Wednesday, February 4, 2009

Sugar, Hydrogen, Bacteria and Maldigestion

There are several ways to cause a nutrient deficiency. The first is to eat too little of a nutrient. Another way is to burn through your body's nutrient stores at an accelerated rate, for example, what omega-6 vegetable oils do to vitamin E, and what wheat bran does to vitamin D. A third way is to eat enough nutrients but fail to absorb them efficiently.

A good way to reduce your absorption of nutrients is to lower your stomach's acidity. This will protect you from those pesky nutrients protein, vitamin B12, and iron (and probably others as well). The stomach is one tough organ. When it receives food, a healthy stomach lowers its pH to roughly 2.0 by secreting hydrochloric acid. That's more acidic than lemon juice and more than 10 times more acidic than vinegar. This begins to break food down, and will kill most bacteria and other pathogens. Stomach acidity is basically the body's way of "cooking" food before further digestion. At the same time, the stomach secretes pepsin, which is an acid-stable enzyme that digests protein.

Insufficient stomach acidity promotes bacterial overgrowth in the small intestine and allows undigested proteins into the intestine. The gastrin knockout mouse, which is incapable of producing stomach acid, suffers from bacterial overgrowth, inflammation, damage and precancerous polyps in its intestines. The same thing happens when you treat mice with a drug that inhibits stomach acidification.

There are a few different ways to reduce your stomach's acidity level. The most straightforward is to take an antacid, or any number of drugs that lower stomach acidity (as in the mouse study above). But can we do it naturally? Sure, all it takes is a little Helicobacter pylori infection! Luckily, most people already have one.

H. pylori is a bacterium that's the main proximal cause of stomach ulcers. Antibiotics are now the standard treatment for ulcers, and they're effective. Treating an asymptomatic H. pylori infection with antibiotics increases stomach acidity, suggesting that H. pylori is capable of suppressing the secretion of stomach acid. In another study, eradicating H. pylori with antibiotics improved nearly all patients suffering from hypochlorhydria (insufficient stomach acid).

Like any organism, H. pylori likes to stay well-fed. Its favorite food is hydrogen gas (H2), and the more it gets, the more it grows. It's not the only bacterium to like H2. Salmonella, of food poisoning fame, requires H2 to become pathogenic. Clostridium bacteria are also associated with elevated H2. H2 is produced by the fermentation of food by bacteria in the digestive tract. It's very small so it diffuses around the body, reaching the stomach lining where it's eagerly gobbled up by H. pylori. It may be equally good food for a number of other parasites around the body.

Now let's stop beating around the bush and get to the meat of this post. It's all summed up in a beautiful title: Fructose Intake at Current Levels in the United States May Cause Gastrointestinal Distress in Normal Adults. Dr. Richard W. McCallum et al. fed doses of isolated fructose to 15 normal adults. Can I say it any better than the abstract?
More than half of the 15 adults tested showed evidence of fructose malabsorption after 25 g fructose and greater than two thirds showed malabsorption after 50 g fructose... Fructose, in amounts commonly consumed, may result in mild gastrointestinal distress in normal people.
Here's where it gets really interesting. One of the measures of malabsorption they used was H2 on the breath. Both the 25g and the 50g doses caused a large increase in H2, especially the 50g dose (5-fold increase). This is the same thing you see in people who are lactose intolerant. Bacterial fermentation is the only significant source of H2 in the human body. That means the fructose was hanging around in the small intestine for long enough to be decomposed by the local bacteria, who took advantage of it to proliferate.

Certain types of fiber also promote H2 production. Resistant starch, as well as certain non-caloric sweeteners, are readily fermented into H2 in some people. Cellulose, the predominant fiber in vegetables and grains, does not increase H2. The large difference in fiber content of rural vs. urban Mexican diets
doesn't seem to correlate with H2 production by intestinal bacteria. Interestingly, both white and whole wheat bread increase H2 production.

Let's put those doses of fructose into perspective. One medium banana contains about 7 grams. A 16-ounce bottle of apple juice contains about 30 grams. A slice of cake contains about 12. One "child-size" 12 ounce cup of Coca-Cola from McDonald's contains 17 grams (as long as you don't get a refill!). One large 32 ounce Coca-Cola contains 47 grams. Your H. pylori will be VERY pleased if you drink one of those, especially if you use it to wash down the white flour bun on your hamburger.

I do think it's important to mention that the study described above used isolated fructose. It's not clear that other sources of fructose would behave the same. For example, the presence of glucose enhances fructose absorption. Fruit, table sugar and high-fructose corn syrup all contain glucose. It's also not clear what the effect would be of eating fructose with a meal rather than in isolation. None of this has been studied to my knowledge, so we're left extrapolating from studies that used pure fructose.

Now let's connect the dots. Excessive fructose, certain types of fiber, and wheat cause bacterial overgrowth and H2 production (if you believe the fructose-H2 connection). Elevated H2 causes overgrowth of H. pylori and possibly other pathogenic bacteria in the body. H. pylori lowers stomach acid, causing further overgrowth of bacteria in the small intestine. This causes inflammation and increases the risk for digestive cancers.

Decreased stomach acid also causes malabsorption of protein, B12, iron and perhaps other nutrients. It allows undigested protein to travel into the small intestine. This could potentially be very important. For example, many people are allergic to the casein in milk. It's one of the two most common alleriges, along with gluten. Both casein and gluten are proteins. A normally functioning stomach at the proper pH should completely digest casein. You can't be allergic to casein if there's none around. I don't know if the same applies to gluten.

Robust digestion may explain why many healthy non-industrial groups do very well eating dairy, sometimes to the exclusion of nearly everything else, yet many people in modern societies do better without dairy protein (butter is typically well tolerated). This phenomenon could also go a long way toward explaining the fact that allergies are becoming more and more common in industrial nations as we consume more sugar.

Thanks to Peter and Matt Stone for some of the ideas I incorporated into this post. Thanks to pbo31 for the CC photo.

43 comments:

toddhargrove said...

Stephan,

Great post! Very interesting about the casein digestion by strong HCL. I guess casein digestion could be undermined by poor lactose digestion, because this would lead to more H2 which would help the bacteria and hurt the HCL. I suppose traditional cultures were more likely to digest lactose properly because their milk was fermented. And isn’t the lactose in raw milk easier to digest than pasteurized milk? This could explain why some people claim that they are allergic (not just intolerant) to pasteurized milk but not raw milk. It could also explain why someone “gets over” an allergy to milk – by somehow improving their HCL.

I would be very interested to know whether strong HCL could break down gluten before it does it damage. I’m very curious how those Sikhs ate so much wheat and remained so strong and healthy (as pointed out by Matt and McCarrison). Maybe they had other aspects of their diet which supercharged their HCL.

Another thing. I have two friends who have persistent issues with gas and bloating. One of their “rules” for avoiding gas (they were told this by another friend, I think its an ayurvedic tip) is to never eat fruit with another food. They say this helps a lot. I wonder if this somehow helps them absorb the fructose better. Maybe this is how fruitarians survive.

gunther gatherer said...

Stephen and Toddhargrove,

I think we're leaving out the possibility that the protein shapes themselves in the milk may be altered in the pasteurization process. Not to mention there are probably tons of enzymes in the milk to aid in a young calf's digestion of it which are completely killed off in dairy processing.

We've yet to do convincing studies on what high heat actually does to food and how it affects digestion in general. But there is tons of anecdotal evidence of people, including myself, who can't tolerate pasteurized dairy but do fine on raw dairy.

And with regards to bacteria, the raw dairy would not only contain necessary digestive enzymes and cofactors, but also good bugs that fight the bad ones in your stomach and/or serve as catalysts for breakdown of food.

chlOe said...

Is there a way to test your stomach acidity easily? Or symptoms perhaps?

And todd, I must say, after eating mostly fruit for 4 months (mostly dates), those problems didn't go away for me.

Cristian Stremiz said...

Salt Doesn't Just Add Flavor to the Diets of Early-Weaned Pigs

COLUMBUS, Ohio – Hog producers who wean early and want healthier, faster-growing and more consistently sized pigs should be saying "pass the salt."

Sodium chloride, commonly known as table salt, helps break down protein and prevent the growth of harmful bacteria in the stomachs of newly weaned pigs, said Ted Wiseman, Ohio State University animal science graduate research associate. The chloride component is particularly important.

Early-weaned pigs with almost three times more sodium and chloride in their diets than the minimum recommendations of the National Research Council are more uniform with better growth rates, Wiseman said.

Wiseman presented research regarding sodium chloride and early-weaned pigs at the American Society of Animal Science/American Dairy Science Association Midwestern Meeting, March 17 in Des Moines, Iowa.

Several years ago, Ohio State researchers found that pigs weaned early have a greater need for chloride. While a young pig nurses the sow, lactose in the milk is broken down in the pig's stomach by bacteria called Lactobacilli, and as a result lactic acid is formed. This acidity in the stomach is what digests food proteins and prevents the growth of harmful bacteria that can cause diarrhea and other health problems.

When pigs are weaned from milk, lactic acid production decreases and is replaced by the natural production of hydrochloric acid within the stomach. However, when a pig is weaned early, hydrochloric acid production has not yet begun, and the resulting low stomach acid levels can cause poor food digestion and bacterial concerns. Chloride helps digest food proteins and keep stomach acid levels high.

"The chloride in sodium chloride helps sooth the transition period of early-weaned pigs from when lactic acid production decreases to when hydrochloric acid production begins," Wiseman said.

Wiseman and Ohio State animal scientist Don Mahan began studying the impact of sodium chloride on pigs weaned at 14 days of age two years ago. They found that the early-weaned pigs fed a plant-protein diet high in sodium chloride grew 10 percent faster during the first two weeks to three weeks after weaning than early-weaned pigs not fed higher amounts of salt.

Young pigs fed animal proteins in their diets with added sodium chloride experienced the same results, but only for the first week. Animal-protein feeds already have higher natural salt levels from processing, so adding more salt doesn't have as much of an impact, Wiseman said.

The National Research Council recommends a pig's diet consist of a minimum of .1 percent chloride from all dietary sources. Wiseman and Mahan recommend the diet of early-weaned pigs contain at least .3 percent chloride.

"Early-weaned pigs can experience poor digestion, diarrhea and a wide range of growth rates," Wiseman said. "Adding salt helps reduce the magnitude of those problems and gets the young pigs off to a better start."

In the future, Ohio State researchers plan to study other forms of chloride, such as potassium chloride and other acidifiers, to see if they also impact the digestion and growth of early-weaned pigs.

chlOe said...

So the study basically is saying that salt will help digestion - making the stomach more acidic? Hm, that's worth trying out. Think that's why also fermented foods could be of digestive significance? Not just enzymes, but salt content? Also, is it the kind of salt that matters - like how highly processed it is.

Scott Miller said...

Truly. Exceptional. Post.

I love the way to slice through studies and find new ways to connect the dots. You definitely have a talent from this, and I think, in part, it comes from having a better "world-view" than most researchers.

Nicely done, Stephan.

I wonder if all of this is related to the fact that a lot of people have too much gas. I know I did, years ago, before I went paleo. And since then it's not been an issue.

madmax said...

Excellent post. As they all are. I'll second Scott Miller's claim. Before going Paleo/Primal/Natural Foods, I always had gas. Now, I never have it. Its amazing what eliminating grains and legumes can do.

Edwin said...

Very nice post man, very interesting. Can I re-post your article in the forum at www.rawpaleoforum.com?

Nancy LC said...

Great post!

Do you know which non-caloric sweeteners increase H2? I like to use them from time to time.

Bryan - oz4caster said...

Another interesting post Stephan! I've been suspicious that inadequate stomach acidity leads to improper digestion of proteins like casein and gluten, which in turn leads to allergies and inflammation. It's interesting that hydrogen gas may be involved as a result of disbiosys and that fructose, resistant starch, and wheat feed that hydrogen production. I wonder what other foods might contribute to this problem?

So many people take antacids and are setting themselves up for more trouble as a consequence. It's ironic that most of these people get indigestion because of inadequate stomach acidity. So what do they do? Take an antacid to make it even less adequate!

For several months now, I have been trying not to drink much liquid during and after a meal in order to help maximize stomach acidity for digesting the meal.

Daniel said...

I also had problems with flatus and bloating before I changed the diet.
I was also intolerant toward dairy products.
Now I can eat 1 litre of whole cream and 1kg cheese on single day without any problems. But as soon as I add fruits, fruit juices to the diet I will no longer tolerate the dairy.

Daniel said...
This comment has been removed by the author.
Daniel said...

I don't know about the Sikhs, but I've a south-east Indian friend and they are consuming huge amount of salt. He's consuming about 500g each month, hell it took me 3 years to consume a 1kg of table salt.
Even though they are eating quite a lot of wheat and lentils, much of it is fermented. I guess pre-fermented food will produce less H2 when fermented in the gastrointestinal system.

Stephan said...

Todd,

I agree, you would expect the lactase in raw milk to prevent abnormal fermentation int he small intestine. Same with fermented milk. Anecdotally, I know several "lactose intolerant" people who can drink raw milk without any trouble.

Gunther,

I don't know for sure, but I think it's a safe bet that the casein in that study I linked to was pasteurized.

Chloe,

Yes, certain doctors can test stomach pH by dangling a sensor into your stomach.

Scott,

Thanks. I think it probably is related to gas. I'm not surprised at all that paleo takes care of it! That might actually be one of its most beneficial effects.

Edwin,

Please do.

Nancy,

Any of the modified sugars that humans can't digest but bacteria can. Examples include xylitol, sorbitol, isomalt.

Stephan said...

Bryan,

I agree, antacids and proton pump inhibitors are a big problem. I've been trying to figure out what other foods could contribute. It may depend on an individual's intestinal flora. There aren't may studies that looked at foods in the context of a meal so that's another factor.

Daniel,

Interesting. Too much fruit bothers me as well. I buy the smallest apples I can find. Fruit on an empty stomach saps my energy. I'm still trying to figure out why.

Conrad said...

Hi Stephan,

http://www.johnberardi.com/articles/nutrition/bases.htm

This link outlines the importance of a pH balance in the body. Consequently, eating alot of meat without veggies/fruit will raise the acidity of your stomach. To rebalance ones pH the body needs to find a Alkali source; generally the bones. And with your bones shedding, can lead to osteoporosis among other things.

What are your thoughts Stephan?

Thanks

Conrad said...

Here's that link, doesn't look like it pasted properly.

http://www.johnberardi.com/articles/nutrition/bases.htm


tHe LiNk Yo~!

Conrad said...

The Link?
Take Two

Senta said...

Great post Stephan, as they all are!

This discussion brings to mind the food combining recommendations popularized by Herbert Shelton. I have been using them pretty sucessfully, even before I adapted to the Paleo/NT type of diet. Things like -

. Eat fruit alone, at least 20 minutes before a meal. I found that if I added some fat, like cream or coconut oil, I didn't get the energy slump. I've been told that is either because the fat prevents the blood sugar spike from the fruit or that the sugar needs to be accompanied by some fat to actually form a triglyceride so that it can enter the cells instead of constantly circulating around in the blood. Any ideas on that?

. Do not eat sugars (or starches that break down into sugars) at the same meal. This kills a lot of typical American meals, like cereal with milk, sandwiches, pasta with meat sauces, etc..

. Eat raw vegetable salads at the end of a meal, not at the beginning. This is something they do in Europe. A raw salad is the slowest to digest and the idea is that if eaten first, it will stop the digestion of the rest of the meal and cause it to ferment instead.

There are some more complicated ways to do food combining but the ones I have listed have sufficed for me to completely avoid indigestion, even when I was still eating grains. Without grains and other starchy carbohydrates, the whole process is even easier.

The people who espouse food combining say it works because of the acid vs. base requirements for digestion of different food types. But your article explains so much more!

Senta said...

Sorry, this paragraph:
. Do not eat sugars (or starches that break down into sugars) at the same meal. This kills a lot of typical American meals, like cereal with milk, sandwiches, pasta with meat sauces, etc..

should say:
. Do not eat sugars (or starches that break down into sugars) at the same meal as proteins. This kills a lot of typical American meals, like cereal with milk, sandwiches, pasta with meat sauces, etc..

Sue said...

Regarding the salt, I remember when I started my baby on solids I made sure I didn't add any salt because that is what is recommended. They say a baby's kidney's can't handle the salt.
My mother would constantly be on at me to add a bit of salt.

chlOe said...

Don't all starches break down into sugars when you eat them... or do you mean when cooking
Because I thought sugars turned to starches when cooking (ex. tomato)

westie said...

How fermentation, butyrate and bacteria fits in this picture? I've learned that fermentation of ceratin kind of plant fibers will increase the amount of short-chain fatty acid, butyrate, which has many benefial effects in the colon, for example it is anticarcinogenic.

What kind bacteria is this H2 producing bacteria and does these probiotics (lactic acid bacteria), which increases butyrate production, also increase H2 production?

Stephan said...

Conrad,

I'm not a proponent of the acid/base balance theory. I wrote about that here
.

Senta,

I can't say I'm convinced by the idea that protein and starch shouldn't be combined, but I can see how too much fruit might interfere with the digestion of a big meal.

Hi Westie,

I'm not sure how that all fits in, except that probiotics have shown some modest anti-H. pylori effects.

Senta said...

Stephan,
You said:

"I can't say I'm convinced by the idea that protein and starch shouldn't be combined, but I can see how too much fruit might interfere with the digestion of a big meal."

I don't really buy the explanations for why proteins and starch should not be combined either. However, actually trying it convinced me. If you try it yourself and it works for you too, I know you will be inspired to come up with a better explanation!

I think eating fruit separately is somewhat explained by your original post. Not only does fruit reduce stomach acidity, but when it is combined with other foods, the proponents of food combining claim that it causes them to bacterially ferment rather than digest. And bacterial fermentation produces H2.

Aaron Blaisdell said...

Senta,

In the past couple of months I've started eating plain yogurt just about every morning, and I add about a quarter cup or so of fruit--either blue berries, strawberries, or bananas. I've seen a marked improvement in the "health" of my gut, that is it feels much better than it used to. I've also noticed a marked decrease in the amount of gas produced. This anecdote doesn't fit the hypothesis that mixing fruit with protein leads to an increased H2 production.

Senta said...

Aaron Blaisdell,
It could be because the yogurt is pre-fermented and the protein is already broken down. I have found it is much better to do the fermenting outside the body. I drink raw milk kefir and have no problems with it mixed with other carbohydrates, including fruit.

From my own perspective, I didn't need any kind of food combining (actually, it would more accurately be called food separation) when I was younger. I didn't start having digestive problems like heartburn until I got into my 30's. So I think the explanation is much more along the lines of Stephan's post about decreased stomach acidity, which seems to accelerate with age. Also, I think enzymes come into play but that's a huge topic in itself.

Krissie said...

Because of this excellent post, I have been doing a little digging about h-pylori.
Your link, Stephan, 'increases stomach acidity' which is this: http://www.ncbi.nlm.nih.gov/pubmed/9696699
says this:
In summary, eradication of H. pylori infection increases gastric acidity by reducing nonparietal gastric secretion from peptic and other cells

So the gastric secretion from nonparietal cells is ALKALINE. So H-pylori reduces gastric acidity by increasing nonparietal cell secretions... I feel like there is still a piece left to the puzzle?? can anyone comment on whether this detail makes a difference?

Another question:
Should people with ulcers/gastric symptoms from h-pylori eradicate the bacteria completely, or just try to suppress overpopulation?

(because of the decrease in gastric pH s/p H-pylori eradication many people develop esophageal reflux and subsequent esophageal cancer risk increase ---it is like exchanging one problem for another --maybe h-pylori should be considered like normal flora for some?)

Stephan Guyenet said...

Hi krissie,

Thank you for pointing that out. Unfortunately, I don't have an answer to your question about eradicating vs. controlling H. pylori.

Bob Parr said...

Stephan,

I just discovered this blog. Very nice post! One question: if we can assume most of us have an H. pylori infection, what can be done short of taking antibiotics? Do you think eating foods with well-known antimicrobial action like garlic and many of the common culinary herbs and spices, along with taking probiotics, would be enough to suppress H. pylori?

Thanks!

Jesse said...

Stepan,

I know you say you are not a supporter of the acid-base balance like John Berardi is, but I would like to clear something up for everyone. That article and this concept have nothing to do with each other. JB is speaking of the acid-base balance of the blood not the stomach, this has to do with after digestion. It has a lot to do with nutrients actually, for example many fruits are alkaline due to the high potassium content and low protein content. Also for those wanting to know about treatment you can buy betaine HCL in capsules which is what Charles Poliquin recommends. If you do some googling I'm sure you can find Charles' recommendations and routine for restoring stomach HCL levels (although I've heard and in my experience, you could just take 1 .5-1g capsule before each protein containing meal to get slower but consistent results). As mentioned you should also reduce sugar and grain intake, for this reason and many other possible health reasons.

Stephan Guyenet said...

Hi Bob,

That's an open question. There are some natural remedies for H. pylori, but as far as I know they're only modestly effective. It may not be necessary to eradicate it completely. Bringing down stomach pH with betaine HCL may help.

Stephan Guyenet said...

Hi Jesse,

Yes, I understand the difference. I've written about the acid-base balance theory as well:

http://wholehealthsource.blogspot.com/2008/10/acid-base-balance.html

Jesse said...

Stephan,

Yes, I figured you did. :) I thought I would clear it up right here for the casual passer by who only ends up reading this one article. Also, I did read that blog post after I posted and you make a good stand on the subject, although it seems you always do from what I've seen so far.

Really enjoying the blog!
Jesse

John said...

Stephan, in response to the question, "Do you know which non-caloric sweeteners increase H2?", you say, "Any of the modified sugars that humans can't digest but bacteria can. Examples include xylitol, sorbitol, isomalt."

Some people claim that xylitol is a *reduced* caloric substance for people that at least harmful mouth bacteria *cannot* digest at all -- it's supposed to aid dental health by being attractive to the bacteria but not metabolizable by them. Eg, "Bacteria are unable to use Xylitol as an energy source. Unlike regular sugar, which gives these bacteria energy, Xylitol literally starves them." from
http://www.cleanwhiteteeth.com/xylitol.htm

Even some responders to your blog have said xylitol helps their teeth.

Cognitive dissonance here. Can you help?

Stephan said...

Hi John,

Bacteria in the mouth can't digest xylitol but bacteria in the gut can.

Krissie said...

I am very excited to post this: I have a family member who has struggled with h-pylori for 8 years with severe symptoms (under a gastro MD's care).
I wrote out a meal/supplement plan including all the recommendations from your post.
She amazingly followed it exactly - and after 2.5 months is h-pylori free for the first time in 8years!
She is very happy, to say the least.
Thank you for this excellent health resource.

Stephan said...

Hi Krissie,

Great to hear. Would you be willing to post the meal/supplement plan she used in another comment so we can see it?

Tuck said...

H. Pylori is very common in South America. So is stomach cancer:

http://www.oncologychannel.com/gastriccancer/index.shtml

H. Pylori is known to cause stomach cancer.

When I first read about H. Pylori I suggested to my Colombian wife that she go get tested. Positive!

I'm not aware of any positive effects of an H. Pylori infection, although some speculation is here:

http://www.nature.com/embor/journal/v7/n5/full/7400699.html

Tim said...

Stephan,

Your blog is outstanding.

Reading this post I was surprised by your statement:

"A normally functioning stomach at the proper pH should completely digest casein."

My understanding of the digestive process is that protein is partially digested in the stomach and completed in the small intestine.

From http://en.wikipedia.org/wiki/Protein_%28nutrient%29#Digestion:

"Digestion typically begins in the stomach when pepsinogen is converted to pepsin by the action of hydrochloric acid, and continued by trypsin and chymotrypsin in the intestine."

I'm guessing you don't need me to tell you that though. The reference you linked to was done in vitro. That makes me suspicious.

Please elaborate.

Thanks
Tim

Lou said...

Neat posting.

This adds an important piece to my understanding of our good friend h pylori. I can see an important possible role for h pylori in balancing digestion while controlling stomach acid post stomach digestion.

Of course like any good symbiote h pylori needs to be in balance to do this. A poor SAD diet full of destructive sugars will certainly proliferate h pylori into destructive amounts.

Thanks

http://healthyprotocols.com/2_h_pylori.htm

elhnad said...

Stephan, you took down your post about the acid - base balance. Have you reposted your current thoughts on it? or is that on a to do list?

Lou said...

"I’m very curious how those Sikhs ate so much wheat and remained so strong and healthy (as pointed out by Matt and McCarrison)."

The people of the USA were also strong and healthy on wheat ...

UNTIL

A new pigmy wheat hybrid was introduced into the USA. This introduction was a pact with the devil; it produced a greatly increased yield of wheat we humans CANNOT eat in a healthy manner.

"Wheat is among the most destructive ingredients in the modern diet, worse than sugar, worse than HFCS, worse than any fat. What other common food can result in such an extensive list of diseases even death?" Life Extension