Agriculture Reference
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compartments of the host. It also opened the way for different administration methods. Indeed,
the fact that there are other compartments in man and animals colonized by symbiotic microor-
ganisms, such as the oral cavity, skin, vagina or fish gills, had been so far neglected. This
is in line with Gatesoupe (1999) who emphasized that in aquaculture, a probiotic treatment
through rearing water could also be of importance since the overall microbiota of fish and
shellfish depends on the external environment. Verschuere
et al
. (2000) presented a similar but
extended definition as follows: 'live microbial adjunct which has a beneficial effect on the host
by modifying the host-associated or ambient microbial community, by ensuring improved use
of the feed or enhancing its nutritional value, by enhancing the host response towards disease,
or by improving the quality of its ambient environment'.
The idea that probiotics may be applied via the rearing water further complicates the defi-
nition process because it impacts upon closely related terms such as bioaugmentation, biore-
mediation and biocontrol. With respect to animals reared in aquatic environments, it has been
suggested that microbes that are antagonistic to pathogens, but are not found to populate the
host's GI tract, should be termed biocontrol agents (Maeda
etal
. 1997; Moriarty 1998). Aquatic
microbial applications which improve water quality by the breakdown of waste or pollutants
have been termed bioaugmentation or bioremediation (Moriarty 1997; 1998; Gatesoupe 1999).
Given the large variations in defining criteria for aquatic probiotic applications, and the overlap
with related concepts, Merrifield
etal
. (2010) proposed a more inclusive and broader definition
for a probiotic intended for use with aquatic animals: 'any microbial cell provided via the diet
or rearing water that benefits the host fish, fish farmer or fish consumer, which is achieved, in
part at least, by improving the microbial balance of the fish'. In this context direct benefits to
the host were considered as immunomodulation, improved disease resistance, reduced stress
response and improved GI morphology, among others, and benefits to the fish farmer or fish
consumer as improved fish appetite, growth performance, feed utilization, improvements in
carcass and flesh quality, and reduced malformations.
In 1996, both Salminen and Schaafsma generalized the definition by not considering the
influence of the indigenous microbiota on the health effects observed. Rather, they attributed
the beneficial effects to the probiotics themselves: 'a live microbial culture or cultured dairy
product which beneficially influences the health and nutrition of the host' (Salminen 1996).
Schaafsma (1996) was also the first to mention the importance of the probiotic dose required
to achieve enhanced effects: 'living microorganisms which upon ingestion in certain numbers
exert health effects beyond inherent basic nutrition'. Salminen
et al.
(1999) introduced the
idea that viability of probiotics was not a prerequisite for functionality, that is, 'microbial cell
preparations or components of microbial cells that have a beneficial effect on the health and
well-being of the host'. However, this implies that bacterial metabolites and bacteria-derived
immunostimulants may then be considered as probiotics. This was based on recent findings
where the use of inactivated cells led to positive health effects (Ouwehand and Salminen 1998).
In fact, this may be considered advantageous with respect to regulatory issues since non-viable
probiotics and microbial cell wall components are less likely to cause safety concerns than
their live counterparts. Despite these findings, a group of experts adopted the following def-
inition in an FAO/WHO report from 2002: 'Live microorganisms which when administered
in adequate amounts confer a health benefit on the host'. In 1988, the US Food and Drug
Administration (FDA) defined live microbes used in animal feeds as 'direct-fed microbials'.
Those intended for therapeutic effect in humans, that is, used as drugs, have been classified
as 'live biotherapeutics' by the FDA's Center for Biologics Evaluation and Research, and the
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