Top Banner
Review on the effects of exposure to spilled oils on human health Francisco Aguilera, a,b,c Josefina Méndez, b Eduardo Pásaro a and Blanca Laffon a * ABSTRACT: Harmful effects of oil spills on diverse flora and fauna species have been extensively studied. Nevertheless, only a few studies have been compiled in the literature dealing with the repercussions of oil exposure on human health; most of them have focused on acute effects and psychological symptoms. The objective of this work was to gather all these studies and to analyze the possible consequences of this kind of complex exposure in the different aspects of human health. Studies found on this topic were related to the disasters of the Exxon Valdez, Braer, Sea Empress, Nakhodka, Erika, Prestige and Tasman Spirit oil tankers. The majority of them were cross-sectional; many did not include control groups. Acute effects were evaluated taking into account vegetative-nervous symptoms, skin and mucous irritations, and also psychological effects. Genotoxic damage and endocrine alterations were assessed only in individuals exposed to oil from Prestige. The results of the reviewed articles clearly support the need for biomonitoring human populations exposed to spilled oils, especially those individuals involved in the cleanup, in order to evaluate not only the possible immediate consequences for their health but also the medium- and long-term effects, and the effectiveness of the protective devices used. Copyright © 2010 John Wiley & Sons, Ltd. Keywords: acute toxicity; endocrine toxicity; epidemiological studies; genotoxic effects; human health; oil spills; psychological effects INTRODUCTION AND BACKGROUND Since the industrial revolution took place in the eighteenth century, the use of fossil fuels, especially petroleum derivatives, has continually increased. It requires their transport from the plat- forms where they are extracted around the world, usually along sea routes in big tankers. The bad state of a considerable number of these, added to the fact that many are still monohull, has led to the high number of accidental spills that have occurred in recent decades. In the last five decades approximately 38 accidents involving supertankers have taken place, affecting the coasts of different countries (International Tankers Owners Pollution Federation Limited; http://www.itopf.com/information-services/data-and- statistics/statistics/index.html#noha/). The major oil spills have occurred in western and Mediterranean Europe, as well as in North Africa; these regions have experienced 13 of the 20 major spills. In this respect and considering the high population density of these geographical areas, they have major interest from the epidemiological point of view. The main ecosystem constituents affected by the spills are gen- erally seaside flora and some fauna such as birds and bivalve mollusks. Nevertheless, when a big spill occurs there is usually a large group of volunteers, in general local inhabitants, who mobi- lize and take part in the cleanup work to minimize the impact of the spill on the natural and economic resources and recover the coastal environment as soon as possible. These individuals con- stitute an exposed population whose health may be potentially affected by the noxious properties of the oil. Harmful effects of oil spills on diverse marine species, espe- cially birds and marine invertebrates, have been extensively studied. It is enough to type the name of any sunken oil tanker (e.g. Exxon Valdez, Nakhodka, Erika, Urquiola, Braer, Sea Empress, Prestige) into a bibliographic search engine (e.g. PubMed) and many studies on the impact of the spill on coastal ecosystems and the contamination and recovery are obtained. Nevertheless, there are only a few studies focused on the repercussions of oil exposure for human health. Most of them are related to acute effects and psychological symptoms. Table 1 displays a summary of the main characteristics of those oil spills for which epidemio- logical studies on the effects on human health have appeared in the literature. The objective of this manuscript is to review the studies on the effects of oil exposure on human health as a result of accidents involving supertankers. Studies were classified according to the type of effect analyzed into acute toxic and psychological effects or genotoxic and endocrine effects; also a section compiling some in vitro works and studies on the bioaccumulation and transference of oil compounds in the food chain is included. *Correspondence to: B. Laffon, Toxicology Unit, University of A Coruña, Edificio de Servicios Centrales de Investigación, Campus Elviña s/n, 15071-A Coruña, Spain. E-mail: blaff[email protected] a Unidad de Toxicología, Dpto. Psicobiología, Universidad de A Coruña, España b Dpto. Biología Celular y Molecular, Universidad de A Coruña, España c Carrera de Tecnología Médica, Facultad de Medicina, Universidad de Valparaíso, Chile Review Received: 11 January 2010, Revised: 25 February 2010, Accepted: 26 February 2010 Published online in Wiley InterScience: 14 April 2010 (www.interscience.wiley.com) DOI 10.1002/jat.1521 291 J. Appl. Toxicol. 2010; 30: 291–301 Copyright © 2010 John Wiley & Sons, Ltd.
11

Review on the effects of exposure to spilled oils on human health

Feb 09, 2023

Download

Documents

Welcome message from author
This document is posted to help you gain knowledge. Please leave a comment to let me know what you think about it! Share it to your friends and learn new things together.
Transcript
Page 1: Review on the effects of exposure to spilled oils on human health

Review on the effects of exposure to spilledoils on human healthFrancisco Aguilera,a,b,c Josefina Méndez,b Eduardo Pásaroa andBlanca Laffona*

ABSTRACT: Harmful effects of oil spills on diverse flora and fauna species have been extensively studied. Nevertheless, only afew studies have been compiled in the literature dealing with the repercussions of oil exposure on human health; most of themhave focused on acute effects and psychological symptoms. The objective of this work was to gather all these studies and toanalyze the possible consequences of this kind of complex exposure in the different aspects of human health. Studies found onthis topic were related to the disasters of the Exxon Valdez, Braer, Sea Empress, Nakhodka, Erika, Prestige and Tasman Spirit oiltankers. The majority of them were cross-sectional; many did not include control groups. Acute effects were evaluated takinginto account vegetative-nervous symptoms, skin and mucous irritations, and also psychological effects. Genotoxic damageand endocrine alterations were assessed only in individuals exposed to oil from Prestige. The results of the reviewed articlesclearly support the need for biomonitoring human populations exposed to spilled oils, especially those individuals involved inthe cleanup, in order to evaluate not only the possible immediate consequences for their health but also the medium- andlong-term effects, and the effectiveness of the protective devices used. Copyright © 2010 John Wiley & Sons, Ltd.

Keywords: acute toxicity; endocrine toxicity; epidemiological studies; genotoxic effects; human health; oil spills; psychologicaleffects

INTRODUCTION AND BACKGROUND

Since the industrial revolution took place in the eighteenthcentury, the use of fossil fuels, especially petroleum derivatives,has continually increased. It requires their transport from the plat-forms where they are extracted around the world, usually alongsea routes in big tankers. The bad state of a considerable numberof these, added to the fact that many are still monohull, has led tothe high number of accidental spills that have occurred in recentdecades.

In the last five decades approximately 38 accidents involvingsupertankers have taken place, affecting the coasts of differentcountries (International Tankers Owners Pollution FederationLimited; http://www.itopf.com/information-services/data-and-statistics/statistics/index.html#noha/). The major oil spills haveoccurred in western and Mediterranean Europe, as well as inNorth Africa; these regions have experienced 13 of the 20 majorspills. In this respect and considering the high population densityof these geographical areas, they have major interest from theepidemiological point of view.

The main ecosystem constituents affected by the spills are gen-erally seaside flora and some fauna such as birds and bivalvemollusks. Nevertheless, when a big spill occurs there is usually alarge group of volunteers, in general local inhabitants, who mobi-lize and take part in the cleanup work to minimize the impact ofthe spill on the natural and economic resources and recover thecoastal environment as soon as possible. These individuals con-stitute an exposed population whose health may be potentiallyaffected by the noxious properties of the oil.

Harmful effects of oil spills on diverse marine species, espe-cially birds and marine invertebrates, have been extensively

studied. It is enough to type the name of any sunken oil tanker(e.g. Exxon Valdez, Nakhodka, Erika, Urquiola, Braer, Sea Empress,Prestige) into a bibliographic search engine (e.g. PubMed) andmany studies on the impact of the spill on coastal ecosystemsand the contamination and recovery are obtained. Nevertheless,there are only a few studies focused on the repercussions of oilexposure for human health. Most of them are related to acuteeffects and psychological symptoms. Table 1 displays a summaryof the main characteristics of those oil spills for which epidemio-logical studies on the effects on human health have appeared inthe literature.

The objective of this manuscript is to review the studies on theeffects of oil exposure on human health as a result of accidentsinvolving supertankers. Studies were classified according to thetype of effect analyzed into acute toxic and psychological effectsor genotoxic and endocrine effects; also a section compilingsome in vitro works and studies on the bioaccumulationand transference of oil compounds in the food chain isincluded.

*Correspondence to: B. Laffon, Toxicology Unit, University of A Coruña, Edificio deServicios Centrales de Investigación, Campus Elviña s/n, 15071-A Coruña, Spain.E-mail: [email protected]

aUnidad de Toxicología, Dpto. Psicobiología, Universidad de A Coruña, España

bDpto. Biología Celular y Molecular, Universidad de A Coruña, España

cCarrera de Tecnología Médica, Facultad de Medicina, Universidad de Valparaíso,Chile

Review

Received: 11 January 2010, Revised: 25 February 2010, Accepted: 26 February 2010 Published online in Wiley InterScience: 14 April 2010

(www.interscience.wiley.com) DOI 10.1002/jat.1521

291

J. Appl. Toxicol. 2010; 30: 291–301 Copyright © 2010 John Wiley & Sons, Ltd.

Page 2: Review on the effects of exposure to spilled oils on human health

IN VITRO STUDIES AND STUDIES ON THEEFFECTS CAUSED BY TRANSFERENCE TO THEFOOD CHAIN

Table 2 displays a summary of the studies included in this section.All of them analyzed effects induced by oil spilled from Erika.Amat-Bronnert et al. (2007) performed an in vitro study in twohuman cell lines, one from hepatoma and another one frombronchial epithelium, treated with an Erika fuel extract. DNAadducts performed by 32P-postlabelling method were onlydetected in hepatoma cells, indicating biotransformation viacytochrome P450 (CYP) 1A2 and 1B1 since the two cell lines donot possess the same metabolic system (hepatoma cells exhibit awide spectrum of metabolic enzymes while bronchial cells donot). Moreover, western blot and densitometry quantificationshowed that exposure to the fuel extract induced some metabo-lizing enzymes such as CYP 1A2, cyclooxygenase 2 and5-lipooxygenase; the latter two are involved in carcinogenic pro-cesses. In epithelial bronchial cells induction of leucotriene B4,a mediator of inflammation, was revealed by inmmunoassay.These results acquire special importance with regard to humanhealth, since inhalation is one of the most representative ways ofabsorbing fuel compounds.

Lemiere et al. (2005) carried out a study to determine thepotential genotoxic risk for consumers of marine food contami-nated with polycyclic aromatic hydrocarbons (PAH) comingfrom oil spills. Mussels (Mytilus sp.) contaminated with Erika oilwere collected and provided daily to rats over periods of 2 and4 weeks. The DNA damage was measured by the single-cell gelelectrophoresis (comet) assay in hepatic, bone marrow andblood cells. While no evidence of genotoxicity was observed inthe peripheral blood samples, significant increases in DNAdamage were observed in the liver and the bone marrow of rats(P < 0.001). The intensity of the DNA damage increased with thePAH contamination level of the mussels. Therefore, this studydemonstrated that oil-contaminated food can cause genotoxicdamage in consumers. Also, it showed that mussels, oftenpresent in the human diet especially in coastal producerregions, carry pollutants in a bioavailable form when contami-nated with oil.

A similar study in rats fed with Erika oil-contaminatedmussels (Mytilus edulis) was performed by Chaty et al. (2008). Ratswere fed for 2 days and CYP 1A1 mRNA expression andethoxyresorufin-O-deethylase (EROD) catalytic activity were ana-lyzed by RT-PCR and a fluorimetric method, respectively. Resultsobtained showed the transient induction of CYP 1A1 mRNA andEROD activity, which reached a maximum after 12 h, returning tobasal levels within 36 h.

The studies presented in this section show evidence for thebioaccumulation of oil compounds and their transference tothe food chain in oil-contaminated marine food, and demonstratethe induction of DNA damage by the products generated bymetabolic enzyme activity transforming many polluting agentsinto even more toxic intermediaries. In this regard, Bro-Rasmussen(1996) indicated that toxic chemicals at low concentrations willnot immediately kill humans; however, depending on their poten-tial to bioconcentrate when climbing the food chain, persistentchemicals may create a human hazard in the case of chronicingestion. For this reason, in vitro and in vivo studies that considernot only bioaccumulation ability, but also the time that the pol-lutants stay in the organisms and the transference rate throughthe different links of the food chain, must be performed, and alsostudies on the optimal way to decontaminate oil-exposed organ-isms to make them safe for human consumption.

EPIDEMIOLOGICAL STUDIES ON ACUTETOXIC AND PSYCHOLOGICAL EFFECTS, ANDSTUDIES ON POTENTIAL TOXICOLOGICALRISK ASSESSMENT

A summary of the studies included in this section is shown inTable 3.

Exxon Valdez

The first oil spill for which studies on the effects on human healthare collected in the literature is the one from Exxon Valdez.Although a variety of studies exist on the ecological impact of thisspill, only a few consider the psychological, psychiatric and socialeffects.

Palinkas et al. (1992) assessed the levels of depressive symp-tomathology between two groups, one of indigenous people(N = 188) and another one of Euro-Americans (N = 371), all ofthem residents in 13 communities of Alaska (11 in the regiondirectly exposed to the oil spill itself and two control communi-ties). The results of these authors suggested that cultural differ-ences played an important role in the perception of thepsychological damage produced by this disaster, which wasrelated to the cleaning work in which the people were involvedand also the damage to fishing grounds, the main sustenance ofthese communities. The group of Euro-Americans showed acertain moderating effect of the damage in relation to familiarsupport; however, this factor did not significantly influence in theindigenous groups. These results emphasize the role of culturaldifferences in the perception of and capacity to overcome thepsychological impact.

Table 1. Oil spills for which epidemiological studies on the effects on human health were reported (ordered by spill size)

Ship name Date Location Spill size (t)

MV Braer 5 January 1993 Southwest Shetland islands, UK 85,000Sea Empress 15 February 1996 Milford Haven, UK 72,000Prestige 19 November 2002 Galicia, Spain 63,000Exxon Valdez 24 March 1989 Bligh ref, Prince William, Alaska, USA 37,000Tasman Spirit 26 July 2003 Karachi, Pakistan 37,000Erika 12 December 1999 South Penmarch, Brittany, France 20,000Nakhodka 2 January 1997 Northeast Oki Island, Sea of Japan, Japan >6,000

292

F. Aguilera et al.

J. App. Toxicol. 2010; 30: 291–301www.interscience.wiley.com/journal/jatwww.interscience.wiley.com/journal/jat Copyright © 2010 John Wiley & Sons, Ltd.

Page 3: Review on the effects of exposure to spilled oils on human health

Later, the same authors (Palinkas et al., 1993) as a result of thissame disaster examined the relationship between exposure andsubsequent cleanup efforts and the prevalence of generalizedanxiety disorder, post-traumatic stress disorder (PTSD) anddepressive symptoms in 13 communities of Alaska. They per-formed a community survey of 599 men and women approxi-mately 1 year after the spill. Prevalences of 20.2 and 9.4% werefound for the generalized anxiety disorder and PTSD, respec-tively. Also, the prevalence of depression scale scores above 16and 18 was 16.6 and 14.2%, respectively. For all the parametersanalyzed, exposed individuals showed scores several timeshigher than unexposed individuals Women were particularly vul-nerable to the effects of exposure to the oil spill and cleanupactivities on the prevalence of generalized anxiety disorder (b =0.22, P < 0.0001; odds ratio = 1.43, 95% CI 1.23–1.67), PTSD (b =0.19, P < 0.001; odds ratio = 1.40, 95% CI = 1.15–1.69) and CES-DScale scores of 18 and above (b = 0.17, P < 0.001; odds ratio = 1.35,95% CI = 1.13–1.60). The authors suggest, on the basis of theirresults, improving the mental health care of disaster victims, par-ticularly in primary care settings.

Gill and Picou (1998) monitored the impact of Exxon Valdez spillon the affected populations by means of a 4-year (1989–1992)longitudinal study in which they applied a survey on social dis-ruption and psychological stress, using random-sampling strate-gies, personal interviews and control communities. Dataobtained revealed the chronic nature of stress. Out-migrationexpectations and desires increased from 1989 to 1991. Socialdisruption was reported by a high proportion of residents in1989, but had declined to just over half in 1991. High levels ofevent-related psychological stress were found in 1989 and 1990but they diminished in the following two years.

Finally, Palinkas et al. (2004) confirmed the prevalence of PTSDassociated with ethnic differences. They reported high levels ofsocial disruption one year after this disaster, in both ethnicgroups (indigenous Alaskan and Euro-Americans). However, lowlevel family support, participation in spill cleanup activities and adecline in subsistence activities were significantly associatedwith PTSD in indigenous Alaskan, but not in Euro-Americans.

MV Braer

Campbell et al. (1993) performed a cross-sectional study in whicha population of individuals exposed to MV Braer oil spill (N = 420)was compared with a control group (N = 92), from Hillswick,95 km north of the incident. They compiled information ondemographic details, smoking and alcohol consumption, percep-tion of health, peak expiratory flow, hematology, liver and renalfunction tests, and blood and urine toxicology. Their resultsshowed that, during the first and second day after the spill, thepopulation reported mainly headaches, irritation of the throatand itchy eyes. The authors did not find significant differencesbetween both groups for any of the biological markers. Takingthese results together, only anecdotal reports of certain acutesymptoms could be confirmed.

Later, the same authors reported longer-term effects in thesame populations (344 exposed individuals and 77 controls;Campbell et al., 1994). Among exposed people, 7% perceivedtheir health to be poor compared with none of the controls (c2 =8.05, d.f. = 3, P < 0.05). Comparison of the symptoms of exposedpeople in the 2 weeks before with their presence immediatelyafter the incident showed more tiredness and fever, and fewerthroat, skin and eye irritations, and headaches (odds ratio = 1.86,

Tab

le2.

Invi

tro

stud

ies

and

stud

ies

onth

eeff

ects

caus

edby

tran

sfer

ence

toth

efo

odch

ain

(inor

der

ofth

ech

rono

logy

ofth

esp

ills)

Acc

iden

t–r

efer

ence

Stu

dy

char

acte

rist

ics

Met

ho

ds

Resu

lts

Erik

a–

Am

at-B

ron

ner

tet

al.(

2007

)In

vitr

og

eno

toxi

city

of

anEr

ika

fuel

extr

act

inh

um

anep

ith

elia

lbro

nch

ialc

ells

and

hu

man

hep

ato

ma

cells

DN

Aad

du

cts.

CY

P1A

1,1A

2,1B

1,2C

9,C

OX

1,C

OX

2an

d5-

LOX

pro

tein

exp

ress

ion

.LT

B4

and

PGE2

det

ecti

on

Ad

du

cts

form

atio

nan

din

du

ctio

no

fC

YP

1A2,

CO

X2

and

5-LO

Xin

hep

ato

ma

cells

.Fo

rmat

ion

of

LTB

4in

bro

nch

ialc

ells

Erik

a–

Lem

iere

etal

.(20

05)

Gen

oto

xici

tyas

soci

ated

wit

hEr

ika

oil-

con

tam

inat

edm

uss

els

con

sum

pti

on

inra

tsfe

dd

aily

for

2an

d4

wee

ks

Co

met

assa

yin

hep

atic

cells

,bo

ne

mar

row

and

blo

od

cells

Do

se–e

ffec

t–ti

me

rela

tio

nsh

ipin

hep

atic

and

bo

ne

mar

row

cells

.N

oef

fect

inb

loo

dce

llsEr

ika

–C

hat

yet

al.(

2008

)C

YP

1A1

ind

uct

ion

asso

ciat

edw

ith

Erik

ao

il-co

nta

min

ated

mu

ssel

sco

nsu

mp

tio

nin

rats

fed

for

2d

ays

CY

P1A

1m

RNA

exp

ress

ion

and

ERO

Dca

taly

tic

acti

vity

inliv

erC

YP

1A1

mRN

Aan

dER

OD

acti

vity

tran

sien

tin

du

ctio

n

COX

,cyc

loox

ygen

ase;

CYP

,cyt

ochr

ome

P450

;ERO

D,e

thox

yres

orufi

n-O

-de-

ethy

lase

;LO

X,l

ipoo

xyge

nase

;LT,

leuc

otrie

ne;P

G,p

rost

agla

ndin

e.

293

Effects of exposure to spilled oils on human health

J. App. Toxicol. 2010; 30: 291–301 www.interscience.wiley.com/journal/jatwww.interscience.wiley.com/journal/jatCopyright © 2010 John Wiley & Sons, Ltd.

Page 4: Review on the effects of exposure to spilled oils on human health

Tab

le3.

Epid

emio

logi

cals

tudi

eson

acut

eto

xic

and

psy

chol

ogic

aleff

ects

,and

stud

ies

onp

oten

tialt

oxic

olog

ical

risk

asse

ssm

ent

(ord

ered

byth

ech

rono

logy

ofth

esp

ills)

Acc

iden

t–

refe

ren

ceSt

ud

ych

arac

teri

stic

sM

eth

od

sRe

sult

s

Exxo

nVa

ldez

–Pa

linka

set

al.(

1992

)C

ross

-sec

tio

nal

.Et

hn

icd

iffer

ence

sin

stre

ss,c

op

ing,

and

dep

ress

ive

sym

pto

ms

inin

dig

eno

us

peo

ple

(N=

188)

and

Euro

-Am

eric

ans

(N=

371)

CES

-Dsc

ale

Leve

lof

exp

osu

resi

gn

ifica

ntl

yas

soci

ated

wit

hC

ES-D

sco

res

inb

oth

gro

up

s.In

dig

eno

us

peo

ple

had

sig

nifi

can

tly

hig

her

mea

nd

epre

ssiv

esy

mp

tom

sco

re.

InEu

ro-A

mer

ican

sp

erce

ived

fam

ilysu

pp

ort

was

am

od

erat

or

of

effe

cts

of

exp

osu

reo

nd

epre

ssiv

esy

mp

tom

s

Exxo

nVa

ldez

–Pa

linka

set

al.(

1993

)C

ross

-sec

tio

nal

,1ye

araf

ter

the

spill

.C

om

mu

nit

yp

atte

rns

of

psy

chia

tric

-dis

ord

ers

inex

po

sed

(N=

437)

and

con

tro

ls(N

=16

2)

CES

-Dsc

ale.

Qu

esti

on

sfr

om

the

Nat

ion

alIn

stit

ute

of

Men

talH

ealt

hD

iag

no

stic

Inte

rvie

wSc

hed

ule

The

exp

ose

dg

rou

psh

ow

edh

igh

erp

reva

len

ceo

fg

ener

aliz

edan

xiet

yd

iso

rder

and

CES

-Dsc

ore

s�

16an

d18

.W

om

enex

po

sed

wer

ep

arti

cula

rly

vuln

erab

le

Exxo

nVa

ldez

–G

illan

dPi

cou

(199

8)Lo

ng

itu

din

al(4

year

s).

Ch

ron

icco

mm

un

ity

stre

ssan

dso

cial

effe

cts

inre

sid

ents

:19

89(N

=11

8)19

91(N

=22

8)19

92(N

=15

2)an

dco

ntr

ols

:19

89(N

=73

)19

91(N

=10

2)19

92(N

=41

)

Qu

esti

on

nai

res

of

ou

t-m

igra

tio

nd

esir

es,

exp

ecta

tio

ns

and

soci

ald

isru

pti

on

.Ps

ych

olo

gic

alst

ress

by

Even

tsSc

ale

Dat

are

veal

edth

ech

ron

icn

atu

reo

fst

ress

.In

resi

den

tsin

crea

sein

ou

t-m

igra

tio

nex

pec

tati

on

san

dd

esir

es,a

nd

hig

hle

vels

of

even

t-re

late

dp

sych

olo

gic

alst

ress

,dim

inis

hin

gw

ith

tim

e,w

aso

bse

rved

Exxo

nVa

ldez

–Pa

linka

set

al.(

2004

)C

ross

-sec

tio

nal

,1ye

araf

ter

the

spill

.Et

hn

icd

iffer

ence

sin

sym

pto

ms

of

PTSD

inin

dig

eno

us

peo

ple

(N=

188)

and

Euro

-Am

eric

ans

(N=

371)

Mo

difi

edfo

rmo

fVer

sio

nIII

of

the

DIS

Hig

hle

vels

of

soci

ald

isru

pti

on

wer

eas

soci

ated

wit

hPT

SDin

bo

thet

hn

icg

rou

ps.

Low

fam

ilysu

pp

ort

,par

tici

pat

ion

incl

ean

up

acti

viti

es,a

nd

ad

eclin

ein

sub

sist

ence

acti

viti

esw

ere

sig

nifi

can

tly

asso

ciat

edw

ith

PTSD

on

lyin

ind

igen

ou

sp

eop

leM

VBr

aer

–C

amp

bel

let

al.(

1993

)C

ross

-sec

tio

nal

.In

itia

lacu

teef

fect

sin

resi

den

ts(N

=42

0)an

dco

ntr

ols

(N=

92)

Qu

esti

on

nai

res

of

acu

tesy

mp

tom

s,p

eak

exp

irat

ory

flow

,hem

ato

log

y,liv

eran

dre

nal

fun

ctio

nte

sts,

blo

od

and

uri

ne

toxi

colo

gy

Prin

cip

alh

ealt

hef

fect

sar

ose

on

day

s1

and

2(h

ead

ach

es,i

tch

yey

es,a

nd

thro

atir

rita

tio

n).

No

sig

nifi

can

td

iffer

ence

sb

etw

een

exp

ose

dan

dco

ntr

ols

wer

efo

un

dfo

ran

yo

fth

eb

iolo

gic

alm

arke

rs.

Toxi

colo

gic

alst

ud

ies

did

no

tsh

ow

any

exp

osu

reth

atar

ekn

ow

nto

affe

cth

um

anh

ealt

hM

VBr

aer

–C

amp

bel

let

al.(

1994

)C

ross

-sec

tio

nal

.Fo

llow

up

afte

r6

mo

nth

so

fac

ute

effe

cts

inre

sid

ents

(N=

344)

and

con

tro

ls(N

=77

)

Gen

eral

hea

lth

qu

esti

on

nai

re.

Peak

exp

irat

ory

flow

,uri

ne

anal

ysis

,h

emat

olo

gy,

and

liver

and

ren

alfu

nct

ion

test

s

The

mea

ng

ener

alh

ealt

hq

ues

tio

nn

aire

sco

reo

fex

po

sed

was

sig

nifi

can

tly

gre

ater

than

that

of

con

tro

ls.

Exp

ose

dh

adg

reat

erov

eral

lsco

res

for

som

atic

sym

pto

ms,

anxi

ety

and

inso

mn

ia,b

ut

no

tfo

rp

erso

nal

dys

fun

ctio

nan

dse

vere

dep

ress

ion

MV

Brae

r–

Cru

m(1

993)

Cro

ss-s

ecti

on

al.

Effe

cto

nre

spir

ato

rytr

act

inch

ildre

nliv

ing

clo

seto

Brae

rsh

ipw

reck

(N=

44at

3d

ays

and

56at

9–12

day

saf

ter

oil

spill

)

Peak

exp

irat

ory

flow

rate

Peak

exp

irat

ory

flow

rate

sw

ere

wit

hin

the

no

rmal

ran

ge

inb

oth

par

tso

fth

est

ud

y,an

dn

od

eter

iora

tio

nw

asse

enov

erth

est

ud

yp

erio

d

Sea

Empr

ess

–Ly

on

set

al.(

1999

)C

ross

-sec

tio

nal

.A

cute

hea

lth

and

psy

cho

log

ical

effe

cts

inex

po

sed

(N=

539)

and

con

tro

ls(N

=55

0)

Qu

esti

on

nai

res

of

acu

tesy

mp

tom

s.H

AD

and

SF-3

6sc

ore

sEx

po

sed

sho

wed

sig

nifi

can

tly

hig

her

anxi

ety

and

dep

ress

ion

sco

res,

wo

rse

men

talh

ealt

han

dse

lf-re

po

rted

hea

dac

he

and

sore

eyes

and

thro

at

Sea

Empr

ess

–G

alla

cher

etal

.(2

007)

Cro

ss-s

ecti

on

al.

Acu

tesy

mp

tom

ath

olo

gy

attr

ibu

tab

leto

psy

cho

log

ical

exp

osu

rein

exp

ose

d(N

=79

4)an

dco

ntr

ols

(N=

791)

Qu

esti

on

nai

res

of

acu

teto

xic

and

no

n-t

oxic

sym

pto

ms

and

Ho

spit

alA

nxi

ety

and

Dep

ress

ion

Scal

e

Perc

eive

dri

skw

asas

soci

ated

wit

hra

ised

anxi

ety

and

no

n-t

oxic

olo

gic

ally

rela

ted

sym

pto

mre

po

rtin

g.To

xic

sym

pto

mre

po

rtin

gw

asas

soci

ated

wit

ho

ilex

po

sure

and

wit

hra

ised

per

ceiv

edri

sk

Nak

hodk

a–

Mo

rita

etal

.(19

99)

Cro

ss-s

ecti

on

al.

Acu

teh

ealt

hp

rob

lem

sin

exp

ose

d(N

=28

2)Q

ues

tio

nn

aire

so

fac

ute

and

toxi

csy

mp

tom

s.Pe

rso

nal

air

sam

ple

rsto

asse

ssca

rcin

og

enic

ben

zen

e,to

luen

ean

dxy

len

e.U

rin

eto

xici

tyle

vels

Leve

lso

fh

ydro

carb

on

sin

air

wer

efa

rb

elo

wth

eo

ccu

pat

ion

alac

cep

tab

lelim

it.

The

pri

nci

pal

com

pla

ints

of

sym

pto

ms

wer

elo

wb

ack

pai

n,h

ead

ach

ean

dsy

mp

tom

so

fey

esan

dth

roat

Erik

a–

Schv

oer

eret

al.

(200

0)C

ross

-sec

tio

nal

.A

cute

hea

lth

effe

cts

inex

po

sed

(N=

3,66

9)Q

ues

tio

nn

aire

san

dte

lep

ho

ne

inte

rvie

ws

on

acu

tesy

mp

tom

sTh

em

ain

des

crib

edac

ute

sym

pto

ms

wer

elu

mb

arp

ain

,mig

rain

e,d

erm

atit

is,

ocu

lar

irri

tati

on

,res

pir

ato

ryp

rob

lem

san

dn

ause

as.

Du

rati

on

of

the

clea

nin

gw

ork

was

iden

tifie

das

risk

fact

or

294

F. Aguilera et al.

J. App. Toxicol. 2010; 30: 291–301www.interscience.wiley.com/journal/jatwww.interscience.wiley.com/journal/jat Copyright © 2010 John Wiley & Sons, Ltd.

Page 5: Review on the effects of exposure to spilled oils on human health

Tab

le3.

Con

tinue

d

Acc

iden

t–

refe

ren

ceSt

ud

ych

arac

teri

stic

sM

eth

od

sRe

sult

s

Erik

a–

Baa

rs(2

002)

Pote

nti

alto

xico

log

ical

risk

asse

ssm

ent

for

peo

ple

invo

lved

incl

ean

ing

acti

viti

esan

dfo

rto

uri

sts

Ris

kch

arac

teri

zati

on

so

nth

eb

asis

of

sup

po

siti

on

so

fth

ep

ote

nti

alex

po

sure

du

rin

gcl

ean

ing

and

tou

rist

acti

viti

es

The

risk

for

the

gen

eral

peo

ple

was

limit

ed.

Incr

ease

dri

skfo

rd

evel

op

ing

skin

irri

tati

on

and

der

mat

itis

,an

dve

rylim

ited

risk

for

dev

elo

pin

gsk

intu

mo

rs,w

ere

des

crib

edfo

rp

eop

lew

ho

had

bee

nin

bar

e-h

and

edco

nta

ctw

ith

the

oil

Erik

a–

Do

ret

al.

(200

3)Po

ten

tial

toxi

colo

gic

alri

skas

sess

men

taf

ter

dec

on

tam

inat

ion

of

36b

each

esp

ollu

ted

by

the

Erik

ao

ilsp

illan

dse

ven

con

tro

lbea

ches

Det

erm

inat

ion

of

the

16PA

Hse

lect

edb

yth

eU

SEP

Ain

san

d,w

ater

and

surf

ace

of

rock

s.Se

ven

scen

ario

so

fex

po

sure

for

peo

ple

usi

ng

the

bea

ches

wer

eco

nte

mp

late

d,an

dth

em

ost

con

serv

ativ

eav

aila

ble

toxi

colo

gic

alva

lues

wer

ese

lect

edfo

rco

mp

uti

ng

risk

s

The

san

dan

dw

ater

wer

esl

igh

tly

po

llute

d,w

ith

valu

essi

mila

rto

tho

sefo

un

din

the

con

tro

lbea

ches

.Th

ero

cky

area

sw

ere

still

hig

hly

po

llute

d.

No

leth

alri

skw

asfo

un

dfo

ra

you

ng

child

wh

oh

adac

cid

enta

llyin

ges

ted

asm

allb

allo

ffu

el.

The

life-

lon

gex

cess

risk

sfo

rsk

inca

nce

ran

dfo

ral

loth

erca

nce

rsw

ere

abo

ut

10-5

insc

enar

ios

incl

ud

ing

con

tact

wit

hth

ep

ollu

ted

rock

s.Th

eh

azar

dq

uo

tien

tfo

rte

rato

gen

icef

fect

sw

asve

rysm

all,

exce

pt

insc

enar

ios

wh

ere

pre

gn

ant

wo

men

wo

uld

wal

kam

on

gro

cks

con

tain

ing

hig

hp

ollu

tio

nle

vels

Pres

tige

–Su

arez

etal

.(2

005)

Cro

ss-s

ecti

on

al.

Acu

teh

ealt

hp

rob

lem

sam

on

gsu

bje

cts

invo

lved

inth

ecl

ean

up

op

erat

ion

afte

rth

esp

ill(N

=80

0)

Qu

esti

on

nai

reo

nex

po

sure

con

dit

ion

s,ac

ute

hea

lth

pro

ble

ms,

and

use

of

pro

tect

ive

mat

eria

l

Bir

dcl

ean

ers

acco

un

ted

for

the

hig

hes

tp

reva

len

ceo

fin

juri

es.

Wo

rkin

gm

ore

than

20d

ays

inh

igh

lyp

ollu

ted

area

sw

asas

soci

ated

wit

hin

crea

sed

risk

of

inju

ryin

allw

ork

ers.

Toxi

cef

fect

sw

ere

hig

her

amo

ng

seam

en.

No

seve

red

iso

rder

sw

ere

iden

tifie

dPr

esti

ge–

Car

rasc

oet

al.(

2006

)C

ross

-sec

tio

nal

.A

sso

ciat

ion

bet

wee

nh

ealt

hin

form

atio

n,u

seo

fp

rote

ctiv

ed

evic

esan

do

ccu

rren

ceo

fac

ute

hea

lth

pro

ble

ms

inex

po

sed

(N=

799)

Qu

esti

on

nai

reo

nex

po

sure

con

dit

ion

s,ac

ute

hea

lth

pro

ble

ms,

use

of

pro

tect

ive

mat

eria

lan

dh

ealt

h-p

rote

ctio

nin

form

atio

nre

ceiv

ed

Hea

lth

-pro

tect

ion

bri

efin

gw

asas

soci

ated

wit

hu

seo

fp

rote

ctiv

ed

evic

esan

dcl

oth

ing.

Un

info

rmed

sub

ject

sre

gis

tere

da

sig

nifi

can

tex

cess

risk

of

itch

yey

es,n

ause

a/vo

mit

ing

/diz

zin

ess,

hea

dac

hes

and

thro

atan

dre

spir

ato

ryp

rob

lem

s.Se

amen

,th

em

ost

exp

ose

dg

rou

p,w

ere

the

wo

rst

info

rmed

and

reg

iste

red

the

hig

hes

tfr

equ

ency

of

toxi

colo

gic

alp

rob

lem

sPr

esti

ge–

Zock

etal

.(2

007)

Lon

git

ud

inal

12-2

4m

on

ths

afte

rth

esp

ill.

Ass

oci

atio

nb

etw

een

par

tici

pat

ion

incl

ean

up

wo

rkan

dre

spir

ato

rysy

mp

tom

sin

exp

ose

d(N

=67

80)

Qu

esti

on

nai

res

wit

hq

ual

itat

ive

and

qu

anti

tati

vein

form

atio

no

ncl

ean

up

acti

viti

esan

dre

spir

ato

rysy

mp

tom

s

The

risk

of

LRTS

incr

ease

dw

ith

the

nu

mb

ero

fex

po

sed

day

s,ex

po

sed

ho

urs

per

day

,an

dn

um

ber

of

acti

viti

es.

The

exce

ssri

sko

fLR

TSd

ecre

ased

wh

enm

ore

tim

eh

adel

apse

dsi

nce

last

exp

osu

rePr

esti

ge–

Car

rasc

oet

al.(

2007

)C

ross

-sec

tio

nal

.H

ealt

h-r

elat

edq

ual

ity

of

life

and

men

talh

ealt

hin

resi

den

tsaf

ter

16m

on

ths

(N=

1350

)an

dco

ntr

ols

(N=

1350

)

Qu

esti

on

nai

res

of

per

ceiv

edso

cial

sup

po

rtan

dm

enta

lhea

lth

SF-3

6,G

HQ

-28,

HA

DS

and

GA

DS

The

SF-3

6sh

ow

edco

asta

lres

iden

tsas

hav

ing

alo

wer

likel

iho

od

of

reg

iste

rin

gsu

bo

pti

mal

valu

esin

ph

ysic

alfu

nct

ion

ing

and

bo

dily

pai

n,a

nd

ah

igh

erfr

equ

ency

of

sub

op

tim

alsc

ore

sin

men

talh

ealt

h

Pres

tige

–Sa

bu

ced

oet

al.(

2009

)C

ross

-sec

tio

nal

.Ps

ych

olo

gic

alim

pac

tin

sub

ject

sfr

om

23co

asta

llo

cati

on

sfr

om

thre

ezo

nes

acco

rdin

gto

thei

rp

roxi

mit

yto

the

loca

tio

no

fth

esp

ill(N

=93

8).

Qu

esti

on

nai

res

on

per

ceiv

edin

volv

emen

tan

dso

cial

sup

po

rt,s

atis

fact

ion

wit

hth

efin

anci

alai

dre

ceiv

edan

dso

cial

rela

tio

nsh

ips.

Mo

difi

edve

rsio

no

fth

eC

RI-A

DU

LT.

Sim

plifi

edve

rsio

no

fth

eSC

L-36

Aff

ecte

dsu

bje

cts

rece

ived

ag

oo

dd

ealo

fso

cial

sup

po

rtan

dw

ere

sati

sfied

wit

hth

eec

on

om

icai

dre

ceiv

ed.

Tho

seaf

fect

edw

ith

hig

hsu

pp

ort

and

sati

sfac

tio

nsc

ore

sw

ere

ina

bet

ter

situ

atio

nth

anth

ose

wit

hlo

wsc

ore

s,an

dev

enb

ette

rth

anth

ose

no

taf

fect

ed

Tasm

anSp

irit

–Ja

nju

aet

al.(

2006

)C

ross

-sec

tio

nal

.A

cute

hea

lth

effe

cts

inex

po

sed

resi

den

ts(N

=21

6)an

dco

ntr

ols

livin

g2

km(N

=83

)an

d20

km(N

=10

1)fa

rfr

om

the

coas

tlin

e

Qu

esti

on

nai

res

on

acu

teh

ealt

hsy

mp

tom

san

do

np

erce

pti

on

abo

ut

the

role

of

oil

spill

inp

rod

uci

ng

illh

ealt

h,a

nd

anxi

ou

snes

sab

ou

tth

eef

fect

of

oil

spill

on

hea

lth

Dat

ash

ow

edm

od

erat

e-to

-str

on

gas

soci

atio

ns

bet

wee

nth

eex

po

sed

gro

up

and

the

sym

pto

ms.

Ther

ew

asa

tren

do

fd

ecre

asin

gsy

mp

tom

-sp

ecifi

cp

reva

len

ceo

dd

sra

tio

sw

ith

incr

ease

ind

ista

nce

fro

mth

esp

illsi

teTa

sman

Spir

it–

Kh

urs

hid

etal

.(2

008)

Cro

ssse

ctio

nal

.H

ealt

hp

aram

eter

so

fp

eop

lew

ork

ing

/liv

ing

inth

evi

cin

ity

of

ano

il-p

ollu

ted

bea

ch(N

=10

0)

Hyd

roca

rbo

n/o

rgan

icco

nte

nt

inse

awat

eran

dsa

nd

sam

ple

s.H

emat

olo

gic

alan

db

ioch

emic

alp

aram

eter

s.Li

ver

and

ren

alfu

nct

ion

test

s

Seaw

ater

had

no

trac

eso

fh

ydro

carb

on

con

ten

t.Ly

mp

ho

cyte

and

eosi

no

ph

ille

vels

wer

esl

igh

tly

incr

ease

d.

Ab

ou

t11

peo

ple

had

rais

edSG

PT,b

ut

this

was

no

tsi

gn

ifica

nt

Tasm

anSp

irit

–M

eoet

al.(

2008

)C

ross

sect

ion

al.

Lun

gfu

nct

ion

inex

po

sed

(N=

20)a

nd

con

tro

ls(N

=31

)

Spir

om

etry

Sig

nifi

can

tre

du

ctio

nin

FVC

,FEV

1,FE

F 25–

75%

and

MV

Vin

exp

ose

d.

Lun

gfu

nct

ion

par

amet

ers

wer

eim

pro

ved

wh

enth

esu

bje

cts

wer

ew

ith

dra

wn

fro

mp

ollu

ted

air

envi

ron

men

t

CES

-D,C

ente

rfo

rEp

idem

iolo

gic

Stud

ies

–D

epre

ssio

n;C

RI-A

DU

LT,c

opin

gre

spon

sein

vent

ory;

DIS

,dia

gnos

ticin

terv

iew

sche

dule

;FEF

25–7

5%,f

orce

dex

pira

tory

flow

;FEV

1,fo

rced

exp

irato

ryvo

lum

ein

first

seco

nd;F

VC,f

orce

dvi

tal

cap

acit

y;G

AD

S,G

oldb

erg

anxi

ety

and

dep

ress

ion

scal

e;G

HQ

,gen

eral

heal

thqu

estio

nnai

re;H

AD

S,ho

spita

lan

xiet

yde

pre

ssio

nsc

ale;

LRTS

,low

resp

irato

rytr

act

sym

pto

mat

holo

gy;M

VV,

max

imum

volu

ntar

yve

ntila

tion;

PAH

,p

olyc

yclic

arom

atic

hydr

ocar

bon

s;PT

SD,p

ost-

trau

mat

icst

ress

diso

rder

;SG

PT,s

erum

glut

amic

pyru

vic

tran

sam

inas

e.

295

Effects of exposure to spilled oils on human health

J. App. Toxicol. 2010; 30: 291–301 www.interscience.wiley.com/journal/jatwww.interscience.wiley.com/journal/jatCopyright © 2010 John Wiley & Sons, Ltd.

Page 6: Review on the effects of exposure to spilled oils on human health

95% CI 1.19–2.92). The mean general health questionnaire scoreof the exposed subjects was significantly greater than that of thecontrols. The high rate of non-responders among individualsselected to participate in this study was reported (59 of the 215non-responders in the first phase of the study and 16 of the 86non-responders in the second phase were surveyed). The mainreasons for non-responding was not feeling that their health hadbeen affected, not interested in the study or did not think thestudy was useful (Foster et al., 1995).

Crum (1993) performed a cross-sectional study evaluating thepeak expiratory flow rate in two groups of children aged 5–12years who were resident within 5 km of the Braer shipwreck. Thefirst measure was carried out three days after the accident in 44children, and a second one in 56 children between 9 and 12 daysafter the oil spill. The main results showed that the children’speak expiratory flow rates were within the normal range in bothparts of the study, and no deterioration was seen over the studyperiod, even in the children known to have asthma. No significantdifference was observed between the two sets of values (P =0.502, Student’s t test for paired samples).

Sea Empress

In the wake of the Sea Empress oil spill, Lyons et al. (1999) inves-tigated the acute health effects (self-reported physical and psy-chological symptoms) in the residents of the vicinities of theaffected area (Milford Haven, southwest Wales). They designed aretrospective cohort study that included 539 exposed and 550controls. Results obtained, after adjustment by age, sex andsmoking status, allowed the conclusion that the people living inthe exposed areas presented high levels of anxiety and depres-sion scores, worse mental health and self-reported headache(odds ratio = 2.35, 95% CI 1.56–3.55), sore eyes (odds ratio = 1.96,95% CI 1.06–3.62) and sore throat (odds ratio = 1.70, 95% CI1.12–2.60). These last three symptoms were expected from theknown toxicological effects of oil, so the authors suggested adirect health effect in the exposed population.

On the basis that exposure to a complex emergency has asubstantial psychological component, Gallacher et al. (2007) per-formed work in 794 exposed individuals and 791 controls inwhich anxiety, depression and symptom reporting were used asmeasures of the health impact. The main results indicated thatperceived risk was associated with raised anxiety and non-toxicologically related symptom reporting (odds ratio = 2.28, 95%CI 1.57–3.31, P < 0.001), whereas physical exposure to oil wasonly associated with toxicologically related symptom reporting.The authors concluded that psychological exposure was a sub-stantially more sensitive measure of health impact than physicalexposure in relation to psychological outcomes.

Nakhodka

Morita et al. (1999), as a result of the Nakhodka oil spill, conducteda study in 282 people (men and women) who joined in cleanupwork. Interviews on health status and determinations of severalhydrocarbon metabolites in urine were carried out. Their resultswere similar to those from Campbell et al. (1993), showing thatpeople suffered mainly from pains in the lumbar region and legs,headaches and irritation of eyes and throat. The multivariatelogistic regression model was applied to clarify the risk factors ofhaving at least one symptom with several relevant variables.Results showed that being of female gender, the number of

working days on cleanup activities, direct exposure to oil andhistory of hypertension and low back pain were significant riskfactors for the development of symptoms (P < 0.05). In the urineanalyses, only three individuals showed higher levels of hippuricacid (>1.0 g l-1) that had returned to normality four months later.In this study the use of personal air samplers by the cleanupworkers was remarkable. They allowed the determination of theconcentrations of carcinogenic benzene, toluene and xylene inthe environmental air, and their results showed that these levelswere lower than the occupational acceptable limits (10 ppm forbenzene, 100 ppm for toluene and 100 ppm for xylene). Thehighest concentration of suspended particles on any given daywas 0.088 mg m-3, also below the occupational acceptable limit(2 mg m-3).

Erika

Schvoerer et al. (2000) presented a cross-sectional investigationon human health risk assessment as a result of the Erika oil spill in3669 interviewed people, who included cleaning workers andvolunteers. Their results indicated that 7.5% of the individualsexperienced some type of wound and 53% some health problem(30% lumbar pain, 22% migraine, 16% dermatitis). They reportedin a smaller degree ocular irritation (9%), respiratory problems(7%) and nausea (6%). The duration of the cleaning work wasidentified as a risk factor.

Baars (2002) evaluated the health risk for people involved inthe cleaning activities after the Erika oil spill and also for tourists,with an emphasis on the carcinogenic properties of the oil, on thebasis of the known toxicological properties of the oil componentsand assumptions on the levels of exposure during the perfor-mance of different activities. In assessing toxic risks the actualexposure levels were compared with limit values taken from theliterature; in assessing carcinogenic risk the actual exposurelevels were compared with the 1:104 lifetime excess risk of devel-oping tumors. The outcome indicated that the risks for thegeneral population were limited. For people who had been inbare-handed contact with the oil there was increased risk ofdeveloping skin irritation and dermatitis, but these effects werein general reversible, and also that of developing skin tumors,which was very limited due to the short contact time with the oil.

Dor et al. (2003) reported an assessment of human health riskafter decontamination of beaches polluted by the Erika oil. Theydetermined the 16 PAH selected by the US EPA in samples ofsand, water and the surface of rocks from 36 cleaned-pollutedbeaches and seven control beaches, and contemplated sevenpossible scenarios of exposure for people using the beaches intourist activities (children, adults and pregnant women) orworking activities. The life-long excess risk for skin cancer andfor all other cancers was about 10-5 in scenarios including contactwith the polluted rocks. The authors concluded that exposurewas mainly associated with polluted water among children andwith contaminated rocks for adults, and that, despite uncertain-ties, decontaminated beaches did not entail any significanthealth risks and could be opened to the public.

Prestige

As a result of the disaster of the tanker Prestige, densely popu-lated coastal regions of Spain (Galicia, Asturias, Cantabria and theBasque country), as well as the neighboring French coasts, with

296

F. Aguilera et al.

J. App. Toxicol. 2010; 30: 291–301www.interscience.wiley.com/journal/jatwww.interscience.wiley.com/journal/jat Copyright © 2010 John Wiley & Sons, Ltd.

Page 7: Review on the effects of exposure to spilled oils on human health

intense activity of extraction of marine resources and tourism,were affected. Several studies were performed after this accidentin order to evaluate the possible human health effects.

Suarez et al. (2005) evaluated the conditions of exposure andthe acute health effects in individuals who participated in thecleanup works in the regions of Asturias and Cantabria (Spain),and the association between these and the type of work. Fourhundred individuals from each region were interviewed. Col-lected data included information on the work performed, use ofprotection devices and acute symptoms. Bird cleaners accountedfor the highest prevalence of lesions (19%, P < 0.001), includingneurovegetative disorders (11.2%, P = 0.169) and low back pain(3.1%, P = 0.281). Working periods longer than 20 days in highlypolluted areas were associated with increased risk of injury in allworkers. A specific analysis restricted to seamen only found astrong and significant association with having worked for morethan 3 days (odds ratio = 14.30 and 11.02 for categories of 3–20days and over 20 days, respectively) and having torn or not wornthe protective suit (odds ratio = 1.20 and 7.79, respectively), butno severe disorders were identified among individuals analyzed.

The same authors reported another study examining the asso-ciation between use of protective devices, frequency of acutehealth problems and health-protection information received by799 exposed individuals, classified according to the tasks per-formed (Carrasco et al., 2006). These authors observed a signifi-cant excess risk of itchy eyes (odds ratio = 2.89; 95% CI 1.21–6.90),nausea/vomiting/dizziness (odds ratio = 2.25; 95% CI 1.17–4.32)and throat and respiratory problems (odds ratio = 2.30; 95% CI1.15–4.61) among uninformed subjects. Furthermore, there wasa noteworthy significant excess risk of headaches (odds ratio =3.86; 95% CI 1.74–8.54) and respiratory problems (odds ratio =2.43; 95% CI 1.02–5.79) among uninformed paid workers.Seamen, the group most exposed to the spilled oil, were theworst informed and registered the highest frequency of toxico-logical problems. Therefore, the authors confirmed the resultsobtained in their previous study and found a significant associa-tion between proper health-protection briefing and use of pro-tective devices and lower frequency of health problems.

Zock et al. (2007) evaluated the prevalence of lower respiratorytract symptoms (LRTS) more than a year after Prestige accident in6780 fishermen who had participated in the cleanup labors(response rate 76%), through questionnaires that included quali-tative and quantitative information. Their results showed thatLRTS was more prevalent in cleanup workers (odds ratio = 1.73;95% CI 1.54–1.94), and that the risk of LRTS increased in relationto the number of exposed days, exposed hours per day andnumber of activities carried out (linear trend, P < 0.0001). Theexcess risk of LRTS decreased with elapsed time since last expo-sure (odds ratio = 2.33, 1.69 and 1.24 for less than 14 months,14–20 months, and more than 20 months, respectively), althoughit was still significant when more than 20 months had elapsed.

Carrasco et al. (2007) performed a new study on the effects ofthe Prestige oil spill on health-related quality of life (HRQoL) andmental health in the affected population, approximately 18months after this disaster, using several questionnaires. The mainresults showed coastal residents as having a lower likelihood ofregistering suboptimal HRQoL values in physical functioning(odds ratio = 0.69; 95% CI 0.54–0.89) and bodily pain (oddsratio = 0.74; 95% CI 0.62–0.91), and a higher frequency of subop-timal scores in mental health (odds ratio = 1.28; 95% CI 1.02–1.58). The authors concluded that, almost one and a half yearsafter the accident, worse HRQoL and mental health levels were

not in evidence among subjects exposed to the spilled oil. Nev-ertheless, a slight impact on the mental health of residents in theaffected areas was suggested by some of the scales applied.

Similar results were obtained by Sabucedo et al. (2009), whoevaluated the psychological impact of Prestige oil spill. Theycarried out a descriptive study that involved 938 men andwomen from 23 localities throughout the Galician coast. Half ofthem were fishermen or workers related to the extraction offishing resources, and the other half were not linked to theseactivities. Questionnaires on different psychological and psycho-social factors were filled in at the time of the accident and oneyear after. The results showed that the affected subjects hadreceived a good deal of social support and were satisfied with theeconomic aid received. In addition, affected individuals with highsupport and satisfaction scores were currently in a better situa-tion than those affected with low scores, and even better thanthose not affected.

Tasman Spirit

Janjua et al. (2006), following the Tasman Spirit shipwreck, con-ducted a study which included an exposed group composed ofadults of both genders living on the affected coastline (N = 216)and two control groups living 2 km (N = 83) and 20 km (N =101),respectively, away from the indicated area. Surveys on acutesymptoms related to eyes, respiratory tract, skin and nervoussystem, as well as consultations of allergies, tobacco consumptionand perceptions on the effect on their health and anxiety abouttheir health effects were performed. Their results showedmoderate-to-strong associations (prevalence odds ratios rangingfrom 2.3 to 37.0) between the exposed group and the symptoms,which decreased with the distance from the spill site, and multiplelinear regression model revealed strong relationship of exposurestatus with the symptoms score (b = 8.24, 95% CI 6.37–10.12).

Khurshid et al. (2008) presented a short-term study in peoplewho were working or living in the vicinity of Karachi beach.Hematological and biochemical parameters were determined,and liver and renal function tests were carried out. They also tookseawater and sand samples and analyzed them for hydrocarbon/organic contents. The results only showed slight rises in the levelsof lymphocytes and eosinophiles. The authors recommendedperforming follow-up studies after oil spills taking samples every3 months for 3–5 years, noting respiratory disorders and anychanges in the skin.

Finally, Meo et al. (2008) assessed, by means of spirometry,lung function and followed up the progression after one year in20 subjects exposed to this oil spill and 31 controls. Subjectsexposed to polluted air had significant reductions in lung func-tion compared with their matched controls (P ranging from 0.001to 0.02 for the different lung function parameters). The reportedimpairment was reversible and lung function parameters wereimproved when the subjects were withdrawn from the pollutedair environment.

In summary, studies performed after Exxon Valdez spill onlyaccounted for psychological effects in the exposed populations.For all the other accidents, there are also studies on acute toxiceffects, and moreover, for the Erika oil spill there are two works onpotential toxicological risk assessment, both concluding thatexposure to pollutants contained in the oil during commonactivities did not entail any significant health risk. Data obtainedin most of these studies indicated that technological disastersthat involve oil spills have acute physical consequences

297

Effects of exposure to spilled oils on human health

J. App. Toxicol. 2010; 30: 291–301 www.interscience.wiley.com/journal/jatwww.interscience.wiley.com/journal/jatCopyright © 2010 John Wiley & Sons, Ltd.

Page 8: Review on the effects of exposure to spilled oils on human health

that diminish with time and are mainly reversible, and psycho-logical consequences and continuing disruptive and stress-provoking consequences for resident communities. The resultsalso suggested that conflicting definitions of long-term effectsand recovery of the natural environment contributed to commu-nity stress.

EPIDEMIOLOGICAL STUDIES ONGENOTOXICITY AND ENDOCRINE TOXICITY

Table 4 displays a summary of the main characteristics of thesestudies.

Braer

Cole et al. (1997) evaluated the possible genotoxicity as a conse-quence of the Braer tanker oil spill. They used blood samples toassess the primary damage in the DNA (DNA adducts in themononuclear cell fraction by a modified 32P-postlabeling methodand mutations at the hprt locus in T lymphocytes). These authorsdid not obtain any evidence of genotoxicity for either end point,but they proposed several issues to be taken into account in thedesign of biomonitoring studies after oil spills.

Prestige

Laffon et al. (2006) conducted a study to determine the possiblegenotoxic damage associated with the exposure to Prestige oil, in34 volunteers, who worked in autopsies and cleaning of oil-contaminated birds, and 35 controls. Environmental concentra-tions of volatile organic compounds (VOC) in the working roomwere determined. Genotoxicity was evaluated by means ofmicronucleus (MN) test and comet assay, and the possible influ-ence of several DNA repair genetic polymorphisms was also ana-lyzed. Their results showed significantly higher DNA damage (P <0.01), but not cytogenetic damage, in relation to the exposuretime (r = 0.376, P < 0.05), and also certain exposure–genotypeinteractions.

Pérez-Cadahía and colleagues performed a study with theobjective of evaluating the genotoxicity and endocrine toxicityrelated to exposure to Prestige oil during the different cleaninglabors. Exposed individuals were classified into three groups:manual volunteers, hired manual workers and hired workersusing high-pressure water machines. The environmental expo-sure levels of VOC were determined, and different biologicalparameters were measured. Their results were published in dif-ferent papers. In an initial stage (Pérez-Cadahía et al., 2006, 2007),a relatively small population (68 total exposed vs 42 controls) wasanalyzed. The data obtained indicated that the highest levels ofVOC were observed in the volunteer environment and that expo-sure to Prestige oil induced genotoxic damage (tests applied:sister chromatid exchanges (SCE), MN test and comet assay), thecomet assay being the most sensitive test to detect it, and alter-ations in hormonal status (prolactin and cortisol plasma concen-trations, significant decreases with P < 0.01). Also, gender, ageand tobacco smoking influenced the levels of genetic damage,while the effect of using protective devices (clothes and mask)was less noticeable than expected.

Later, they enlarged the study with the aim of checking thevalidity of their previous data, including 180 exposed subjects

and 60 controls. Their results showed significant increases in thelevels of blood heavy metals (aluminum, nickel and lead) andDNA damage, and alterations in the endocrine status of theexposed populations (significantly higher prolactin plasma con-centrations, P < 0.01; Pérez-Cadahía et al., 2008a). They also foundgeneral increases in MN frequency and decreases in the prolifera-tion index in the individuals with longer times of exposure (Pérez-Cadahía et al., 2008b). Moreover, significant influence of severalgenetic polymorphisms in metabolizing enzymes and DNA repairproteins was observed. In addition, their previous resultsshowing the absence of effect of using protective devices wereconfirmed.

Finally, the same authors (Pérez-Cadahía et al., 2008c) investi-gated the relationship between blood levels of heavy metals andgenotoxic or endocrine parameters in the individuals exposed toPrestige oil. Cortisol plasma concentration appeared to be themost sensitive parameter to the effects of metal exposure, since itwas significantly influenced by blood concentrations of alumi-num, nickel (both inversely) and cadmium (positively), and jointlyby aluminum and nickel. On this basis, the authors suggestedplasma levels of cortisol as a potentially relevant biomarker toassess the effects of exposure to heavy metals.

Taking into account the known genotoxic, cancer-provokingand endocrine disrupting properties of many compounds con-tained in the spilled oils, it seems surprising that only for two oilspills (Braer and Prestige) are there studies contemplating theseconsequences for human health in exposed individuals. Theresults obtained in most of these studies provide evidence ofgenotoxicity and alterations in the hormonal status related to theexposure. The only work with negative results (Cole et al., 1997)comprised a relatively small population (26 exposed vs 9 con-trols), and nothing is specified on the participation of theexposed individuals in the cleanup tasks; only their status as resi-dents in the polluted area is mentioned. It seems probable thatdirect participation in the cleanup work involved a higher expo-sure to the oil toxic compounds than that experienced by zoneinhabitants who did not participate in the cleaning.

CONCLUSIONS

Until now there have been 38 large oil spills, but only for seven ofthem have studies on the repercussions of the exposure to spilledoils on human health been performed. Most of these investiga-tions correspond to cross-sectional epidemiological studies thatanalyze acute physical effects or psychological consequences inthe affected people. Some of them do not include a matchedcontrol population, which makes the information provided con-fusing and difficult to interpret. A smaller number of studies arein vitro or in vivo approaches aiming to investigate the effects atthe cellular level and the ability of the oil compounds to be trans-ferred into the food chain and induce damage in consumers;others are focused on biological markers indicative of genotoxi-city and/or endocrine toxicity.

On the occasion of the Prestige oil spill, Porta and Castaño-Vinyals (2003) recommended performing epidemiologicalstudies of exposure to the spilled oil on the medium- and long-term impact on human health. In addition to a first transversalstage, they recommend the monitoring of the exposed popula-tions in a second longitudinal stage. This would allow (i) deter-mination of whether the biomarkers of internal dose, ofbiologically effective dose and of early biological response

298

F. Aguilera et al.

J. App. Toxicol. 2010; 30: 291–301www.interscience.wiley.com/journal/jatwww.interscience.wiley.com/journal/jat Copyright © 2010 John Wiley & Sons, Ltd.

Page 9: Review on the effects of exposure to spilled oils on human health

Tab

le4.

Epid

emio

logi

cals

tudi

eson

geno

toxi

city

and

endo

crin

eto

xici

ty(o

rder

edby

the

chro

nolo

gyof

the

spill

s)

Acc

iden

t–

refe

ren

ceSt

ud

ych

arac

teri

stic

sM

eth

od

sR

esu

lts

Brae

r–

Co

leet

al.

(199

7)Lo

ng

itu

din

al.

Gen

oto

xici

tyin

resi

den

ts(N

=26

)an

dco

ntr

ols

(N=

9)at

3sa

mp

ling

tim

es(1

0d

ays,

10w

eeks

and

1ye

araf

ter

the

acci

den

t)

DN

Aad

du

cts

inth

em

on

on

ucl

ear

cell

frac

tio

nan

dfr

e-q

uen

cyo

fh

prt

mu

tati

on

sin

Tly

mp

ho

cyte

sN

oev

iden

ceo

fg

eno

toxi

city

was

ob

tain

edfo

rei

ther

end

po

int

Pres

tige

–La

ffo

net

al.

(200

6)C

ross

-sec

tio

nal

.G

eno

toxi

city

inin

div

idu

als

per

form

ing

auto

psi

esan

dcl

ean

ing

of

oil-

con

tam

inat

edb

ird

s(N

=34

)an

dco

n-

tro

ls(N

=35

)

Envi

ron

men

talV

OC

.C

om

etas

say

and

MN

test

.DN

Are

pai

rg

enet

icp

oly

mo

r-p

his

ms

(XRC

C1,

XRC

C3,

APE

1)

Sig

nifi

can

tin

crea

sein

the

com

etas

say,

bu

tn

ot

inth

eM

Nte

st,r

elat

edto

the

tim

eo

fex

po

sure

.Ex

po

sed

ind

ivid

ual

sca

rryi

ng

XRC

C1-

399G

lno

rA

PE1-

148G

lual

lele

ssh

ow

edin

crea

sed

DN

Ad

amag

ePr

esti

ge–

Pére

z-C

adah

íaet

al.(

2006

)C

ross

-sec

tio

nal

.G

eno

toxi

city

invo

lun

teer

san

dh

ired

wo

rker

sp

arti

ci-

pat

ing

inth

ecl

ean

up

(N=

68)a

nd

con

tro

ls(N

=42

)

Envi

ron

men

talV

OC

.C

om

etas

say,

SCE,

MN

test

Hig

hes

tV

OC

leve

lsin

the

volu

nte

er’s

envi

ron

men

t.Si

gn

ifica

nt

incr

ease

inth

eco

met

assa

yin

exp

ose

din

di-

vid

ual

s.In

fluen

ceo

fse

x,ag

ean

dto

bac

cosm

oki

ng

on

the

gen

oto

xici

tyva

riab

les.

No

effe

cto

fu

sin

gp

rote

ctiv

em

ask

du

rin

gcl

ean

up

lab

ors

Pres

tige

–Pé

rez-

Cad

ahía

etal

.(20

07)

Cro

ss-s

ecti

on

al.

Gen

toxi

city

and

end

ocr

ine

alte

rati

on

sin

volu

nte

ers

and

hir

edw

ork

ers

par

tici

pat

ing

inth

ecl

ean

up

(N=

68)a

nd

con

tro

ls(N

=42

)

Envi

ron

men

talV

OC

.H

eavy

met

als

inb

loo

d(A

l,C

d,N

i,Pb

,Zn

).SC

E.Pr

ola

ctin

and

cort

iso

l.M

etab

olic

gen

etic

po

lym

orp

his

ms

(GST

M1,

GST

T1,

GST

P1)

Hig

hes

tV

OC

leve

lsin

the

volu

nte

er’s

envi

ron

men

t.Si

gn

ifica

nt

incr

ease

inth

ele

vels

of

Al,

Nia

nd

Pb,a

nd

dec

reas

eo

fZ

n,i

nex

po

sed

ind

ivid

ual

s.Si

gn

ifica

nt

incr

ease

inSC

Era

tein

exp

ose

d,in

fluen

ced

by

age,

sex,

smo

kin

gan

dG

STM

1p

oly

mo

rph

ism

.Si

gn

ifica

nt

dec

reas

ein

pro

lact

inan

dco

rtis

oll

evel

sin

exp

ose

dsu

bje

cts

Pres

tige

–Pé

rez-

Cad

ahía

etal

.(2

008a

)

Cro

ss-s

ecti

on

al.

Gen

toxi

city

and

end

ocr

ine

alte

rati

on

sin

volu

nte

ers

and

hir

edw

ork

ers

par

tici

pat

ing

inth

ecl

ean

up

(N=

180)

and

con

tro

ls(N

=60

)

Hea

vym

etal

sin

blo

od

(Al,

Cd,

Ni,

Pb,Z

n).

Co

met

assa

y.Pr

ola

ctin

and

cort

iso

l.M

etab

olic

gen

etic

po

lym

orp

his

ms

(CY

P1A

1,EP

HX

1,G

STM

1,G

STT1

,GST

P1)

Sig

nifi

can

tin

crea

sein

the

leve

lso

fA

l,N

ian

dPb

,an

dd

ecre

ase

of

Zn

,in

exp

ose

din

div

idu

als.

Sig

nifi

can

tin

crea

sein

com

etas

say

and

dec

reas

ein

cort

iso

llev

els

inex

po

sed

ind

ivid

ual

s.H

igh

erD

NA

dam

age

was

rela

ted

toC

YP

1A1

and

EPH

X1

vari

ant

alle

les,

and

low

erD

NA

dam

age

toG

STM

1an

dG

STT1

nu

llg

eno

typ

esPr

esti

ge–

Pére

z-C

adah

íaet

al.

(200

8b)

Cro

ss-s

ecti

on

al.

Gen

toxi

city

invo

lun

teer

san

dh

ired

wo

rker

sp

arti

cip

at-

ing

inth

ecl

ean

up

(N=

159)

and

con

tro

ls(N

=60

)

MN

test

.M

etab

olic

gen

etic

po

lym

orp

his

ms

(CY

P1A

1,C

YP

1B1,

EPH

X1,

GST

M1,

GST

T1,G

STP1

).D

NA

rep

air

gen

etic

po

lym

orp

his

ms

(XRC

C1,

XRC

C3,

XPD

)

Gen

eral

incr

ease

sin

MN

freq

uen

cyan

dd

ecre

ases

inth

ep

rolif

erat

ion

ind

exw

ere

ob

serv

edin

ind

ivid

ual

sw

ith

lon

ger

tim

eo

fex

po

sure

.A

llth

ep

oly

mo

rph

ism

san

alyz

ed,e

xcep

tin

gfo

rC

YP

1B1

and

XRC

C1,

influ

ence

dcy

tog

enet

icd

amag

ele

vels

Pres

tige

–Pé

rez-

Cad

ahía

etal

.(2

008c

)

Cro

ss-s

ecti

on

al.

Rela

tio

nsh

ipb

etw

een

blo

od

con

cen

trat

ion

so

fh

eavy

met

als

and

cyto

gen

etic

and

end

ocr

ine

par

amet

ers

inex

po

sed

by

mea

ns

of

un

ivar

iate

stat

isti

cs(g

ener

allin

ear

mo

del

)(N

=17

9).

Hea

vym

etal

sin

blo

od

(Al,

Cd,

Ni,

Pb,Z

n).

Co

met

assa

y,SC

E,M

Nte

st.

Pro

lact

inan

dco

rtis

ol

Pbw

asre

late

dto

the

com

etas

say.

Co

rtis

olp

lasm

aco

nce

ntr

atio

nw

asin

fluen

ced

by

Al

and

Nii

nver

sely

and

by

Cd

po

siti

vely

.In

wo

men

ther

ew

asa

stro

ng

asso

ciat

ion

bet

wee

nC

dan

dp

rola

ctin

leve

ls

MN

,mic

ronu

cleu

ste

st;S

CE,

sist

erch

rom

atid

exch

ange

s;VO

C,v

olat

ileor

gani

cco

mp

ound

s.

299

Effects of exposure to spilled oils on human health

J. App. Toxicol. 2010; 30: 291–301 www.interscience.wiley.com/journal/jatwww.interscience.wiley.com/journal/jatCopyright © 2010 John Wiley & Sons, Ltd.

Page 10: Review on the effects of exposure to spilled oils on human health

remain stable with time or undergo variations; (ii) determinationof certain factors influencing the mentioned biomarkers; and (iii)analysis of the levels of biomarkers or any other factor associatedwith the appearance of a particular illness, subclinical effects orinteresting alterations (physiological, genotoxic, etc.).

Some studies compare the evaluated or estimated exposurelevels with occupational acceptable exposure limits, or use theselimits to calculate the potential toxicological risk. Nevertheless,this comparison is not entirely correct, since the occupationallimits are usually defined for exposures of 8 h/day during a wholeworking life, i.e. considering a chronic exposure. Exposure tospilled oils takes place over several days or some months at themost, involving time periods much shorter than occupationalexposures.

In summary, most of the studies collected in this reviewprovide evidence on the relationship between exposure tospilled oils and the appearance of acute physical, psychological,genotoxic and endocrine effects in the exposed individuals. Con-sidering the relatively high frequency of this kind of environmen-tal disaster, it seems necessary to establish detailed interventionprotocols that include some mechanisms to detect and controlthe possible harmful health effects that exposure can induce,including performing the immediate collection of biologicalsamples from the beginning of the cleanup work, in order toestablish the levels of individual internal exposure effects at theacute and chronic level, especially those related to genotoxicity.This will permit not only determination of the risk that exposuremay involve, but also evaluation of whether protective devicesused by the individuals in each case adequately fulfilled theirfunction, or on the contrary they did not exert the required pro-tection and therefore require to revision of material characteris-tics and improved briefing sessions on their correct use.

Acknowledgments

This work was funded by a grant from the Xunta de Galicia(INCITE08PXIB106155PR). F. Aguilera was supported by a fellow-ship from the Fundación Carolina.

REFERENCES

Amat-Bronnert A, Castegnaro M, Pfohl-Leszkowicz A. 2007. Genotoxicactivity and induction of biotransformation enzymes in two humancell lines after treatment by Erika fuel extract. Environ. Toxicol. Phar-macol. 23: 89–95.

Baars BJ. 2002. The wreckage of the oil tanker ‘Erika’ human health riskassessment of beach cleaning, sunbathing and swimming. Toxicol.Lett. 128: 55–68.

Bro-Rasmussen F. 1996. Contamination by persistent chemicals in foodchain and human health. Sci. Total Environ. 188(Suppl. 1): 45–60.

Campbell D, Cox D, Crum J, Foster K, Chrístie P, Brewster D. 1993. Initialeffects of the grounding of the tanker Braer on health in Shetland. BMJ307: 1251–1255.

Campbell D, Cox D, Crum J, Foster K, Rilley A. 1994. Later effects ofgrounding of tanker Braer on health in Shetland. BMJ 309: 773–774.

Carrasco J, Lope V, Pérez-Gómez B, Aragonés N, Suárez B, López-AbenteG, Rodríguez-Artalejo F, Pollan M. 2006. Association between healthinformation, use of protective devices and occurrence of acute healthproblems in the Prestige oil spill clean-up in Asturias and Cantabria(Spain): a cross-sectional study. BMC Public Health 6: 1–9.

Carrasco J, Pérez-Gómez B, García-Mendizábal M, Lope V, Aragones N,Forjaz M, Guellar-Castillón P, López-Abente G, Rodríguez-Artalejo F,Pollán M. 2007. Health-related quality of life and mental health in themedium-term aftermath of the Prestige oil spill in Galicia (Spain): across-sectional study. BMC Public Health 7: 245–256.

Chaty S, Rodius F, Lanhers M-C, Burnel D, Vasseur P. 2008. Induction ofCYP1A1 in rat liver after ingestion of mussels contaminated by Erikafuel oils. Arch. Toxicol. 82: 75–80.

Cole J, Beare D, Waugh A, Capulas E, Aldridge K, Arlett C, Green M, CrumJ, Cox D, Garner R, Dingley K, Martin E, Podmore K, Heydon R, FarmerP. 1997. Biomonitoring of possible human exposure to environmentalgenotoxic chemicals: Lessons from a study following the wreck of theoil tanker Braer. Environ. Mol. Mutagen. 30: 97–111.

Crum J. 1993. Peak expiratory flow rate in schoolchildren living close toBraer oil spill. BMJ 307: 23.

Dor F, Bonnard R, Gourier-Fréry C, Cicolella A, Dujardin R, Zmirou D. 2003.Health risk assessment after decontamination of the beaches pol-luted by the wrecked Erika tanker. Risk. Anal. 23: 1199–1208.

Foster K, Campbell D, Crum J, Stove M. 1995. Non-response in a popula-tion study after an environmental disaster. Public Health 109: 267–273.

Gallacher J, Bronstering K, Palmer S, Fone D, Lyons R. 2007. Symptoma-thology attributable to psychological exposure to a chemicalincident: a natural experiment. J. Epidemiol Commun. Hlth 61: 506–512.

Gill D, Picou J. 1998. Technological disaster and chronic community stress.Soc. Natur. Resour. 11: 795–815.

Janjua NZ, Kasi PM, Nawaz H, Farrooqui SZ, Khuwaja UB, Hassan NU, JafriSN, Lutfi SA, KadirMM, Sathiakumar N. 2006. Acute health effects ofthe Tasman Spirit oil spill on residents of Karachi, Pakistan. BMC PublicHealth 6: 84.

Khurshid M, Sheikh M, Iqbal S. 2008. Health of people working/living inthe vicinity of an oil-polluted beach near Karachi, Pakistan. EMHJ14:179–182.

Laffon B, Fraga-Iriso R, Pérez-Cadahía B, Méndez J. 2006. Genotoxicityassociated to exposure to Prestige oil during autopsies and cleaningof oil-contaminated birds. Food Chem. Toxicol. 44: 1714–1723.

Lemiere S, Cossu-Leguille, Bispo A, Jourdain MJ, Lanhers MC, Burnel D,Vasseur P. 2005. DNA damage measured by the single-cell gel elec-trophoresis (comet) assay in mammals fed with mussels contami-nated by the ‘Erika’ oil-spill. Mutat. Res. 581: 11–21.

Lyons R, Temple J, Evans D, Fone D, Palmer R. 1999. Acute health effects ofthe Sea Empress oil spill. J. Epidemiol. Commun. Hlth 53: 306–310.

Meo S, Al-Dress A, Meo I, Al-Saadi M, Azeem M. 2008. Lung function insubjects exposed to crude oil spill into sea water. Mar. Pollut. Bull. 56:88–94.

Morita A, Kusaka Y, Deguchi Y, Moriuchi A, Nakanaga Y, Iki M, Miyazaki S,Kawahara K.1999. Acute health problems among the people engagedin the cleanup of the Nakhodka oil spill. Environ. Res. 81: 185–194.

Palinkas LA, Russell AJ, Downs MA, Petterson JS. 1992. Ethnic-differencesin stress, coping, and depressive symptoms after the Exxon Valdezoil-spill. J. Nerv. Ment. Dis. 180: 287–295.

Palinkas LA, Petterson JS, Russell J, Downs MA. 1993. Community patternsof psychiatric-disorders after the Exxon-Valdez oil-spill. Am. J. Psychiat.150: 1517–1523.

Palinkas LA, Petterson JS, Russell J, Downs MA. 2004. Ethnic differences insymptoms of post-traumatic stress after the Exxon Valdez oil spill. PDM19: 102–112.

Pérez-Cadahía B, Laffon B, Pásaro E, Méndez J. 2006. Geneticdamage induced by accidental environmental pollutants.TheScientificWorldJOURNAL 6: 1221–1237.

Pérez-Cadahía B, Lafuente A, Cabaleiro T, Pásaro E, Méndez J, Laffon B.2007. Initial study on the effects of Prestige oil on human health.Environ. Int. 33: 176–185.

Pérez-Cadahía B, Méndez J, Pásaro E, Lafuente A, Cabaleiro T, Laffon B.2008a. Biomonitoring of human exposure to Prestige oil: Effects onDNA and endocrine parameters. Environ. Health Insights 2: 83–92.

Pérez-Cadahía B, Laffon B, Porta M, Lafuente A, Cabaleiro T, López T,Caride A, Pumarega J, Romero A, Pásaro E, Méndez J. 2008b. Relation-ship between blood concentrations of heavy metals and cytogeneticand endocrine parameters among subjects involved in cleaningcoastal areas affected by the‘Prestige’tanker oil spill. Chemosphere 71:447–455.

Pérez-Cadahía B, Laffon B, Valdiglesias V, Pásaro E, Méndez J. 2008c. Cyto-genetic effects induced by Prestige oil on human populations: The roleof polymorphisms in genes involved in metabolism and DNA repair.Mutat. Res. 653: 117–123.

Porta M, Castaño-Vinyals G. 2003. The impact on human health of Prestigecatastrophe: proposals for its study (in Spanish). Arch. Prev. RiesgosLabor. 6: 52–54.300

F. Aguilera et al.

J. App. Toxicol. 2010; 30: 291–301www.interscience.wiley.com/journal/jatwww.interscience.wiley.com/journal/jat Copyright © 2010 John Wiley & Sons, Ltd.

Page 11: Review on the effects of exposure to spilled oils on human health

Sabucedo J, Arce C, Ferraces M, Merino H, Durán M. 2009. Psychologicalimpact of the Prestige catastrophe. Int. J. Clin. Health Psychol. 9: 105–116.

Schvoerer C, Gourier-Frery C, Ledrans M, Germonneau P, Derrien J, Prat M,Mansotte F, Guillaumot P, Tual F, Vieuxbled J, Marzin M. 2000.Epidemiologic study on short-term health alterations in people par-ticipating in the cleanup of places contaminated by Erika oil (inFrench); available from: http://www.invs.sante.fr/publications/erika3/rapmaree_dist.pdf [accessed 11 January 2009].

Suarez B, Lope V, Perez-Gomez B, Aragones N, Rodriguez-Artalejo F,Marques F, Guzman A, Viloria L J, Carrasco J M, Martin-Moreno J M,Lopez-Abente G, Pollan M. 2005. Acute health problems among sub-jects involved in the cleanup operation following the Prestige oil spillin Asturias and Cantabria (Spain). Environ. Res. 99: 413–424.

Zock JP, Rodriguez-Trigo G, Pozo-Rodriguez F, Barbera JA, Bouso L,Torralba Y, Anto JM, Gomez FP, Fuster C, Verea HS, SEPAR-PrestigeStudy Group. 2007. Prolonged respiratory symptoms in clean-upworkers of the Prestige oil spill. Am. J. Resp. Crit. Care 176: 610–616.

301

Effects of exposure to spilled oils on human health

J. App. Toxicol. 2010; 30: 291–301 www.interscience.wiley.com/journal/jatwww.interscience.wiley.com/journal/jatCopyright © 2010 John Wiley & Sons, Ltd.