Prorenin anno 2008 For many years , prorenin has been considered to be nothing more than the inactive precursor of renin . Yet , its elevated levels in diabetic subjects with microvascular complications and its extrarenal production at various sites in the body suggest otherwise . This review discusses the origin , regulation , and enzymatic activity of prorenin , its role during renin inhibition , and the angiotensin-dependent and angiotensin-independent consequences of its binding to the recently discovered -LRB- pro -RRB- renin receptor . The review ends with the concept that prorenin rather than renin determines tissue angiotensin generation . Introduction Despite nearly 40 years of research on prorenin , the renin precursor is still the least well-understood component of the renin -- angiotensin system -LRB- RAS -RRB- . Initially , it was thought to have no function at all . Yet , it circulates in human plasma in excess to renin , sometimes at concentrations that are 100 times higher , and in plasma of anephric subjects , prorenin , but not renin , is still present -LSB- 1 , 2 -RSB- . This suggests that prorenin , in contrast with renin , is also of extrarenal origin . Prorenin is particularly elevated in diabetic subjects with microvascular complications -LSB- 3 -RSB- . Moreover , the renal vasodilator response to captopril in diabetic subjects correlated better with plasma prorenin rather than with plasma renin -LSB- 4 -RSB- . Thus , -LRB- circulating -RRB- prorenin may have a function after all . Possibly , it is prorenin -LRB- and not renin -RRB- which is responsible for tissue angiotensin generation . Obviously , this would require local prorenin -- renin conversion , for which no evidence exists -LSB- 5 -RSB- . In support of this concept , however , transgenic rodents with -LRB- inducible -RRB- prorenin expression in the liver display increased cardiac angiotensin -LRB- Ang -RRB- I levels , cardiac hypertrophy , and/or vascular damage -LSB- 6 , 7 -RSB- . Origin and regulation of prorenin The juxtaglomerular epithelioid cells , located in the walls of renal afferent arterioles , are the main source of renin in the body . Renin is synthesized as preprorenin . Preprorenin is converted to prorenin upon insertion into the endoplasmatic reticulum . The majority -LRB- 75 % -RRB- of prorenin is secreted constitutively , while the remainder is targeted to dense core secretory granules . In these granules , an acidic pH is created to optimize the activity of the proteases -LRB- cathepsin B , prohormone convertases -RRB- that cleave off the prosegment to yield renin . Prorenin and renin levels are highly correlated but do not alter in parallel under all circumstances -LSB- 1 -RSB- . Acute stimuli of renin will not affect prorenin levels , whereas chronic stimuli -LRB- like a decrease in Ang II -RRB- increase both renin and prorenin . This suggests that renin is stored as active enzyme and is released immediately upon stimulation of the juxtaglomerular apparatus . Prorenin is released constitutively , and no acute responses occur . Chronic stimulation causes more prorenin to be converted to renin , leading to an increased renin/prorenin ratio in plasma . However , some exceptions to this rule exist . A well-known example is , as mentioned above , diabetes mellitus complicated by retinopathy and nephropathy -LSB- 3 -RSB- . Pregnant women also have high plasma prorenin levels , derived from the ovaries -LSB- 8 -RSB- . The function of this prorenin is unknown , as is the function of prorenin in amniotic fluid , in which prorenin was discovered . The reproductive organs , together with the adrenal , eye , and submandibular gland , are sites of extrarenal renin gene expression -LSB- 9 -RSB- . For reasons that are not understood , these tissues predominantly , if not exclusively , synthesize and release prorenin . Enzymatic activity of prorenin ? A 43-amino-acid N-terminal propeptide explains the absence of enzymatic activity of prorenin . This propeptide covers the enzymatic cleft and obstructs access of angiotensinogen to the active site of renin . Prorenin can be activated in two ways : proteolytic or nonproteolytic -LSB- 10 -RSB- . Proteolytic activation is irreversible : it involves actual removal of the propeptide . Nonproteolytic activation of prorenin is reversible . It can best be imagined as an unfolding of the propeptide from the enzymatic cleft . Nonproteolytic activation can be induced by exposure to low pH -LRB- pH = 3.3 -RRB- or cold -LRB- 4 °C -RRB- -LSB- 10 -RSB- . Nonproteolytically activated prorenin is enzymatically active and can be recognized by monoclonal antibodies that are specific for the active site . Kinetic studies of the nonproteolytic activation process have indicated that an equilibrium exists between the closed -LRB- inactive -RRB- and open -LRB- active -RRB- forms of prorenin . The inactivation step is highly temperature dependent and occurs very rapidly at neutral pH and 37 °C . Consequently , under physiological conditions , < 2 % of prorenin is in the open and active form , i.e. , displays enzymatic activity , and > 98 % is closed and inactive . Prorenin receptor -LRB- s -RRB- ? The beneficial effects of RAS blockers are due , at least in part , to blockade of the generation or action of Ang II at tissue sites -LSB- 11 -RSB- . In tissues that are believed not to express the renin gene , like the heart and vascular wall , such angiotensin generation depends on renin/prorenin taken up from the circulation . Simple diffusion can not explain the relatively high renin levels in these organs , and thus a receptor-mediated mechanism may exist . Two candidates currently have been proposed : the mannose 6-phosphate/insulin-like growth factor II receptor -LRB- M6P/IGF2R -RRB- -LSB- 12 -- 14 -RSB- and the -LRB- pro -RRB- renin receptor -LSB- 15 -RSB- . The M6P/IGF2R nonselectively binds M6P-containing proteins like renin and prorenin . However , such binding did not result in angiotensin generation , and it is now believed that the M6P/IGF2R is a clearance receptor for renin/prorenin -LSB- 16 -RSB- . This leaves the -LRB- pro -RRB- renin receptor as the most promising candidate for tissue uptake of circulating renin/prorenin . This receptor , a 350-amino-acid protein with a single transmembrane domain , binds prorenin with higher affinity than renin -LSB- 17 -RSB- and , unlike the M6P/IGF2R , does not internalize these proteins . Interestingly , binding to the receptor allowed prorenin to become catalytically active without proteolytic cleavage of the prosegment -LSB- 15 , 17 -RSB- . Apparently , therefore , binding induces a conformational change in the prorenin molecule , similar to the change occurring after exposure to cold or low pH. Angiotensin-independent effects of prorenin ? After the discovery of the receptor , -LRB- pro -RRB- renin receptor antagonists were designed based on the idea that the prosegment contains a ` handle region ' which binds to the receptor -LSB- 18 -RSB- . These -LRB- peptidic -RRB- antagonists -LRB- also known as ` handle region peptides ' , HRP -RRB- mimic the handle region and thus may bind to the receptor instead of prorenin . In support of this concept , HRP infusion normalized the elevated renal angiotensin content in diabetic rats -LSB- 18 -RSB- and simultaneously prevented the development of diabetic nephropathy . Surprisingly , identical effects occurred in diabetic angiotensin II type 1A receptor-deficient mice -LSB- 19 -RSB- . Since such mice no longer display the normal -LRB- constrictor -RRB- response to Ang II -LSB- 20 -RSB- , the effect of the -LRB- pro -RRB- renin receptor antagonist in these mice can not be due to suppression of local angiotensin generation . Thus , prorenin may also exert direct angiotensin-independent effects , possibly via the above described -LRB- pro -RRB- renin receptor -LRB- Fig. 1 -RRB- . Indeed , prorenin -LRB- and renin -RRB- induced p42/p44 mitogen-activated protein kinase -LRB- MAPK -RRB- activation and transforming growth factor-β1 release in mesangial cells -LSB- 15 , 21 -RSB- , and these effects did not occur following deletion of the receptor with siRNA -LSB- 21 -RSB- . Moreover , in cardiomyocytes , prorenin concentration dependently activated p38 MAPK and phosphorylated heat shock protein 27 -LSB- 22 -RSB- . Fig. 1Model depicting prorenin activation by the -LRB- pro -RRB- renin receptor -LRB- P -RRB- RR , allowing prorenin to generate angiotensin I from angiotensinogen . In addition , prorenin binding to the receptor results in effects -LRB- intracellular signaling -RRB- that are independent of angiotensin generation . HRP is assumed to block both prorenin activation and the direct prorenin-induced effects -LRB- see text for further explanation -RRB- Overexpression of the human -LRB- pro -RRB- renin receptor in rats resulted in elevated blood pressure , increased plasma aldosterone , and/or glomerulosclerosis -LSB- 23 , 24 -RSB- . Since such overexpression was not accompanied by changes in renin or Ang II , angiotensin-independent effects of the receptor may underlie this phenotype . HRP prevented the development of glomerulosclerosis in -LRB- pro -RRB- renin receptor transgenic rats -LSB- 25 -RSB- . Yet , transgenic rats with inducible hepatic prorenin expression -LRB- resulting in a > 200-fold rise in plasma prorenin -RRB- did not develop glomerulosclerosis -LSB- 26 -RSB- , although such animals did develop hypertension . Moreover , HRP blocked neither prorenin binding to cells overexpressing the human -LRB- pro -RRB- renin receptor -LSB- 17 -RSB- nor prorenin-induced signaling in U937 monocytes -LSB- 27 -RSB- . Thus , it is uncertain to what degree the beneficial in vivo effects of HRP are solely due to prorenin blockade . Such effects are unlikely to involve renin , since HRP will not block renin -- -LRB- pro -RRB- renin receptor interaction . Prorenin and renin inhibition Prorenin levels will rise during renin inhibition , as they do during any type of RAS blockade . Renin inhibitors affect the equilibrium between the open and closed forms of prorenin , because such drugs -LRB- due to their high affinity for the active site -RRB- prevent inactivation -LSB- 10 -RSB- . Therefore , renin inhibitors , like low pH , cold , and the -LRB- pro -RRB- renin receptor , are capable of nonproteolytically ` activating ' prorenin although , of course , due to the presence of the renin inhibitor , this open prorenin can not display enzymatic activity . Open prorenin will however be recognized by the active site-directed antibodies applied in renin immunoradiometric assays , thus leading to an overestimation of the renin rise during renin inhibition -LSB- 28 -RSB- . Theoretically , the elevated -LRB- pro -RRB- renin levels during renin inhibition might result in -LRB- pro -RRB- renin receptor activation . In vitro studies suggest that renin inhibitors do not interfere with this process . The consequence of such overstimulation is unknown . However , since such a rise also occurs during other types of RAS blockade , its detrimental effects , if present , should have been known by now . A possible explanation comes from the work of Schefe et al. -LSB- 29 -RSB- , who showed that , on activation of the receptor , the transcription factor promyelocytic zinc finger is translocated to the nucleus and represses transcription of the -LRB- pro -RRB- renin receptor itself , thus creating a short negative feedback loop . In other words , high -LRB- pro -RRB- renin levels , as occurring during RAS blockade , will suppress -LRB- pro -RRB- renin receptor expression , thereby preventing excessive receptor activation . Furthermore , the members of a family with a mutated renin allele , resulting in high plasma prorenin levels , were phenotypically normal -LSB- 30 -RSB- . Conclusion After many years , it now seems that a function for prorenin has been found . The ` inactive ' renin precursor gains Ang I-generating activity by binding to a receptor , without undergoing proteolytic cleavage . This mechanism explains how prorenin might contribute to tissue angiotensin generation , even when no prorenin -- renin conversion occurs outside the kidney . Renin inhibitors will bind to such open activated prorenin , to the same degree as they bind to renin , and may thus be the ideal tools to block tissue angiotensin generation . In vitro studies suggest that prorenin also acts as an agonist of the -LRB- pro -RRB- renin receptor , inducing intracellular signaling pathways in an angiotensin-independent manner . However , given the contradictory data obtained with the -LRB- pro -RRB- renin receptor blocker HRP , more work is needed to verify the in vivo importance of such prorenin-induced -LRB- pro -RRB- renin receptor activation .

O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O B B O O O O O O O O O O O B O B I O O O O O O O O O O O O O B O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O B I O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O B O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O B O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O B B O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O B B O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O B B O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B B O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B B O O O O O O O O O O O O O O O O O O O O O B O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O B O O O O O O O O O O O O O O O B B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B B O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O B O O O O B B O O O O B O O O O O O B O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O B B O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O B O O B O O O O O O O O O O O O B O O B O O O O O O O B B O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O B B O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O B B O O O O O B O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O B O O O O O O O O O O O O O O B I O O O O O O O B O O O O O O B O O O O O O O O O O O O O O O O O B O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O B B O O O B O O O O O O O O O O O O O O O O O O B B O O O O O O O O O O O O O O O O O O O B B O O

renin
diabetes
signaling
tissue angiotensin
receptor

(pro)renin receptor
renin angiotensin system
renin inhibitor


Language

Preferences

on

Websites

and

in

Google

Searches

for

Human

Health

and

Food

Information

Background

While

it

is

known

that

the

majority

of

pages

on

the

World

Wide

Web

are

in

English

little

is

known

about

the

preferred

language

of

users

searching

for

health

information

online

Introduction

The

World

Wide

Web

has

more

than

billion

pages

-LSB-

-RSB-

and

has

become

an

important

source

of

health-related

information

-LSB-

-RSB-

In

the

United

States

for

example

it

has

been

reported

that

of

female

users

and

of

male

users

used

the

Internet

to

obtain

medical

information

on

a

routine

basis

-LSB-

-RSB-

Google

searches

have

even

been

shown

to

assist

physicians

in

the

correct

diagnosis

of

medical

ailments

-LSB-

-RSB-

However

two

thirds

of

the

pages

on

the

Web

are

published

in

English

-LSB-

-RSB-

even

though

the

world

has

over

billion

non-English

speakers

-LSB-

-RSB-

including

approximately

million

non-English-speaking

Internet

users

-LSB-

-RSB-

In

fact

the

vast

majority

of

the

world

's

living

linguistic

groups

-LSB-

-RSB-

have

little

Web

content

available

in

their

language

-LSB-

-RSB-

Adding

to

this

problem

search

engines

such

as

Google

do

not

translate

search

terms

into

other

languages

-LSB-

-RSB-

perhaps

a

surprise

to

many

users

To

overcome

linguistic

barriers

the

World

Health

Organization

-LRB-

WHO

-RRB-

and

the

Food

and

Agricultural

Organization

-LRB-

FAO

-RRB-

now

publish

their

websites

in

six

and

four

major

languages

respectively

However

other

globally

authoritative

organizations

such

as

the

Centers

for

Disease

Control

-LRB-

CDC

-RRB-

in

the

United

States

primarily

publish

online

information

in

only

one

or

two

languages

of

domestic

importance

In

spite

of

the

significant

challenges

created

by

linguistic

differences

in

effectively

communicating

health

information

to

the

world

's

peoples

online

we

could

find

little

quantitative

data

on

this

issue

Do

the

world

's

online

users

presumably

wealthier

and

more

educated

than

the

general

population

primarily

search

online

for

health

information

in

their

local

language

or

do

they

employ

Web-prevalent

languages

such

as

English

Are

current

online

translation

efforts

by

the

world

's

health

and

food

agencies

beneficial

and

should

these

agencies

be

spending

more

resources

on

these

efforts

In

a

world

of

human

migration

which

language

-LRB-

s

-RRB-

should

domestic

governments

and

international

agencies

use

in

order

to

communicate

online

health

information

to

target

populations

To

transmit

information

to

front-line

health

professionals

in

developing

nations

a

group

that

can

include

international

aid

workers

from

wealthy

nations

which

language

-LRB-

s

-RRB-

should

be

employed

to

target

a

particular

nation

Do

indigenous

peoples

search

for

online

health-related

information

using

search

terms

belonging

to

their

own

language

or

the

colonial

language

Real-time

accurate

communication

of

health

information

might

be

especially

critical

during

a

pandemic

infectious

disease

outbreak

or

famine

To

begin

to

answer

these

questions

we

have

used

a

case-study

approach

that

examines

linguistic

preferences

in

Internet

search

engine

queries

Specifically

we

measured

search

patterns

on

Google

for

four

health

and

food-related

terms

in

seven

languages

in

nations

The

four

search

terms

we

chose

for

our

study

were

avian

flu

tuberculosis

schizophrenia

and

maize

-LRB-

corn

-RRB-

We

chose

avian

flu

because

it

is

an

ideal

model

for

searching

for

online

information

concerning

an

emerging

infectious

disease

pandemic

as

of

August

avian

influenza

-LRB-

virus

subtype

-RRB-

had

killed

people

in

countries

-LSB-

-RSB-

in

addition

to

prompting

the

slaughter

of

millions

of

animals

-LSB-

-RSB-

We

chose

tuberculosis

because

it

is

a

good

model

for

searching

an

established

global

infectious

disease

as

it

is

a

major

cause

of

death

for

HIV-positive

patients

-LSB-

-RSB-

and

currently

afflicts

about

million

people

in

nations

-LSB-

-RSB-

We

chose

schizophrenia

because

psychiatric

and

neurological

diseases

affect

more

than

million

people

globally

-LSB-

-RSB-

and

because

online

mental

health

information

has

the

potential

to

help

nations

that

have

few

mental

health

specialists

-LSB-

-RSB-

Schizophrenia

afflicts

over

million

people

worldwide

-LSB-

-RSB-

Finally

because

there

are

currently

around

million

chronically

undernourished

people

in

the

world

-LSB-

-RSB-

under

frequent

threat

of

famine

and

because

malnutrition

is

a

major

underlying

contributor

to

infectious

disease

susceptibility

-LSB-

-RSB-

we

chose

maize

-LRB-

corn

-RRB-

because

it

is

an

important

search

term

for

global

food

security

agencies

Maize

supplies

one

third

of

all

human

calories

in

Latin

America

and

Sub-Saharan

Africa

-LSB-

-RSB-

and

combined

with

its

genetic

relatives

rice

and

wheat

supplies

approximately

of

all

human

calories

globally

either

directly

or

via

animal

feed

-LSB-

-RSB-

In

this

paper

we

quantitatively

demonstrate

the

need

for

health

and

food

website

translation

that

not

only

targets

the

world

's

major

languages

but

also

linguistic

minorities

within

nations

including

immigrants

foreign

aid

workers

and

indigenous

groups

Methods

Measuring

the

Extent

to

Which

Health

and

Food

Agencies

Translate

Websites

When

an

online

publisher

translates

its

Web

site

across

languages

the

same

source

domain

name

can

be

found

in

the

different

result

lists

of

a

search

engine

when

entering

different

translated

search

terms

In

an

URL

the

domain

name

is

the

identifier

before

the

first

slash

-LRB-

eg

for

the

WHO

the

domain

name

is

-RRB-

Therefore

to

estimate

the

percentage

of

institutions

news

agencies

and

other

sources

that

translate

their

health

and

food

websites

we

measured

the

frequency

that

domain

names

overlap

-LRB-

institutional

sources

overlap

-RRB-

in

different

results

lists

when

Google

is

queried

using

different

language

translations

of

the

same

search

term

-LRB-

eg

English

tuberculosis

versus

Bahasa

Indonesia

tuberkulosa

-RRB-

The

language

translations

used

in

this

study

are

shown

in

Multimedia

Appendix

We

first

extracted

URLs

from

Google.com

listed

as

the

most

relevant

-LRB-

about

URLs

-RRB-

based

on

the

Google

page

rank

algorithm

-LSB-

-RSB-

on

July

We

then

excluded

nonunique

domain

names

from

within

each

query

group

the

remaining

unique

subset

was

then

compared

to

the

URLs

retrieved

using

the

comparison

language

Measurements

of

Online

Search

Rates

and

Language

Choice

For

each

of

the

four

terms

and

their

translations

we

measured

the

rate

at

which

users

from

different

countries

searched

Google

-LRB-

Multimedia

Appendix

-RRB-

The

country

of

origin

for

each

search

was

identified

using

the

geographic

locations

of

Internet

Protocol

-LRB-

IP

-RRB-

addresses

The

search

rates

were

based

on

proprietary

Google

Inc.

-LRB-

Mountain

View

CA

-RRB-

data

using

an

algorithm

that

measured

of

all

first-page

Web

search

queries

from

January

to

April

The

search

rate

M

for

a

term

T

originating

from

a

specific

country

was

then

estimated

from

this

large

sample

the

algorithm

calculated

the

ratio

of

searches

using

a

specific

term

-LRB-

T

-RRB-

divided

by

all

searches

-LRB-

A

-RRB-

from

that

nation

during

the

time

period

such

that

M

T/A

Multimedia

Appendix

contains

the

standard

error

-LRB-

SE

-RRB-

for

each

search

rate

To

calculate

the

standard

error

a

normal

distribution

for

the

statistic

was

assumed

To

convert

standard

error

to

the

confidence

interval

of

the

estimate

the

following

formula

was

used

CI

M

-LRB-

SE

-RRB-

Only

the

search

rates

for

selected

languages

are

shown

for

each

nation

not

the

total

search

rate

across

languages

or

the

total

number

of

searches

which

are

proprietary

For

ease

of

database

searching

and

validation

we

chose

languages

that

share

a

Latin-based

script

similar

to

English

For

detailed

analysis

the

languages

chosen

were

English

Bahasa

Indonesia

Spanish

Portuguese

German

and

French

as

they

represent

the

primary

or

secondary

language

of

about

million

people

worldwide

and/or

are

significant

post-colonial

languages

-LSB-

-RSB-

Because

Turkey

has

reported

cases

of

avian

influenza

-LSB-

-RSB-

Turkish

was

added

as

a

language

of

interest

A

search

term

may

be

common

to

multiple

languages

not

all

of

which

are

noted

here

Multimedia

Appendix

contains

a

complete

list

of

the

language

translations

used

to

retrieve

search

rate

data

from

the

Google

database

Health

and

Food

Security

Indicators

For

the

number

of

human

avian

influenza

cases

-LRB-

subtype

-RRB-

we

employed

the

WHO

Epidemic

and

Pandemic

Alert

and

Response

Database

-LSB-

-RSB-

updated

on

August

For

the

number

of

poultry

outbreaks

of

type

since

we

used

the

August

Avian

Flu

Update

from

the

Organisation

Mondiale

de

la

Santé

Animale

-LRB-

OiE

-RRB-

-LSB-

World

Organisation

for

Animal

Health

-RSB-

-LSB-

-RSB-

For

tuberculosis

-LRB-

TB

-RRB-

we

used

Millennium

Development

Goal

-LRB-

MDG

-RRB-

Indicator

the

estimated

TB

prevalence

in

from

the

Global

Tuberculosis

Database

of

the

WHO

Global

Health

Atlas

-LSB-

-RSB-

The

number

of

psychiatrists

per

people

in

was

obtained

from

Project

Atlas

Resources

for

Mental

Health

and

Neurological

Disorders

from

the

WHO

Global

Health

Atlas

Database

-LSB-

-RSB-

The

most

recent

maize

consumption

data

-LRB-

kcal/person/day

in

-RRB-

was

from

the

Supply

Utilization

Accounts

-LRB-

SUA

-RRB-

Database

of

the

Food

and

Agricultural

Organization

Statistical

Division

-LRB-

FAOSTAT

-RRB-

-LSB-

-RSB-

Results

Measuring

the

Extent

to

Which

Institutions

Currently

Translate

Online

Information

We

measured

the

extent

to

which

the

world

's

institutions

including

health

and

food

agencies

news

organizations

and

other

sources

currently

publish

Web

content

in

multiple

languages

To

quantify

this

we

measured

the

institutional

source

-LRB-

host-domain

-RRB-

overlap

between

search

results

-LRB-

first

URLs

-RRB-

retrieved

using

English-language

queries

versus

select

comparison

languages

-LRB-

Table

-RRB-

For

example

as

shown

in

Table

avian

flu

resulted

in

hits

which

included

unique

hosts

The

same

search

in

French

resulted

in

hits

which

included

hosts

Only

of

the

hosts

found

in

the

English

search

were

also

found

in

the

French

search

while

of

the

hosts

found

with

the

French

search

were

also

found

in

the

English

search

This

means

that

approximately

of

all

hosts

have

an

English/French

translation

For

avian

flu

which

has

afflicted

people

in

Indonesia

-LSB-

-RSB-

only

and

of

institutional

domain

names

overlapped

between

Bahasa

Indonesia

searches

and

English-language

searches

respectively

-LRB-

Table

-RRB-

For

tuberculosis

we

discovered

only

about

overlap

in

the

institutional

domain

names

retrieved

for

English

and

French/Portuguese

translations

French

and

Portuguese

are

widely

spoken

by

TB-afflicted

nations

in

Africa

and

Brazil

-LSB-

-RSB-

The

host

domain

overlap

was

typically

less

than

between

European

languages

we

were

surprised

by

this

low

rate

given

the

presence

of

common

governmental

institutions

in

Europe

-LRB-

eg

European

Union

-RRB-

We

extrapolate

that

of

health

and

food-related

institutions

do

not

translate

their

websites

into

multiple

languages

even

when

the

information

concerns

pandemic

disease

This

does

not

exclude

the

possibility

that

other

agencies

such

as

domestic

health

agencies

might

be

translating

this

information

We

then

specifically

screened

for

Web

pages

belonging

to

the

WHO

and

the

CDC

both

authoritative

agencies

for

infectious

disease

information

Because

the

first

page

of

search

results

is

the

most

viewed

-LSB-

-RSB-

the

rank

order

in

which

search

results

appear

is

critical

When

we

searched

for

avian

flu

in

English

on

Google.com

the

CDC

website

was

the

first

hit

followed

second

by

the

WHO

website

In

the

French

translation

however

no

CDC-affiliated

Web

pages

appeared

in

the

first

hits

When

we

searched

Google

Indonesia

using

the

Bahasa

Indonesia

translation

of

avian

flu

a

WHO-affiliated

Web

page

did

not

appear

until

page

three

of

the

search

results

-LRB-

rank

-RRB-

and

the

first

CDC-affiliated

page

appeared

on

page

six

-LRB-

rank

-RRB-

Most

significant

by

searching

for

avian

flu

in

Turkish

using

Google

Turkey

we

were

unable

to

retrieve

the

websites

of

either

the

WHO

or

CDC

in

the

first

search

results

As

a

cautionary

note

we

found

that

a

single

accent

or

special

character

in

the

search

term

sometimes

changed

the

rank

order

of

health

search

results

significantly

consistent

with

more

detailed

analysis

conducted

for

nonmedical

terms

-LSB-

-RSB-

for

example

for

avian

flu

we

found

that

gripe

aviária

-LRB-

accent

Portuguese

-RRB-

yielded

top

search

results

of

Brazilian

origin

-LRB-

ie

br

in

domain

name

-RRB-

whereas

gripe

aviaria

-LRB-

no

accent

Portuguese

-RRB-

yielded

top

search

results

from

Spanish-speaking

nations

and

only

search

results

from

Brazil

This

is

significant

because

we

found

that

Brazil

Portugal

and

other

Portuguese-speaking

nations

-LRB-

Angola

Mozambique

-RRB-

searched

Google

for

this

term

with

and

without

the

accent

at

nearly

equal

rates

-LRB-

Multimedia

Appendix

-RRB-

Table

Overlap

in

the

institutional

domain

names

retrieved

by

Google

to

measure

the

extent

to

which

institutions

translate

websites

across

languages

English

Search

Term

Comparison

Language

English

Language

Search

Comparative

Language

Search

URLs

Unique

Hosts

Host

Overlap

with

Comparison

Languages

URLs

Unique

Hosts

Host

Overlap

with

English

Avian

flu

French

Avian

flu

Indonesian

Tuberculosis

FrenchPortugueseDutch

Tuberculosis

GermanDanishAfrikaans

Tuberculosis

Bahasa

Indonesia

Schizophrenia

SpanishPortuguese

Schizophrenia

Bahasa

IndonesiaMalay

-LRB-

Bahasa

Malayu

-RRB-

Maize

Spanish

Language-Specific

Searching

of

Infectious

Disease

Information

Though

we

did

not

retrieve

many

WHO

and

CDC-affiliated

Web

pages

when

we

searched

across

different

languages

one

possibility

is

that

Internet

users

many

of

whom

are

well-educated

are

supplementing

their

Google

searches

for

online

health

information

by

searching

in

English

If

true

then

there

would

be

less

of

a

need

for

the

WHO

and

other

global

agencies

to

translate

online

information

into

diverse

languages

In

our

case

study

we

found

the

actual

results

to

be

variable

-LRB-

Table

Multimedia

Appendix

-RRB-

for

avian

flu

we

often

found

that

only

of

searches

in

non-English-speaking

nations

were

in

English

whereas

for

tuberculosis

or

schizophrenia

about

of

searches

in

non-English

countries

employed

English

Brazil

which

had

an

estimated

cases

of

TB

in

-LSB-

-RSB-

had

an

higher

query

rate

for

tuberculose

-LRB-

Portuguese

-RRB-

than

tuberculosis

-LRB-

English

-RRB-

However

the

comparison

is

more

important

for

languages

that

have

much

less

Web

content

such

as

Bahasa

Indonesia

and

Turkish

Indonesia

which

had

the

highest

number

of

reported

cases

of

human

viral

infections

in

-LSB-

-RSB-

had

a

higher

query

rate

for

avian

flu

in

Bahasa

Indonesia

-LRB-

flu

burung

-RRB-

than

in

English

We

found

that

Turks

used

Turkish

to

search

Google

for

health

terms

at

to

over

higher

rates

than

English

French

German

or

Spanish

-LRB-

Table

Multimedia

Appendix

-RRB-

We

did

however

find

sites

in

Turkish

that

had

translated

information

from

the

WHO

Whether

or

not

the

WHO

CDC

and

FAO

wish

to

leave

it

up

to

others

to

translate

their

information

accurately

and

rapidly

must

be

decided

based

on

their

confidence

level

of

the

eHealth

capabilities

of

each

target

nation

Given

the

Google

language-based

search

patterns

we

conclude

that

during

times

of

infectious

disease

outbreaks

though

English

may

be

useful

global

agency

affiliated

Web

pages

translated

into

local

languages

would

likely

be

highly

accessed

and

would

have

the

benefits

of

being

viewed

as

authoritative

and

accurate

and

of

being

transmitted

in

real

time

Language

of

Online

Mental

Health

Information

Searches

In

terms

of

mental

health

many

developing

nations

have

to

fewer

psychiatrists

per

capita

than

many

developed

nations

-LSB-

-RSB-

-LRB-

Table

-RRB-

For

this

reason

global

accessibility

of

online

mental

health

information

has

the

potential

to

be

very

beneficial

to

physicians

and

families

of

patients

in

developing

nations

-LSB-

-RSB-

Given

ethnic

taboos

-LSB-

-RSB-

we

first

asked

whether

or

not

Internet

users

from

developing

nations

are

searching

online

for

mental

health

information

potentially

useful

information

for

global

mental

health

experts

Indeed

we

found

that

the

search

rate

for

schizophrenia

was

similar

between

developed

and

developing

nations

in

the

local

language

demonstrating

an

active

need

for

online

mental

health

information

in

poor

countries

We

have

made

the

full

mental

health

dataset

available

-LRB-

Multimedia

Appendix

-RRB-

Given

that

Google

estimates

more

search

results

concerning

schizophrenia

in

English

versus

the

next

languages

combined

-LRB-

data

not

shown

-RRB-

we

asked

whether

middle

and

low-income

nations

searched

for

this

topic

in

English

We

found

that

people

from

Brazil

a

nation

of

about

million

people

searched

for

schizophrenia

in

Portuguese

at

a

higher

rate

than

in

English

-LRB-

Table

-RRB-

Table

Google

search

rates

for

selected

health

terms

in

local

languages

relative

to

English

Search

Term

Country

Public

Health

Comparison

Metric

Local

Language

English

Searches

-LRB-

of

Local

Language

Searches

-RRB-

Avian

flu

Human

Cases

-LRB-

Poultry

Outbreaks

-RRB-

United

States

-LRB-

-RRB-

English

France

-LRB-

-RRB-

French

Germany

-LRB-

-RRB-

German

Turkey

-LRB-

-RRB-

Turkish

Democratic

Republic

of

Congo

-LRB-

-RRB-

French

Cote

d'Ivoire

-LRB-

-RRB-

French

Burkina

Faso

-LRB-

-RRB-

French

Mozambique

-LRB-

-RRB-

Portuguese

Mexico

-LRB-

-RRB-

Spanish

Brazil

-LRB-

-RRB-

Portuguese

Indonesia

-LRB-

-RRB-

Bahasa

Indonesia

Tuberculosis

TB

Cases

United

States

English

France

French

Germany

German

Turkey

Turkish

Democratic

Republic

of

Congo

French

Cote

d'Ivoire

French

Burkina

Faso

French

Mozambique

Portuguese

Mexico

Spanish

same

term

Brazil

Portuguese

Indonesia

Bahasa

Indonesia

Schizophrenia

Psychiatrists

per

People

United

States

English

France

French

Turkey

Turkish

Democratic

Republic

of

Congo

French

Cote

d'Ivoire

French

Burkina

Faso

French

Mozambique

Portuguese

Mexico

Spanish

Brazil

Portuguese

Indonesia

Bahasa

Indonesia

Based

on

sampling

of

all

searches

on

Google.com

from

January

to

April

Subtype

from

the

WHO

Epidemic

and

Pandemic

Alert

and

Response

Database

-LSB-

-RSB-

updated

August

Type

outbreaks

since

from

the

OiE

-LSB-

-RSB-

updated

August

Estimated

TB

prevalence

in

from

the

WHO

Global

Tuberculosis

Database

-LSB-

-RSB-

data

from

Project

Atlas

Resources

for

Mental

Health

and

Neurological

Disorders

from

the

WHO

Global

Health

Atlas

Database

-LSB-

-RSB-

In

contrast

people

from

Indonesia

a

nation

of

million

people

searched

for

schizophrenia

at

similar

rates

in

Bahasa

Indonesia

as

in

English

As

with

infectious

disease

searching

our

data

would

suggest

that

users

from

most

nations

tend

to

search

Google

for

schizophrenia

in

their

official

language

at

up

to

higher

rates

than

other

languages

-LRB-

Multimedia

Appendix

-RRB-

Many

of

the

world

's

people

might

therefore

benefit

if

the

world

's

most

authoritative

mental

health

agencies

-LRB-

eg

US

National

Institute

of

Mental

Health

-RRB-

translated

information

into

other

languages

even

though

this

is

not

part

of

their

domestic

mandate

The

Online

Search

Rates

of

Immigrant

Minorities

In

some

developed

nations

there

is

concern

that

immigrant

groups

might

spread

infectious

diseases

In

Europe

the

TB

prevalence

is

people

in

Turkey

but

lower

in

wealthier

nations

such

as

Germany

-LRB-

-RRB-

in

Asia

the

TB

prevalence

is

people

in

Indonesia

compared

to

in

Singapore

-LSB-

-RSB-

-LRB-

Table

-RRB-

Unlike

many

of

their

neighbors

both

Turkey

and

Indonesia

have

reported

human

cases

of

avian

influenza

-LSB-

-RSB-

Governments

may

be

interested

to

know

whether

their

immigrant

communities

consult

infectious

disease

related

websites

originating

from

their

adopted

country

or

their

native

country

As

a

case

study

we

examined

the

search

rates

of

Turks

and

Indonesians

after

they

migrated

to

other

nations

in

Europe

or

Asia

respectively

as

determined

by

searches

in

Turkish

and

Bahasa

Indonesia

originating

outside

Turkey

and

Indonesia

The

Turkish

and

Indonesian

languages

are

distinct

relative

to

many

of

their

surrounding

nations

permitting

us

to

discern

the

search

behavior

of

these

populations

after

they

have

emigrated

provided

they

search

in

their

native

language

As

shown

in

Table

we

detected

searches

in

Turkish

for

avian

flu

and

tuberculosis

throughout

Europe

including

high

rates

in

Belgium

and

Austria

respectively

In

Asia

we

could

detect

searches

in

Bahasa

Indonesia

for

tuberculosis

and

very

high

rates

for

avian

flu

throughout

Asia

and

the

Pacific

region

including

Hong

Kong

Singapore

and

Australia

We

can

not

exclude

that

these

-LRB-

presumed

-RRB-

Turkish

and

Indonesian

immigrants

also

searched

online

in

their

adopted

language

-LRB-

s

-RRB-

nor

could

we

measure

the

fraction

of

their

searches

in

their

native

language

versus

adopted

language

-LRB-

s

-RRB-

However

based

on

the

fraction

of

a

country

's

population

that

belongs

to

a

particular

immigrant

group

versus

the

fraction

of

searches

conducted

in

the

immigrant

language

compared

to

the

adopted

language

then

if

every

person

in

a

country

searched

the

Internet

for

the

same

term

at

the

same

rate

but

in

different

languages

we

could

then

extrapolate

that

Turkish

immigrants

in

Belgium

searched

for

avian

flu

schizophrenia

and

tuberculosis

and

of

the

time

respectively

in

Turkish

rather

than

French

-LRB-

Table

-RRB-

Using

the

same

simplistic

assumptions

in

Austria

of

searches

for

tuberculosis

by

Turkish

immigrants

were

in

Turkish

rather

than

German

In

reality

immigrant

groups

are

likely

searching

for

a

term

such

as

avian

flu

at

a

higher

rate

than

the

general

population

when

the

corresponding

disease

affects

their

homeland

and

is

in

the

news

However

we

also

found

high

search

rates

for

tuberculosis

and

even

schizophrenia

in

Turkish

in

these

nations

which

are

less

featured

in

the

news

We

conclude

that

it

is

important

for

health

officials

to

be

aware

that

if

they

wish

to

disseminate

health

information

to

susceptible

immigrant

groups

they

should

not

rely

on

websites

published

in

the

majority

language

-LRB-

s

-RRB-

of

the

nation

High

priority

domestic

health-related

websites

should

be

multilingual

particularly

those

that

concern

infectious

disease

Our

analysis

also

revealed

surprises

for

example

in

Bangladesh

one

of

the

world

's

poorest

and

most

populated

nations

with

million

residents

we

found

that

the

search

rate

for

avian

flu

in

Bahasa

Indonesia

-LRB-

flu

burung

-RRB-

was

equivalent

to

the

search

rate

in

English

-LRB-

Table

-RRB-

the

Bahasa

Indonesia

translation

of

schizophrenia

was

also

high

in

Bangladesh

The

high

Bahasa

Indonesia

search

rate

may

reflect

the

fact

that

many

Bangladeshi

citizens

work

in

Singapore

and

Malaysia

nations

that

speak

a

similar

language

Malay

-LRB-

Bahasa

Malayu

-RRB-

-LSB-

-RSB-

it

would

appear

that

when

they

return

to

Bangladesh

Bangladeshis

continue

to

use

the

terminology

they

learned

while

away

but

the

reason

is

unclear

We

suggest

that

international

health

organizations

aiding

Bangladesh

should

publish

or

meta

tag

health

information

in

Malay

-LRB-

Bahasa

Malayu

-RRB-

to

reach

health

practitioners

in

that

nation

This

result

also

highlights

the

practical

value

of

analyzing

linguistic

preferences

during

online

searching

Finally

we

were

surprised

to

find

that

online

searches

for

avian

flu

schizophrenia

and

maize/corn

in

Spanish

in

the

United

States

occurred

at

less

than

of

the

English

search

rate

-LRB-

Table

-RRB-

The

US

online

Hispanic

population

-LRB-

legal

and

illegal

-RRB-

is

estimated

to

be

of

the

total

US

online

population

of

which

nearly

half

use

Spanish

for

some

-LRB-

-RRB-

or

all

-LRB-

-RRB-

of

their

Internet

usage

-LSB-

-RSB-

Therefore

our

data

suggest

that

Latin

American

immigrant

groups

in

the

United

States

search

for

health

information

to

a

lesser

degree

in

Spanish

than

might

be

predicted

although

these

data

could

also

be

a

result

of

the

digital

divide

between

the

groups

Table

Online

search

rates

of

immigrant

minorities

Search

Term

Country

Immigrant

Language

Comparative

Major

Language

of

Adopted

Country

Immigrant

Language

Searches

per

Major

Language

Searches

Relevant

Immigrants

per

Total

Population

Turkish

immigrants

in

Europe

Avian

flu

Belgium

Turkish

French

Switzerland

Turkish

German

United

Kingdom

Turkish

English

Tuberculosis

Austria

Turkish

German

Belgium

Turkish

French

Germany

Turkish

German

Switzerland

Turkish

German

United

Kingdom

Turkish

English

Schizophrenia

Belgium

Turkish

French

Switzerland

Turkish

French

United

Kingdom

Turkish

English

Indonesian/Malaysian

immigrants

in

Asia/Pacific

Avian

flu

Australia

Bahasa

Indonesia

English

Bangladesh

Bahasa

Indonesia

English

Hong

Kong

Bahasa

Indonesia

English

India

Bahasa

Indonesia

English

Singapore

Bahasa

Indonesia

English

Tuberculosis

Hong

Kong

Bahasa

Indonesia

English

Singapore

Bahasa

Indonesia

English

Schizophrenia

Australia

Bahasa

Indonesia

English

Bangladesh

Bahasa

Indonesia

English

Hong

Kong

Bahasa

Indonesia

English

India

Bahasa

Indonesia

English

Spanish

immigrants

in

English-Speaking

North

America

Avian

flu

Unites

States

Spanish

English

Schizophrenia

Unites

States

SpanishPortuguese

English

Corn

-LRB-

maize

-RRB-

Unites

States

SpanishIndigenous

-LRB-

choclo

elote

-RRB-

English

a

major

language

for

which

Google

search

rates

were

accessible

not

necessarily

the

largest

linguistic

group

of

the

nation

Total

population

data

are

from

United

Nations

Population

Division

data

URL

Data

are

from

Institut

National

De

Statistique

data

Population

et

Ménages

Mouvement

de

la

population

et

migrations

Immigrations

extérieures

par

nationalité

et

groupe

d'âges

Belgique

URL

Data

are

from

Statistics

Austria

Volkszählung

Hauptergebnisse

I

Österreich

census

data

URL

statistik.at

neuerscheinungen/vzaustria

shtml

Data

are

from

Statistisches

Bundesamt

-LRB-

Federal

Statistical

Office

Germany

-RRB-

data

URL

Data

are

from

Australia

Bureau

of

Statistics

Cultural

and

Language

Diversity

Census

data

URL

Tuberculosis

is

not

included

as

it

is

the

same

term

in

both

English

and

Spanish

Data

are

from

Department

of

Homeland

Security

Yearbook

of

Immigration

Statistics

Legal

immigrants

data

URL

The

search

term

used

was

corn

Table

Search

rates

in

European

languages

in

Sub-Saharan

Africa

Country

Colonial

Language

Minority

Language

Minority

Language

Searches

per

Colonial

Language

Searches

Search

Term

Avian

Flu

Angola

Portuguese

English

Cameroon

French

German

Ghana

English

French

Ghana

English

German

Ghana

English

Dutch

Kenya

English

French

Mozambique

Portuguese

English

Mozambique

Portuguese

French

Nigeria

English

French

Nigeria

English

German

Rwanda

French

English

Senegal

French

English

Search

Term

Tuberculosis

Angola

Portuguese

French

EnglishSpanish

Cameroon

French

Portuguese

English

Democratic

Republic

of

Congo

French

Portuguese

EnglishSpanish

Ghana

English

FrenchPortuguese

Kenya

English

FrenchPortuguese

Mozambique

Portuguese

French

EnglishSpanish

Nigeria

English

FrenchPortuguese

Rwanda

French

Portuguese

EnglishSpanish

South

Africa

English

Afrikaans

Search

Term

Schizophrenia

Angola

Portuguese

Spanish

English

Cameroon

French

English

Democratic

Republic

of

Congo

French

English

Ghana

English

French

Mozambique

Portuguese

Spanish

English

Rwanda

French

English

Senegal

French

English

When

two

languages

are

noted

the

term

is

the

same

in

both

languages

Search

Rates

in

European

Languages

in

Sub-Saharan

Africa

Sub-Saharan

Africa

suffers

from

high

rates

of

infectious

disease

including

TB

and

HIV

-LSB-

-RSB-

and

high

rates

of

malnutrition

-LSB-

-RSB-

As

demonstrated

in

Table

our

search

results

suggest

that

the

dissemination

of

online

health

or

food

security

information

to

this

region

by

international

agencies

should

not

be

limited

to

the

colonial

language

-LRB-

s

-RRB-

of

the

target

nations

For

example

in

English-speaking

Ghana

of

searches

for

avian

flu

were

in

French

-LRB-

grippe

aviaire

-RRB-

in

German

-LRB-

vogelgrippe

-RRB-

and

in

Dutch

-LRB-

vogelgriep

-RRB-

relative

to

English

-LRB-

Table

-RRB-

In

Mozambique

a

former

Portuguese

colony

we

found

times

more

searches

for

avian

flu

in

English

relative

to

Portuguese

and

a

high

rate

in

French

In

the

Democratic

Republic

of

Congo

-LRB-

DRC

-RRB-

a

former

French

colony

with

more

than

TB

infections

in

-LSB-

-RSB-

of

the

searches

for

tuberculosis

were

in

English

relative

to

French

Because

Internet

use

is

only

is

Ghana

in

Mozambique

and

in

DRC

-LSB-

-RSB-

it

is

plausible

that

these

high

rates

of

non-colonial

language

searches

using

Google

may

reflect

searches

by

health

professionals

trained

in

other

nations

including

workers

from

international

agencies

who

would

be

expected

to

have

better

Internet

access

than

the

general

population

The

Effect

of

Region-Specific

Cultural

and

Indigenous

Terminology

Finally

we

measured

the

effects

of

cultural

bias

within

the

same

linguistic

group

using

a

term

important

for

human

nutrition

and

food

security

maize

Maize

is

eaten

directly

but

it

is

also

a

major

source

of

animal

feed

worldwide

Maize

is

known

as

corn

in

the

United

States

and

the

United

Kingdom

but

as

maize

in

many

other

English-speaking

nations

We

found

that

the

US

searches

for

corn

were

at

a

higher

rate

than

for

maize

while

other

English-speaking

nations

such

as

Nigeria

and

Zimbabwe

queried

maize

at

a

to

higher

rate

than

corn

respectively

-LRB-

Table

-RRB-

in

the

latter

nations

corn

may

also

refer

to

any

large

cereal

grain

-LRB-

eg

wheat

-RRB-

This

search

behavior

has

consequences

as

we

found

only

three

domain

names

that

overlapped

between

searches

for

maize

versus

corn

out

of

the

first

unique

Google

search

results

Therefore

when

African

nations

attempt

to

retrieve

information

about

growing

maize

in

English

they

may

unknowingly

be

excluding

authoritative

information

from

the

United

States

and

other

Western

English-speaking

nations

such

as

practical

information

from

the

US

National

Corn

Growers

Association

whose

website

does

not

appear

in

the

first

Google

hits

for

maize

but

ranks

sixth

when

corn

is

searched

Similarly

when

international

organizations

such

as

the

FAO

wish

to

transmit

knowledge

for

example

using

Spanish

or

Portuguese

in

Latin

America

indigenous

terminology

usage

may

make

some

of

this

information

inaccessible

Maize

originated

from

Southern

Mexico

and

fed

indigenous

Latin

American

civilizations

-LSB-

-RSB-

In

Mexico

and

Guatemala

we

found

that

an

indigenous

synonym

for

maize

elote

was

searched

at

a

similar

rate

to

the

Spanish

term

maíz

-LRB-

Table

-RRB-

In

Peru

however

we

found

that

a

different

indigenous

term

choclo

was

searched

at

a

higher

rate

than

maíz

We

conclude

that

cultural

and

indigenous

linguistic

divisions

may

be

preventing

large

numbers

of

food

security

and

nutrition

websites

from

reaching

those

people

aiding

malnourished

people

or

billion

agricultural

workers

that

live

in

developing

countries

-LSB-

-RSB-

Cultural

and

indigenous

bias

may

be

particularly

prevalent

for

terms

related

to

crops

diseases

or

pathogens

that

have

pre-colonial

origins

Table

The

effect

of

region-specific

cultural

and

indigenous

terminology

Country

Calories

from

Maize

-LRB-

kcal/person/day

-RRB-

Search

Term

Comparison

Search

Rate

Ratio

Canada

corn

maize

United

States

corn

maize

United

Kingdom

corn

maize

India

corn

maize

Nigeria

corn

maize

Kenya

corn

maize

Tanzania

corn

maize

Zimbabwe

corn

maize

Spain

maíz

elote

choclo

Venezuela

maíz

elote

choclo

Colombia

maíz

elote

choclo

Mexico

maíz

elote

choclo

Guatemala

maíz

elote

choclo

Peru

maíz

elote

choclo

Argentina

maíz

elote

choclo

Data

from

FAOSTAT

-LSB-

-RSB-

Data

not

available

Discussion

Principal

Results

In

a

world

where

infectious

disease

pandemics

and

threats

of

famine

are

always

present

and

in

spite

of

the

fact

that

the

World

Wide

Web

offers

great

hope

for

rapid

and

accurate

sharing

of

information

between

peoples

we

have

demonstrated

that

one

linguistic

group

does

not

or

can

not

access

the

health

and

food

security

websites

of

a

different

linguistic

group

Our

data

suggest

at

least

three

reasons

for

this

The

first

reason

is

that

the

websites

of

most

institutions

are

not

published

in

more

than

one

or

two

languages

When

we

sampled

Web

pages

found

by

the

English-language

queries

avian

flu

tuberculosis

schizophrenia

and

maize/corn

and

their

counterpart

queries

in

other

languages

the

Google

search

results

typically

overlapped

by

only

less

than

in

terms

of

the

domain

names

retrieved

indicating

that

of

the

relevant

Web

pages

had

not

been

translated

into

at

least

two

languages

-LRB-

see

Table

-RRB-

For

example

when

Turkish

or

Bahasa

Indonesia

was

used

as

the

search

language

Web

pages

from

very

authoritative

sources

such

as

the

CDC

or

WHO

were

not

retrieved

by

Google

We

also

found

that

a

single

linguistic

accent

or

special

character

in

the

search

query

could

significantly

alter

the

number

and

content

of

health-related

search

results

retrieved

by

Google

Therefore

one

reason

for

the

linguistic

digital

divide

is

that

the

majority

of

health

and

food

Web

pages

are

not

translated

into

multiple

languages

and/or

that

their

cross-language

retrieval

by

search

engines

is

poor

The

first

problem

would

not

be

important

if

the

world

's

online

community

better

educated

than

the

general

public

searched

in

English

since

the

majority

of

the

world

's

Web

pages

are

published

in

English

-LSB-

-RSB-

However

we

found

that

there

was

a

to

higher

Google

search

rate

for

health

and

food

terms

in

the

native

language

of

a

country

compared

to

English

-LRB-

see

Table

-RRB-

Finally

within

a

nation

it

might

be

assumed

that

language

would

not

be

a

problem

if

a

domestic

agency

only

published

their

health

websites

in

the

majority

language

of

their

own

people

However

we

found

that

in

Asia

and

Western

Europe

a

subset

of

immigrants

from

Indonesia

and

Turkey

respectively

searched

Google

for

health

and

food

information

in

their

native

language

not

the

language

-LRB-

s

-RRB-

of

their

adopted

countries

-LRB-

see

Table

-RRB-

In

Sub-Saharan

Africa

we

detected

unexpectedly

high

search

rates

for

health

information

in

non-colonial

European

languages

-LRB-

see

Table

-RRB-

perhaps

reflecting

the

presence

of

international

aid

workers

Finally

in

Latin

America

we

found

that

indigenous

words

were

used

to

search

Google

for

information

about

food

rather

than

the

colonial

language

of

Spanish

-LRB-

see

Table

-RRB-

Therefore

domestic

agencies

in

addition

to

global

agencies

face

a

linguistic

challenge

when

publishing

information

online

their

target

audiences

still

require

information

to

be

published

in

different

languages

even

though

Internet

users

are

presumably

more

educated

and

thus

more

multilingual

than

the

general

population

Recommendations

Given

our

observation

that

the

world

's

peoples

appear

to

be

searching

for

health

and

food

terms

in

their

local

language

or

mother

tongue

not

in

English

previous

online

language

translation

efforts

by

the

WHO

and

FAO

have

no

doubt

been

worthwhile

This

is

also

revealed

by

the

high

page

rank

-LRB-

first

page

results

-RRB-

of

WHO-affiliated

search

results

when

Google

is

searched

for

infectious

disease

information

in

one

of

the

WHO

's

six

online

languages

We

recommend

that

these

efforts

be

continued

and

further

expanded

to

include

more

languages

this

recommendation

applies

to

global

agencies

but

also

to

domestic

agencies

in

order

to

meet

immigrant

or

indigenous

needs

and/or

to

make

information

accessible

to

other

nations

To

achieve

such

translation

goals

better

health-specific

translation

software

must

be

developed

and

more

translators

are

needed

who

specialize

in

human

health

and

food

security

terminology

For

example

improved

cross-language

search

retrieval

-LSB-

-RSB-

of

health

information

by

online

search

engines

would

be

beneficial

These

investments

should

then

be

used

to

initially

target

health

and

food

security

information

to

the

world

's

most

important

linguistic

groups

which

include

speakers

of

Chinese

-LRB-

million

people

-RRB-

Hindi

-LRB-

about

million

-RRB-

English

-LRB-

million

-RRB-

Spanish

-LRB-

million

-RRB-

Arabic

-LRB-

million

-RRB-

Portuguese

-LRB-

million

-RRB-

Bengali

-LRB-

million

-RRB-

Russian

-LRB-

million

-RRB-

Bahasa

Indonesia

-LRB-

million

-RRB-

Japanese

-LRB-

million

-RRB-

Punjabi

-LRB-

million

-RRB-

German

-LRB-

million

-RRB-

and

French

-LRB-

million

-RRB-

-LSB-

-RSB-

In

a

world

that

is

primarily

non-English

speaking

such

attempts

will

help

to

reduce

the

linguistic

digital

divide

in

health

and

food

information

on

the

World

Wide

Web

Furthermore

as

we

did

in

this

study

-LRB-

see

Table

to

Table

-RRB-

we

recommend

that

when

global

or

domestic

health

and

food

security

organizations

wish

to

use

the

Internet

to

disseminate

information

to

other

nations

-LSB-

-RSB-

or

to

their

own

immigrant

or

indigenous

communities

they

should

first

consult

search

engine

query

rates

for

different

translations

of

possible

search

terms

in

order

to

determine

which

online

languages

are

most

needed

Multimedia

Appendix

contains

extensive

linguistic

online

search

pattern

data

to

help

health

and

food

agencies

better

select

languages

for

targeted

website

publishing

In

order

to

measure

search

rates

for

other

subjects

of

interest

we

note

that

free

online

tools

exist

such

as

Google

Trends

In

some

situations

such

as

targeting

indigenous

groups

who

often

speak

the

majority

language

of

a

nation

all

that

may

be

needed

is

to

imbed

translated

keywords

into

a

majority-language

website

-LRB-

eg

Spanish

-RRB-

so

that

search

engines

such

as

Google

can

cross-retrieve

relevant

information

Future

Studies

Though

this

study

examined

the

extent

to

which

agencies

such

as

the

WHO

are

publishing

information

in

multiple

languages

we

did

not

systematically

address

the

quality

of

health

and

food

information

available

in

different

languages

Quality

analysis

would

especially

be

important

for

minor

languages

that

have

little

content

available

on

the

Web

for

example

we

estimate

that

there

are

more

than

fewer

search

results

in

Bahasa

Indonesia

than

in

English

for

tuberculosis

more

than

fewer

search

results

for

avian

flu

in

Arabic

or

Japanese

than

in

English

and

about

fewer

search

results

for

schizophrenia

in

Arabic

than

in

English

Though

these

precise

numbers

are

considered

to

be

unreliable

-LSB-

-RSB-

they

do

illustrate

the

point

that

most

of

the

world

's

linguistic

groups

even

major

ones

have

much

less

available

online

health

information

relative

to

English

As

to

the

quality

of

the

websites

that

are

available

this

will

require

systematic

analysis

which

poses

significant

methodological

problems

-LSB-

-RSB-

One

could

however

perform

a

subjective

survey-based

evaluation

by

multilingual

physicians

as

has

been

performed

to

evaluate

disease-specific

websites

published

in

English

-LSB-

-RSB-

Such

a

survey

should

include

quantifying

to

what

extent

online

information

from

the

WHO

CDC

and

FAO

is

being

translated

into

the

world

's

minor

languages

in

order

to

help

these

agencies

determine

where

they

need

to

target

their

online

translation

efforts

B O O O O O B O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O B O O O O O O O O O O O B O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O B O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O B O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O B O O O O O O O O O O B O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O B O O O O O O O O O O O O O B O O O B O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O B O O O O O O O O O O O B O O B O O O O O O O O O O O O O O O O O O O O O O B I O O O B O O O B O O O O B O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O B O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O B I O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O B O O O O O O O O O O O O B O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O B O O O O B O O O O O O O O O O O B O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O B O O B O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O B O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O B O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O B O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O B O B O O B O O O O O O O O O O O O O O O O B I O O O O O O O O O B I O O O O O O O O O B O O O O O O O O O B O O O O O O O O O B O O O O O O O O O O B O O O O O O O O O B O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O B O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O B O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O B O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O B O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O B O O O O O O O O B O O O O O O O O O O O O B O O O O O O O O O O O B O O O O O O O O B O O O O O O O O O O O B O O O O O O O O O O B O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O B O O O O B O O O O O O O O O O O O B O O O B O O O O O O B O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O B O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O B O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O B I O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O B O O B O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O B B O O O O B O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O B O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O B O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O B O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O B O O O B O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O B O O O O O O O O O B O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O B I O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O B O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O B B O O B O O O O B B O O O O B O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O B O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O B O O B O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O B O B O O O O B O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O B I O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O B O O O O B O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O B O O O O O O O O O O O O O B O O O O O O O O B O B I O O B O O B O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O B O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O B O O O O O O B O O O O O O O O O O O O O O O O B O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O B B O O O O O O O B I O B O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O B O O O O O O O O O O O O O O O B O O O O O O B O O O O O O B O O O O O B O O O O O B O O O O O B O O O O O B O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O B O B I O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O B O O O B O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O B O O O O O O O B O O O O O O O O O O O O O O O O O O O O O B O O O O O O O B O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O B O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O B O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O B O O O O O O B O O O B O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O B O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O B O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O B I O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O B O B I O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O B I O O O O O B O O O O O O O O O O O O O B O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O B O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O B I O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O

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