RISK FACTORS

The effects of waterpipe tobacco smoking onhealth outcomes: a systematic reviewElie A Akl,1,2� Swarna Gaddam,2 Sameer K Gunukula,2 Roland Honeine,1

Philippe Abou Jaoude1 and Jihad Irani3

1Department of Medicine, State University of New York at Buffalo, Buffalo, NY, USA, 2Department of Family Medicine, StateUniversity of New York at Buffalo, Buffalo, NY, USA and 3Faculty of Health Sciences, University of Balamand, Beirut, Lebanon

�Corresponding author. Department of Medicine, State University of New York at Buffalo, ECMC-CC 142, 462 Grider Street,Buffalo, NY 14215, USA. E-mail: elieakl@buffalo.edu

Accepted 5 January 2010

Background There is a need for a comprehensive and critical review of theliterature to inform scientific debates about the public healtheffects of waterpipe smoking. The objective of this study wastherefore to systematically review the medical literature for theeffects of waterpipe tobacco smoking on health outcomes.

Methods We conducted a systematic review using the Cochrane Collabora-tion methodology for conducting systematic reviews. We rated thequality of evidence for each outcome using the Grading of Recom-mendations Assessment, Development and Evaluation (GRADE)methodology.

Results Twenty-four studies were eligible for this review. Based on theavailable evidence, waterpipe tobacco smoking was significantlyassociated with lung cancer [odds ratio (OR)¼ 2.12; 95% confi-dence interval (CI) 1.32–3.42], respiratory illness (OR¼ 2.3; 95%CI 1.1–5.1), low birth-weight (OR¼ 2.12; 95% CI 1.08–4.18) andperiodontal disease (OR¼ 3–5). It was not significantly associatedwith bladder cancer (OR¼ 0.8; 95% CI 0.2–4.0), nasopharyngealcancer (OR¼ 0.49; 95% CI 0.20–1.23), oesophageal cancer(OR¼ 1.85; 95% CI 0.95–3.58), oral dysplasia (OR¼ 8.33; 95% CI0.78–9.47) or infertility (OR¼ 2.5; 95% CI 1.0–6.3) but the CIs didnot exclude important associations. Smoking waterpipe in groupswas not significantly associated with hepatitis C infection(OR¼ 0.98; 95% CI 0.80–1.21). The quality of evidence for thedifferent outcomes varied from very low to low.

Conclusion Waterpipe tobacco smoking is possibly associated with a numberof deleterious health outcomes. There is a need for high-qualitystudies to identify and quantify with confidence all the healtheffects of this form of smoking.

Keywords Oesophageal neoplasms, infant, low birth-weight, lung neoplasms,hepatitis C, tobacco, waterpipe

BackgroundTobacco smoking using waterpipe—also known asarguileh, hookah and shisha—is an older form of

tobacco consumption traditional of the easternMediterranean region (Figure 1).1 The waterpipedevice indirectly heats the tobacco. The resulting

Published by Oxford University Press on behalf of the International Epidemiological Association

� The Author 2010; all rights reserved. Advance Access publication 4 March 2010

International Journal of Epidemiology 2010;39:834–857

doi:10.1093/ije/dyq002

834

by guest on October 14, 2011

ije.oxfordjournals.orgD

ownloaded from

smoke then passes through a column of water beforebeing inhaled through the mouth using a pipe.2 Thesetwo unique features of this form of smoking areassumed to minimize its tobacco-related health haz-ards. Also, waterpipe tobacco smoke is produced at amuch lower temperature than cigarette smoke, sug-gesting that the toxins may be different for these dif-ferent forms of tobacco smoking.3 Another uniquefeature is the social nature of waterpipe smoking,whereby family members and friends may share thesame device, which has been hypothesized to causethe transmission of communicable diseases.

Waterpipe tobacco smoking has been spreadingglobally at a remarkable pace.4 Although its use inthe eastern Mediterranean region has been, untilrecently, confined to adults, it is now gaining popu-larity among university students5,6 and teenagers.7–9

Waterpipe smoking is also spreading to Westerncountries such as Australia,10 the UK,11 Canada12

and the USA,13 where it is also affecting youngpeople and adolescents.14,15

Waterpipe tobacco smoking is generally consideredas a public health threat and the American LungAssociation has recently called it the ‘emergingdeadly trend’.2 In fact, waterpipe smoking has beensuspected to be a risk factor for a number oftobacco-related diseases such as lung cancer,16 oeso-phageal cancers,17 cardiovascular disease18 and

adverse pregnancy outcomes.19 In addition, the water-pipe device may expose its user (via its non-tobaccocomponents) to metals and cancer-causing chemi-cals.20,21 The potential association of waterpipe smok-ing with communicable diseases such as hepatitis C22

and tuberculosis23 (via its shared and repetitive usewithout proper sanitation) has also been investigated.

While one article reviewed the effects of waterpipesmoking on health outcomes,24 we have identified nopublished systematic review or meta-analysis of thetopic. The objective of this study was therefore to sys-tematically review the medical literature for theeffects of waterpipe tobacco smoking on healthoutcomes.

MethodsEligibility criteriaWe included observational studies (i.e. cohort studies,case–control studies and cross-sectional studies)assessing the association between waterpipe tobaccosmoking and health outcomes. We excluded casereports, case series, outbreak investigations andabstracts. We also excluded studies assessing physio-logical outcomes [e.g. Forced Expiratory Volume in 1Second (FEV1)], assessing waterpipe use fornon-tobacco smoking purposes (e.g. marijuana smok-ing), not distinguishing waterpipe smoking fromother forms of smoking, and not reporting any mea-sure of association.

Search strategyIn June 2008, we electronically searched the followingdatabases: MEDLINE (1950 onwards; access viaOVID), EMBASE (1980 onwards; access via OVID)and ISI the Web of Science using a detailed searchstrategy with no language restrictions (Appendix 1).We designed the strategy based on a preliminaryreview of relevant articles, an extensive Internetsearch for waterpipe synonyms and the search strat-egy of a systematic review on interventions for water-pipe smoking cessation.25 Two medical librariansreviewed and commented on the search strategy. Wealso reviewed the reference lists of included and rel-evant papers and used the ‘Related Articles’ feature inPubMed.

Selection processTwo reviewers independently screened the title andabstract of identified citations for potential eligibilityusing a standardized screening guide. We retrievedthe full texts of citations judged potentially eligibleby at least one reviewer. Then, two reviewers indepen-dently screened the full texts for eligibility using astandardized and pilot-tested form. They resolvedtheir disagreements by discussion or by consulting athird reviewer.

Figure 1 Annotated figure of a waterpipe device

THE EFFECTS OF WATERPIPE TOBACCO SMOKING ON HEALTH 835

by guest on October 14, 2011

ije.oxfordjournals.orgD

ownloaded from

Data abstractionTwo reviewers used a standardized and pilot-testedform to independently abstract data. They resolvedtheir disagreements by discussion or by consultinga third reviewer. The abstracted data related tostudy design, population, exposure, outcomes, meth-odological features, results and funding. For exposuremeasurement, we assessed whether the instrumentwas standardized to measure the unique smoking pat-terns and characteristics of waterpipe smoking. Werecorded the results of analyses restricted to waterpipeonly smokers (i.e. people who smoked only water-pipe) as well as the results of analyses that includedall waterpipe smokers (i.e. people who smoked water-pipe and other forms of tobacco). We recorded theeffect measures derived from the regression modelsthat adjusted for the maximum number of covariates.We rated the overall quality of evidence for each out-come using the Grading of RecommendationsAssessment, Development and Evaluation (GRADE)approach (Appendix 2).26

Data analysisWe calculated the kappa statistic to evaluate theagreement between the two reviewers assessing full

texts for eligibility. We conducted meta-analyses forthe outcomes for which at least two studies reportedeffect estimates of their association with waterpipetobacco smoking. When the authors reportedodds ratios (ORs) for more than one analysis weselected the OR according to the following order:(i) analysis adjusted for other forms of tobaccosmoking (choosing the one adjusting for the maxi-mum number of confounders); (ii) analysisrestricted to waterpipe only smokers; (iii) analysisnot adjusted for other forms of tobacco smokingand not restricted to waterpipe only smokers.We used the ORs to calculate the correspondingln(ORs) and standard errors. We then pooled, foreach outcome, the ln(ORs) of eligible studies usingthe generic inverse variance and the random effectsmodel in Review Manager Version 5.0.20. Wemeasured homogeneity across study results usingthe I2 statistic.27 We checked for possible publicationbias using inverted funnel plots.

ResultsFigure 2 shows the study flow. We included 23reports on: lung cancer (n¼ 6),16,28–32 bladder cancer

1658 citations identified

1570 citations screened for retrieval 25 papers excluded: • report of already reported data (4) • case reports or case series (4) • review of the literature (1) • inappropriate study design (3) • no distinction from other forms of smoking (4) • no outcome of interest reported (5)

• no measure of association reported (2)

• abstract (1)

• about long stem pipes, not waterpipes (1)

44 potentially eligible papers retrieved

23 reports included in systematic review

88 duplicate citations

10 studies (11 analyses) included in meta-analyses

2 papers published after search date and identified 2 papers identified through checking of citations list

Figure 2 Study flow diagram

836 INTERNATIONAL JOURNAL OF EPIDEMIOLOGY

by guest on October 14, 2011

ije.oxfordjournals.orgD

ownloaded from

(n¼ 1),33 oesophageal cancers (n¼ 1),17 nasopharyn-geal cancer (n¼ 1),34 dysplasia of the oral mucosa(n¼ 1),35 pregnancy outcomes (n¼ 3),19,36,37 peri-odontal disease (n¼ 5),38–42 hepatitis C infection(n¼ 3),22,43,44 respiratory illness (n¼ 1)45 and infertil-ity (n¼ 1).46 Agreement between reviewers for studyeligibility was excellent (kappa¼ 0.963).

Lung cancerFive of the six included studies were case–controlstudies assessing lung cancer diagnosis,16,28–31 andone was a retrospective cohort study assessing lungcancer mortality (Table 1).32 One was conducted inNorthern India,28 one was conducted in Tunisia,31

whereas rule four reported data from the same pop-ulation in China. While in the recent global epidemicthe tobacco is processed and flavoured and indirectlyheated by the charcoal, in most of the included stu-dies (conducted in China and India) the tobacco istypically unprocessed and burned directly by charcoal.

The pooled OR for the association of waterpipetobacco smoking with lung cancer diagnosis was2.12 [95% confidence interval (CI) 1.32–3.42;I2¼ 0%] (Figure 3). We judged the overall quality of

evidence to be very low (Appendix 3). The calculatedcrude relative risk (RR) for the association with lungcancer mortality was 4.39 (3.82–5.04). We judged theoverall quality of evidence to be very low (Appendix3). A sensitivity analysis restricted to studies with nomajor methodological limitations, included the studyby Hsairi et al.31 for which the OR was 3.0 (95% CI1.2–7.6).

Bladder cancerThe one included case–control study33 reported apotentially protective association between waterpipetobacco smoking and bladder cancer diagnosis of 0.8(95% CI 0.2–4.0) (Table 1). A stratified analysis by theamount of cigarette smoking suggested a potentialinteraction between waterpipe and cigarette smokingbut the CI overlapped and no interaction test wasreported. An interaction test we ran was statisticallynot significant (P¼ 0.55). We judged the overall qual-ity of evidence to be very low (Appendix 3).

Oesophageal cancerThe one study assessing oesophageal cancer diagnosiswas a case–control study (Table 1).17 The reported ORfor the association of waterpipe tobacco smoking withoesophageal cancer diagnosis was 1.85 (95% CI 0.95–3.58). We judged the overall quality of evidence to below (Appendix 3).

Nasopharyngeal cancerThe one included study was a case–control study(Table 1). The OR for the association of waterpipetobacco smoking with nasopharyngeal cancer was

0.49 (95% CI 0.20–1.23). We judged the overall qual-ity of evidence to be very low (Appendix 3).

Oral dysplasiaThe one included study was a cross-sectionalstudy that recruited exclusively subjects who prac-ticed ‘takhzeen al-qat’, i.e. a practice that is distinctfrom waterpipe smoking and consists of chewinga green-leaved plant for its stimulant effect(Table 1).35 The OR for the association of waterpipetobacco smoking with dysplasia of the oral mucosa onchewing side was 8.33 (95% CI 0.78–9.47). There wereno events observed in either group on non-chewingside. We judged the overall quality of evidence to bevery low (Appendix 3).

Pregnancy outcomesOf the three included studies, two were retrospectivecohort studies19,36 and one was a case–control study(Table 2).37 All three studies assessed lowbirth-weight. One study also reported on Apgarscore, pulmonary problems, malformations and peri-natal complications.19 The pooled OR for the associa-tion of waterpipe tobacco smoking with lowbirth-weight was 2.12 (95% CI 1.08–4.18; I2

¼ 0%)(Figure 4). The reported OR for the association ofwaterpipe tobacco smoking with newborn pulmonaryproblems was 3.65 (95% CI 1.52, 8.75). The associa-tions were not significant for Apgar scores at 1 and 5min, malformations or perinatal complications. Wejudged the overall quality of evidence for pregnancyoutcomes to be low (Appendix 3).

Periodontal diseaseOf the five included studies,38–42 four were conductedin the same (or in a subgroup of the same) group ofparticipants (Table 3).39–42 These four studies werecross-sectional and evaluated the same outcome (i.e.periodontal disease) using different outcome mea-surement (periodontal bone height loss, plaqueindex and gingivitis, deepening of the sulci or pockets,vertical periodontal bone loss). We did not pool thefour related studies evaluating periodontal disease astheir data were derived from the same participants.Their results were consistent in showing a statisticallysignificant association of waterpipe tobacco smokingwith periodontal disease (OR¼ 3–5). We judged theoverall quality of evidence to be low (Appendix 3).

The fifth included study was a cohort study with7 days follow-up after surgical removal of mandibularthird molars and evaluated the outcome of drysocket.38 Dry socket, or alveolar osteitis, is the mostcommon complication following tooth extractions. Itis caused by the dislodgement of the blood clot at thesite of the tooth extraction, exposing underlying boneand nerves and causing increasing pain. The reportedRR for the association of waterpipe tobacco smoking

THE EFFECTS OF WATERPIPE TOBACCO SMOKING ON HEALTH 837

by guest on October 14, 2011

ije.oxfordjournals.orgD

ownloaded from

Ta

ble

1C

hara

cter

isti

cso

fin

clu

ded

stu

die

sass

essi

ng

the

effe

cto

fw

ate

rpip

eto

bacc

osm

ok

ing

on

can

cer

ou

tco

mes

Stu

dy

Po

pu

lati

on

Ex

po

sure

Ou

tco

me

sM

eth

od

olo

gic

al

fea

ture

sR

esu

lts

Qia

o1

6

�S

tud

yd

esig

n:

case

–co

ntr

ol

stu

dy

�F

un

din

g:

Ch

ina

Sta

teS

cien

cean

dT

ech

no

logy

Co

mm

issi

on

;an

dth

eU

SN

ati

on

al

Can

cer

Inst

itu

tegra

nt

�S

etti

ng

an

dp

erio

d:

Gej

iuci

ty,

Yu

nn

an

Pro

vin

ce,

Ch

ina,

inte

rvie

ws

con

-d

uct

edin

19

85

�C

ase

s:1

07

lun

gca

nce

rca

ses

inm

ale

s3

5–8

0ye

ars

old

rep

ort

edto

Lab

or

Pro

tect

ion

Inst

itu

teo

fth

eY

un

nan

Tin

Co

rpo

rati

on

(YT

C)

du

rin

g1

96

7–8

4�

Co

ntr

ols

:1

07

con

tro

lsch

ose

nsy

stem

ati

call

yb

yse

lect

ing

ever

y2

0th

per

son

fro

mth

eli

sto

fall

livi

ng

past

or

pre

sen

tw

ork

ers

of

the

YT

C;

on

eco

ntr

ol

per

case

�T

ype:

Ch

ines

ew

ate

rp

ipes

,ci

gare

ttes

�M

easu

rem

ent

too

l:se

lf-d

evel

op

edq

ues

-ti

on

nair

e,n

ost

an

-d

ard

izati

on

rep

ort

ed;

cum

ula

tive

con

-su

mp

tio

nca

lcu

late

das

pip

eye

ars

�E

xp

osu

rele

vels

:C

ase

s:m

ean

pip

eye

ars¼

17

7(r

an

ge

0–5

60

);C

on

tro

ls:

mea

np

ipe

years¼

12

2(r

an

ge

0–4

80

)

Lu

ng

can

cer

dia

gn

osi

s�

Mea

sure

men

tto

ol:

det

ecte

db

yra

dio

logy

an

dco

nfi

rmed

by

his

tolo

gy

or

cyto

logy

�B

lin

din

go

fo

utc

om

ead

ju-

dic

ato

r:n

ot

rep

ort

ed

�S

elec

tio

nb

ias:

seri

eso

fin

cid

ent

case

sb

ut

un

clea

rw

het

her

all

inci

den

tca

ses

rep

ort

ed,

con

tro

lsw

ere

sele

cted

fro

mth

esa

me

stu

dy

base

as

case

s�

Info

rmati

on

bia

s:o

bje

ctiv

eo

utc

om

eev

alu

ati

on

:ye

s;st

an

dard

ized

exp

osu

rem

easu

rem

ent:

no

.S

urr

ogate

sw

ere

inte

r-vi

ewed

for

10

%o

fca

ses

an

d6

%o

fco

ntr

ols

�C

on

fou

nd

ing:

matc

hin

gfo

rage;

ad

just

men

tfo

rage;

no

ad

just

men

tre

po

rted

for

rad

on

�P

art

icip

ati

on

rate

:n

ot

rep

ort

ed

OR

com

pare

dw

ith

nev

ersm

ok

ing:

�1

.9(9

5%

CI

0.4

–9

.4)

(wate

rpip

eo

nly

smo

kin

g)

�2

.1(9

5%

CI

0.5

–9

.1)

(wate

rpip

ean

dci

gare

tte

smo

kin

g)

�0

.9(9

5%

CI

0.1

–5

.4)

(cig

are

tte

on

lysm

ok

ing)

Sta

tist

icall

ysi

gn

ific

an

td

ose

resp

on

seto

wate

rp

ipe

smo

kin

gO

R¼

3.4

(1.3

–8

.1)

by

qu

art

ero

fp

ipe-

years

Lu

bin

29

�S

tud

yd

esig

n:

case

–co

ntr

ol

stu

dy

�F

un

din

g:

Ch

ina

Sci

ence

an

dT

ech

no

logy

Co

mm

issi

on

;an

dth

eU

SN

ati

on

al

Can

cer

Inst

itu

te�

Un

clea

rw

het

her

this

isa

rep

ort

on

asu

b-

po

pu

lati

on

of

Qia

o1

8

�S

etti

ng

an

dp

erio

d:

Gej

iuci

ty,

Yu

nn

an

Pro

vin

ce,

Ch

ina,

stu

dy

con

du

cted

in1

98

5�

Case

s:7

4lu

ng

can

cer

case

sin

male

sw

ith

mea

nage

62

years

(ran

ge

35

–8

0)

ali

veat

the

tim

eo

fth

est

ud

yre

po

rted

toL

ab

or

Pro

tect

ion

Inst

itu

teo

fth

eY

TC

du

rin

g1

98

1–8

4�

Co

ntr

ols

:7

4co

ntr

ols

cho

sen

fro

mth

eli

sto

fall

livi

ng

past

or

pre

sen

tw

ork

ers

of

the

YT

C;

on

eco

ntr

ol

per

case

�T

ype:

Ch

ines

ew

ate

rp

ipes

,ci

gare

ttes

�M

easu

rem

ent

too

l:se

lf-d

evel

op

edq

ues

-ti

on

nair

e,n

ost

an

-d

ard

izati

on

rep

ort

ed;

cum

ula

tive

con

-su

mp

tio

nca

lcu

late

das

pip

eye

ars

�E

xp

osu

rele

vels

of

incl

ud

edsu

bje

cts:

nu

mb

ero

fp

ipe

years

(case

s/co

ntr

ols

):0

(6/1

6);

1–1

14

(18

/2

3);

11

5–2

20

(21

/1

5);

52

20

(29

/20

)

Lu

ng

can

cer

dia

gn

osi

s�

Mea

sure

men

tto

ol:

case

sco

nfi

rmed

by

an

ind

epen

-d

ent

pan

elo

fp

ath

olo

gis

ts,

clin

icia

ns

an

dcy

tolo

gis

ts�

Bli

nd

ing

of

ou

tco

me

ad

ju-

dic

ato

r:n

ot

rep

ort

ed

�S

elec

tio

nb

ias:

seri

eso

fin

cid

ent

case

sb

ut

un

clea

rw

het

her

all

inci

den

tca

ses

rep

ort

ed;

excl

ud

edth

ose

wh

oh

ad

die

db

yth

eti

me

of

the

stu

dy;

con

tro

lsw

ere

sele

cted

fro

mth

esa

me

stu

dy

base

as

case

s�

Info

rmati

on

bia

s:o

bje

ctiv

eo

utc

om

eev

alu

ati

on

:ye

s;st

an

dard

ized

exp

osu

rem

easu

rem

ent:

no

;va

li-

date

dco

nfo

un

der

mea

-su

rem

ent

(ars

enic

):n

o�

Co

nfo

un

din

g:

matc

hin

gfo

rage

(wit

hin

5-y

ear

age

gro

up

s)�

Part

icip

ati

on

rate

:n

ot

rep

ort

ed�

Data

wer

esp

ars

ean

dau

tho

rsw

ere

un

ab

leto

ad

just

for

imp

ort

an

tco

n-

fou

nd

ing

fact

ors

OR

com

pare

dw

ith

no

tob

acc

osm

ok

ing:

�3

.6(w

ate

rpip

eo

nly

smo

kin

g)

�1

.2(c

igare

tte

on

lysm

ok

ing)

�3

.5(m

ixed

smo

kin

g)

(co

nti

nu

ed)

838 INTERNATIONAL JOURNAL OF EPIDEMIOLOGY

by guest on October 14, 2011

ije.oxfordjournals.orgD

ownloaded from

Ta

ble

1C

on

tin

ued

Stu

dy

Po

pu

lati

on

Ex

po

sure

Ou

tco

me

sM

eth

od

olo

gic

al

fea

ture

sR

esu

lts

Lu

bin

30

�S

tud

yd

esig

n:

case

–co

ntr

ol

stu

dy

�F

un

din

g:

no

tre

po

rted

�S

etti

ng

an

dp

erio

d:

Gej

iuci

ty,

Yu

nn

an

Pro

vin

ce,

Ch

ina

�C

ase

s:4

27

male

lun

gca

nce

rp

ati

ents

,m

ean

age

63

years

(ran

ge

35

–7

5);

rep

ort

edb

etw

een

19

84

an

d1

98

8to

the

Can

cer

Reg

istr

yo

fth

eL

ab

or

Pro

tect

ion

Inst

itu

teo

fY

TC

or

toth

eG

ejiu

Cit

yC

an

cer

Reg

istr

y;3

39

fro

mY

un

nan

Tin

Co

rpo

rati

on

an

d8

8fr

om

Gej

iuC

ity

�C

on

tro

ls:

10

11

male

con

-tr

ols

,tw

oco

ntr

ols

per

case

,m

ean

age

62

years

(ran

ge

35

–7

5),

77

0fr

om

YT

Can

d2

41

fro

mG

ejiu

city

�T

ype:

Ch

ines

ew

ate

rpip

e,ci

gare

ttes

�M

easu

rem

ent

too

l:se

lf-d

evel

op

edst

an

-d

ard

ized

stru

ctu

red

qu

esti

on

nair

e,n

ost

an

dard

izati

on

rep

ort

ed;

con

sum

p-

tio

nca

lcu

late

das

pip

eye

ars

�E

xp

osu

rele

vels

of

incl

ud

edsu

bje

cts:

mea

nd

ura

tio

no

fp

ipe

on

lysm

ok

ing

is4

1ye

ars

Lu

ng

can

cer

dia

gn

osi

s�

Mea

sure

men

tto

ol:

con

-fi

rmed

by

ind

epen

den

tp

an

elo

fp

ath

olo

gis

ts,

clin

icia

ns,

rad

iolo

gis

tsan

dcy

tolo

gis

ts�

Bli

nd

ing

of

ou

tco

me

ad

ju-

dic

ato

r:n

ot

rep

ort

ed

�S

elec

tio

nb

ias:

seri

eso

fin

cid

ent

case

s,co

ntr

ols

wer

eco

mm

un

ity

base

dan

dse

lect

edfr

om

the

sam

est

ud

yb

ase

as

case

s;�

Info

rmati

on

bia

s:o

bje

ctiv

eo

utc

om

eev

alu

ati

on

:ye

s;st

an

dard

ized

exp

osu

rem

easu

rem

ent:

no

�C

on

fou

nd

ing:

matc

hin

gfo

rage

(wit

hin

5-y

ear

age

gro

up

s);

ad

just

men

tfo

rage,

nu

mb

ero

fye

ars

of

wo

rku

nd

ergro

un

d,

sou

rce

of

sub

ject

,ty

pe

of

resp

on

den

t�

Part

icip

ati

on

rate

:7

2%

for

case

s,8

8%

for

con

tro

ls

OR

com

pare

dw

ith

no

smo

kin

g:

�1.8

(95%

CI

0.8

–4.2

)(w

ate

rpip

eon

lysm

ok

ing)

�2.6

(95%

CI

1.1

–6.2

)(c

igare

tte

on

ly)

OR

sfo

rp

ipe

use

rssh

ow

incr

easi

ng

tren

dw

ith

incr

ease

dd

ura

tio

no

fu

se(t

est

for

tren

dst

a-

tist

icall

ysi

gn

ific

an

t)

Hsa

iri3

1

�S

tud

yd

esig

n:

case

–co

ntr

ol

stu

dy

�F

un

din

g:

no

tre

po

rted

�S

etti

ng

an

dp

erio

d:

Ari

an

a,

Tu

nis

,D

ecem

ber

19

88

toM

ay

19

89

�C

ase

s:1

10

lun

gca

nce

rp

ati

ents

;ep

ider

mo

id(5

6%

),an

ap

last

icsm

all

cell

(17

%),

un

dif

fere

n-

tiate

d(1

3%

),ad

eno

carc

i-n

om

a(1

2%

),an

ap

last

icla

rge

cell

(3%

),�

Co

ntr

ols

:1

10

resi

den

tso

fth

esa

me

are

a

�T

ype:

wate

rpip

e,p

ipe,

inh

ale

dto

bacc

o,

can

nab

is�

Mea

sure

men

tto

ol:

self

-dev

elo

ped

too

l,n

ost

an

dard

izati

on

rep

ort

ed�

Ex

po

sure

leve

lso

fin

clu

ded

sub

ject

s:n

ot

rep

ort

ed

Lu

ng

can

cer

dia

gn

osi

s�

Mea

sure

men

tto

ol:

his

tolo

gi-

call

yco

n-

firm

edin

70

%o

fca

ses,

‘ver

yp

rob

ab

le’

in3

0%

of

case

sb

ase

do

ncl

ini-

cal,

rad

iolo

gic

al

an

den

do

-sc

op

icsu

spic

ion

�B

lin

din

go

fo

utc

om

ead

ju-

dic

ato

r:n

ot

rep

ort

ed

�S

elec

tio

nb

ias:

seri

eso

fin

cid

ent

case

s,co

ntr

ols

wer

eco

mm

un

ity

base

dan

dse

lect

edfr

om

the

sam

est

ud

yb

ase

as

case

s.�

Info

rmati

on

bia

s:o

bje

ctiv

eo

utc

om

eev

alu

ati

on

:ye

s;st

an

dard

ized

exp

osu

rem

easu

rem

ent:

no

�C

on

fou

nd

ing:

matc

hin

gfo

rage,

sex

,co

nsu

mp

tio

no

fci

gare

ttes

per

day;

ad

just

-m

ent

for

age,

sex

,ci

gare

tte

con

sum

pti

on

,o

ccu

pati

on

al

risk

s�

Part

icip

ati

on

rate

:n

ot

rep

ort

ed

OR

com

pare

dw

ith

no

smo

kin

g:

�3.0

(95%

CI

1.2

–7.6

)a

Gu

pta

28

�S

tud

yd

esig

n:

case

–co

ntr

ol

stu

dy

�F

un

din

g:

Inte

rnati

on

al

Agen

cy

�S

etti

ng

an

dp

erio

d:

No

rth

ern

Ind

ia;

recr

uit

-m

ent,

Jan

uary

19

95

toJu

ne

19

97

�T

ype:

cigare

ttes

,b

idis

,h

oo

kah

�M

easu

rem

ent

too

l:se

lf-d

evel

op

edto

ol,

no

stan

dard

izati

on

Lu

ng

can

cer

dia

gn

osi

s�

Mea

sure

men

tto

ol:

det

ecte

db

yra

dio

logy

�S

elec

tio

nb

ias:

seri

eso

fh

osp

ital

base

din

cid

ent

case

s,co

mm

un

ity-

base

dco

ntr

ols

sele

cted

fro

mth

esa

me

stu

dy

base

as

case

s

OR

com

pare

dw

ith

no

smo

kin

g:

�1

.94

(95

%C

I0

.85

–4

.44

)(h

oo

kah

smo

kin

g)

inm

en

(co

nti

nu

ed)

THE EFFECTS OF WATERPIPE TOBACCO SMOKING ON HEALTH 839

by guest on October 14, 2011

ije.oxfordjournals.orgD

ownloaded from

Ta

ble

1C

on

tin

ued

Stu

dy

Po

pu

lati

on

Ex

po

sure

Ou

tco

me

sM

eth

od

olo

gic

al

fea

ture

sR

esu

lts

for

Res

earc

ho

nC

an

cer,

Lyo

nF

ran

ce;

an

dth

eIn

tern

ati

on

al

can

cer

rela

ted

tech

no

logy

tran

sfer

fell

ow

ship

aw

ard

�C

ase

s:2

65

inci

den

tca

ses

of

lun

gca

nce

r�

Co

ntr

ols

:5

25

visi

tors

an

datt

end

an

tso

fth

ep

ati

ents

;tw

oco

ntr

ols

per

case

�P

art

icip

an

tsw

ere

85

%m

ale

,o

fd

iffe

ren

tre

ligio

ns,

ages

ran

gin

gfr

om

<5

0to

47

0li

vin

gin

rura

lo

ru

rban

are

as

rep

ort

ed;

cum

ula

tive

con

sum

pti

on

calc

u-

late

das

pack

-yea

req

uiv

ale

nt

of

cigar-

ette

s(1

hook

ah¼

4ci

gare

ttes

)st

rati

fied

info

ur

gro

up

s(0

–9

;1

0–1

9;

20

–2

9;

30þ

)�

Ex

po

sure

leve

lso

fin

clu

ded

sub

ject

s:in

com

ple

tely

rep

ort

ed

an

dco

nfi

rmed

by

his

tolo

gy

or

cyto

logy

�B

lin

din

go

fo

utc

om

ead

ju-

dic

ato

r:n

ot

rep

ort

ed

�In

form

ati

on

bia

s:o

bje

ctiv

eo

utc

om

eev

alu

ati

on

:ye

s;st

an

dard

ized

exp

osu

rem

easu

rem

ent:

no

�C

on

fou

nd

ing:

matc

hin

gfo

rage

an

dse

x;

ad

just

men

tfo

rage,

an

ded

uca

tio

n.

No

ad

just

men

tfo

ran

yco

n-

fou

nd

ing

fact

or

incl

ud

ing

oth

erfo

rms

of

tob

acc

oco

nsu

mp

tion

�P

art

icip

ati

on

rate

:n

ot

rep

ort

ed�

Mis

sin

gd

ata

:5

4.3

%fo

rex

po

sure

�N

um

ber

sfo

rw

om

enw

ere

too

small

tod

eriv

est

ab

leri

skes

tim

ate

s

Haze

lto

n3

2

�S

tud

yd

esig

n:

retr

o-

spec

tive

coh

ort

stu

dy

�F

un

din

g:

Nati

on

al

Inst

itu

teo

fH

ealt

h

�S

etti

ng

an

dp

erio

d:

Gej

iuci

ty,

Yu

nn

an

Pro

vin

ce,

Ch

ina,

12

years

foll

ow

-up

(19

76

–8

8)

�E

xp

ose

d:

12

89

male

wate

rpip

e-o

nly

smo

ker

san

d2

30

6m

ale

wate

rpip

ean

dci

gare

tte

smo

ker

s�

No

n-e

xp

ose

d:

84

16

male

s

�T

ype:

Ch

ines

ew

ate

rpip

e,ci

gare

tte

�M

easu

rem

ent

tool:

no

tre

po

rted

,ca

lcu

-la

ted

as

cum

ula

tive

exp

osu

rean

dca

te-

go

rize

din

toq

uart

iles

of

lian

g/m

on

thye

ar

�M

easu

rem

ent

tim

ep

oin

ts:ev

ery

5ye

ars

�E

xp

osu

rele

vels

of

incl

ud

edsu

bje

cts:

cum

ula

tive

dose

qu

art

iles

:0

(n¼

84

16

),0

.16

–4

.44

(n¼

87

7),

4.4

4–6

.25

(n¼

88

8),

6.2

5–9

.21

(n¼

90

6),

9.2

1–8

2.1

9(n¼

92

4)

Lu

ng

can

cer

mo

rtali

ty�

Mea

sure

men

tto

ol:

no

tre

po

rted

�B

lin

din

go

fo

utc

om

ead

ju-

dic

ato

r:n

ot

rep

ort

ed�

Inci

den

ce:

7%

�S

elec

tio

nb

ias:

smo

ker

sw

ere

rep

rese

nta

tive

of

the

stu

dy

base

,n

on

-sm

ok

ers

sele

cted

fro

mth

esa

me

com

mu

nit

yas

smo

ker

s�

Info

rmati

on

bia

s:u

nli

kel

yfo

rm

ort

ali

tyo

utc

om

e;st

an

dard

ized

exp

osu

rem

easu

rem

ent:

no

�C

on

fou

nd

ing:

no

ad

just

-m

ent

(no

ad

just

edR

Rre

po

rted

;cr

ud

eR

Rca

lcu

-la

ted

fro

mre

po

rted

data

)�

Part

icip

ati

on

rate

:n

ot

rep

ort

ed�

8%

lost

tofo

llo

w-u

p

�R

Rco

mp

are

dw

ith

no

smo

kin

g¼

4.3

9(9

5%

CI

3.8

2–5

.04

)(w

ate

rp

ipe

smo

kin

g)

Bed

wan

i33

�S

tud

yd

esig

n:

case

–co

ntr

ol

stu

dy

�F

un

din

g:

Nati

on

al

Res

earc

hC

ou

nci

l-A

pp

lica

zio

ni

clin

ich

ed

ella

rice

rca

on

colo

-gic

a(C

NR

-AC

RO

Pro

ject

);an

dIt

ali

an

�S

etti

ng

an

dp

erio

d:

Gre

ate

rA

lex

an

dri

a,

Egyp

t;st

ud

yco

nd

uct

ed,

Jan

uary

19

94

toJu

ly1

99

6�

Case

s:1

51

male

inci

den

tca

ses

of

inva

sive

bla

dd

erca

nce

rw

ith

med

ian

age

61

years

(ran

ge

31

–7

4)

ad

mit

ted

toa

net

wo

rko

f

�T

ype:

wate

rpip

e,ci

gare

tte,

hash

ish

�M

easu

rem

ent

tool:

self

-dev

elo

ped

stru

c-tu

red

qu

esti

on

nair

e;st

an

dard

izati

on

not

rep

ort

ed;

part

icip

an

tsca

tego

rize

das

ever

smo

ker

san

dn

ever

Bla

dd

erca

nce

rd

iagn

osi

s�

Mea

sure

men

tto

ol:

cen

trall

yre

view

edh

is-

top

ath

olo

gic

al

dia

gn

osi

s�

Bli

nd

ing

of

ou

tco

me

�S

elec

tio

nb

ias:

ho

spit

al-

base

dca

ses

of

bla

dd

erca

nce

rco

nfi

rmed

wit

hin

the

year

pre

ced

ing

inte

r-vi

ew,

ho

spit

al-

base

dco

n-

tro

lsse

lect

edfr

om

the

sam

est

ud

yb

ase

as

case

s.S

elec

tio

nre

late

dto

exp

o-

sure

statu

s(i

nth

eca

seo

f

OR

com

pare

dw

ith

nev

ersm

ok

ing:

�0

.8(9

5%

CI

0.2

–4

.0)

(wate

rpip

esm

ok

ing)

�5

.4(9

5%

CI

2.4

–1

2.1

)(<

20

/day

cigare

tte

smo

kin

g) (c

on

tin

ued

)

840 INTERNATIONAL JOURNAL OF EPIDEMIOLOGY

by guest on October 14, 2011

ije.oxfordjournals.orgD

ownloaded from

Ta

ble

1C

on

tin

ued

Stu

dy

Po

pu

lati

on

Ex

po

sure

Ou

tco

me

sM

eth

od

olo

gic

al

fea

ture

sR

esu

lts

Ass

oci

ati

on

for

Can

cer

Res

earc

hgen

eral

an

dte

ach

ing

ho

spit

als

.�

Co

ntr

ols

:1

57

male

sad

mit

ted

for

acu

te,

no

n-

neo

pla

stic

,n

on

-uri

nary

tract

,n

on

-sm

ok

ing-r

elate

dco

nd

itio

ns,

med

ian

age

50

years

(ran

ge

32

–7

4)

�3

9fe

male

case

san

d3

0fe

male

con

tro

lsw

ere

excl

ud

edb

ecau

se‘o

nly

on

efe

male

case

was

asm

ok

er’

smo

ker

s.A

ge

at

start

ing,

du

rati

on

of

hab

it,

ave

rage

dail

yco

nsu

mp

tio

nex

tract

edfr

om

his

-to

ryb

ut

no

tre

po

rted

�E

xp

osu

rele

vels

of

incl

ud

edsu

bje

cts:

no

tre

po

rted

ad

jud

icato

r:n

ot

rep

ort

edfe

male

san

dp

ati

ents

wit

hn

on

-sm

ok

ing-r

elate

dco

nd

itio

ns)

�In

form

ati

on

bia

s:o

bje

ctiv

eo

utc

om

eev

alu

ati

on

:ye

s;st

an

dard

ized

exp

osu

rem

easu

rem

ent:

no

�C

on

fou

nd

ing:

adju

stm

entf

orag

e,ed

uca

tion

,typ

eofh

ou

se,

his

tory

of

sch

isto

som

iasi

s,h

igh

-ris

kocc

up

atio

n,

tob

acco

smok

ing

�P

art

icip

ati

on

rate

:4

95

%o

fel

igib

lesu

bje

cts

part

ici-

pate

din

the

inte

rvie

w

�7

.6(9

5%

CI

3.4

–1

6.8

)fo

r5

20

/d

ay

cigare

tte

smo

kin

g

Nasr

oll

ah

zad

eh1

7

�T

ype

of

des

ign

:ca

se–

con

tro

lst

ud

y�

Fu

nd

ing:

Dig

esti

veD

isea

seR

esea

rch

Cen

ter:

Teh

ran

Un

iver

sity

of

Med

ical

Sci

ence

s(D

DR

C/T

UM

S);

an

dN

ati

on

al

Can

cer

Inst

itu

teat

Nati

on

al

Inst

itu

teo

fH

ealt

h

�S

etti

ng

an

dp

erio

d:

Atr

ak

Cli

nic

inG

on

bad

Cit

y,ea

ster

nG

ole

stan

Pro

vin

ceo

fIr

an

,D

ecem

ber

20

03

toJu

ne

20

07

�C

ase

s:3

00

oes

op

hagea

lsq

uam

ou

sce

llca

rcin

om

aca

ses,

50

%m

ale

s,m

ean

age

64

.5ye

ars

�C

on

tro

ls:

57

1co

ntr

ols

,tw

op

op

ula

tio

n-b

ase

dm

atc

hed

con

tro

lsu

bje

cts

per

case

for

90

%o

fca

ses

�T

ype:

ho

ok

ah

,ci

gar-

ette

s,n

ass

chew

ing,

op

ium

�M

easu

rem

ent

too

l:se

lf-d

evel

op

edq

ues

-ti

on

nair

e,te

sted

for

reli

ab

ilit

yan

dva

lid

-it

y,cu

mu

lati

veco

n-

sum

pti

on

calc

ula

ted

as

ho

ok

ah

-yea

rsan

dca

tego

rize

din

ton

ever

use

rs,4

32

ho

ok

ah

-yea

rs,4

32

ho

ok

ah

-yea

rs�

Ex

po

sure

leve

lso

fin

clu

ded

sub

ject

s:m

edia

no

f3

2h

oo

kah

-yea

rs

Oes

op

hagea

lsq

uam

ou

sce

llca

rcin

om

ad

iagn

osi

s�

Mea

sure

men

tto

ol:

his

to-

path

olo

gic

all

yco

nfi

rmed

�B

lin

din

go

fo

utc

om

ead

ju-

dic

ato

r:n

ot

rep

ort

ed

�S

elec

tio

nb

ias:

seri

eso

fin

cid

ent

case

s(7

0%

of

inci

-d

ent

case

sre

gis

tere

dw

ith

loca

lca

nce

rre

gis

try

wer

ere

ferr

edto

the

Atr

ak

Cli

nic

),co

ntr

ols

wer

ese

lect

edfr

om

the

sam

est

ud

yb

ase

as

case

s�

Info

rmati

on

bia

s:o

bje

ctiv

eo

utc

om

eev

alu

ati

on

:ye

s;st

an

dard

ized

exp

osu

rem

easu

rem

ent:

yes

�C

on

fou

nd

ing:m

atch

ing

for

age,

sex,r

esid

ence

;ad

just

-m

ent

for

edu

cati

on

,eth

ni-

city

,oth

erty

pes

of

tob

acco

use

,tota

lin

tak

eof

fru

itan

dve

get

able

s�

Part

icip

ati

on

rate

:n

ot

rep

ort

ed

OR

com

pare

dw

ith

no

smo

kin

g:

�1

.85

(95

%C

I0

.95

–3

.58

)(h

oo

kah

smo

kin

g)

�1

.69

(95

%C

I0

.76

–3

.77

)(h

oo

kah

on

lysm

ok

ing)

�1

.50

(95

%C

I0

.92

–2

.43

)(c

igare

tte

on

lysm

ok

ing)

�T

est

for

tren

dsi

gn

if-

ican

tfo

rin

ten

sity

(P¼

0.0

3)

bu

tn

ot

for

du

rati

on

,to

tal

am

ou

nt,

or

age

start

ed)

Fen

g3

4

�S

tud

yd

esig

n:

case

–co

ntr

ol

stu

dy

�F

un

din

g:

Ass

oci

ati

on

for

Inte

rnati

on

al

Can

cer

Res

earc

h

�S

etti

ng

an

dp

erio

d:

five

ho

spit

als

inA

lger

ia,

Mo

rocc

o,

an

dT

un

isia

,Ja

nu

ary

20

02

toM

arc

h2

00

5�

Case

s:6

36

inci

den

tca

ses

of

naso

ph

ary

ngea

lca

nce

r

�T

ype:

cigare

tte,

shis

ha,

snu

ff,

can

nab

is�

Mea

sure

men

tto

ol:

inte

rvie

ws,

self

-d

evel

op

edq

ues

tio

n-

nair

e,n

ost

an

dard

i-za

tio

nre

po

rted

;

Naso

ph

ary

ngea

lca

rcin

om

a�

Mea

sure

men

tto

ol:

case

sid

enti

fied

by

clin

icia

nin

the

On

colo

gy

an

d

�S

elec

tio

nb

ias:

seri

eso

fh

osp

ital-

base

din

cid

ent

case

s(2

00

1–0

4),

con

tro

lsw

ere

ho

spit

al-

base

do

rfr

ien

ds

an

dfa

mil

yo

fca

ses,

an

dre

cru

ited

fro

mth

esa

me

stu

dy

base

as

case

s

OR

com

pare

dw

ith

nev

ersm

ok

ing:

0.4

9(9

5%

CI

0.2

0–1

.23

)(e

ver

shis

ha

smo

kin

g)

(co

nti

nu

ed)

THE EFFECTS OF WATERPIPE TOBACCO SMOKING ON HEALTH 841

by guest on October 14, 2011

ije.oxfordjournals.orgD

ownloaded from

Ta

ble

1C

on

tin

ued

Stu

dy

Po

pu

lati

on

Ex

po

sure

Ou

tco

me

sM

eth

od

olo

gic

al

fea

ture

sR

esu

lts

�C

on

tro

ls:

61

5co

ntr

ols

[pati

ents

ho

spit

ali

zed

for

no

n-c

an

cer

dis

ease

s(6

1%

)an

dfr

ien

ds

an

dfa

mil

yo

fn

on

-can

cer

pati

ents

(39

%)]

part

icip

an

tsca

tego

r-iz

edas

ever

smo

ker

san

dn

ever

smo

ker

s.A

ges

of

start

ing,

an

dq

uit

tin

gd

ail

yco

n-

sum

pti

on

extr

act

edfr

om

his

tory

bu

tn

ot

rep

ort

ed�

Ex

po

sure

leve

lso

fin

clu

ded

sub

ject

s:n

ot

rep

ort

ed

rad

ioth

erap

yd

epart

men

ts�

Bli

nd

ing

of

ou

tco

me

ad

ju-

dic

ato

r:n

ot

rep

ort

ed

�In

form

ati

on

bia

s:o

bje

ctiv

eo

utc

om

em

easu

rem

ent:

yes,

stan

dard

ized

exp

osu

rem

easu

rem

ent:

no

�C

on

fou

nd

ing:

matc

hin

gfo

rh

osp

ital,

age,

sex

,h

ou

se-

ho

ldty

pe

(urb

an

/ru

ral)

;ad

just

men

tfo

rage

�P

art

icip

ati

on

rate

:4

90

%

Ali

35

�S

tud

yd

esig

n:

cro

ss-

sect

ion

al

stu

dy

�F

un

din

g:

no

tre

po

rted

�S

etti

ng

an

dp

erio

d:

Yem

en;

per

iod

no

tre

po

rted

�P

op

ula

tio

n:

Yem

eni

volu

n-

teer

s(2

7m

enan

dsi

xw

om

en)

all

chew

ers

of

al-

qat,

mea

nage

38

.5ye

ars

(ran

ge

22

–5

8),

all

of

them

free

fro

man

ysy

stem

ati

cd

isea

ses.

11

wate

rpip

esm

ok

ers,

11

cigare

tte

smo

ker

s,1

1n

on

-sm

ok

ers

�T

ype:

cigare

tte

smo

kin

g,

wate

rpip

esm

ok

ing

�M

easu

rem

ent

too

l:in

terv

iew

s,st

an

dar-

diz

ati

on

no

tre

po

rted

,su

bje

cts

cate

go

rize

das

hea

vyci

gare

tte

smo

ker

s(4

20

/day)

,n

on

-sm

o-

ker

san

dw

ate

rpip

esm

ok

ers

�E

xp

osu

rele

vels

of

incl

ud

edsu

bje

cts:

no

tre

po

rted

Dys

pla

sia

of

ora

lm

uco

sad

iagn

osi

s�

Mea

sure

men

tto

ol:

his

to-

path

olo

gic

al

exam

inati

on

of

bu

ccal

mu

cosa

bio

psi

es�

Bli

nd

ing

of

ou

tco

me

ad

ju-

dic

ato

r:n

ot

rep

ort

ed

�S

elec

tio

nb

ias:

volu

nte

erre

cru

itm

ent

into

the

stu

dy

�In

form

ati

on

bia

s:o

bje

ctiv

eo

utc

om

em

easu

rem

ent:

yes,

stan

dard

ized

exp

osu

rem

easu

rem

ent:

no

�C

on

fou

nd

ing:

no

matc

hin

go

rad

just

men

tin

the

an

a-

lysi

sre

po

rted

�P

art

icip

ati

on

rate

:n

ot

rep

ort

ed

OR

com

pare

dw

ith

no

smo

kin

g:

�8

.33

(95

%C

I0

.78

–9

.47

)(w

ate

rpip

esm

ok

ing)

Res

ult

sare

rest

rict

edto

the

chew

ing

sid

e;n

oev

ents

inei

ther

gro

up

on

no

n-c

hew

ing

sid

e.O

Rca

lcu

late

dfr

om

rep

ort

edn

um

ber

s

aN

inet

yfi

vep

erce

nt

ad

just

edO

Ran

dC

Ire

po

rted

as

5.7

(1.2

–7

.6).

As

the

effe

ctes

tim

ate

was

no

tco

nsi

sten

tw

ith

the

po

siti

on

of

the

low

eran

du

pp

erb

ord

ers

of

the

CI

an

dgiv

enth

eu

nad

just

edO

Rw

as

4.8

,an

das

we

wer

eu

nab

leto

con

tact

the

au

tho

rs,

we

use

dO

R¼

3.0

wh

ich

we

calc

ula

ted

base

do

nth

eC

Io

f1

.2–7

.6.

842 INTERNATIONAL JOURNAL OF EPIDEMIOLOGY

by guest on October 14, 2011

ije.oxfordjournals.orgD

ownloaded from

with dry socket was 3.7 (P¼ 0.001). We judged theoverall quality of evidence to be low (Appendix 3).

Infectious diseaseWe identified three studies on hepatitis C. The threecross-sectional studies were conducted in Egypt andrestricted to male participants exposed to groupwaterpipe tobacco smoking (Table 4).22,43,44 Thepooled OR for the association of group waterpipetobacco with hepatitis C was 0.98 (95% CI 0.80–1.21; I2

¼ 0%) (Figure 5). We judged the overall qual-ity of evidence to be very low (Appendix 3).

We did not identify any eligible study assessing theassociation between waterpipe smoking and thetransmission of tuberculosis. We did identify tworeports of outbreak investigations suggesting an asso-ciation between tuberculosis and sharing tobaccowaterpipe23 and marijuana waterpipe.47

Respiratory illnessOne cross-sectional study evaluated the associationbetween waterpipe smoking and respiratory illness(defined as perennial rhinitis and including nasalcongestion and wheezing) (Table 5).45 The studyreported significant association of waterpipe tobacco

smoking (OR¼ 2.3; 95% CI 1.1–5.1) and of waterpipeand/or cigarette smoking (OR¼ 2.5; 95% CI 1.6–3.8)with respiratory illness. We judged the overall qualityof evidence to be very low (Appendix 3).

InfertilityOne case–control study evaluated the associationbetween waterpipe smoking and male factor infertility(based on semen analysis) (Table 5).46 The reportedOR for the association of waterpipe tobacco smokingwith male factor infertility was not statistically signif-icant (OR¼ 2.5; 95% CI 1.0–6.3). We judged the over-all quality of evidence to be very low (Appendix 3).

DiscussionWe systematically reviewed the medical literature forthe effects of waterpipe tobacco smoking on healthoutcomes. Based on the available evidence, waterpipetobacco smoking was significantly associated withlung cancer, respiratory illness, low birth-weight andperiodontal disease. It was not significantly associatedwith bladder cancer, nasopharyngeal cancer, oesopha-geal cancer, oral dysplasia or infertility but the CIs did

Study or Subgroup

Gupta 2001

Hsairi 1993

Lubin 1992

Qiao 1989

Total (95% CI)

Heterogeneity: Tau² = 0.00; Chi ² = 0.74, df = 3 (P = 0.86); I ² = 0%

Test for overall effect: Z = 3.09 (P = 0.002)

log[OR]

0.662688

1.098612

0.587787

0.64185389

SE

0.422432

0.474253

0.432295

0.81574276

Weight

33.2%

26.3%

31.7%

8.9%

100.0%

IV, Random, 95% CI

1.94 (0.85, 4.44)

3.00 (1.18, 7.60)

1.80 (0.77, 4.20)

1.90 (0.38, 9.40)

2.12 (1.32, 3.42)

OR

IV, Random, 95% CI

0.01 0.1 1 10 100Protective effect

OR

Harmful effect

Figure 3 Association between waterpipe tobacco smoking and lung cancer

Study or Subgroup

Aghamolaei 2007

Nuwayhid 1998

Tamim 2008

Total (95% CI)

Heterogeneity: Tau ² = 0.00; Chi ² = 1.19, df = 2 (P = 0.55); I ² = 0%

Test for overall effect: Z = 2.17 (P = 0.03)

log[OR]

1.252763

0.774727

0.277632

SE

0.653538

0.546211

0.614272

Weight

28.1%

40.2%

31.8%

100.0%

IV, Random, 95% CI

3.50 (0.97, 12.60)

2.17 (0.74, 6.33)

1.32 (0.40, 4.40)

2.12 (1.08, 4.18)

OR

IV, Random, 95% CI

0.01 0.1 1 10 100Protective effect

OR

Harmful effect

Figure 4 Association between waterpipe tobacco smoking and low birth-weight

THE EFFECTS OF WATERPIPE TOBACCO SMOKING ON HEALTH 843

by guest on October 14, 2011

ije.oxfordjournals.orgD

ownloaded from

Ta

ble

2C

hara

cter

isti

cso

fin

clu

ded

stu

die

sass

essi

ng

the

effe

cto

fw

ate

rpip

eto

bacc

osm

ok

ing

on

pre

gn

an

cyo

utc

om

es

Stu

dy

Po

pu

lati

on

Ex

po

sure

Ou

tco

me

sM

eth

od

olo

gic

al

fea

ture

sR

esu

lts

Nu

wayh

id1

9

�S

tud

yd

esig

n:

retr

o-

spec

tive

coh

ort

stu

dy

�F

un

din

g:

Hari

riF

ou

nd

ati

on

;an

dU

niv

ersi

tyR

esea

rch

Bo

ard

at

the

Am

eric

an

Un

iver

sity

of

Bei

rut

�S

etti

ng

an

dp

erio

d:

ho

spit

als

inL

eban

on

;1

99

3an

d1

99

5�

Part

icip

an

ts:

pre

g-

nan

tw

om

end

eli-

veri

ng

inh

osp

itals

.1

06

narg

hil

esm

o-

ker

s(m

ean

age

27

.6ye

ars

),2

77

cigare

tte

smo

ker

s(m

ean

age

29

.1)

an

d5

12

no

n-

smo

ker

s(m

ean

age

28

.5)

�T

ype

of

exp

osu

re:

narg

hil

e,ci

gare

ttes

�M

easu

rem

ent

too

l:in

terv

iew

s,st

an

dar-

diz

ati

on

no

tre

po

rted

;ca

tego

rize

din

to<

1vs

51

per

day;

an

dst

art

edsm

ok

ing

du

rin

gfi

rst

vsse

con

do

rth

ird

trim

este

r�

Mea

sure

men

tti

me

po

ints

:n

ot

rep

ort

ed�

Ex

po

sure

leve

lso

fin

clu

ded

sub

ject

s:<

1p

erd

ay

(n¼

38

);5

1p

erd

ay

(n¼

67

)p

erd

ay;

firs

ttr

ime-

ster

(n¼

78

);se

con

do

rth

ird

trim

este

r(n¼

25

)

Lo

wb

irth

-wei

gh

t,A

pgar

sco

re<

7(1

an

d5

min

),p

ulm

on

ary

pro

ble

ms,

malf

orm

ati

on

s,p

eri-

nata

lco

mp

lica

tio

ns

�M

easu

rem

ent

too

l:m

edic

al

reco

rds;

low

bir

th-w

eigh

td

efin

edas

ab

irth

wei

gh

t<

25

00

g�

Bli

nd

ing

of

ou

tco

me

ad

jud

icato

r:n

ot

rep

ort

ed

�S

elec

tio

nb

ias:

un

clea

rw

het

her

sam

ple

isre

pre

sen

tati

ve(d

ata

coll

ecti

on

ina

few

nu

mb

ero

fh

osp

itals

)�

Info

rmati

on

bia

s:o

bje

ctiv

eo

utc

om

em

ea-

sure

men

t:ye

sb

ut

base

do

nm

edic

al

reco

rds,

stan

dard

ized

exp

osu

rem

easu

rem

ent:

no

�C

on

fou

nd

ing:

ad

just

-m

ent

for

age,

ho

spit

al

loca

tio

n,

ges

tati

on

al

age,

exp

osu

reto

pass

ive

smo

kin

g,

an

dp

revi

ou

slo

wb

irth

-wei

gh

t�

Part

icip

ati

on

rate

:n

ot

rep

ort

ed�

<1

0%

mis

sin

gd

ata

OR

for

narg

hil

esm

ok

ing

com

pare

dw

ith

no

smo

kin

g�

low

bir

th-w

eigh

t¼

2.1

7(9

5%

CI

0.7

4–6

.33

)�

low

bir

th-w

eigh

t¼

2.3

6(9

5%

CI

0.5

2–1

0.7

3)

(<1

/day)

�lo

wb

irth

-wei

gh

t¼

2.0

7(9

5%

CI

0.5

4–7

.94

)(5

1/d

ay)

�lo

wb

irth

-wei

gh

t¼

2.9

3(9

5%

CI

0.9

7–8

.83

)(n

arg

hil

esm

ok

ing

start

edin

firs

ttr

imes

ter)

�T

est

for

tren

dfo

rlo

wb

irth

-wei

gh

tn

ot

sign

ific

an

tfo

rin

ten

sity

(P<

0.1

8)

�A

pgar

sco

re<

7at

1m

in¼

1.7

3(9

5%

CI

0.7

3–4

.14

)�

Ap

gar

sco

re<

7at

5m

in¼

3.3

9(9

5%

CI

0.5

4–2

1.4

2)

�P

ulm

on

ary

pro

ble

ms¼

3.6

5(9

5%

CI

1.5

2–8

.75

)�

Malf

orm

ati

on

s¼

2.0

1(9

5%

CI

0.5

9–6

.88

)�

Per

inata

lco

mp

lica

tio

ns¼

1.6

7(9

5%

CI

0.8

2–3

.41

)O

Rfo

rci

gare

tte

smo

kin

gco

mp

are

dw

ith

no

smo

kin

g�

Lo

wb

irth

-wei

gh

t¼

2.0

0(9

5%

CI

0.9

6–4

.20

)�

low

bir

th-w

eigh

t¼

2.2

5(9

5%

CI

1.0

4–4

.86

)(n

arg

hil

esm

ok

ing

start

edin

firs

ttr

imes

ter)

�A

pgar

sco

re<

7at

1m

in¼

1.5

9(9

5%

CI

0.8

2–3

.07

)�

Ap

gar

sco

re<

7at

5m

in¼

2.6

2(9

5%

CI

0.5

6–1

2.2

9)

�P

ulm

on

ary

pro

ble

ms¼

1.7

6(0

.80

–3

.87

)�

Malf

orm

ati

on

s¼

1.3

6(0

.49

–3

.80

)�

Per

inata

lco

mp

lica

tio

ns¼

1.5

0(0

.87

–2

.57

)

(co

nti

nu

ed)

844 INTERNATIONAL JOURNAL OF EPIDEMIOLOGY

by guest on October 14, 2011

ije.oxfordjournals.orgD

ownloaded from

Ta

ble

2C

on

tin

ued

Stu

dy

Po

pu

lati

on

Ex

po

sure

Ou

tco

me

sM

eth

od

olo

gic

al

fea

ture

sR

esu

lts

Agh

am

ola

ei3

7

�S

tud

yd

esig

n:

case

–co

ntr

ol

stu

dy

�F

un

din

g:

no

tre

po

rted

�S

etti

ng

an

dp

erio

d:

Sh

ari

ati

Ho

spit

al

of

Ban

dar

Ab

bas,

So

uth

of

Iran

;p

erio

dn

ot

rep

ort

ed�

Case

s:6

0In

tra-u

ter-

ine

gro

wth

reta

rda-

tio

nin

fan

ts�

Co

ntr

ols

:6

0n

orm

al

bir

thin

fan

ts�

Incl

ud

edsu

bje

cts:

all

term

infa

nts

wit

hges

tati

on

al

age

37

–4

2w

eek

s;2

9m

ale

san

d3

1fe

male

sin

each

gro

up

.‘N

on

eo

fin

clu

ded

mo

ther

ssm

ok

edan

du

sed

alc

oh

ol

du

rin

gp

reg-

nan

cyan

dn

on

eo

fth

emh

ad

dia

bet

es’

�T

ype:

ho

ok

ah

smo

k-

ing

by

mo

ther

�M

easu

rem

ent

too

l:st

ruct

ure

dq

ues

tio

n-

nair

ead

min

iste

red

tom

oth

ers,

stan

dar-

diz

ati

on

no

tre

po

rted

�E

xp

osu

rele

vels

of

incl

ud

edsu

bje

cts:

no

tre

po

rted

Intr

au

teri

ne

gro

wth

reta

rdati

on

(IU

GR

)�

Def

init

ion

:te

rmin

fan

tsw

ith

ab

irth

-w

eigh

t<

25

00

g�

Mea

sure

men

tto

ol:

bir

thw

eigh

td

eter

-m

ined

up

to1

0m

ino

fd

eliv

ery

usi

ng

ad

igit

al

bab

ysc

ale

�B

lin

din

go

fo

utc

om

ead

jud

icato

r:n

ot

rep

ort

ed

�S

elec

tio

nb

ias:

seri

eso

fin

cid

ent

case

so

fIU

GR

inm

ate

rnit

yw

ard

s,co

ntr

ols

sele

cted

fro

mth

esa

me

stu

dy

base

as

the

case

s�

Info

rmati

on

bia

s:o

bje

ctiv

eo

utc

om

em

ea-

sure

men

t:ye

s,st

an

dar-

diz

edex

po

sure

mea

sure

men

t:n

o�

Co

nfo

un

din

g:

exp

lore

d1

8p

ote

nti

al

risk

fact

ors

an

dad

just

edfo

rm

ate

rnal

wo

rk,

hyp

er-

ten

sio

n,

an

ten

ata

lca

re�

Part

icip

ati

on

rate

:n

ot

rep

ort

ed

�O

Rfo

rh

oo

kah

smo

kin

gd

uri

ng

pre

gn

an

cyco

mp

are

dw

ith

no

ho

ok

ah

smo

kin

gd

uri

ng

pre

gn

an

cy¼

3.5

(95

%C

I1

.1–1

2.6

)

Tam

im3

6

�S

tud

yd

esig

n:

retr

osp

ecti

veco

ho

rtst

ud

y�

Fu

nd

ing:

Leb

an

ese

Nati

on

al

Co

un

cil

for

Sci

enti

fic

Res

earc

h;

the

Med

ical

Pra

ctic

eP

lan

;an

dth

eU

niv

ersi

tyR

esea

rch

Bo

ard

at

the

Am

eric

an

Un

iver

sity

of

Bei

rut

�S

etti

ng

an

dp

erio

d:

six

majo

rh

osp

itals

ingre

ate

rB

eiru

t,L

eban

on

,A

ugu

st2

00

0to

Au

gu

st2

00

3�

Po

pu

lati

on

:3

78

sin

-gle

ton

new

bo

rns

tow

om

enex

clu

sive

narg

hil

esm

ok

ers,

92

9si

ngle

ton

new

-b

orn

sto

wo

men

excl

usi

veci

gare

tte

smo

ker

s,8

4si

ngle

-to

nn

ewb

orn

sto

wo

men

smo

kin

gb

oth

typ

eso

fto

bacc

o,

72

01

sin

-gle

ton

new

bo

rns

tow

om

enn

on

-sm

ok

ers

�T

ype:

narg

hil

e,ci

gare

ttes

�M

easu

rem

ent

too

l:in

terv

iew

s,q

ues

tio

n-

nair

ep

ilo

tte

sted

;n

arg

hil

esm

ok

ers

cate

go

rize

din

to4

1vs

41

per

day;

cate

-go

rize

din

to<

1vs

51

per

day;

an

dst

art

edsm

ok

ing

du

rin

gfi

rst

vsse

con

do

rth

ird

trim

este

r�

Mea

sure

men

tti

me

po

ints

:n

ot

rep

ort

ed�

Ex

po

sure

leve

lso

fin

clu

ded

sub

ject

s:4

1p

erd

ay

(n¼

23

3);4

1p

erd

ay

(n¼

14

5);

firs

ttr

imes

ter

(n¼

30

9);

seco

nd

or

thir

dtr

i-m

este

r(n¼

69

)

Lo

wb

irth

-wei

gh

t�

Mea

sure

men

tto

ol:

data

coll

ecti

on

fro

mo

bst

etri

can

dn

urs

ery

chart

s,lo

wb

irth

-w

eigh

td

efin

edas

42

50

0g

�B

lin

din

go

fo

utc

om

ead

jud

icato

r:n

ot

rep

ort

ed

�S

elec

tio

nb

ias:

sam

ple

rep

rese

nta

tive

of

po

pu

-la

tio

ns

of

six

majo

rh

osp

itals

inG

reate

rB

eiru

t�

Info

rmati

on

bia

s:o

bje

ctiv

eo

utc

om

em

ea-

sure

men

t:ye

sb

ut

base

do

nm

edic

al

reco

rds,

stan

dard

ized

exp

osu

rem

easu

rem

ent:

no

(pil

ot

test

edo

nly

)�

Co

nfo

un

din

g:

ad

just

-m

ent

for

mate

rnal/

pate

rnal

edu

cati

on

,m

oth

er’s

wo

rkin

gst

atu

s,m

oth

er’s

age,

pari

ty,

dia

bet

es,

ble

ed-

ing,

pre

gn

an

cyh

yper

-te

nsi

ved

iso

rder

s,ges

tati

on

al

age,

an

dp

ass

ive

smo

kin

g�

Part

icip

ati

on

rate

:n

ot

rep

ort

ed

OR

for

narg

hil

eo

nly

smo

kin

gco

mp

are

dw

ith

no

smo

kin

g�

low

bir

th-w

eigh

t¼

1.3

2(9

5%

CI

0.3

9–4

.40

)(O

Rp

oo

led

for

41

day

an

d4

1d

ay)

�lo

wb

irth

-wei

gh

t¼

0.7

(95

%C

I0.3

–1.6

)(4

1d

ay)

�lo

wb

irth

-wei

gh

t¼

2.4

(95

%C

I1.2

–5.0

)(4

1d

ay)

�lo

wb

irth

-wei

gh

t¼

1.2

(95

%C

I0

.6–2

.2)

(narg

hil

esm

ok

ing

start

edin

firs

ttr

imes

ter)

�O

Rfo

rci

gare

tte

on

lysm

ok

ing

com

pare

dw

ith

no

smo

kin

g¼

1.3

2(9

5%

CI

0.9

1–1

.90

)

THE EFFECTS OF WATERPIPE TOBACCO SMOKING ON HEALTH 845

by guest on October 14, 2011

ije.oxfordjournals.orgD

ownloaded from

Ta

ble

3C

hara

cter

isti

cso

fin

clu

ded

stu

die

sass

essi

ng

the

effe

cto

fw

ate

rpip

eto

bacc

osm

ok

ing

on

per

iod

on

tal

dis

ease

Stu

dy

Po

pu

lati

on

Ex

po

sure

Ou

tco

me

sM

eth

od

olo

gic

al

fea

ture

sR

esu

lts

Natt

o3

9

�S

tud

yd

esig

n:

cro

ss-

sect

ion

al

stu

dy

�F

un

din

g:

Min

istr

yof

Hea

lth

inS

au

di

Ara

bia

;an

dS

au

di

Ara

bia

nC

ult

ura

lB

ure

au

Off

ice

inB

on

n

�S

etti

ng

an

dp

erio

d:

Jed

dah

,S

au

di

Ara

bia

,p

erio

dn

ot

rep

ort

ed�

Part

icip

an

ts:

35

5vo

lun

-te

ers,

28

%fe

male

s,m

ean

age

36

.9ye

ars

(ran

ge

17

–6

0),

havi

ng

20

teet

han

dn

ot

pre

gn

an

t

�T

ype:

wate

rpip

e,ci

gare

ttes

�M

easu

rem

ent

too

l:st

an

dard

ized

qu

esti

on

-n

air

ead

min

iste

red

inin

terv

iew

s,st

an

dard

iza-

tio

nn

ot

rep

ort

ed;

cal-

cula

ted

as

run

-yea

rs(p

rod

uct

of

wate

rpip

eru

ns

per

day

wit

hye

ars

of

smo

kin

g;

aru

nis

the

com

ple

tio

no

fth

ew

ate

rpip

esm

ok

ing

un

til

the

tob

acc

ois

bu

rnt)

;h

eavy

exp

osu

rew

as

def

ined

as5

40

run

-yea

rs�

Ex

po

sure

leve

lso

fin

clu

ded

sub

ject

:m

ean

exp

osu

reo

f5

6.8

run

-ye

ars

for

wate

rpip

esm

ok

ers

Per

iod

on

tal

dis

ease

mea

sure

das

per

iod

-o

nta

lb

on

eh

eigh

tlo

ss�

Mea

sure

men

tto

ol:

dig

ital

pan

ora

mic

rad

iogra

ph

s.B

on

elo

ssd

efin

edas

bo

ne

hei

gh

t4

70

%.

Mea

nb

on

eh

eigh

tp

erin

div

idu

al

isth

era

tio

of

the

per

iod

-o

nta

lb

on

eh

eigh

tto

the

roo

tle

ngth

�B

lin

din

go

fo

utc

om

ead

jud

icato

r:ye

s

�S

elec

tio

nb

ias:

volu

n-

teer

sre

cru

ited

by

new

spap

eran

no

un

cem

ents

�In

form

ati

on

bia

s:o

bje

ctiv

eo

utc

om

em

ea-

sure

men

t:ye

s,st

an

dar-

diz

edex

po

sure

mea

sure

men

t:n

o�

Co

nfo

un

din

g:

ad

just

-m

ent

for

age

on

ly�

Part

icip

ati

on

rate

:n

ot

rep

ort

ed

OR

com

pare

dw

ith

no

smo

kin

g�

3.5

(95%

CI

1.6

–7.6

)(w

ate

rpip

eon

lysm

ok

ing)

�1.0

(95%

CI

0.3

–3.1

)(l

igh

tw

ate

rpip

eo

nly

smo

kin

g)

�7

.5(9

5%

CI

3.0

–1

8.3

)(h

eavy

wate

r-p

ipe

on

lysm

ok

ing)

�T

he

ass

oci

ati

on

bet

wee

nw

ate

rpip

esm

ok

ing

an

db

on

eh

eigh

tre

main

edst

a-

tist

icall

ysi

gn

ific

an

taft

erco

ntr

oll

ing

for

‘ed

uca

tion

as

asu

r-ro

gate

for

soci

o-e

co-

no

mic

stan

dard

an

do

ther

vari

ab

les’

�D

iffe

ren

ces

bet

wee

nli

gh

tan

dh

eavy

exp

osu

res

wer

est

a-

tist

icall

ysi

gn

ific

an

t(P

<0

.00

1)

Natt

o4

0

�S

tud

yd

esig

n:

cro

ss-

sect

ion

al

stu

dy

�F

un

din

g:

no

tre

po

rted

�S

etti

ng

an

dp

erio

d:

Wes

tern

part

of

Sau

di

Ara

bia

,p

erio

dn

ot

rep

ort

ed�

Part

icip

an

ts:

24

4vo

lun

-te

ers,

34

%fe

male

s,m

ean

age

37

.4ye

ars

(ran

ge

25

–7

0),

havi

ng

20

teet

han

dn

ot

pre

gn

an

t

�T

ype:

wate

rpip

e,ci

gare

ttes

�M

easu

rem

ent

too

l:st

an

dard

ized

qu

esti

on

-n

air

ead

min

iste

red

inin

terv

iew

s,st

an

dard

iza-

tio

nn

ot

rep

ort

ed;

cal-

cula

ted

as

run

-yea

rs(p

rod

uct

of

wate

rpip

eru

ns

per

day

wit

hye

ars

of

smo

kin

g;

aru

nis

the

com

ple

tio

no

fth

ew

ate

rpip

esm

ok

ing

un

til

the

tob

acc

ois

bu

rnt)

�E

xp

osu

rele

vels

of

incl

ud

edsu

bje

ct:

no

tre

po

rted

Per

iod

on

tal

dis

ease

mea

sure

das

pla

qu

ein

dex

an

dgin

giv

itis

�M

easu

rem

ent

too

l:P

laq

ue:

clin

ical

exam

inati

on

,p

re-

sen

ceo

fvi

sib

led

enta

lp

laq

ue

was

reco

rded

acc

ord

ing

toth

ecr

iter

iao

fS

iln

ess

an

dL

oe

�B

lin

din

go

fo

utc

om

ead

jud

icato

r:n

ot

rep

ort

ed

�S

elec

tio

nb

ias:

24

4o

fth

e3

55

volu

nte

ers

par-

tici

pati

ng

inan

oth

erst

ud

y38

volu

nte

ered

for

acl

inic

al

exam

inati

on

�In

form

ati

on

bia

s:o

bje

ctiv

eo

utc

om

em

ea-

sure

men

t:ye

s,st

an

dar-

diz

edex

po

sure

mea

sure

men

t:n

o�

Co

nfo

un

din

g:

ad

just

-m

ent

for

age,

den

tal

care

hab

it�

Part

icip

ati

on

rate

:6

8%

�T

her

ew

as

an

ove

rall

sign

ific

an

tass

oci

a-

tio

nb

etw

een

smo

k-

ing

an

dp

laq

ue

ind

exan

dgin

giv

al

ind

ex.

No

effe

ctes

tim

ate

sre

po

rted

(co

nti

nu

ed)

846 INTERNATIONAL JOURNAL OF EPIDEMIOLOGY

by guest on October 14, 2011

ije.oxfordjournals.orgD

ownloaded from

Ta

ble

3C

on

tin

ued

Stu

dy

Po

pu

lati

on

Ex

po

sure

Ou

tco

me

sM

eth

od

olo

gic

al

fea

ture

sR

esu

lts

Natt

o4

1

�S

tud

yd

esig

n:

cro

ss-

sect

ion

al

stu

dy

�F

un

din

g:

Min

istr

yo

fH

ealt

hin

Sau

di

Ara

bia

;an

dS

au

di

Ara

bia

nC

ult

ura

lB

ure

au

Off

ice

inB

on

n

�S

etti

ng

an

dp

erio

d:

Jed

dah

,S

au

di

Ara

bia

,p

erio

dn

ot

rep

ort

ed�

Po

pu

lati

on

:2

62

volu

nte

ers,

35

%fe

male

s,m

ean

age

36

.5(r

an

ge

17

–6

0).

Part

icip

an

tsw

ere

req

uir

edto

have

20

teet

han

dn

ot

be

pre

gn

an

t.5

1ci

tize

ns

wit

hp

erio

do

nta

ld

isea

sean

d2

11

citi

zen

sw

ith

ou

tp

erio

do

nta

ld

isea

se

�T

ype:

wate

rpip

e,ci

gare

ttes

�M

easu

rem

ent

too

l:st

an

dard

ized

qu

esti

on

-n

air

ead

min

iste

red

inin

terv

iew

s,st

an

dard

iza-

tio

nn

ot

rep

ort

ed;

cal-

cula

ted

as

run

-yea

rs(p

rod

uct

of

wate

rpip

eru

ns

per

day

wit

hye

ars

of

smo

kin

g;

aru

nis

the

com

ple

tio

no

fth

ew

ate

rpip

esm

ok

ing

un

til

the

tob

acc

ois

bu

rnt)

;h

eavy

exp

osu

rew

as

def

ined

as5

40

run

-yea

rs�

Ex

po

sure

leve

lso

fin

clu

ded

sub

ject

:m

ean

exp

osu

reo

f3

5.8

run

-ye

ars

for

wate

rpip

esm

ok

ers

Per

iod

on

tal

dis

ease

mea

sure

das

dee

pen

-in

go

fth

esu

lci

or

po

cket

s�

Mea

sure

men

tto

ol:

clin

ical

exam

inati

on

pro

bin

gth

ed

epth

of

the

sulc

io

rp

ock

ets

wit

ha

2-m

mgra

du

-ate

dp

erio

do

nta

lp

rob

e;p

erio

do

nta

ld

isea

sed

efin

edas

51

0si

tes

wit

ha

pro

bin

gd

epth

55

mm

�B

lin

din

go

fo

utc

om

ead

jud

icato

r:n

ot

rep

ort

ed

�S

elec

tio

nb

ias:

26

2o

fth

e3

55

volu

nte

ers

par-

tici

pati

ng

inan

oth

erst

ud

y18

volu

nte

ered

for

acl

inic

al

exam

inati

on

�In

form

ati

on

bia

s:o

bje

ctiv

eo

utc

om

em

ea-

sure

men

t:ye

s,st

an

dar-

diz

edex

po

sure

mea

sure

men

t:n

o�

Co

nfo

un

din

g:

ad

just

-m

ent

for

age

on

ly�

Part

icip

ati

on

rate

:7

4%

OR

com

pare

dw

ith

no

smo

kin

g�

5.1

(95

%C

I2

.0–1

3.5

(wate

rpip

eo

nly

smo

kin

g)

�8

.2(9

5%

CI

2.9

–2

2.9

)(h

eavy

wate

r-p

ipe

smo

kin

g)

�2

.9(9

5%

CI

1.7

–4

.8)

(lig

ht

wate

rpip

esm

ok

ing)

�3

.8(9

5%

CI

1.3

–1

1.0

)(c

igare

tte

on

lysm

ok

ing)

�5

.0(9

5%

CI

1.6

–1

6.2

),P

<0

.00

1(h

eavy

cigare

tte

on

lysm

ok

ing)

�1

.5(9

5%

CI

1.1

–2

.0),

P<

0.0

01

(lig

ht

cigare

tte

on

lysm

ok

ing)

�D

iffe

ren

ces

bet

wee

nli

gh

tan

dh

eavy

exp

osu

rew

ere

sta-

tist

icall

ysi

gn

ific

an

t

Balj

oo

n4

2

�S

tud

yd

esig

n:

cro

ss-

sect

ion

al

stu

dy

�F

un

din

g:

Min

istr

yo

fH

ealt

hin

Sau

di

Ara

bia

;an

dS

au

di

Ara

bia

nC

ult

ura

lB

ure

au

Off

ice

inB

on

n

�S

etti

ng

an

dp

erio

d:

Jed

dah

,S

au

di

Ara

bia

,p

erio

dn

ot

rep

ort

ed�

Po

pu

lati

on

:1

03

volu

nte

ers

wit

hve

rtic

al

per

iod

on

tal

bo

ne

loss

an

d1

59

ind

ivid

-u

als

wit

ho

ut

vert

ical

per

i-o

do

nta

lb

on

elo

ss

�T

ype:

wate

rpip

e,ci

gare

ttes

�M

easu

rem

ent

too

l:st

an

dard

ized

qu

esti

on

-n

air

ead

min

iste

red

inin

terv

iew

s,st

an

dard

iza-

tio

nn

ot

rep

ort

ed;

cal-

cula

ted

as

run

-yea

rs(p

rod

uct

of

wate

rpip

eru

ns

per

day

wit

hye

ars

of

smo

kin

g;

aru

nis

the

com

ple

tio

no

fth

ew

ate

rpip

esm

ok

ing

un

til

the

tob

acc

ois

bu

rnt)

;h

eavy

exp

osu

rew

as

def

ined

as5

40

run

-yea

rs

Per

iod

on

tal

dis

ease

mea

sure

das

vert

ical

per

iod

on

tal

bo

ne

loss

�M

easu

rem

ent

too

l:in

tra-o

ral

rad

io-

gra

ph

s;ve

rtic

al

per

i-o

do

nta

lb

on

elo

ssd

efin

edas

on

e-si

ded

bo

ne

reso

rpti

on

of

the

inte

rden

tal

mar-

gin

al

bo

ne5

2m

mth

at

had

aty

pic

al

an

gu

lati

on

tow

ard

sei

ther

the

mes

ial

or

dis

tal

asp

ect

of

the

roo

t�

Bli

nd

ing

of

ou

tco

me

ad

jud

icato

r:ye

s

�S

elec

tio

nb

ias:

26

2o

fth

e3

55

volu

nte

ers

par-

tici

pati

ng

inan

oth

erst

ud

y,5

1,5

2vo

lun

teer

edto

part

icip

ate

inth

isst

ud

y�

Info

rmati

on

bia

s:o

bje

ctiv

eo

utc

om

em

ea-

sure

men

t:ye

s,st

an

dar-

diz

edex

po

sure

mea

sure

men

t:n

o�

Co

nfo

un

din

g:

ad

just

-m

ent

for

age

on

ly�

Part

icip

ati

on

rate

:7

4%

OR

com

pare

dw

ith

no

smo

kin

g�

2.9

(95

%C

I1

.2–7

.0)

(wate

rpip

eo

nly

smo

kin

g)

�4

3.3

(95

%C

I1

2.1

–7

1.6

)(h

eavy

wate

r-p

ipe

smo

kin

g)

�0

.6(9

5%

CI

0.3

–1

.4)

(lig

ht

wate

rpip

esm

ok

ing)

�6

.6(9

5%

CI

2.6

–1

7.1

)(c

igare

tte

on

lysm

ok

ing)

�1

8.3

(95

%C

I6

.2–

53

.9),

P<

0.0

01

(hea

vyci

gare

tte

on

lysm

ok

ing) (c

on

tin

ued

)

THE EFFECTS OF WATERPIPE TOBACCO SMOKING ON HEALTH 847

by guest on October 14, 2011

ije.oxfordjournals.orgD

ownloaded from

Ta

ble

3C

on

tin

ued

Stu

dy

Po

pu

lati

on

Ex

po

sure

Ou

tco

me

sM

eth

od

olo

gic

al

fea

ture

sR

esu

lts

�E

xp

osu

rele

vels

of

incl

ud

edsu

bje

ct:

mea

nex

po

sure

of

56

.8ru

n-

years

for

wate

rpip

esm

ok

ers

�1

.3(9

5%

CI

0.5

–3

.4),

P<

0.0

01

(lig

ht

cigare

tte

on

lysm

ok

ing)

�D

iffe

ren

ces

bet

wee

nli

gh

tan

dh

eavy

exp

osu

res

wer

est

a-

tist

icall

ysi

gn

ific

an

t(P

<0

.00

1)

Al-

Bel

asy

38

�S

tud

yd

esig

n:

coh

ort

stu

dy

wit

h7

days

foll

ow

-up

aft

ersu

r-gic

al

rem

ova

lo

fm

an

dib

ula

rth

ird

mo

lars

�F

un

din

g:

no

tre

po

rted

�S

etti

ng

an

dp

erio

d:

Man

sou

raE

gyp

t,Ja

nu

ary

20

00

toF

ebru

ary

20

02

�E

xp

ose

d:

10

0m

ale

shis

ha

smo

ker

s,m

ean

age

28

.7ye

ars

(ran

ge

22

–3

9),

10

0m

ale

cigare

tte

smo

ker

s,m

ean

age

28

.7ye

ars

(ran

ge

20

–3

8)

�N

on

-ex

po

sed

:1

00

male

sn

on

-sm

ok

ers,

mea

nage

27

.7ye

ars

(ran

ge

20

–3

7)

�In

clu

ded

sub

ject

sw

ere

req

uir

edto

be

hea

lth

yn

ot

tak

ing

med

icati

on

sat

the

tim

eo

fth

est

ud

yan

dw

ith

un

ilate

ral

hig

hm

eso

an

gu

-la

rim

pact

ion

sw

ith

exp

ose

do

cclu

sal

surf

ace

s.P

ati

ents

wit

hre

cen

tan

ti-

bio

tic

use

or

the

med

ial

nee

dfo

ran

tib

ioti

cp

ro-

ph

ylax

isw

ere

excl

ud

ed

�T

ype:

shis

ha,

cigare

ttes

�M

easu

rem

ent

too

l:se

lf-

rep

ort

,st

an

dard

izati

on

no

tre

po

rted

�M

easu

rem

ent

tim

ep

oin

ts:

on

day

of

the

surg

ery,

on

the

firs

tan

dse

con

dp

ost

-op

erati

ved

ays

�E

xp

osu

rele

vels

of

incl

ud

edsu

bje

cts:

no

tre

po

rted

Dry

sock

et�

Mea

sure

men

tto

ol:

clin

ical

dia

gn

osi

so

nth

eb

asi

so

fco

nst

an

tra

dia

tin

gp

ain

no

tre

liev

edb

yth

ean

alg

esic

,acc

om

pa-

nie

db

ya

den

ud

edso

cket

or

nec

roti

ccl

ot

an

da

feti

dsm

ell

�B

lin

din

go

fo

utc

om

ead

jud

icato

r:n

ot

rep

ort

ed

�S

elec

tio

nb

ias:

on

lyh

ealt

hy

pati

ents

no

tta

kin

gm

edic

ati

on

sw

ere

incl

ud

ed,

no

n-

smo

ker

sse

lect

edfr

om

the

sam

eco

mm

un

ity

as

smo

ker

s�

Info

rmati

on

bia

s:ob

ject

ive

ou

tcom

em

ea-

sure

men

t:ye

s,st

an

dar-

diz

edex

po

sure

mea

sure

men

t:n

o;

sam

ed

ura

tio

nfo

llo

w-u

pfo

rb

oth

gro

up

s�

Con

fou

nd

ing:

no

matc

hin

gor

ad

just

men

tin

the

an

aly

sis

rep

ort

ed�

Part

icip

ati

on

rate

:n

ot

rep

ort

ed�

Att

riti

on

rate

:n

ot

rep

ort

ed

�‘S

his

ha

smo

ker

sh

ad

thre

eti

mes

the

risk

of

no

n-s

mo

ker

sfo

rd

evel

op

ing

dry

sock

et’

(RR¼

3.7

;P¼

0.0

01

);tr

end

of

dev

elo

pin

gd

ryso

cket

wit

hfr

e-q

uen

cyo

fsh

ish

asm

ok

ing

was

stati

s-ti

call

ysi

gn

ific

an

t(P¼

0.0

01

)�

Co

mp

are

dw

ith

no

n-

smo

ker

s,sh

ish

asm

ok

ers

wh

osm

ok

edth

ed

ay

of

surg

ery

or

the

firs

td

ay

aft

ersu

rger

yh

ad

asi

gn

ific

an

tly

incr

ease

din

cid

ence

of

dry

sock

et(d

ay

0,

P¼

0.0

01

;d

ay

1,

P¼

0.0

05

)

848 INTERNATIONAL JOURNAL OF EPIDEMIOLOGY

by guest on October 14, 2011

ije.oxfordjournals.orgD

ownloaded from

Ta

ble

4C

hara

cter

isti

cso

fin

clu

ded

stu

die

sass

essi

ng

the

effe

cto

fw

ate

rpip

eto

bacc

osm

ok

ing

on

hep

ati

tis

Cin

fect

ion

Stu

dy

Po

pu

lati

on

Ex

po

sure

Ou

tco

me

sM

eth

od

olo

gic

al

fea

ture

sR

esu

lts

Hab

ib2

2

�S

tud

yd

esig

n:

cro

ss-

sect

ion

al

stu

dy

�F

un

din

g:

Hep

ati

tis

CP

reve

nti

on

Pro

ject

(US

AID

gra

nt)

�S

etti

ng

an

dp

erio

d:

Agh

ou

rE

lS

ou

gh

ra,

aru

ral

vill

age

inN

ile

Del

ta,

in1

99

7�

Po

pu

lati

on

:m

ale

vill

age

inh

ab

itan

tssc

reen

edfo

rH

epati

tis

C.

Fo

ur-

hu

nd

red

an

dfi

fty-

five

test

edp

osi

tive

for

Hep

ati

tis

Can

d1

37

2te

sted

neg

ati

vefo

rH

epati

tis

C(s

tud

yals

ore

cru

ited

fem

ale

sb

ut

rest

rict

edgo

zaan

a-

lysi

sto

male

s)

�T

ype:

Gro

up

go

zasm

ok

ing

(ass

esse

din

men

on

ly)

�M

easu

rem

ent

too

l:q

ues

tio

nn

air

e,st

an

-d

ard

izati

on

no

tre

po

rted

�E

xp

osu

rele

vels

of

incl

ud

edsu

bje

cts:

no

tre

po

rted

Hep

ati

tis

Cin

fect

ion

�M

easu

rem

ent

too

l:se

con

dgen

erati

on

En

zym

eIm

mu

no

ass

ay

(Ab

bo

ttH

CV

EIA

2.0

)�

Bli

nd

ing

of

ou

tco

me

ad

jud

icato

r:n

ot

rep

ort

ed

�S

elec

tio

nb

ias:

sam

ple

was

‘sys

tem

ati

call

yse

lect

ed’

�In

form

ati

on

bia

s:o

bje

ctiv

eo

utc

om

em

ea-

sure

men

t:ye

s,st

an

dar-

diz

edex

po

sure

mea

sure

men

t:n

o�

Co

nfo

un

din

g:

ad

just

-m

ent

for

age,

sex

,m

ar-

ital

statu

s,ed

uca

tio

n,

his

tory

of

inva

sive

med

ical

pro

ced

ure

san

dd

enta

lp

roce

du

res

�P

art

icip

ati

on

rate

:h

alf

of

ho

use

ho

lds

sele

cted

�0

.15

%m

issi

ng

data

�T

wo

sub

ject

s(g

oza

smo

ker

s)ex

clu

ded

for

age

<2

0ye

ars

�It

isn

ot

clea

rh

ow

fem

ale

sub

ject

sw

ere

dea

ltw

ith

inth

ere

gre

ssio

nan

aly

ses

�O

Rfo

rgro

up

go

zasm

ok

ing

com

pare

dw

ith

no

n-g

rou

pgo

zasm

ok

ing¼

1.1

95

%C

I(0

.7–1

.5)

(male

s5

20

years

old

)

Med

hat4

4

�S

tud

yd

esig

n:

cro

ss-

sect

ion

al

stu

dy

�F

un

din

g:

Hep

ati

tis

CP

reve

nti

on

Pro

ject

[US

AID

gra

nt]

�S

etti

ng

an

dp

erio

d:

Co

mm

un

ity

inU

pp

erE

gyp

t,p

erio

dn

ot

rep

ort

ed.

�P

op

ula

tio

n:

male

vill

age

inh

ab

itan

tssc

reen

edfo

rH

epati

tis

C.

30

8te

sted

po

siti

vefo

rH

epati

tis

Can

d2

40

9te

sted

neg

ati

vefo

rH

epati

tis

C(s

tud

yals

ore

cru

ited

fem

ale

sb

ut

rest

rict

edgo

zaan

a-

lysi

sto

male

s)

�T

ype:

gro

up

go

zasm

ok

ing

(ass

esse

din

men

on

ly)

�M

easu

rem

ent

too

l:q

ues

tio

nn

air

e,st

an

-d

ard

izati

on

no

tre

po

rted

�E

xp

osu

rele

vels

of

incl

ud

edsu

bje

cts:

no

tre

po

rted

Hep

ati

tis

Cin

fect

ion

�M

easu

rem

ent

too

l:se

con

dgen

erati

on

En

zym

eIm

mu

no

ass

ay

(Ab

bo

ttH

CV

EIA

2.0

).O

fth

e5

23

part

icip

an

ts,

51

4w

ith

po

siti

vean

ti-

HC

Vte

stre

sult

sw

ere

test

edfo

rH

CV

RN

Ab

ya

on

e-st

epre

vers

etr

an

scri

pta

se-

po

lym

erase

chain

react

ion

met

ho

d�

Bli

nd

ing

of

ou

tco

me

ad

jud

icato

r:n

ot

rep

ort

ed

�S

elec

tio

nb

ias:

sam

ple

rep

rese

nts

62

.8%

of

vil-

lage

inh

ab

itan

ts�

Info

rmati

on

bia

s:o

bje

ctiv

eo

utc

om

em

ea-

sure

men

t:ye

s,st

an

dar-

diz

edex

po

sure

mea

sure

men

t:n

o�

Co

nfo

un

din

g:

ad

just

-m

ent

for

age,

inje

ctio

nh

isto

ry,

ho

spit

al

or

clin

ical

exp

erie

nce

s,d

enta

ltr

eatm

ents

,o

bst

etri

cex

po

sure

s(w

om

en5

20

years

),sh

ari

ng

razo

rsw

ith

infa

mil

y(m

ale

so

nly

),ci

rcu

mci

sio

n,

shavi

ng

at

com

mu

nit

yb

arb

er(m

eno

nly

),ea

rp

ierc

ing

�O

Rfo

rgro

up

go

zasm

ok

ing

com

pare

dw

ith

no

n-g

rou

pgo

zasm

ok

ing¼

0.9

(0.4

–2

.0)

(male

s4

30

years

old

)�

OR

for

gro

up

go

zasm

ok

ing

com

pare

dw

ith

no

n-g

rou

pgo

zasm

ok

ing¼

0.8

(0.5

–1

.2)

(male

s4

30

years

old

) (co

nti

nu

ed)

THE EFFECTS OF WATERPIPE TOBACCO SMOKING ON HEALTH 849

by guest on October 14, 2011

ije.oxfordjournals.orgD

ownloaded from

Ta

ble

4C

on

tin

ued

Stu

dy

Po

pu

lati

on

Ex

po

sure

Ou

tco

me

sM

eth

od

olo

gic

al

fea

ture

sR

esu

lts

(fem

ale

so

nly

),ta

tto

o,

cau

tery

�P

art

icip

ati

on

rate

:6

03

3(5

3.7

%)

of

the

11

22

7vi

llage

inh

ab

itan

tsw

ere

incl

ud

edin

the

stu

dy

�It

isn

ot

clea

rh

ow

fem

ale

sub

ject

sw

ere

dea

ltw

ith

inth

ere

gre

ssio

nan

aly

ses

El-

Sad

aw

y43

�S

tud

yd

esig

n:

cro

ss-

sect

ion

al

stu

dy

�F

un

din

g:

no

tre

po

rted

�S

etti

ng

an

dp

erio

d:

Urb

an

an

dru

ral

are

as

of

Sh

ark

iaG

ove

rno

rate

,E

gyp

t;p

erio

dn

ot

rep

ort

ed�

Po

pu

lati

on

:m

ale

vill

age

inh

ab

itan

tssc

reen

edfo

rh

epati

-ti

sC

.2

17

test

edp

osi

tive

for

Hep

ati

tis

Can

d5

65

test

edn

egati

vefo

rH

epati

tis

C(s

tud

yals

ore

cru

ited

fem

ale

sb

ut

rest

rict

edgo

zaan

a-

lysi

sto

male

s)

�T

ype:

Gro

up

go

zasm

ok

ing

(ass

esse

din

men

on

ly)

�M

easu

rem

ent

too

l:sp

ecif

icall

yd

esig

ned

qu

esti

on

nair

e;p

ilo

tte

sted

bef

ore

surv

eyfo

rre

liab

ilit

y�

Ex

po

sure

leve

lso

fin

clu

ded

sub

ject

s:n

ot

rep

ort

ed

Hep

ati

tis

Cin

fect

ion

�M

easu

rem

ent

too

l:an

tib

od

yto

HC

Vass

esse

db

yM

EIA

an

dH

CV

RN

Ate

sted

by

real-

tim

eP

CR

�B

lin

din

go

fo

utc

om

ead

jud

icato

r:n

ot

rep

ort

ed

�S

elec

tio

nb

ias:

use

d‘s

trati

fied

ran

do

msa

m-

pli

ng,

wh

ich

incl

ud

edsy

stem

ati

csa

mp

lin

g�

Info

rmati

on

bia

s:o

bje

ctiv

eo

utc

om

em

ea-

sure

men

t:ye

s;h

ow

ever

,w

hil

e2

5.8

%te

sted

po

siti

veb

yM

EIA

,7

.66

%te

stp

osi

tive

by

PC

R;

stan

dard

ized

exp

osu

rem

easu

rem

ent:

no

(pil

ot

test

edo

nly

)�

Co

nfo

un

din

g:

un

clea

rw

het

her

rep

ort

edre

sult

sw

ere

ad

just

edfo

rp

ote

nti

al

con

fou

nd

ers

�P

art

icip

ati

on

rate

no

tre

po

rted

�M

issi

ng

data

no

tre

po

rted

�O

Rfo

rgro

up

go

zasm

ok

ing

com

pare

dw

ith

no

n-g

rou

pgo

zasm

ok

ing¼

1.0

2(0

.64

–1

.62

)(m

ale

s)

ME

IA,

mic

ro-p

art

icle

enzy

me

imm

un

oass

ay;

PC

R,

po

lym

erase

chain

react

ion

.

850 INTERNATIONAL JOURNAL OF EPIDEMIOLOGY

by guest on October 14, 2011

ije.oxfordjournals.orgD

ownloaded from

not exclude important associations. Smoking water-pipe in groups was not significantly associated withhepatitis C infection. The overall quality of evidencevaried from very low to low.

To our knowledge, this is the first meta-analysis ofstudies assessing the association of waterpipe smok-ing with health outcomes. While Knishkowy et al.24

reviewed the health effects of waterpipe tobaccosmoking, they did not use systematic methods, for-mally evaluate the quality of the evidence or use sta-tistical methods to pool the results across studies. Themain strength of our study is the use of the CochraneCollaboration methodology for conducting systematicreviews, i.e. using a very sensitive and comprehensivesearch strategy, a duplicate and independent selectionprocess, a duplicate and independent data abstractionprocess, and a rigorous appraisal of the methodolog-ical quality of included studies. We also used theGRADE approach to rate the overall quality of evi-dence for each outcome.

For most of the outcomes of interest the evidencewas either lacking, indirect or of lower quality. Interms of indirectness, lung cancer studies were con-ducted mostly in China and India where tobacco istypically unprocessed and burned directly by charcoal.The practice of waterpipe smoking that is involved inthe recent global epidemic involves tobacco that isprocessed and flavoured and indirectly heated by thecharcoal. In terms of quality, the one methodologicalstudy limitation that affected our rating of the qualityof evidence for most outcomes was measurementbias, which has been reported in similar systematicreviews.48 In fact, only one study used a standardizedexposure measurement tool in spite of the fact thatthe practice of waterpipe smoking can vary widely.Variables include the quantity of tobacco used, thetype of tobacco used, the concomitant use of othersubstances, the frequency of smoking sessions, andthe length of sessions, the number of years of smok-ing. In addition, no study reported using a standard-ized measurement tool for other forms of tobacco

smoking in spite of the variety of these forms andthe need to account for passive smoking and pastsmoking history.

The other methodological study limitation thataffected our rating of the quality of evidence formany outcomes was the inappropriate handling ofconfounding, particularly for other forms of tobaccosmoking and for factors such as radon exposureamong miners as a risk factor for lung cancer.Furthermore, although many studies reported sepa-rate ORs for waterpipe and cigarette smoking, nonereported tests for interactions between these twoforms of smoking. This type of information isneeded given that a significant proportion of water-pipe smokers also smoke cigarettes.11,49

In spite of the many methodological study limita-tions for lung cancer and pregnancy outcomes, thefindings showed consistency (i.e. the low heterogene-ity) across studies. Similarly, the lack of associationbetween smoking waterpipe in groups and hepatitis Cinfection was characterized by the consistency acrossstudies and a relatively narrow CI. These findings areconsistent with current pathophysiological knowledgeof the spread of hepatitis C by blood-to-blood contact.While the lack of evidence for an association betweenwaterpipe smoking with bladder cancer, nasopharyn-geal cancer, oral dysplasia and infertility could reflecta true absence of association, it could also beexplained by lack of power to detect any existingassociation given their relatively wide CIs. Indeed,the lack of studies and of insufficient data on suchlong-term health effects is related to the short epide-miological time frame of the recent waterpipeepidemic.

The one study that reported on coronary heartdisease was excluded because of its publicationexclusively as an abstract.18 The quality of the evi-dence from that study was very low and the ORwas 2.2 (95% CI 0.9–5.4) for ever smokers and 0.7(95% CI 0.3–1.9) for current smokers compared withnever smokers.

Study or Subgroup

El-Sadawy 2004

Habib 2001

Medhat 2002 A

Medhat 2002 B

Total (95% CI)

Heterogeneity: Tau² = 0.00; Chi² = 1.57, df = 3 (P = 0.67); I ² = 0%

Test for overall effect: Z = 0.18 (P = 0.86)

log[OR]

0.019803

0.09531

–0.10536

–0.22314

SE

0.236032

0.158242

0.407402

0.20687

Weight

20.6%

45.8%

6.9%

26.8%

100.0%

IV, Random, 95% CI

1.02 (0.64, 1.62)

1.10 (0.81, 1.50)

0.90 (0.41, 2.00)

0.80 (0.53, 1.20)

0.98 (0.80, 1.21)

OR

IV, Random, 95% CI

0.01 0.1 1 10 100Protective effect

OR

Harmful effect

Figure 5 Association between waterpipe tobacco smoking and hepatitis C infection

THE EFFECTS OF WATERPIPE TOBACCO SMOKING ON HEALTH 851

by guest on October 14, 2011

ije.oxfordjournals.orgD

ownloaded from

Ta

ble

5C

hara

cter

isti

cso

fin

clu

ded

stu

die

sass

essi

ng

the

effe

cto

fw

ate

rpip

eto

bacc

osm

ok

ing

on

oth

ero

utc

om

es

Stu

dy

Po

pu

lati

on

Ex

po

sure

Ou

tco

me

sM

eth

od

olo

gic

al

fea

ture

sR

esu

lts

Tam

im4

5

�S

tud

yd

esig

n:

cro

ss-

sect

ion

al

stu

dy

�F

un

din

g:

no

tre

po

rted

�S

etti

ng

an

dp

erio

d:

stu

den

tsin

the

seco

nd

an

dth

ird

inte

rmed

iate

class

esfr

om

five

pri

-m

ary

sch

oo

lsin

Gre

ate

rB

eiru

tare

a,

inA

pri

l2

00

0�

Po

pu

lati

on

:6

25

stu

-d

ents

wit

hm

ean

age

13

years

(ran

ge

10

–1

5).

14

3st

ud

ents

(85

male

s)re

po

rted

resp

irato

rytr

act

sym

pto

ms,

48

2st

ud

ents

(23

7m

ale

s)re

po

rted

no

sym

pto

ms

�T

ype:

seco

nd

-han

dex

po

sure

toci

gar-

ette

s,n

arg

hil

e�

Mea

sure

men

tto

ol:

qu

esti

on

nair

e,st

an

-d

ard

izati

on

no

tre

po

rted

�E

xp

osu

rele

vels

of

incl

ud

edsu

bje

cts:

no

tre

po

rted

Res

pir

ato

ryil

lnes

sth

rou

gh

ou

tth

eye

ar

(no

tse

aso

nal)

incl

ud

ing

nasa

lco

n-

ges

tio

no

rw

hee

zin

g�

Mea

sure

men

tto

ol:

qu

esti

on

nair

eass

es-

sin

gcl

inic

al

con

di-

tio

nth

rou

gh

ou

tth

eye

ar

�B

lin

din

go

fo

utc

om

ead

jud

icato

r:n

ot

rep

ort

ed

�S

elec

tio

nb

ias:

sam

ple

rep

rese

nta

tive

of

po

pu

-la

tio

ns

of

the

five

pri

-m

ary

sch

oo

ls�

Info

rmati

on

bia

s:o

bje

ctiv

eo

utc

om

em

ea-

sure

men

t:n

o,

stan

dar-

diz

edex

po

sure

mea

sure

men

t:n

o�

Co

nfo

un

din

g:

no

matc

hin

go

rad

just

men

tin

the

an

aly

sis

rep

ort

ed�

Part

icip

ati

on

rate

:n

ot

rep

ort

ed

OR

com

pare

dw

ith

no

exp

osu

reat

ho

me

�2

.39

5%

CI

(1.1

–5

.1)

(narg

hil

eo

nly

exp

osu

re)

�2

.5(1

.6–3

.8)

(nar-

gh

ile

an

d/o

rci

gare

tte

exp

osu

re)

�3

.2(1

.9–5

.4)

(cig

ar-

ette

on

lyex

po

sure

)

Inh

ort

n4

6

�S

tud

yd

esig

n:

case

–co

ntr

ol

stu

dy

Fu

nd

ing:

Nati

on

al

Sci

ence

Fou

nd

ati

on

,th

eF

ulb

righ

tIn

stit

ute

for

Inte

rnati

on

al

Ed

uca

tio

n,

the

US

Dep

art

men

to

fE

du

cati

on

Fu

lbri

gh

t-H

ays

Do

cto

ral

Dis

sert

ati

on

Res

earc

hA

bro

ad

Pro

gra

man

dth

eS

oro

pti

mis

tsIn

tern

ati

on

al

Fo

un

der

Reg

ion

Fel

low

ship

Pro

gra

m

�S

etti

ng

an

dp

erio

d:

infe

rtil

ity

clin

ico

fth

eU

niv

ersi

tyo

fA

lex

an

dri

a’s

Sh

atb

yH

osp

ital,

the

pu

bli

co

bst

etri

cs/g

ynaec

olo

gy

teach

ing

ho

spit

al,

rura

lare

as

of

the

no

rth

wes

-te

rnN

ile

Del

tare

gio

n,

Egyp

t;O

cto

ber

19

88

toD

ecem

ber

19

89

�C

ase

s:h

usb

an

ds

of

40

fem

ale

pati

ents

of

the

un

iver

sity

infe

rtil

ity

clin

icw

ho

wer

ed

iag-

no

sed

of

male

-fact

or

infe

rtil

ity

(pro

ble

ms

of

sem

enan

dsp

erm

)�

Co

ntr

ols

:h

usb

an

ds

of

90

fert

ile

fem

ale

pati

ents

of

the

un

iver

-si

tyh

osp

ital

�P

art

icip

an

ts:

15

–4

5ye

ars

old

,lo

wer

an

dlo

wer

-mid

dle

soci

o-e

co-

no

mic

class

es

�T

ype:

hu

sban

ds’

wate

rpip

ean

dci

gar-

ette

smo

kin

gb

ehavi

ou

rs�

Mea

sure

men

tto

ol:

inte

rvie

ws,

self

-d

evel

op

edse

mi-

stru

ctu

red

qu

esti

on

-n

air

e,n

ost

an

dard

i-za

tio

nre

po

rted

;p

art

icip

an

tsca

tego

r-iz

edas

regu

lar

smo

-k

ers

an

dn

ever

smo

ker

s�

Ex

po

sure

leve

lso

fin

clu

ded

sub

ject

s:n

ot

rep

ort

ed

Co

up

lein

fert

ilit

yass

o-

ciate

dw

ith

male

-fa

ctor

infe

rtil

ity

�M

easu

rem

ent

too

l:m

edic

al

reco

rds

of

sem

enan

aly

ses

�B

lin

din

go

fo

utc

om

ead

jud

icato

r:n

ot

rep

ort

ed

�S

elec

tio

nb

ias:

pre

vale

nt

case

so

fin

fert

ilit

y,co

n-

tro

lsw

ere

ho

spit

al-

base

dan

dre

cru

ited

fro

mth

esa

me

stu

dy

base

as

case

s�

Info

rmati

on

bia

s:o

bje

ctiv

eo

utc

om

em

ea-

sure

men

t:ye

s,st

an

dar-

diz

edex

po

sure

mea

sure

men

t:n

o(s

eco

nd

-han

din

form

ati

on

)�

Co

nfo

un

din

g:

matc

hin

gfo

rage

gro

up

,so

cio

-ec

on

om

iccl

ass

;ad

just

-m

ent

for

cigare

tte

smo

kin

g,

tea

dri

nk

ing,

mari

tal

du

rati

on

,h

us-

ban

d’s

age,

hu

sban

d’s

edu

cati

on

�P

art

icip

ati

on

rate

:49

8%

OR

com

pare

dw

ith

nev

ersm

ok

ing:

2.5

(1.0

–6

.3)

(reg

ula

rw

ate

rpip

esm

ok

ing)

852 INTERNATIONAL JOURNAL OF EPIDEMIOLOGY

by guest on October 14, 2011

ije.oxfordjournals.orgD

ownloaded from

This study indicates the need for more research, asthe World Health Organization (WHO) has alreadyadvised.50 The overall quality of evidence for the dif-ferent outcomes was mostly low, limiting our confi-dence in the results. There is a need for high-qualitycohort studies to identify and quantify with confi-dence all the health effects of waterpipe smokingand to explore its interaction with other forms ofsmoking. The high quality of future studies willdepend on the use of standardized exposure measure-ment tools,49 another area of research need.

The study also has important implications for publichealth practice. Public health policy makers have todeal with suggestive but generally weak evidence ofthe association of waterpipe tobacco smoking withdeleterious health outcomes. One approach could beto prioritize public health resources to deal with otherpublic health crises (such as youth cigarette smoking)

for which the evidence is much stronger, while await-ing further evidence regarding waterpipe smoking.Another approach could be to devote the necessaryresources to control at a relatively early stage therapid growth of the waterpipe trend. Whatever thedecision policy makers make, it should be based onan objective consideration of the current available evi-dence in the proper public health context.

AcknowledgementsThe authors thank Ms Ann Grifasi for her adminis-trative assistance and Dr Ranime Saliba for her assis-tance. Those acknowledged have confirmed theiragreement.

Conflict of interest: None declared.

KEY MESSAGES

� Waterpipe tobacco smoking is possibly associated with a number of deleterious health outcomesincluding lung cancer, respiratory illness, low birth-weight and periodontal disease.

� There is a need for higher quality evidence to determine with confidence all the health effects ofwaterpipe tobacco smoking

References1 Chaouachi K. The medical consequences of narghile

(hookah, shisha) use in the world. Revue d Epidemiologieet de Sante Publique 2007;55:165–70.

2 American Lung Association. An Emerging Deadly Trend;Waterpipe Tobacco Use. American Lung Association:Washington, DC, 2007.

3 Sukumar A, Subramanian R. Elements in hair and nailsof residents from a village adjacent to New-Delhi—influ-ence of place of occupation and smoking-habits. BiologicalTrace Element Res 1992;34:99–105.

4 Maziak W, Ward KD, Soweid RAA, Eissenberg T. Tobaccosmoking using a waterpipe: a re-emerging strain in aglobal epidemic. Tobacco Control 2004;13:327–33.

5 Chaaya M, El Roueiheb Z, Chemaitelly H, Azar G, Nasr J,Al-Sahab B. Argileh smoking among universitystudents: a tobacco epidemic. Nicotine Tobacco Res 2004;6:457–63.

6 Al-Turki YA, Al-Turki YA. Smoking habits among medicalstudents in Central Saudi Arabia. Saudi Med J 2006;27:700–3.

7 Al-Haddad N, Hamadeh RR. Smoking among secondary-school boys in Bahrain: prevalence and risk factors. EastMediterr Health J 2003;9:78–86.

8 Kelishadi R, Ardalan G, Gheiratmand R et al.Smoking behavior and its influencing factors in a natio-nal-representative sample of Iranian adolescents:CASPIAN study. Preventive Med 2006;42:423–6.

9 El-Roueiheb Z, Tamim H, Kanj M, Jabbour S, Alayan I,Musharrafieh U. Cigarette and waterpipe smoking among

Lebanese adolescents, a cross-sectional study, 2003–2004.Nicotine Tobacco Res 2008;10:309–14.

10 Carroll T, Poder N, Perusco A. Is concern about waterpipetobacco smoking warranted? Aust N Z Publ Health 2008;32:181–2.

11 Jackson D, Aveyard P. Waterpipe smoking in students:prevalence, risk factors, symptoms of addiction, andsmoke intake. Evidence from one British university. BMCPublic Health 2008;8:174.

12 Roskin J, Aveyard P. Canadian and English students’beliefs about waterpipe smoking: a qualitative study.BMC Public Health 2009;9:10.

13 Eissenberg T, Ward KD, Smith-Simone S, Maziak W.Waterpipe tobacco smoking on a US collegecampus: Prevalence and correlates. J Adolesc Health 2008;42:526–9.

14 Weglicki LS, Templin TN, Rice VH, Jamil H, Hammad A.Comparison of cigarette and water-pipe smoking by Araband non-Arab-American youth. Am J Prev Med 2008;35:334–9.

15 Weglicki LS, Templin T, Hammad A et al. Tobacco usepatterns among high school students: do Arab Americanyouth differ? Ethn Dis 2007;17(2 Suppl 3):S3-22–S3-4.

16 Qiao YL, Taylor PR, Yao SX et al. Relation of radonexposure and tobacco use to lung cancer among tinminers in Yunnan Province, China. Am J Ind Med 1989;16:511–21.

17 Nasrollahzadeh D, Kamangar F, Aghcheli K et al. Opium,tobacco, and alcohol use in relation to oesophageal squa-mous cell carcinoma in a high-risk area of Iran. Br JCancer 2008;98:1857–63.

THE EFFECTS OF WATERPIPE TOBACCO SMOKING ON HEALTH 853

by guest on October 14, 2011

ije.oxfordjournals.orgD

ownloaded from

18 Jabbour S, El-Roueiheb Z, Sibai AM. Nargileh (Water-Pipe) smoking and incident coronary heart disease: acase-control study. Ann Epidemiol 2003;13:570.

19 Nuwayhid IA, Yamout B, Azar G et al. Narghile (hubble-bubble) smoking, low birth weight, and other pregnancyoutcomes. Am J Epidemiol 1998;148:375–83.

20 Shihadeh A, Saleh R. Polycyclic aromatic hydrocarbons,carbon monoxide, ‘‘tar’’, and nicotine in the mainstreamsmoke aerosol of the narghile water pipe. Food & ChemToxicol 2005;43:655–61.

21 Shihadeh A. Investigation of mainstream smoke aerosolof the argileh water pipe. Food Chem Toxicol 2003;41:143–52.

22 Habib M, Mohamed MK, Abdel-Aziz F et al. Hepatitis Cvirus infection in a community in the Nile Delta: riskfactors for seropositivity. Hepatology 2001;33:248–53.

23 Steentoft J, Wittendorf J, Andersen JR, Amitai Y.Tuberculosis and water pipes as source of infection.Ugeskr Laeger 2006;168:904–7.

24 Knishkowy B, Amitai Y, Knishkowy B, Amitai Y. Water-pipe (narghile) smoking: an emerging health risk beha-vior. Pediatrics 2005;116:e113–9.

25 Maziak W, Ward KD, Eissenberg T. Interventions forwaterpipe smoking cessation. Cochrane Database ofSystematic Rev 2007;4:CD005549.

26 Guyatt GH, Oxman AD, Vist GE et al. GRADE: an emer-ging consensus on rating quality of evidence and strengthof recommendations. BMJ 2008;336:924–6.

27 Higgins JPT, Thompson SG, Deeks JJ, Altman DG.Measuring inconsistency in meta-analysis. BMJ 2003;327:557–60.

28 Gupta D, Boffetta P, Gaborieau V et al. Risk factors oflung cancer in Chandigarh, India. Indian J Med Res2001;113:142–50.

29 Lubin JH, Qiao YL, Taylor PR et al. Quantitative evalua-tion of the radon and lung cancer association in a casecontrol study of Chinese tin miners. Cancer Res 1990;50:174–80.

30 Lubin JH, Li JY, Xuan XZ et al. Risk of lung cancer amongcigarette and pipe smokers in southern China. Int J Cancer1992;51:390–5.

31 Hsairi M, Achour N, Zouari B. Facteurs etiologiques ducancer bronchique primitif en Tunisie. La Tunisie Medicale1993;71:265–8.

32 Hazelton WD, Luebeck EG, Heidenreich WF,Moolgavkar SH. Analysis of a historical cohort ofChinese tin miners with arsenic, radon, cigarette smoke,and pipe smoke exposures using the biologically basedtwo-stage clonal expansion model. Radiat Res 2001;156:78–94.

33 Bedwani R, ElKhwsky F, Renganathan E et al.Epidemiology of bladder cancer in Alexandria, Egypt:Tobacco smoking. Int J Cancer 1997;73:64–7.

34 Feng BJ, Khyatti M, Ben-Ayoub W et al. Cannabis,tobacco and domestic fumes intake are associated withnasopharyngeal carcinoma in North Africa. Br J Cancer2009;101:1207–12.

35 Ali AA. Histopathologic changes in oral mucosa ofYemenis addicted to water-pipe and cigarette smoking

in addition to takhzeen al-qat. Oral Surg Oral Med OralPathol Oral Radiol Endod 2007;103:e55–9.

36 Tamim H, Yunis KA, Chemaitelly H et al. NationalCollaborative Perinatal Neonatal Network Beirut L.Effect of narghile and cigarette smoking on newbornbirthweight. BJOG 2008;115:91–7.

37 Aghamolaei T, Eftekhar H, Zare S. Risk factors associatedwith Intrauterine Growth Retardation (IUGR) in BandarAbbas. J Med Sci 2007;7:665–9.

38 Al-Belasy FA. The relationship of ‘‘shisha’’ (water pipe)smoking to postextraction dry socket. J Oral MaxillofacSurg 2004;62:10–4.

39 Natto S, Baljoon M, Bergstrom J. Tobacco smoking andperiodontal bone height in a Saudi Arabian population. JClin Periodontol 2005;32:1000–6.

40 Natto S, Baljoon M, Abanmy A et al. Tobacco smokingand gingival health in a Saudi Arabian population. OralHealth Prev 2004;2:351–7.

41 Natto S, Baljoon M, Bergstrom J. Tobacco smokingand periodontal health in a Saudi Arabian population.J Periodontol 2005;76:1919–26.

42 Baljoon M, Natto S, Abanmy A et al. Smoking and verticalbone defects in a Saudi Arabian population. Oral HealthPrev 2005;3:173–82.

43 El-Sadawy M, Ragab H, el-Toukhy H et al. Hepatitis Cvirus infection at Sharkia Governorate, Egypt: seropreva-lence and associated risk factors. J Egypt Soc Parasitol2004;34(Suppl 1):367–84.

44 Medhat A, Shehata M, Magder LS et al. Hepatitis C in acommunity in Upper Egypt: risk factors for infection. AmJ Trop Med Hyg 2002;66:633–8.

45 Tamim H, Musharrafieh U, El Roueiheb Z et al. Exposureof children to environmental tobacco smoke (ETS) and itsassociation with respiratory ailments. J Asthma 2003;40:571–6.

46 Inhorn MC, Buss KA. Ethnography, epidemiology andinfertility in Egypt. Soc Sci Med 1994;39:671–86.

47 Munckhof WJ, Konstantinos A, Wamsley M et al. A clus-ter of tuberculosis associated with use of a marijuanawater pipe. Int J Tuberc Lung Dis 2003;7:860–5.

48 Pirie K, Beral V, Peto R et al. Passive smoking and breastcancer in never smokers: prospective study and meta-analysis. Int J Epidemiol 2008;37:1069–79.

49 Maziak W, Ward KD, Afifi Soweid RA, Eissenberg T.Standardizing questionnaire items for the assessment ofwaterpipe tobacco use in epidemiological studies. PublicHealth 2005;119:400–4.

50 WHO Study Group on Tobacco Product Regualation(TobReg). Advisory Note. Waterpipe Tobacco Smoking:Health Effects, Research Needs and Recommended Actions byRegulators. WHO: Geneva, 2005.

51 Onder M, Oztas M, Arnavut O. Nargile (Hubble-Bubble)smoking-induced hand eczema. Int J Dermatol 2002;41:771–2.

52 Szyper-Kravitz M, Lang R, Manor Y, Lahav M. Early inva-sive pulmonary aspergillosis in a leukemia patient linkedto aspergillus contaminated marijuana smoking. LeukemiaLymphoma 2001;42:1433–7.

854 INTERNATIONAL JOURNAL OF EPIDEMIOLOGY

by guest on October 14, 2011

ije.oxfordjournals.orgD

ownloaded from

Appendix 1 Electronic search strategiesMEDLINE (1950 onward)

Waterpipe�.mp.‘‘water pipe�’’.mp.shisha�.mp.sheesha�.mp.hooka�.mp.huqqa�.mp.guza�.mp.goza�.mp.narghil�.mp.nargil�.mp.arghil�.mpargil�.mp(hubbl� adj3 bubbl�).mp.or/1–13

EMBASE (1988 onward)Waterpipe�.mp.‘‘water pipe�’’.mp.shisha�.mp.sheesha�.mp.

hooka�.mp.huqqa�.mp.guza�.mp.goza�.mp.narghil�.mp.nargil�.mp.arghil�.mpargil�.mp(hubbl� adj3 bubbl�).mp.or/1-13

ISI the Web of Science(waterpipe� OR ‘‘water pipe�’’ OR shisha� ORsheesha� OR hooka� OR huqqa� OR guza� OR goza�

OR narghil� OR nargil� OR argil� OR arghil� OR(hubbl� SAME bubbl�)) AND (smoking OR smokeOR health OR disease OR cancer� OR malignan� ORlung� OR pulmonary OR heart OR cardiac OR vascularOR stroke) (in Title or Topic)

Appendix 2 GRADE approach for rating the quality of evidence

Factors that lower the quality ofevidence

(1) Limitations of design� Selection bias� Measurement bias for risk factor (validity of

risk factor measurement instrument, blinding

of risk status data collector and blinding ofrisk status adjudicator)

� Measurement bias for outcome (validity ofoutcome measurement instrument, blinding ofoutcome data collector and blinding outcomeadjudicator)

� Inappropriate handling of confounding(stratification, adjustment)

Quality is first assignedbased on study design

Quality of evidence Quality is lowered ifa Quality is raised ifa

Randomized trials ! 4 ¼ High Limitations of design Large effect�1 Serious þ 1 Large�2 Very serious þ 2 Very large

3 ¼ Moderate Inconsistency Dose response�1 Serious þ 1 Evidence of a gradient�2 Very seriousIndirectness All plausible confounding

Observational study ! 2 ¼ Low �1 Serious þ 1 Would reduce a demonstrated effect, or�2 Very seriousImprecision þ 1 Would suggest a spurious effect

when results show no effect�1 Serious1 ¼ Very low �2 Very serious

Publication bias�1 Likely�2 Very likely

The quality of evidence reflects the extent of confidence that an estimate of effect is correct.a1, move up or down one grade (for example from high to intermediate); 2, move up or down two grades (for example from highto low).

THE EFFECTS OF WATERPIPE TOBACCO SMOKING ON HEALTH 855

by guest on October 14, 2011

ije.oxfordjournals.orgD

ownloaded from

� Attrition (for cohort studies)(2) Inconsistency

Inconsistency in the estimates of the associationacross studies (i.e. heterogeneity) suggests truedifferences in underlying cause–effect relation-ship that may arise from differences in:� populations (e.g. different association in

populations with differing other specific expo-sures or other genetic profiles);

� risk factor (e.g. larger association with higherexposure or different associations with varyingforms of the same exposure);

� outcomes (e.g. different associations with dif-ferent length of follow-up because of dimin-ishing or increasing association with time).

When heterogeneity exists, but investigators failto identify a plausible explanation, the quality ofevidence should be downgraded by one or twolevels, depending on the magnitude of the incon-sistency in the results.

(3) IndirectnessThe question being addressed by the authors of asystematic review is different from the availableevidence regarding:� population (e.g. general population vs popu-

lation of miners);� risk factor (e.g. cigarette use vs pipe use);� outcome (e.g. intra-uterine growth vs low

birth-weight)(4) Imprecision

Results are imprecise when studies include rela-tively few patients and few events and thus havewide CIs around the estimate of the effect. The95% CI (or alternative estimate of precision)

around the pooled or best estimate of associationincludes both negligible association and appreci-able benefit or appreciable harm.

(5) Publication biasPublication bias is a systematic underestimate oran overestimate of the underlying beneficial orharmful effect due to the selective publicationof studies (publication bias). That is, investiga-tors fail to report studies they have undertaken(typically those that show no effect).

Factors that increase the quality of evidence

(1) Large magnitude of effectWhen methodologically strong observational stu-dies yield large or very large and consistent esti-mates of the magnitude of association, we maybe confident about the results. The larger themagnitude of effect, the stronger becomes theevidence.

(2) Dose–response gradientA gradient dose–response may increase our con-fidence in the findings and thus enhance theassigned quality of evidence.

(3) Plausible confounding, which would reduce ademonstrated effectOn occasion, all plausible confounders or biasesfrom observational studies would result in anunderestimate of the association estimate. If,for instance, only sick patients have an exposure,yet they still fare better, it is likely that the expo-sure effect is even larger than the data suggest.

Appendix 3 Rating the quality of evidence for different associationusing the GRADE framework

Outcome Factors lowering the rating of quality Factors raising the rating ofquality

Finalrating

Lung cancerdiagnosis

Limitations of design: four of five studies didnot appropriately deal with confounding

Dose response: two studiesreported statistically signifi-cant dose–response relation-ships in terms of the totalamount of exposure andduration of exposure

Very low

Indirectness: most studies likely usedunprocessed tobacco burned directly bycharcoal

Lung cancermortality

Limitations of design: included study did notappropriately deal with confounding

None Very low

Indirectness: study likely used unprocessedtobacco burned directly by charcoal

Bladdercancerdiagnosis

Limitations of design: use of prevalent cases None Very lowImprecision

None Low

(continued)

856 INTERNATIONAL JOURNAL OF EPIDEMIOLOGY

by guest on October 14, 2011

ije.oxfordjournals.orgD

ownloaded from

Published by Oxford University Press on behalf of the International Epidemiological Association

� The Author 2010; all rights reserved. Advance Access publication 25 March 2010

International Journal of Epidemiology 2010;39:857–859

doi:10.1093/ije/dyq054

Commentary: The waterpipe—a globalepidemic or a passing fadWasim Maziak1,2*

1School of Public Health, University of Memphis, Memphis, TN, USA and 2Syrian Center for Tobacco Studies, Aleppo, Syria

*Corresponding author. Browning Hall 112, 3820 DeSoto Avenue, Memphis 38152-3340, TN, USA. E-mail: wmaziak@memphis.edu

Accepted 15 February 2010

Six years ago, we published in Tobacco Control the firstcomprehensive review about the waterpipe (also

known as shisha, hookah, arghile and narghile) inresponse to what seemed to be a burgeoning global

Oesophagealcancer

Dose response: the includedstudy reported statisticallysignificant dose response rela-tionship in terms of intensityof use

Imprecision

Nasopharyng-eal cancer

Limitations of design: investigators usedmatching and adjusted the analysis for anumber of confounding factors but not forother types of smoking

None Very low

ImprecisionOral dysplasia Limitations of design: not reporting dealing

with confounding factors; also the analysiswas stratified by chewing side (i.e. analy-sis of outcome occurring on the chewingside separate from the analysis of outcomeoccurring on the non-chewing side)

None Very low

ImprecisionPregnancy

outcomesNone None Low

Periodontaldisease

Limitations of design: included studies par-tially dealt with confounding factors (threeadjusted for age only and one adjusted forage and dental care habit)

Dose response: two studiesfound a statistically significantdose response relationship interms of total amount ofexposure

Low

Dry socket Limitations in design: study did not ade-quately deal with confounding factors

Dose response: statistically sig-nificant dose response rela-tionship in terms of totalamount of exposure

Low

Hepatitis Cinfection

Limitations in design: study reported discre-pancies between the results of MEIA andPCR

None Very low

Respiratoryillness

Limitations in design: study did not ade-quately deal with confounding factors

None Very low

Infertility NoneImprecision

None Very low

THE WATER PIPE 857

by guest on October 14, 2011

ije.oxfordjournals.orgD

ownloaded from