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"...I read the Sterile Gut article. Real eye opening! It sure discribes what I have been experiencing." Richard Rolloff -Belgian Waterslagers

Dr Rob Marshall has written this article
to explain his thoughts on the sterile bowel theory.

At an Association of Avian Veterinarian International Conference held in 1989 I was surprised when first hearing that both Dr Gerry Dorrestein and Dr Helga Gerlach believed the bowel of healthy finches and canaries was sterile. At Veterinary school I had been taught that bacteria played a vital role in the continuing health of the animals we studied (dogs, cats, cows, horses as well as poultry). I instantly accepted the opinions of these two eminent bird pathologists and immediately used this new found knowledge to help me understand the special nature of Passerines in general and finches in particular.

The Sterile Bowel Theory is supported by the following facts:

1. Finches belong to the most advanced order of birds: Oscine passerines.
2. Oscine passerines have developed specialized adaptive anatomical and physiological systems that are different from the more primitive bird orders (eg Galliformes)
3. The high metabolic rate of Oscine Passerines (eg finches) requires much more additional energy. In passerines more advanced and improved chemical digestion and intestinal absorption provide this additional energy.
4. Bacterial fermentation is an inefficient source of energy. Birds with caeca utilise bacteria to help digest fibrous matter. Finches have no caeca.
5. Finches have no resident bowel or so-called "friendly bacteria". "Friendly Bacteria" is a concept that explains the theory of probiotics.

Knowledge of the special position Passerines hold in the bird world should help you understand the notion of a sterile bowel in these birds.

Passerines are the most recent and advanced order of bird species. They account for approximately three fifths of all living birds, or some 5,739 of the 9,702 species of 1,168 genera. Other birds such as poultry (Galliformes) belong to much older and more primitive orders of birds.

Passerines broke away from the normal avian (more primitive bird orders) mould to become the most successful group of birds. They appeared in force by adaptive radiation after the Paleogene time period moving them into unexploited and unrestricted ecological zones largely because their complex nest building behaviour released them from the limited resource of cavity nesting. Passerines were so successful during the late Tertiary period that lines of demarcation among families and higher groups are poorly defined, so that differences among many passerine families are not as great as those among non-passerine genera. Almost all recent workers have considered the order Passeriniformes to be monophyletic sharing many anatomic and physiological similarities (a special type of palate and syringeal anatomy, bundled spermatozoa, the distinctive passerine foot and an elevated metabolic rate).

The elevated basal metabolic rates of Passerines compared to other birds are an indication of the uniqueness of this group of birds. This finding also supports a view that their bowel is sterile. The basal (at rest) metabolic rates of Passerines average some 50-60% higher than non-passerines of equivalent size. This feature found in Passerines reflects a significant move away from the physiology established in more primitive bird forms such as Galliformes (poultry).

Passerines can be divided into two broad groups: Suboscines and Oscines. The Oscines constitute about four fifths of the Passerine birds and are extremely uniform in their morphology. They are referred to as the "songbirds" that largely inhabit temperate zones of the world. Finches are a part of the Oscine group of Passerines. The suboscines are slightly less morphological uniformity and are prominent in neo tropical regions. The Australian Lyrebird and scrub birds do not fit into the classical definition of suboscines or Oscines.

Our interest lies in the Oscines that occupies temperate zones of the world. The Oscines represent an absolute extreme among birds and perhaps all living vertebrates in their morphological uniformity. Most are small land birds primarily adapted for feeding on insects, small fruits and seeds and therefore many of the differences we do see among them are in the feeding mechanism and bill structures that are often convergent rather than indicative of any evolutionary link. Similarly the digestive tract of the seed-eating finches should be viewed as an adaptive change with no evolutionary link to more primitive orders of birds.

The lack of major gaps among many Oscine families suggest the adaptive radiation of modern, advanced Oscines is probably quite recent perhaps dating to the Medial to late Tertiary period of time. For this reason we should not assume any evolutionary link between the digestive physiology of primitive birds forms such as Galliformes (poultry) and the most advanced and recent birds; the Passerine Oscines.

Current knowledge of the digestion of food in birds is the result of scientific studies performed on poultry. Poultry belong the Galliformes a most primitive form of birds. In these birds the crop, proventriculus, gizzard, small intestine and caeca are all involved in the digestive process. The gastric apparatus includes the proventriculus (secretes acid gastric juice and pepsin) and gizzard action (grinding action and acid proteolysis).The principle organ for chemical digestion and absorption takes place in the small intestine. Here the chyme from the gizzard is neutralised by the highly buffered bile, pancreas juice and Sulcus Entricus so the pH especially in the ileum is between 6-8. Chemical digestion of starch is effected largely in the small intestine through activities of pancreatic amylase and of intestinal and pancreatic maltase. Lactose and sucrose are hydrolysed by lactase and maltase respectively in the Sulcus Entricus.

In birds that must digest fibrous plant foods the caeca (birds have paired caeca) are well developed and the combined length of the caeca may be the length of the small intestine. The caeca harbour bacteria that help break down plant cellulose into simple digestible carbohydrates. Food reaches the caeca by anti-peristaltic movements of the rectum. Recent research has shown that bacterial fermentation in the caeca supplies only a small fraction of the total energy requirements of birds, so the real importance of the caeca in the domestic fowl is in doubt. Finches have no caeca.

Although microbiological digestion and fermentation of cellulose occur in the caeca of some Galliform species, the frequently repeated suggestions that these processes also occur in granivore species such as parrots, pigeons and finches which have no functional caeca has not been experimentally substantiated.

Passerines have no caeca and therefore no intestinal flora for microbiological digestion.

Food eaten by finches is digested chemically and then absorbed in the small intestine without the presence of symbiotic bacteria. Passerines are not considered to have a permanent gut flora. The microscopic examination of faecal smears from healthy finches does not reveal bacteria or other organisms. Routine aerobic microbiological cultures taken from droppings of passerine birds do not produce any bacterial growth.

Discussion
It is commonly accepted that Oscine Passerines are the most modern and advanced of birds. Their small size and high metabolic rate (65% greater than for non-passerine birds) that has allowed them to occupy their dominant numerical position in the bird world has meant that further physiological adaptations have also become necessary. The Oscines require an increased source of energy to maintain their high body temperature (2 degrees Celsius higher than other birds).They must eat (up to 30% of their body weight daily) and drink (25-30mls per 100grams body weight daily) relatively enormous amounts to maintain their energy levels. As well the food must be digested and absorbed as quickly as possible. Death from haemorrhagic diathesis that occurs in finch species that have not eaten within 48 hours is testament to the vascularity and highly efficient absorption mechanism of the small intestines of finches.

Bacteria present in the bowel of the more primitive bird forms (eg Galliformes) that help with digestion and also produce vitamins and other metabolites are not required in Passerines. The extremely high-energy requirements of these small birds are covered by an increased activity of the enzymes lipase and amylase. Refined chemical (enzymes) digestion and enhanced absorption capabilities present in finches is a far more efficient method of energy production. The environmental niches occupied by the more mobile oscines are also more likely to provide the required dietary vitamins and other metabolites.

Resident bacteria exist in many bird species. They help repel potentially harmful environmental bacteria. These "friendly bacteria" vary from one bird species to another and relate to their natural environment, for example, my studies on the wild Budgerigar have revealed the presence of Streptococcus faecalis as a normal inhabitant the bowel. Under adverse conditions this normal bacteria may produce disease. Poultry have a wide range of normal gut bacteria as they have adapted to an environment rich in these bacteria and germs. Probiotics have been produced mainly for poultry species in order to counteract the potential harmful effects of normally encountered bacteria. In order to work properly, probiotics must colonise the bowel and to do so they must be part of the normal gut microflora.

Consequently, probiotics designed for poultry will not be effective for parrots or paserines. The acidifying effect of Lactobacillus acidophillus, a common ingredient of probiotics, is responsible for a beneficial effect experienced with "generic" probiotic use. Probiotics do not apply to Oscine Passerines (finches) because it is commonly agreed that the healthy finch has no resident gut bacteria.

The notion that finches have a sterile gut is important but often misunderstood. Autolysis that occurs after death does not require the presence of bacteria in the bowel. The proteolytic tissue damage that results following death allows anaerobic bacteria to colonise these tissues from the outside to the body. Resident bacteria found in the more primitive bird species play a part in preventing bowel infections but the more conventional immune modulators remain the main barriers to infection from environmental germs in these species. The role of the very high body temperature of finches should not be underestimated as an important supporting role in preventing colonisation of the bowel with harmful bacteria.

I thank www.ladygouldian.com for the opportunity to outline the theory of the "sterile gut". Please submit your questions to Support@ladygouldianfinch.com.

References

1. Seminars in Avian & Exotic Pet Medicine Volume 12 Number 1 Jan 2003, pages 12-22
2. Origin & Evolution of Birds. Feduccia, pages 346ff
3. Birds: Structure and Function. King and McLelland, pages 104,105
4. Disease of Cage and Aviary Birds. Petrak Edition 2, page 189
5. Manual of Ornithology: Avian Structure and Function. Proctor and Lynch, page 18
6. Avian Medicine Principles and Application Ritchie, Harrison and Harrison, page 1187

Q & A

Q: Laraine is Dr. Marshall implying in his article that we should not use probiotics on finches? I just wanted to confirm before I continue using them. Serge, Ontario, Canada

A: Yes Serge, Dr. Marshall, along with several other respected veternarians believe that finches do not have any "resident friendly gut bacteria" which would be used to digest and process their food intake. Because of the requirement that finches have for large amounts of quick energy, they have evolved with the ability to digest food through a chemical process which does not involve bacterial digestion.

I used probiotics on my birds for 20 years, so giving it to our caged finches doesn't appear to cause harm, although we are providing them something that isn't natural to their physiology. My understanding is that it does help the finch to maintain an "acid" condition in the gut because Lactobacillus produces lactic acid. But there are other ways to help our finches maintain the "acid state" of their gut.

Most probiotic research is based upon work done in the poultry industry. Since each species has it's own particular "friendly gut bacteria", it would be better if we were giving the bacteria specific to the species. Therefore many of the one's currently available contain multistrain avian origin bacteria. Since many of the large pet birds like the hook bills do have "friendly bacteria" they would need probiotics under certain circumstances.

Q & A

Q: I have read your article entitled STERILE BOWEL THEORY. Well done on your article. It is going to be a great help to a great many people, me included.

You wrote :

4. Bacterial fermentation is an inefficient source of energy. Birds with caeca utilize bacteria to help digest fibrous matter. Finches have no caeca.
   
5. Finches have no resident bowel or so-called "friendly bacteria".

Since passerines do not have resident bacteria, then does this mean that the intestinal lining of passerines has not structurally evolved to being colonized by any bacteria, pathogenic or otherwise? The structure of the epithelial intestinal lining of passerines may well hold an answer as to HOW these birds maintain a sterile gut in the wild. The reason I ask this question is because much is made of the importance of giving Lactobacillus strains from a bird and not a cow, to chickens for example because the epithelial lining of chickens is better designed to accommodate avian as opposed to mammalian strains of the Lactobacillus. Please tell me if you think this is correct information.

If the intestinal lining of passerines has NOT structurally evolved to being colonized by bacteria, yeasts or protozoa, why is it that Candida, Avian Gastric Yeast, Campylobacter, E. coli and Trichomonas for example can invade the gastro intestinal tract of a finch and make them quite ill ? If the intestinal lining of passerines HAS structurally evolved to being colonized by any bacteria, yeasts or protozoa, then how is it possible for the gastro intestinal tract of passerines to remain sterile?

Weak organic acids such as apple cider vinegar and grapefruit seed extract solutions and certain herbs can suppress the growth of or probably even kill the bacteria and yeast from the beak and throat to the crop. But according to my information, the antibacterial, antifungal or antiprotozoal power of these weak inorganic acids and herbs will be substantially reduced from the stomach to the anus because they will be in turn chemically digested in the stomach of the passerine and so lose their antibacterial, etc. properties for the most part.

So it would seem that UNLESS the passerine is QUICK in ingesting the antibacterial, antifungal or antiprotozoal self medicating substance in time for the pathogens to be destroyed in THE CROP where food is stored initially before making its way to the stomach, any pathogens that the passerine ingests and are able to survive its digestive chemicals, WILL BE ABLE TO FLOURISH from the stomach to the anus. Please tell me if you think this is correct information.

You also wrote :

3. The high metabolic rate of Oscine Passerines (eg finches) requires much more additional energy. In passerines more advanced and improved chemical digestion and intestinal absorption provide this additional energy.

Can you list the chemicals that are involved in passerine digestion please?
Do the gastric cells in the stomach lining produce these chemicals or are they produced in the body interior and then passed on to the stomach?

Regarding the improved intestinal absorption, where does absorption take place in a passerine and does this mean that bacterial, fungal and protozoa pathogens are able to be absorbed INTO THE BLOOD STREAM with improved efficiency or does this improved absorption only relate to digested food?

I am VERY interested in you as a person and in your work and I think the Sterile Bowel Theory rounds up some of the most important aspects of understanding our pet finches. :)

Thank you.

Sincerely, William Astor

A: Oscine passerines are highly evolved. They are a most recent family of passerine birds that has developed a highly sophisticated digestive system. Advanced methods of immunity (cell based) are used to control exposure to bowel infection.

It is not the structure of the epithelial lining that is the answer to how they maintain a sterile gut, but their entire immune system and organs that operate on a cellular level. There is a good reference book on immunity and the nature of disease. I believe you will find this text very enlightening. (1)

Finches are more susceptible to those organisms for which it has had little genetic and environmental exposure. This occurs, for example, in both Gouldians and Budgerigars. Both are a desert/arid-evolved species. Candida, E. coli, Coccidiosis and Trichomonosis are often rapidly fatal diseases in both species because these are diseases of a wet environment to which they have had little genetic exposure.

Campylobacter, for example, is of no concern for Bengalese finches, because they have an innate immunity to this disease. Gouldians, genetically, have had no exposure to Campylobacter and in juveniles this may also be a rapidly fatal disease. Megabacteria is a complex disease intimately related to the pH levels of the proventriculus. Conditions that change the acidity of the proventriculus (eg. Coccidiosis and Thrush infections) predispose birds to Megabacteria infections. Thrush (Candida albicans) colonizes keratinized surfaces only. Therefore Thrush cannot and does not colonize the small intestine. It will colonize the mouth, crop and gizzard. These are the organs where Megamix & KD exert their beneficial effect on Thrush and other germs in finches

We must remember all bowel infections originate from ingestion of contaminated sources. Organic acids are not corrosive but are used to change pH levels in the crop and sometimes in the bowel. The pH level changes we are talking about have a range of only 1 pH unit. Further information regarding the normal acidity of the finch digestive tract and the function of organic acids is explained in the Gouldian & Finch Health book. Organic acids may be buffered or un-buffered. Buffered organic acids will have an effect on the crop and beyond. Organic acids are not intended to cure disease but are used to help prevent alkaline related bowel diseases. They do not kill organisms but retard their multiplication. In doing so, they allow normal immune function (a complex chain of events) to re-establish a healthy bowel. The most important part of recovery is to identify the reasons the bowel has become alkaline.

In birds, the digestive process involves in part, proteolytic enzymes that are produced in the pancreas and stomach (proventriculus). Current knowledge concerning the digestion of food in birds is the result of scientific studies performed on poultry. Poultry belong to the Galliformes, a most primitive form of birds. In these birds, the crop, proventriculus, gizzard, small intestine and caeca are all involved in the digestive process. The gastric apparatus includes the proventriculus (secretes acid gastric juice and pepsin) and gizzard action (grinding action and acid proteolysis). The principle organ for chemical digestion and absorption is the small intestine. Here the chyme from the gizzard is neutralized by the highly buffered bile, pancreas juice and Sulcus Entricus. The pH, especially in the ileum, usually falls between 6-8. The chemical digestion of starch is effected largely in the small intestine through activities of pancreatic amylase and of intestinal and pancreatic maltase. Lactose and sucrose are hydrolyzed by lactase and maltase respectively in the Sulcus Entricus.

Remember, absorption and nutrition takes place mostly in the stomach and small intestine. In some species, there is also cloacal reabsorption. Absorption of nutrients differs from absorption of microbes. The referenced texts listed at the end of the Sterile Gut Theory article are good references for the differences between absorption of nutrients and the absorption of microbes.

Thank you very much for your interesting questions.
Rob Marshall

REFERENCES
1. MECHANISMS OF DISEASE. By Slauthon and Cooper, Published by Mosby

Q & A

Q: Dear Dr. Marshall,
You wrote..

"Buffered organic acids will have an effect on the crop and beyond."

If by this you mean all the way to the cloaca, then it means that alkaline related diseases in our pet finches could be a thing of the past. The all-important question therefore is: How can I make a buffered version of apple cider vinegar? Is it possible to make a buffered version of grapefruit seed extract [ not grapeseed extract ] solution? Is it possible to make a buffered version of various herbal teas?

A: The above three questions require the help of a chemist.

Q: You wrote...

"Organic acids are not intended to cure disease but are used to help prevent alkaline related bowel diseases. They do not kill organisms but retard their multiplication. In doing so, they allow normal immune function (a complex chain of events) to re-establish a healthy bowel."

Am I right in thinking that in slowing down pathogen multiplicaton, organic acids make it less likely for these pathogens to migrate to other parts of the body? In other words, am I right in thinking that it takes a certain population density of pathogens in the gut of the finch before any of those pathogens can migrate to other parts of the body ?

A: This is true. Overwhelming numbers of pathogens colonize the bowel lining and may then be absorbed into the bloodstream and then move to other parts of the body. Most have a local effect alone.

Q: You wrote...

"The most important part of recovery is to identify the reason.."

After several years of keeping Gouldians, I found that the birds would succumb to Candida sooner or later even though I gave them sterilized food and drink containers each day to eat and drink from and even though the air was not moist. In my bird-room at the moment, I also see evidence of a serious yeast problem. I have come up with the following explanation.

The cause I think is that in indoor bird-rooms of the Temperate Zone, bird breeders are forced to keep the windows shut for most of the year due to the intense cold air outside. This sets the stage for any air transmissible pathogens to wreak havoc on the birds. Many times I have heard of how bird-rooms were filled with dead birds when a bird with a virus e.g. Newcastle disease virus was introduced in one of the cages.

But even if the virus itself is not normally air transmissible, there is evidence to indicate that inhaling skin or dust particles may infect birds as well. Again air is playing a role. Fungi like Aspergillosis and Ergot in such a situation, can easily invade the birds because the spores cannot be spread and thinned out by the wind. In the still air of the indoor bird-room with shut windows, the birds have no choice but to breathe in the spores in the air until they succumb.

A: This is very true with airborne infection.

Q: Yeasts like Candida [I don’t know whether Megabacteria can produce spores like Candida can] reproduce asexually by a process called budding but a few yeasts, such as Candida, also produce clusters of asexual reproductive spores. I think the reason why birds succumb so often to Candida in these situations is because this yeast can reproduce by air transmissible spores. The birds defecate. Their droppings contain Candida. In the watery environment of the dropping, the Candida reproduces and forms spores. At least this is what I think is happening. Unfortunately I do not have access to a laboratory of my own as you do.

A: I do not believe Candida is an airborne disease but certainly in a watery environment, it reproduces and forms spores. A dehumidifier or humidity control unit may be of great advantage.

Q: If what I am saying is correct, I am thinking that it may be a good idea to install a UVC box. According to what I have been told, it is UVC which kills all air pathogens but the scary bit about UVC is that it is extremely dangerous, leading to problems such as cancers and permanent eye damage - even total blindness in humans if it is not fully contained in a protective box. So I will have to proceed very carefully in building a UVC air purification device. What I have to do is find some material that will thoroughly absorb UVC radiation and somehow build a box that will contain a tube in there.

A: I believe airborne pathogens may be a problem and a UVC air purification system would be helpful.

Q: I have found an American website that sells these devices at : www.aircleanerforbirds.com

But they are prohibitively expensive. Cost is about 1100 Australian dollars and the HEPA filters each cost 110 dollars and they are to be replaced every 3 months.

I think using a UVC tube to get rid of air pathogens is a lot cheaper than having to replace a HEPA filter once every 3 months. This is the reason why I would be persuaded to build a UVC device myself.

Another aspect to this is that I think it would be stupid to have the air completely devoid of pathogens because it is important for the birds to be exposed to some pathogens so that their immune system will have be able to manufacture antibodies that the hens can pass on to their offspring so that the offspring in turn will be able to fight off pathogens, The idea is to REDUCE the number of air pathogens but NOT TO STERILIZE the air space in the bird-room.

A: I agree, although I have no experience with the UVC. Regular cleaning surface disinfection would be a good practice. This would decrease pathogen levels. Regular filter disinfection on air conditioner filters is also an excellent idea.

Q: I am wondering how many hours you would recommend leaving this UVC device switched on in a bird-room 5 meters x 3 m x 2 m in order to achieve this objective.

Thank you.
William Astor

PS: This is Laraine speaking now... my new aviary has been set up to control the excessively high humidity that we experience here in Georgia. Therefore the birds are now in a humidity controlled, but not temperature controlled environment. My husband, being a HVAC technician, has designed a recycled air system which is UVC and HEPA filtered. My water supply for the birds has been UVC filtered for 2 years now. I will soon have an article on this web site relating the procedures involved and the effect this environment is having on my birds.

GLOSSARY
Sterile Bowel Theory

Adaptive Radiation the gene pool of a species undergoing changes, where the best suited gene becomes more frequent in the species' population, depending upon the environment. Over time the same species can diversify into other species; each trying to be as adaptive as possible in their environment.

Aerobic microbiological cultures culturing of droppings in the presence of oxygen (normal culture technique) as opposed to anaerobic (special technique) where no oxygen is present during culturing

Anaerobic Bacteria bacteria not capable of survival in the presence of oxygen (gangrene or botulism)

Autolysis the normal decaying process of tissue after death

Bacterial Fermentation a chemical change producing energy by the multiplication and growth of bacteria

Basal Metabolic Rate a body's metabolic rate while in a resting state

Caeca organ in the digestive tract of most birds, attached to the intestine in the area of the rectum, equivalent to the human appendix. Cellulose breakdown by bacteria occurs in the caeca of more primitive orders of birds. When present in a finch it is small and plays no part in digestion

Chyme lymphatic fluids, a semi-fluid mass of partly digested food after passing from the stomach into the intestines

Friendly Bacteria referring to bacteria which is naturally occurring in the gut for a particular species; as in yogurt cultures for human health

Galliformes a primitive order of birds including game birds (pheasants, grouse etc.) and domestic poultry

Granivore species seed eating birds

Hemorrhagic diathesis clotting defect associated with shock like syndrome which causes hemorrhage from the bowel and subsequent bleeding to death

Hydrolyzed breaking down food into a more usable form

Monophyletic derived from a single common ancestral form

Oscine the most recently developed group of Passerines which have a highly specialized vocal apparatus, songbirds

Paleogene, Medial and Teriary Periods geological time periods lasting millions of years

Pancreatic Amylase and Maltase enzymes used in digestion

Passerines birds belonging to an order of birds called Passeriniformes

Passeriniformes an order of birds which perch, comprising more than half of all living birds, songbirds

Proteolytic processes in digestion, the breaking down of proteins in food eaten to form simpler soluble products

Suboscines a more primitive group of Passeriniformes than Oscines

Sulcus Entricus folds in the intestinal lining

Symbiotic Bacteria "friendly bacteria" living within a species causing no harm to the host but playing a part in certain processes within the host organism

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