc
Nematodes
Anisakis simplex
Anisakiasis
Seafoodb
a Autochthonous =
indigenous to the system; allochthonous = foreign to the system
b Raw or
undercooked seafood
c Water
ingestion—accidental during recreation or potable water
contaminated with seawater or feces
d Water
contact—usually accidental, during recreation or occupational
exposure.
Page 46
In addition to the viruses and bacteria, there are a few
waterborne animal parasites and fungi that cause human disease. The
best known are the avian schistosomes that cause swimmer's itch,
the nematode that causes anisakiasis (Deardorff and Overstreet,
1991), and the yeast that causes candidiasis. Outbreaks of
infection by these agents are relatively rare (toxic algae are also
microbial agents of human disease, and will be discussed in Chapter
3 of this report). Stings inflicted by anemones, jellys, and
stingrays associated with recreational use of coastal waters
provides sites for infection. Such infections usually result from
autochthonous bacteria such as the vibrios (Thomas and Scott,
1997).
Detection and Prevention
Classic detection methods for microbial agents of disease have
relied on microscopy and cultivation. Microscopy is useful only for
the larger organisms that can be identified by their morphology.
Fluorescence microscopy increases the options for visual
identification by using fluorescent dyes coupled to bacteria- or
virus-specific antibodies or gene probes. The traditional method
for detecting viruses and bacteria is cultivation. Suspect samples
of water and seafood are inoculated into nutritive broths or on
nutritive solid media (bacteria), or tissue cultures (viruses).
Positive cultures allow for the identification of the agents. In
some tests, samples are injected into animals, which are then
monitored for symptoms of disease.
Although cultivation is often successful in isolating pathogens,
it is now recognized that many bacteria remain undetected because
they are in a viable but nonculturable state (Grimes et al., 1986;
Roszak and Colwell, 1987; Xu et al., 1982). They can be visualized
by microscopy, but they cannot be grown using currently available
media and protocols. Most of the bacteria listed in Table 2-1 are
capable of entering a nonculturable phase (Grimes et al., 1986;
Roszak and Colwell, 1987), and no methods for their cultivation
from this phase have yet been formulated. Hence, testing water and
seafood for the presence of pathogenic bacteria by using culture
techniques can be misleading.
Detection and counting of specific bacteria, historically
referred to as fecal indicator bacteria, have comprised the
generally accepted method for estimating the public health safety
of both drinking and recreational water and seafood (Dufour, 1984).
This technique relies on the culture of coliforms, a term used to
include several genera and species, including Escherichia coli,
Enterobacter aerogenes, Klebsiella pneumoniae, and even some
Salmonella serotypes, thought to derive from the colon of
warm blooded animals. Originally, this group of bacteria was
employed to estimate the extent of fecal contamination of water
samples and, hence, the potential of enteric disease (Dufour,
1984). However, it was realized as early as 1900 that some
coliforms are frequently associated with natural bodies of water
including estuaries. Klebsiella pneumoniae, for example, is
commonly associated with plants and can wash into estuaries and the
coastal ocean during heavy rains. If present, these
non-sewage-related coliforms will
Page 47
cause falsely high estimates of pollution, making the use of
total coliforms as an indicator of enteric disease questionable and
sometimes misleading. Although the introduction of the fecal
coliform count improved the specificity of the test, false
positives from other non-fecal bacteria remain a problem. Today, it
is accepted that the fecal coliforms provide public health
practitioners with a useful indicator; however, it is also widely
recognized that the fecal coliform test has some serious
disadvantages:
•
Not only fecal, but also non-fecal bacteria such as K.
pneumoniae, make up the fecal coliform group, reducing the
accuracy of the test;
•
Fecal coliforms have little, if any, quantifiable association
with specific pathogens that are important in human disease,
including viral diseases (Table 2-1);
•
Fecal coliforms survive for a long time in aquatic habitats,
notably in estuaries and in shellfish, either in the detectable
(culturable) or dormant (nonculturable) state; and
•
Fecal coliforms do not provide a meaningful indication of the
disinfection of water, wastewater, and seafood because commonly
employed procedures (e.g., chlorination and ultraviolet light)
accelerate the transition of these bacteria from a culturable to a
nonculturable state.
In the early 1980s, the U.S. Environmental Protection Agency (EPA)
recommended replacing the fecal coliform recreational water index
with Escherichia coli and/or enterococci counts in
freshwater and enterococci counts in marine and estuarine waters.
In one epidemiologic study (Cabelli et al., 1982) the incidence of
enteric disease among swimmers was compared with incidence of
selected fecal indicator bacteria including coliforms, fecal
coliforms, Escherichia coli, and enterococci in the water
off bathing beaches. There was a high correlation between the
incidence of enteric disease and the levels of enterococci found in
marine and estuarine waters. Even so, the only coastal states that
have adopted the EPA recommended standards for marine and estuarine
waters include Connecticut, Hawaii, Maine, New Hampshire, and South
Carolina (NRDC, 1998).
Finally, it should be noted that certain strains of E.
coli are themselves pathogenic for humans (e.g., E. coli
0157:H7), and these toxin-producing strains can survive in seawater
in the viable but nonculturable state for several days to weeks
(Grimes and Colwell, 1986). For example, a recreational outbreak of
E. coli disease occurred in a water park in June, 1998 (CDC,
1998a), infecting 26 children and causing one death. Clearly, E.
coli is more than an indicator of fecal pollution; it may be a
preferred indicator of contamination for freshwater and possibly
low salinity water. Certain pathogenic strains of E. coli
are themselves candidates for surveillance.
The fecal coliform test continues to be the standard used for
shellfish and waters where shellfish are grown, as established by
the National Shellfish Sanitation Program (NSSP; FDA, 1996).
Although numerous studies have reported that fecal coliforms do not
correlate with any of the current diseases that can be
contracted
Page 48
from eating raw or undercooked oysters (Goyal et al., 1979; Koh
et al., 1994), there is a reluctance for the NSSP to abandon them
as its index of public health safety.
Some investigators have suggested that enterococci may be the
preferred indicator, but these microorganisms have some of the same
limitations as the fecal coliforms (Koh et al., 1994). Because of
these limitations and reliance on the existing database for fecal
coliforms, the enterococci have not been universally accepted by
state, county, and local regulatory agencies as a substitute
indicator group, even though some states have adopted the new E.
coli and enterococcus standards. In addition, the presence of
enterococci or E. coli does not always correlate with the
presence of viruses.
New indicator systems are being proposed, some of which are
based on molecular genetic methods. The coliphages, viruses
attacking the coliform bacteria, have been suggested as an
indicator of risk of infection with human enteric viruses,
including hepatitis A virus. They have a quantifiable association
with specific viral pathogens representing an improvement over
fecal coliforms (Paul et al., 1997). Presence of Clostridium
perfringens spores may be helpful in distinguishing long-term
accumulation or movement of sewage in aquatic habitats. This is
because C. perfringens is fecal specific and the spores can
survive for many years (Emerson and Cabelli, 1982). Of greatest
interest, however, are the gene probes now being used in clinical
laboratories to detect pathogenic microorganisms. Gene probes can
be highly specific, capable of detecting genetic sequences common
to, or evolutionarily conserved in, pathogens of concern. For
example, gene probes can be used in environmental testing to
detect, directly identify, and quantitate pathogens such as
Salmonella thus obviating the need for culturing (Brasher et
al., 1998). Also, amplified nucleic acid sequences, using the
polymerase chain reaction (PCR), allows detection of very small
numbers of bacteria and viruses in a given sample. For example,
Brasher et al. (1998) have developed a series of gene probes that
show promise for the direct detection of enteric pathogens in
seawater and seafood. Monoclonal antibodies also have been shown to
be useful for direct detection of pathogens in estuarine and
seawater samples, especially when coupled with fluorescent dyes
(Huq et al., 1990). Finally, the use of immunoglobulin A as a
human-specific indicator of fecal pollution has received some
recent interest (Middlebrooks, 1993). It is predicted that the new
biotechnological methods will eventually replace the cumbersome and
inaccurate fecal indicator tests for public health assessments of
the safety of water and shellfish. For a recent review of detecting
viruses in the environment, the reader is referred to Metcalf et
al. (1995).
Coastal Oceans, Estuaries, and
Waterborne Disease Transmission
Allochthonous materials enter estuaries and the coastal ocean by
four routes: point sources, nonpoint sources, direct disposal or
discharge, and atmospheric
Page 49
fallout or rainout. Point sources include sewage outfalls and
industrial wastewater outfalls. Nonpoint sources include storm
runoffs, storm sewer outfalls, and rivers. Both point and nonpoint
sources of pollution have the potential to contaminate receiving
waters with human pathogens. In past years, disposal of sewage
sludge contributed pathogens to both the water column and marine
sediments. Direct disposal of wastes into the ocean is now largely
prohibited as a result of the London Dumping Treaty (Zeppetello,
1985) and the Ocean Dumping Act of 1988, and, therefore, refuse
discharge is no longer a major source of human pathogens in the
ocean. A recently recognized source of human pathogens is bilge and
ship ballast discharge. Ships that take on ballast water in foreign
ports can inadventently take on water contaminated with pathogens
and then discharge those pathogens into previously uncontaminated
waters. The National Research Council recently published a report
on the introduction of non-native species by ballast water (NRC,
1996), and McCarthy and her colleagues have studied this problem in
the Gulf of Mexico (McCarthy and Gaines, 1992; McCarthy and
Khambaty, 1994; McCarthy, 1996). The scope of this problem is not
yet clear, but ship ballast discharge has the potential to spread
microorganisms throughout the world's coastal ocean. Less clear are
contamination problems from atmospheric fallout or rainout, but a
recent publication suggests that pathogens can be spread by air
(Rosas et al., 1997). Contributions due to atmospheric fallout or
rainout occur, but are not well understood (Rosas et al.,
1997).
Point sources of allochthonous materials continue to be an
important source of pathogens in the estuaries and the coastal
ocean of the United States. Sewage treatment plants in the United
States discharge approximately 2.3 trillion gallons of effluent
into marine waters annually, and more than 2.8 billion gallons of
industrial wastewater are released daily (NOAA, 1998c). Even though
much of this effluent is receiving some type of treatment prior to
discharge, it is still contributing pathogens, nutrients, and toxic
chemicals to the coastal ocean of the United States. While point
sources therefore continue to cause degradation of coastal areas,
it is now generally believed that nonpoint sources are equally if
not more important. Nationwide, it has been estimated that indirect
loadings account for more than half of the suspended solids,
nutrients, fecal coliforms, and metals entering coastal waters
annually (NOAA, 1998a). The two largest sources of nonpoint
pollutants are agricultural runoff and storm sewer discharge.
It is estimated that over 9.1 billion gallons of domestic sewage
and industrial wastewater enter the coastal ocean of the United
States each day (NOAA, 1998a). When combined with accidental spills
(e.g., oil spills) and nonpoint source runoff, the net result is a
vast and complex mixture of chemicals, both organic and inorganic,
entering the coastal ocean of the United States. These chemicals
primarily cause two alterations in coastal ocean ecosystems. Some
serve as growth stimulating nutrients, either directly as sources
of food for marine plants, animals, and microorganisms or
indirectly as essential growth factors (e.g., vitamins). Other
chemicals are toxic to living organisms, causing alterations in
Page 50
growth (e.g., stunting and neoplasms) or death. In some cases,
chemicals that are toxic to some forms of life can actually serve
as growth stimulating nutrients for others, especially
microorganisms. A good example of this is the ability of
carcinogenic polycyclic aromatic hydrocarbons (PAHs) to serve as a
growth medium for certain marine vibrios, including pathogenic
vibrios (West et al., 1984). Another example is the shift in
bacterial communities that was described in the mid-Atlantic Ocean
by Grimes et al. (1984). Thus, it is possible that certain toxic
chemicals entering the coastal ocean of the world have multiple
effects. Some of these chemicals could be making fish and marine
mammals more susceptible to disease by altering their resistance
(immune system), while at the same time stimulating the growth of
agents capable of causing the disease. It is worth noting that the
vibrios are capable of degrading a wide variety of organic
compounds, including aliphatic and aromatic hydrocarbons, and this
generalization includes the pathogenic vibrios. However, proper
experiments have not been done to establish linkages between toxic
chemicals, declining fisheries, human disease, and densities of
pathogenic vibrios.
Most of the waterborne and seafood-borne diseases throughout the
world are caused by viruses. The major agents of waterborne viral
disease are listed in Table 2-1, and they include several
well-known groups. The agents in these groups are all RNA
(Ribonucleic Acid) viruses, and most have not been cultured. Viral
hepatitis is now known to be caused by two related viruses,
hepatitis A and E. These viruses are very resistant to
environmental extremes, including toxic chemicals, and they are
concentrated from water by filter-feeding shellfish, especially
oysters. The human caliciviruses include the Norwalk virus and all
cause gastroenteritis. It is estimated that most shellfish-borne
and waterborne disease in the United States is caused by the
Norwalk virus (GAO, 1984). None of the caliciviruses can yet be
cultured and they are detected by antibody-based tests (e.g.,
Enzyme-Linked Immunosorbent Assay [ELISA]) and RT-PCR (reverse
transcriptase PCR). The NRC Committee on Evaluation of the Safety
of Fishery Products reviewed the incidence of Norwalk and
Norwalk-like agents (IOM, 1991). The rotaviruses and astroviruses
are responsible for widespread diarrheal disease, especially in
children. It is estimated that rotaviruses kill 870,000 children in
the world annually (U.S. Department of Health and Human Services,
1998). As described for the caliciviruses, their detection is
dependent on RT-PCR assays and immunologic procedures. Recently, a
rotavirus immunization procedure was approved for children.
Finally, the enteroviruses represent a large and diverse group of
viruses that include the poliovirus. Enteroviruses cause a variety
of clinical syndromes, including aseptic meningitis, paralysis,
myocarditis, rash, pneumonia, fever, and undifferentiated febrile
illness. The only common link among these viruses is their mode of
transmission (fecal-oral route, which can include water and food as
intermediaries) and their nucleic acid content is RNA. It is
doubtful that global climate change events will have any
significant direct effect on these viruses, because they are not
conveyed by vectors and are incapable
Page 51
of growing in ocean habitats. However, changing demographics and
anthropogenic pressures (e.g., sewage contamination) very
definitely contribute to the epidemiology of these diseases. Avian
schistosomes are a problem for recreational users of coastal
waters, causing what is known as swimmer's itch or clam digger's
itch. The cercariae (free-swimming larvae) of these schistosomes
penetrate human skin; but humans are not hosts for the parasite and
the cercariae die in the skin causing mild to severe itching due to
an allergic reaction to the foreign protein. Human anisakiasis is
caused by a nematode that infects humans via raw or inadequately
prepared seafood (Deardorff and Overstreet, 1991). The incidence of
this parasitic disease is very low in the United States, but may be
on the increase because of the current popularity of raw fish as a
delicacy (e.g., sushi and sashimi). In Japan, over 3,000 cases of
anisakiasis are reported annually (IOM, 1991). It is difficult to
predict how global climate change events would affect these two
parasites. It is possible that increased water temperatures could
disrupt life cycles of these parasites by changing the range of
their hosts (e.g., snails, birds, fish, marine mammals) and, hence,
accessibility to humans. Demographics (e.g., continued population
shifts to the coast) and cultural food preferences (e.g.,
consumption of raw fish) could also have a definite effect.
Global Climate Change and Infectious
Disease
One of the first documented associations of a human pathogen
with an estuarine animal subject to climate-induced fluctuations
was the Vibrio parahaemolyticus-zooplankton relationship
described by Kaneko and Colwell (1973) in the Chesapeake Bay. They
determined that V. parahaemolyticus overwintered in
Chesapeake Bay sediments and entered the water column when water
temperatures reached 14 ± 1 ¹C. Upon entering the water
column, the vibrios became associated with zooplankton, primarily
on the surfaces of copepods. The abundance of the vibrios increased
in direct proportion to the growth of the copepod population.
Kaneko and Colwell (1973) also demonstrated a direct relationship
between water temperature, numbers of zooplankton, and V.
parahaemolyticus. Over 10 years later, Watkins and Cabelli
(1985) observed a similar relationship between V.
parahaemolyticus and zooplankton in Narragansett Bay. In
addition, they demonstrated that fecal pollution had an indirect
effect on V. parahaemolyticus densities. Nutrients
associated with the wastewater stimulated the growth of
phytoplankton boosting zooplankton populations, which in turn
supported greater densities of the vibrios. Clearly, coastal ocean
nutrient enrichment can increase the prevalence of pathogenic
vibrios, indicating that climatic events that change the abundance
of plankton also have the potential to affect the spread of
disease. It is interesting to note that elevated water temperatures
have been implicated in the largest reported outbreak in North
America of shellfish-borne V. parahaemolyticus. During July
and August, 1997, 209 persons became ill and one person died from
consuming raw oysters harvested from California, Oregon,
Page 52
and Washington in the United States and British Columbia in
Canada. All 209 infections were culture-confirmed as V.
parahaemolyticus (CDC, 1998b). In early summer 1998, the Food
and Drug Administration warned consumers not to eat raw oysters
from Galveston Bay, Texas, because they might contain harmful
levels of V. parahaemolyticus (FDA, 1998). By the end of
July, 368 persons had become ill from consuming raw oysters
harvested from Galveston Bay, Texas; so far V.
parahaemolyticus has been confirmed in 66 of those cases (AP,
1998b).
It has become clear that Vibrio vulnificus also has a
preference for warmer temperatures, making it a candidate for the
list of pathogens that could be influenced by climate-induced
increases in water temperature. Motes et al. (1998) investigated
the temperature and salinity parameters of waters where oysters
were linked to seafood-borne V. vulnificus infections, and
found that abundance of this pathogen was directly correlated with
water temperature. Numbers of V. vulnificus increased with
water temperatures up to 26 ¹C and were constant at higher
temperatures. Salinity also played a factor and high V.
vulnificus levels were associated with intermediate salinities
(5 to 25 ppt1).
Colwell (1996) noted that coincident with an outbreak of cholera
in Peru, an El Niño event that began in 1990 had warmed the
nutrient- and phytoplanktonrich waters off the Peruvian coast. The
Peruvian outbreak, which began in January 1991, quickly spread to
most of the neighboring countries in South America (Mata, 1994). In
3 weeks, the epidemic had covered over 2,000 km of coastal Peru and
caused 30,000 cases of cholera; it claimed 114 lives in the first 7
days. Since V. cholerae, like V. parahaemolyticus,
associates with planktonic copepods (Colwell, 1996), it can be
hypothesized that the South American cholera outbreak resulted from
increased levels of V. cholerae that grew in response to the
warmer water and nutrients in terrestrial runoff from increased
rainfall. Although this conclusion was not reached by direct
experimentation, the V. parahaemolyticus model indicates
that this proposed link is worthy of further scientific
investigation.
More recently, Colwell noted a relationship between sea surface
temperature in the Bay of Bengal and cholera cases reported in
Bangladesh (Colwell, 1996). A plot of the percent of diarrheal
disease caused by V. cholerae versus seasonal sea surface
temperature data obtained by remote sensing, revealed a correlation
between the cholera case data and increasing water temperature. As
with the Peruvian hypothesis, direct experiments to relate the two
observations were not performed. However, the data are compatible
with the ecology of the vibrios, and should be followed up with
carefully planned interdisciplinary studies including epidemiology,
meteorology, and oceanography. Plate VI shows that sea surface
temperature was elevated from December through April off the
western coast of South America during the 1997–98 El
Niño. Sea surface height (Plate VII), however,
1 ppt = parts
per thousand.
Plate Section has been moved to the
back of the book.
Page 53
peaked during December, and corresponds with the seasonal name
for this phenomenon (El Niño refers to the birth of Jesus).
These data could be collected and coordinated with water sampling
for zooplankton, V. cholerae, nutrients, and chlorophyll,
and with epidemiology for cholera incidence.
Storms fueled by the 1997–1998 El Niño increased
urban runoff, saturated septic tank leach fields thereby causing
overflows, and caused a weakened sewage main to break and spill 120
million gallons of raw sewage into Santa Monica Bay. As a result,
public health officials in California closed beaches on 50 days
during the period May 1997 through April 1998; this was more
closure days than in the three previous years combined for Santa
Monica Bay (Alamillo and Gold, 1998).
Vector-Borne Diseases
Introduction
The ocean influences climate and weather (see Chapter 1) and
hence indirectly affect infectious disease agents that are
sensitive to changes in temperature and/or rainfall (Pearce et al.,
1995). Global warming may affect the incidence of certain
protozoal, bacterial, and viral diseases, because increased
temperatures tend to change the geographic distribution and
reproductive success of many vectors that carry these diseases. For
example, higher temperatures may increase the range of some
species, but it may also shorten insect survival hence decreasing
the transmission of some vector-borne diseases. Indirect effects of
climate change may have an impact on human health, but accurate
assessment of the risk requires a better understanding of how
vectors and their pathogens respond to changes in weather patterns.
Indications of how global climate change can affect the spread of
vector-borne infectious diseases may be discerned from studying the
effects of periodic weather events such as El Niño/Southern
Oscillation (ENSO). Weather events such as ENSO bring extremes of
both rainfall and drought and change the capability of disease
vectors to spread their pathogens to humans. Some of these changes
appear to be due to an increase or decrease in habitat, but the
spread of vector-borne diseases is also modified by the effects of
these disasters on the water supply and public hygiene. Specific
effects of ENSO on several of the vector-borne diseases are
described below.
Major Disease Agents and their
Vectors
Malaria: In the aftermath of a severe marine weather
event such as a hurricane or monsoon, there is frequently a higher
risk of malaria from an increase in standing water breeding habitat
and in some cases from a disruption of malaria control measures.
Malaria remains one of the most prevalent parasitic diseases in the
tropics. The disease agents are the protozoa, belonging to the
genus Plasmodium,
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a parasite transmitted by the anopheline mosquito. Worldwide
prevalence of the disease is estimated to be 300–500 million
clinical cases per year, with 90% occurring in sub-Saharan Africa
and most of the remainder in India, Brazil, Sri Lanka, Viet Nam,
Colombia, and the Solomon Islands (WHO, 1996). Paradoxically, an
increase in malaria transmission may be associated with either
drought or rainfall as seen in the Indian subcontinent before the
introduction of residual insecticides. In the arid Punjab, rainfall
improved the breeding and survival of mosquitoes. However, in the
high rainfall area of Sri Lanka, lack of rainfall from the failure
of the monsoons led to reduced flow of rivers and the formation of
standing pools of water that provided favorable breeding conditions
(Bouma and van der Kaay, 1996). Drought associated with the failure
of the south-west monsoons are twice as frequent in the year
following an El Niño (Dilley and Heyman, 1995) and correlate
with past malaria epidemics. Improved predictions of malaria
transmission may be possible through the application of
hydrological models to estimate available surface water for
mosquito breeding (Patz et al., 1998a).
In Venezuela and Colombia the incidence of malaria morbidity and
mortality increased substantially (35–37%) in the years
following an El Niño. In these countries, the increase
correlated more strongly with drought in the first year of the El
Niño as opposed to rainfall in the second year (Bouma and
Dye, 1997 and Bouma et al., 1997a). It is not clear how drought
promotes disease in these countries; however, the authors suggest
that in the dry year there is a loss of mosquito predators which
allows the mosquito population to increase unchecked in the
following wet year.
There has been some question as to whether El Niño
conditions gave rise to the epidemics of malaria that occurred
during 1983 in Bolivia, Ecuador, and Peru. A review of the data
reported by each country on malaria shows that the incidence of
this disease began to rise in each of these countries in 1983.
However, the overall trend from 1970 to 1996 was an increase in the
number of cases reported, while in other El Niño years
(1971–1972, 1976–1977, 1991–1992) the incidence
of malaria seldom increased over that of previous years. It is
known that, during this time, national malaria control programs in
Latin America switched from a strategy of rigid eradication to
flexible control. This alone could have caused the observed
increase. Conversely, a good eradication program may have been
masking the impact of El Niño in previous El Niño
years. Establishment of an association between an El Niño
event and outbreaks of malaria will require future research that
emphasizes accurate reporting of outbreaks and consideration of the
impact of malaria control measures.
Rift Valley Fever: Rift valley fever (RVF) is a
vector-borne viral disease transmitted by the Aedes
mosquitoes that primarily affects livestock but which also afflicts
humans. Incidence of this disease is highly correlated with
excessive rainfall, such that high rainfall in an El Niño
year may trigger an outbreak of RVF. However, heavy rains are not
sufficient to predict an epidemic of RVF. Transmission is also
dependent on the presence of both the competent vector
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(Aedes mosquito) and the pathogen. In 1997, the eastern
African countries of Kenya and Somalia experienced 60–100
times the normal rainfall in some areas. This was followed by an
outbreak of 89,000 cases of RVF in northeastern Kenya and southern
Somalia, possibly the largest ever reported (WHO, 1998).
Conversely, Kenya did not experience an outbreak of RVF during the
1982–83 El Niño, despite heavy rainfall.
Dengue: Dengue and Dengue Hemorrhagic Fever (DHF) are
caused by four distinct, but closely related, viruses carried by
the Aedes mosquito. This mosquito has become adapted to
urban habitats, breeding in manmade collections of rainwater as
well as water stored for drinking and washing. The occurrence of
this disease has increased dramatically in the past few decades,
from 9 countries prior to 1970 to 41 countries by 1995. Currently,
both the Aedes mosquito and dengue viruses are endemic to
the tropics worldwide. Each year, dependent on the frequency of
outbreaks, there are an estimated 100 million cases of dengue
fever, and several hundred thousand cases of DHF, a leading cause
of death and hospitalization of children in Southeast Asia (Gubler,
1998). As with malaria, it is difficult to demonstrate
scientifically that changes in the distribution of dengue are the
result of climate variability. PAHO/WHO, in its preliminary study
in the Americas, did not find a correlation between national
statistics and increased rainfall (PAHO, 1998b). In fact, peaks in
reports of dengue did not occur during past El Niños in the
Americas.
It is too early in the current El Niño year to evaluate
fully the effects on the incidence of dengue; however, 1998 may be
the worst year on record for dengue in some areas. In Viet Nam,
there were twice as many cases as of June 1998 than in the previous
year and 1997 was the worst year since 1991. Similarly, in Brazil
there were as many cases of dengue in June as there were for the
entire year in 1997, despite the initiation of an eradication
program in 1997. Some researchers have proposed models that link
potential changes in global climate with changes in the
distribution of dengue transmission (Jetten and Focks, 1997; Patz
et al., 1998b). However, the overall spread of the disease during
the last few decades argues that factors other than weather are
responsible for the current increased prevalence of dengue (Gubler,
1998).
There are several other viral diseases that may be affected by
changing weather and climate patterns including yellow fever,
hantavirus, and viral encephalitis as well as other parasitic
diseases such as schistosomiasis and sleeping sickness since the
vectors are sensitive to changes in temperature and rainfall
(Rogers and Packer, 1993; Stone, 1995).
Evaluating the Impacts of ENSO on
Vector-borne Disease
Future research should aim to improve the quality of the
indicators and data on disease exposure and health outcome. The
poor quality of epidemiologically-based surveillance systems and
disease reporting in many countries sometimes
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BOX 2-1 ENSO Experiment
The ENSO Experiment is a program specifically designed to study
the human health impacts of the 1997–1998 El Nino/Southern
Oscillation (ENSO) event and determine the potential application of
forecasting to public health preparedness. This program is
coordinated through the NOAA Office of Global Programs and the
International Research Institute for Climate Prediction. The ENSO
experiment takes an interdisciplinary approach to examining the
ENSO-related changes in weather that have direct and indirect
effects on the waterborne and vector-borne infectious diseases that
afflict humans.
precludes environmental analysis and hinders the planning and
implementationof analytic epidemiologic studies. Analysis of
aggregated data at the nationallevel by PAHO has not shown a
significant correlation between ENSO and communicablediseases.
However, because of limitations in the available data, it
ispossible that correlations were present but not detected.
Epidemiological studiesand meaningful conclusions on the impact of
ENSO or communicable diseaseswill require a long-term temporal and
spatial (geographic) perspective with asustained quality of data
that quick short term investigations will not provide.International
cooperation between scientists, countries, and WHO is required
todevelop the global surveillance system required to respond to
these global challenges.Although it is impossible to determine how
much human illness is directlycaused by ENSO, specific weather
patterns give an indication of potentialoutbreaks of vector-borne
diseases. It will be very difficult to separate the effectsof El
Niño from other factors that impact the transmission of
these diseases. Oneprogram that is currently being conducted to
address these issues is the ENSOExperiment (Box 2-1).
Conclusions
Given current world population dynamics, including growing
populations near coastal waters and increased recreational use of
ocean and coastal waters, particularly in developing countries,
there are several pressing scientific needs for better
understanding the ocean and infectious diseases. The spectrum of
infectious diseases in the United States related to several routes
of exposure needs to be more thoroughly and comprehensively studied
and monitored, nationwide and internationally. These disease
categories include: waterborne infectious diseases, vector-borne
diseases, infectious diseases related to consumption of tainted
seafood, and the infectious diseases related to swimming, boating,
fishing, and
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water use. New tests are needed to detect waterborne pathogens
more quickly and efficiently, and more definitive research in the
changing epidemiology of infectious diseases is needed. The primary
areas deserving attention are listed below.
1. Newly developed tests, including gene probes for bacteria,
viruses, and other pathogens and monoclonal/polyclonal antibody
direct detection methods, are available and should be applied to
environmental monitoring and quality assessment. However, they must
be field tested for application in different geographic locations
to expand the database and, if successful, should be adopted by
enforcement agencies as standard methods. To achieve this goal,
coordination of funding and enforcement agencies, at all levels of
government, with industry and academia, will be necessary. Specific
suggestions include:
•
Evaluate cost/benefits of the use of coliforms as indicators of
fecal pollution in estuaries and seawater, as introduction of newer
molecular genetic and immunological methods for direct detection
and evaluation of pathogens proves applicable.
•
Where practical, begin application of such tests for shellfish
quality assurance with emphasis on accuracy, precision, speed,
cost, and safety.
•
Coordinate and integrate environmental monitoring for pathogens
with targeted epidemiological investigations to quantify population
risk in high-risk areas.
•
Evaluate the efficacy and comprehensiveness of current disease
surveillance programs aimed at monitoring infectious diseases that
are waterborne and related to consumption of seafood. Assess the
adequacy of federal programs and the need for coordination with
state efforts, especially for coastal states.
2. Interdisciplinary research should be emphasized/encouraged to
assess the potential for global climate change to affect the spread
of human diseases. Investigative teams should include, at a
minimum, microbiologists, meteorologists, oceanographers, remote
sensing experts, epidemiologists, parasitologists,
biostatisticians, entomologists, ecologists, botanists, and
behavioral scientists. Specific suggestions include:
•
Investigate the cause and effect relationships between sea
surface temperature, nutrients, plankton, Vibrio cholerae,
disease incidence, and global climate change.
•
Plan and monitor long-term campaigns for the assessment and
control of vector-borne diseases that have the potential for being
influenced by global climate change.
•
Coordinate efforts between the World Health Organization (WHO),
U.S. Agency for International Development (USAID), Centers for
Disease Control (CDC), U.S. Department of Defense (DOD), and other
international organizations
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•
to monitor temporal and geographic disease trends in all nations
of the world, so that early warning of emerging diseases can be
effective.
•
Develop better testing methods for autochthonous pathogens and
elucidate their niche (i.e., distribution and role in their natural
habitat), so that disease transmission to humans can be
prevented.
•
Seek advice and participation from key organizations in
developing epidemiological methods for application to global
climate change issues (EIS Program/CDC; American Teachers of
Preventative Medicine; American College of Epidemiology; Society
for Epidemiology Research; International Society for Environmental
Epidemiology; American Public Health Association; American Society
for Microbiology).