Implications
Climate change is expected to exert an overwhelming negative effect on livestock health
and welfare. Several studies suggest that the expected increase of air temperatures
might reduce the risk of death and improve health and welfare of humans and livestock
living in areas with very cold winters.
The negative effects of climate change on animal health and welfare will be the consequence
of combined changes of air temperature, precipitation, frequency, and magnitude of
extreme weather events and may be both direct and indirect.
The direct effects of climate change may be due primarily to increased temperatures
and frequency and intensity of heat waves. Depending on its intensity and duration,
heat stress may affect livestock health by causing metabolic disruptions, oxidative
stress, and immune suppression causing infections and death.
The indirect effects of climate change are primarily those linked to quantity and
quality of feedstuffs and drinking water and survival and distribution of pathogens
and/or their vectors.
Development and application of methods linking climate data with disease occurrence
should be implemented to prevent and/or manage climate-associated diseases.
Introduction
Climate is one of many factors with the potential to alter disease states and is expected
to exert an overwhelming negative effect on the health of humans and animals (Rabinowitz
and Conti, 2013). In addition, several studies suggested that the increase of temperature
might reduce mortality and/or improve health and welfare related aspects in humans
and livestock living in geographic areas with cold winters (Ballester et al., 2011;
Rose et al., 2015).
The effect of climate change on animal health may be either direct or indirect (Figure
1) and may be due primarily to changes in environmental conditions, which include
air temperature, relative humidity, precipitation, and frequency and magnitude of
extreme events (i.e., heat waves, severe droughts, extreme precipitation events, and
coastal floods). Although this article focuses on the effects of environmental factors,
it should be noted that factors leading to the effects of climate change on health
are extremely complex, involving not only environmental forces, but also ecological
and social aspects, economical interests, and individual and community behaviors (Forastiere,
2010).
Figure 1.
Schematic representation of the impact of climate change on animal health.
The direct effects of climate change on health include temperature-related illness
and death. Indirect impacts follow more intricate pathways and include those derived
from the influence of climate on microbial density and distribution, distribution
of vector-borne diseases, food and water shortages, or food-borne diseases (Lacetera
et al., 2013). The aim of this article is to summarize the current state of knowledge
regarding the influence of climate and climate change on the health of food-producing
animals.
Direct Effects
The direct effects of climate change on health may be due primarily to increased temperatures
and frequency and intensity of heat waves (Gaughan et al., 2009). These effects are
mediated by induction of heat stress conditions. Depending on its intensity and duration,
heat stress may negatively affect livestock health by causing metabolic alterations,
oxidative stress, immune suppression, and death (Figure 2).
Figure 2.
Schematic representation of the most frequent consequences of heat stress on animal
health.
Metabolic Disorders
Homeothermic animals respond to high temperatures by increasing heat loss and reducing
heat production in their attempt to avoid increased body temperature (hyperthermia).
Such responses include an increase in respiratory and sweating rates and a decrease
in feed intake. These physiological events may provide a significant contribution
to explain the occurrence of metabolic disorders in heat-stressed animals (Figure
3).
Figure 3.
Schematic representation of some mechanisms through which heat stress may cause metabolic
disorders in farm animals.
Heat stress can contribute to the occurrence of lameness in dairy and beef cows (Shearer,
1999). Lameness in cattle may be defined as any foot abnormality that causes an animal
to change the way that it walks. Lameness can be caused by a range of foot and leg
conditions, themselves caused by disease, management, or environmental factors and
is one of the most significant health, welfare, and productivity issues. The contribution
of heat stress to lameness is perhaps due to ruminal acidosis or increased output
of bicarbonate (Cook and Nordlund, 2009). Heat-stressed cattle eat less frequently
during cooler times of the day, but they eat more at each feeding. Reduced feed intake
during the hotter part of the day, followed by increased feeding when the ambient
temperature cools down, can cause acidosis which is considered a major cause of laminitis
(Shearer, 1999). As ambient temperatures rise, the respiratory rate increases with
panting progressing to open-mouth breathing. A consequence is respiratory alkalosis
resulting from a rapid loss of carbon dioxide. Cattle compensate by increasing urinary
output of bicarbonate. Rumen buffering is affected by a decreased salivary bicarbonate
pool. Lameness, with sole ulcers and white line disease, will appear in a few weeks
to a few months after heat stress.
The reduction of feed intake combined with increased energy expenditure for maintenance
may alter energy balance and explain why heat-stressed animals lose body weight and/or
mobilize adipose tissue during heat stress. In particular, during summer, early lactating
dairy cows are more likely to experience subclinical or clinical ketosis (Lacetera
et al., 1996) and are at higher risk to develop liver lipidosis (Basiricò et al.,
2009). Ketosis is a metabolic disease that occurs when the animal is in a severe state
of negative energy balance, undergoes intense lipomobilization, and accumulates ketone
bodies, which derive from incomplete catabolism of fat. Liver lipidosis is another
consequence of the intense mobilization of fat from adipose tissue. Compromised liver
function in heat-stressed cattle is testified by reduced albumin secretion and liver
enzyme activities (Ronchi et al., 1999).
Oxidative Stress
In farm animals, oxidative stress may be involved in several pathological conditions,
including conditions that are relevant for animal production and the general welfare
of individuals (Lykkesfeldt and Svendsen, 2007). Oxidative stress results from an
imbalance between oxidant and antioxidant molecules and may depend on the excess of
oxidant and/or lack of antioxidant substances (Figure 4). In the last 10 to 15 yr,
the involvement of heat stress in inducing oxidative stress in farm animals has received
increasing interest (Bernabucci et al., 2002; Akbarian et al., 2016). The total antioxidant
status concentrations in serum of heifers were lower in the summer than in the winter
in peri- and postpartum periods (Mirzad et al., 2018). In mid-lactating cows, plasma
values of reactive oxygen metabolite substances were increased during summer. Total
carotenes and vitamin E were decreased during summer. Increased oxidant and decreased
antioxidant molecules in blood during the hot summer season have been reported both
in dairy and buffalo cows. Finally, heat stress has been associated with an increase
of antioxidant enzyme activities (e.g., superoxide dismutase, catalase, and glutathione
peroxidase), which has been interpreted as an adaptation response to increased levels
of reactive oxygen species.
Figure 4.
Balance between oxidants and antioxidants molecules in animal health and disease (from
Knoefler et al., 2014).
Immune Suppression
The immune system has evolved as a complex of mechanisms to protect the host from
invasion by pathogenic organisms. A number of factors may affect the proper functioning
of the immune system (Lacetera, 2012). Several studies reported that heat stress may
impair the function of the immune system in food-producing animals. Effects of heat
stress on immune function are not always straightforward and may depend on the species,
breed, genotype, age, social status, acclimation level, and intensity and duration
of the exposure to the unfavorable conditions.
Immune suppression facilitates the occurrence of infections, which impairs reproductive
efficiency, overall production efficiency, and may compromise animal welfare and increase
the use of antimicrobials. Increased use of antimicrobials may lead to development
of antimicrobial resistance in microorganisms.
Briefly, Regnier and Kelley (1981) reported that chronic exposure to heat stress impaired
immune response in avian species. Nardone et al. (1997) indicated that severe heat
stress reduced colostral immunoglobulins (IgG and IgA) in dairy cows with negative
consequences on immunization and survival of newborn calves. Lacetera et al. (2005)
described a dramatic depression in lymphocyte function in severely heat stressed peri-parturient
dairy cows, which may increase their vulnerability to pathogens and also reduce the
efficacy of vaccinations. Finally, Lecchi et al. (2016) reported that high temperatures
impaired significantly the functionality of neutrophils, which have a central role
in the protection of the mammary gland against infections. Mastitis is a major endemic
disease of dairy cattle and usually occurs as an immune response to bacterial invasion
of the teat canal or as a result of chemical, mechanical, or thermal injury to the
cow’s udder. Several studies reported the increased occurrence of mastitis during
the summer months (Morse et al., 1988; Waage et al., 1998). Results of a recent 2-yr
study on the largest Italian dairy farm demonstrated that the greater risk of the
occurrence of clinical mastitis in primiparous dairy cows was recorded in July (Vitali
et al., 2016). Heat stress may improve the survival capability or growth of pathogens
or their vectors (Chirico et al., 1997), and they may surely be involved in these
important epidemiological findings. Further epidemiological studies are necessary
to determine whether high environmental temperatures are associated with a higher
incidence of other infections. The potential for impairment of immune cell function
under hot environment supports the use of management practices (i.e., cooling, altered
nutritional programs, improved animal hygiene, etc.), which may help to limit the
increase of body temperature to prevent outbreaks of infections.
Death
A series of studies have described a greater risk of mortality during the hottest
months (Dechow and Goodling, 2008; Vitali et al., 2009) and an increased death rate
during extreme weather events (Hahn et al., 2002; Vitali et al., 2015). High temperatures
may cause heat stroke, heat exhaustion, heat syncope, heat cramps, and ultimately
organ dysfunction. These heat-induced complications occur when the body temperature
rises 3 to 4 °C above normal.
In an Indian study, Purusothaman et al. (2008) reported an increase of mortality in
Mecheri sheep during summer season. Another series of studies on the effects of temperatures
on mortality in farm animals described an increase of deaths during extreme weather
events. Hahn and Mader (1997) and Hahn et al. (2002) described the impact on livestock
from a weeklong heat wave in the mid-central United States during July 1995. A heat
wave is generally defined as a prolonged period of excessively hot weather. It was
also reported that during the severe and prolonged heat waves which occurred in Europe
during summer 2003, over 35,000 people and thousands of pigs, poultry, and rabbits
died in the French regions of Brittany and Pays-de-la-Loire (http://lists.envirolink.org/pipermail/ar-news/Week-of-Mon-20030804/004707.html).
Vitali et al. (2015) indicated that summer mortality in dairy cows was greater during
days in a heat wave compared with days not in a heat wave. Furthermore, the risk of
mortality continued to be higher during the three days after the end of the heat wave.
Mortality also increased with the length of the heat wave. Considering deaths stratified
by age, cows up to 28 mo old were not affected by heat waves, whereas all the other
age categories of cows (29 to 60, 61 to 96, and >96 mo) showed a greater mortality
when exposed to a heat wave. The risk of death during a heat wave was higher in the
early summer months. In particular, the highest risk of mortality was observed during
a heat wave in June.
The temperature–humidity index combines temperature and humidity into a single value
and is widely considered a useful tool to predict the effects of the environment on
farm animals.
An epidemiological study with dairy cows (Vitali et al., 2009) indicated that 80 and
70 are the daily maximum and minimum temperature–humidity index values, respectively,
above which heat-induced death rate increases. In addition, the same study indicated
that 87 and 77 are the daily upper critical maximum and minimum temperature–humidity
index, respectively, above which the risk of heat-induced death becomes maximum.
A recent study with swine in Italy reported the effects of month, length of the journey,
and temperature–humidity index on mortality of heavy slaughter pigs (approximately
160 kg live weight) during transport and lairage (Vitali et al., 2014). The aggregated
data of the summer vs. nonsummer months showed a greater risk of pigs dying during
the hot season when considering both transport and lairage. The month with the greatest
frequency of deaths was July, whereas the lower mortality risk ratios were recorded
for January and March. The mortality risk ratio during transport increased significantly
for journeys longer than 2 h. Finally, 78.5 and 73.6 temperature–humidity index were
the thresholds above which the mortality rate increased significantly during transport
and at lairage, respectively. In a long-term study on scenarios of temperature-related
mortality in Europe, Ballester et al. (2011) predicted a change in the seasonality
of mortality, with maximum monthly incidence progressively shifting from winter to
summer from 1950 to 2100.
Indirect Effects
As already described earlier, weather and climate change are likely to affect the
biology and distribution of vector-borne infections. For example, temperature changes,
global wind and precipitation patterns, and changes in relative humidity in temperate
climates will affect positively the reproduction of insects and, consequently, their
population density. Thus, some tropical diseases, especially those transmitted by
insects, may probably move from their natural basin of endemic to other countries.
Simulating an increase of temperature values by 2 °C, a model tested by Wittmann et
al. (2001) indicated the possibility of an extensive spread of Culicoides imicola,
which represents the major vector of the bluetongue virus. This virus is responsible
for an infectious arthropod-borne disease primarily of domestic and wild ruminants.
Infection with bluetongue virus is common in a broad band across the world. Since
1990, this virus has spread considerably due to changing climatic and environmental
conditions necessary to support the Culicoides vectors.
Another mechanism through which climate change may alter livestock and human health
is represented by the favorable effects that high temperatures and moisture may exert
on growth of mycotoxin-producing fungi. Growth of these fungi and the associated toxin
production are closely related to the temperature and degree of moisture, which are
dependent on weather conditions at harvest and techniques for drying and storage of
grains (Frank, 1991). Mycotoxins can cause acute disease episodes when animals consume
critical quantities of contaminated feeds. These mycotoxins may have a negative effect
on specific tissues and organs such as liver, kidney, oral and gastric mucosa, brain,
or reproductive tract. Most frequently, however, concentrations of mycotoxin in feeds
are below those that can cause acute disease. At low concentrations, mycotoxins may
reduce the growth rate of young animals. Some mycotoxins may interfere with the native
mechanisms of disease resistance and may impair immunologic responsiveness, making
the animals more susceptible to infection (Bernabucci et al., 2011).
Finally, other examples of how climate change may affect animal health are provided
from parasitic diseases. In this context, gastrointestinal nematodes are important
parasites of livestock, causing mortality and morbidity. Because a significant part
of the life cycle of these parasites is completed outside of the host, their survival
and development are susceptible to climate change. In this regard, a recent simulation
study (Rose et al., 2015) predicted that future climatic data for a temperate region
will have an opposite effect on annual infection pressure (increase or decrease) depending
on the species of parasites.
Conclusions
Although further epidemiological studies are needed, a significant amount of research
has already demonstrated that climate change will affect animal health and welfare.
Heat stress conditions as a result of global warming, high air temperatures, and higher
frequency of extreme weather events and droughts may negatively affect animal health
and welfare. Such effects may take place by direct and/or indirect mechanisms. Tools
and techniques for an animal disease surveillance system to incorporate animal data
with relevant climate conditions are also needed. Development and application of methodology
to link climate data with disease surveillance systems should be implemented to improve
prevention of diseases as well as mitigation and adaptation responses of animals to
heat stress.