AMERICAN JOURNAL OF INDUSTRIAL MEDICINE 54:971–979 (2011)

An Analysis of the Respiratory Health StatusAmong Seafarers in the Russian Trawler

and Merchant Fleets

Olga Shiryaeva, MD,1,2� Lisbeth Aasmoe, PhD,2,3 Bjørn Straume, MD, PhD,1 andBerit Elisabeth Bang, PhD

2,3

Objectives Trawler fishermen and merchant seafarers have tough working conditions.While workers in both occupations are exposed to a challenging environment, trawlerfishermen are also engaged in onboard fish processing, which is considered to beadditional exposure. The aim of the present study was to characterize respiratoryhealth status in both groups of seamen.Methods In total 127 trawler fishermen and 118 merchant seafarers were enrolledduring their regular medical health examinations. The study protocol comprised astandardized questionnaire, lung function test and measurements of fractional nitricoxide concentrations (FENO) in exhaled air.Results Doctor-diagnosed asthma was reported only by trawler fishermen (3.9%,P < 0.05, Pearson Chi-square test). Adjusted odds ratios (OR) of respiratory symp-toms were more often elevated in trawler fishermen compared to merchant seafarers.Trawler fishermen had reduced spirometric parameters: FEV1 % of predicted values(adjusted b: �5.28, 95%CI: �9.28 to �1.27), FVC % of predicted values (adjusted b:�5.21, 95%CI: �9.25 to �1.17). Increased OR of the work-related cough with phlegm(OR: 6.6, 95% CI: 1.8–21.9), running nose (OR: 3.0, 95%CI: 1.2–7.7), and frequentsneezing (OR: 3.4, 95%CI: 1.0–12.7) were found among those trawler workers whosework tasks included filleting of fish. FENO levels were not significantly differentbetween trawler and merchant seamen.Conclusions The present study indicated that trawler fishermen exhibited impairedlung function and were more likely to have asthma. The environment of the onboardfactories where fishermen fillet fish is suggested as a risk factor for work-related respi-ratory symptoms. Am. J. Ind. Med. 54:971–979, 2011. � 2011 Wiley Periodicals, Inc.

KEY WORDS: seafarers; lung function; occupational epidemiology; respiratorysymptoms; exhaled nitric oxide

1Institute of Community Medicine, Faculty of Health Sciences, University of Tromsoe,Tromsoe,Norway

2Department of Occupational and Environmental Medicine, University Hospital NorthNorway,Tromsoe,Norway

3Medical Pharmacology and Toxicology, Institute of Medical Biology, Faculty of HealthSciences,University of Tromsoe,Norway

Contract grant sponsor: Northern Norway Regional Health Authority (Helse Nord RHF),Norway.

*Correspondence to: Olga Shiryaeva MD, Department of Occupational and EnvironmentalMedicine, University Hospital North Norway, Tromsoe, Norway, Sykehusveien 38, 9038Tromsoe,Norway.E-mail: Olga.Shiryaeva@uit.no

Accepted 23May 2011DOI10.1002/ajim.20978.Published online 20 June 2011inWiley Online Library

(wileyonlinelibrary.com).

�2011WileyPeriodicals,Inc.

INTRODUCTION

Transportation of goods by sea and fishing are activi-

ties which provide employment for thousands of people in

Russia. Arkhangelsk is a port-city in the north-west of

Russia and has two main types of fleets: trawl and mer-

chant. These industries play an important role in the city

economy by providing massive employment for the inhab-

itants of Arkhangelsk.

Arkhangelsk Trawl Fleet (ATF) is the oldest fleet in

the North of Russia and has 24 fishing vessels. ATF pro-

duces cod, haddock, redfish, flounder, herring, blue whit-

ing, mackerel and offers also cod’s tongues and cheeks,

scallops, fishmeal, and fish preserves.

The Arkhangelsk Merchant fleet (AMF) represents

the commercial port for the transfer of general cargo,

pulp, cardboard, lumber, metal, containers, heavy equip-

ment, fertilizers and bulk cargo, handling up to 4.5 million

tonnes of cargo per year.

Living and working conditions of seamen differ fun-

damentally from those of employees working ashore due

to unusual working hours, monotony during long cruises,

and separation from their social environment, which are

considered to be important stressors [Agterberg and

Passchier, 1998; Roberts, 2002; Jensen et al., 2006;

Lodde et al., 2008; Oldenburg et al., 2009, 2010]. Their

health is affected by noise, vibration, inhalation of exhaust

particles from engines, fatigue, and overwork. In case of

sudden illness or injuries during the ship’s voyage, the

chances of receiving proper and effective medical treat-

ment are poor. Seafaring is therefore considered a danger-

ous occupation with higher morbidity and mortality rate

than most occupations onshore [Schilling, 1966, 1971; Fil-

ikowski, 1977, 1987, 1989; Neutel, 1990; Filikowski

et al., 1998; Lawrie et al., 2004; Oldenburg et al., 2010;

Roberts, 2010].

In addition to the mentioned stress factors, fishermen

are also exposed to the fish that they process on board in

fish-processing plants. Plants vary in the levels of technol-

ogy, with workplaces relying on both manual handling of

the fish and automated processes. Fish processing has po-

tential for bioaerosol production [Jeebhay et al., 2004,

2005; Jeebhay and Cartier, 2010]. Vessels with onboard

processing facilities are commonly characterized by inade-

quate ventilation systems and confined spaces [Lucas

et al., 2006].

Despite the risky nature of the occupation, very little

research has been conducted on seafarers’ health. Unusual

working patterns, involving long periods of time at sea

and only short periods of time on shore, make fishermen

and seafarers difficult to contact and thus a challenging

population to recruit for research. The majority of studies

conducted were focused on mortality rates and accidents.

In addition, most studies were conducted 10 years ago or

more and some of them more than 20–30 years ago, there-

fore reducing their relevance.

In our research of onshore Norwegian seafood indus-

try we have previously found that workers involved in fish

processing are exposed to various bioaerosol constituents

and exhibit respiratory symptoms and impaired lung func-

tion [Bang et al., 2005a; Shiryaeva et al., 2010]. Respira-

tory reactions may be the result of biological agents and

additional factors such as cold air, strenuous physical

activity associated with work tasks during the processing

of the fish.

In the present study we aimed to estimate respiratory

health status of both groups of seamen: trawl fishermen

from ATF and merchant seamen from AMF.

Merchant seafarers and fishermen regularly undergo

medical examination and receive health certificates,

according to the national regulations. Medical examina-

tions are implemented throughout the year. All workers

are obliged to medical exams once per year and health

certificates are valid for 1 year.

We intended to characterize the respiratory health of

seafarers by means of a questionnaire, lung function tests

and measurements of nitric oxide concentration in exhaled

air of the workers by joining to ongoing medical check-up

in December 2009 and January 2010 at the Central

Seamen Polyclinic in Arkhangelsk, Russia.

MATERIALS AND METHODS

Study Design and Population

The study is a cross-sectional study among trawler

fishermen and merchant seafarers. The field work was car-

ried out between December 2009 and January 2010.

Trawler fishermen as well as the merchant seafarers were

invited to take part in the study during regular medical

health examinations at the Central Seamen Polyclinic,

Arkhangelsk, Russia.

Study subjects were informed of the objectives of the

study as well as its practical procedure. Written informed

consent was obtained from all participants. The survey

was approved by the Regional Committee for Medical

Research Ethics at Northern State Medical University,

Arkhangelsk, Russia and by Regional Committee for

Medical Research Ethics in Northern Norway, Tromsoe.

All merchant seafarers and trawler fishermen who

were obliged to undergo medical examinations in the peri-

od from December 2009 to January 2010 were invited to

participate in the study. In total, 247 seafarers and fisher-

men underwent medical check-up in this period, of which

245 took part in the present study (response rate 99%).

Inclusion criteria for the study were: age above 18,

trawler fishermen who were engaged in on-board fish

processing and were employed in trawl fleet for at least 1

972 Shiryaeva et al.

year, or merchant seafarers who had never worked in trawl

fleet before and were employed for at least 1 year in mer-

chant fleet.

Questionnaire

The questionnaire used in the present study was the

same as previously used in our earlier conducted studies

[Bang et al., 2005a; Shiryaeva et al., 2010]. The question-

ing was carried out anonymously. The seafarers were

guaranteed that their given answers would not be for-

warded to their employers and would not influence the

outcome of their fitness test for nautical service.

The questionnaires were translated into Russian and

included questions on personal background, health and oc-

cupational characteristics, and had two main sections.

The first section contained questions regarding demo-

graphic data, smoking habits, respiratory and allergic dis-

eases. Asthma, allergy and eczema were defined as

positive answers to the two questions: ‘‘Do you have asth-

ma/allergy/eczema?’’ and if ‘‘yes,’’ ‘‘was your asthma/

allergy/eczema diagnosed by a doctor?’’ The time of onset

of the diseases was limited to adult age (>15 years old).

The questions on general respiratory symptoms were de-

fined as symptoms present in the last 12 months, apart

from a cold. Smoking status was categorized as never

smoker (subjects, who had never smoked regularly), for-

mer smoker (subjects, who reported smoking regularly

one or more cigarettes per day in the past, but who had

stopped smoking at least 1 year before the time they filled

out the questionnaire), or current smoker (subjects, who

reported smoking regularly one or more cigarettes a day

for at least 1 year).

The second section of the questionnaire asked for

symptoms that the subjects attributed directly to their

work. All questions on work-related symptoms were limit-

ed to the last 12 months and defined as symptoms that

were present during or immediately after working hours.

Symptoms were divided into two groups: (1) upper respi-

ratory symptoms: frequent sneezing, running nose, sore

throat; (2) lower respiratory symptoms: dry cough, cough

with phlegm, wheezing, shortness of breath, chest

tightness.

The questionnaire included a list of fish species proc-

essed and specific work tasks in which trawler fishermen

were involved when processing fish at the onboard trawler

factory. The list included the following main work tasks:

slaughtering (degutting and heading of fish), filleting (fil-

leting with automatic equipment and manual filleting),

bagging (fish quality and weight control and, packing),

freezing, others (waste utilization, preserving, and fish-

meal production). Each worker might be involved in sev-

eral work tasks and in processing of different species if

fish.

Lung Function Test

Spirometry was undertaken by means of a

Vitalograph-MDI compact 1 (Vitalograph Ltd, Bucking-

ham, England). Age, height, and weight were recorded to

calculate the percentage of the predicted values. Tests

were conducted with the subjects seated. Forced vital ca-

pacity (FVC) and forced expiratory volume in one second

(FEV1) were obtained by instructing the person to expire

forcefully after a maximum inspiratory maneuver. Forced

expiratory maneuvers were performed until satisfying the

recommended criteria ATS 1995 [Standardization of

Spirometry, 1994 Update. American Thoracic Society,

1995]. The highest values of FVC (L), FEV1 (L/sec) and

FEV1/FVC (%) were retained for the analysis. Subjects

with technically unsatisfactory spirometry were excluded

from the analyses. Calculations of predicted values were

based on equations proposed by Castellsague et al. [1998].

Reduced lung function was characterized as FEV1 and

FVC less than 80% of predicted values. Criteria for air-

ways obstruction was defined as FEV1/FVC ratio below

the 5th percentile of the predicted values [Pellegrino et al.,

2005; Hansen et al., 2007].

Fractional Exhaled Nitric Oxide(FENO) Measurements

FENO was measured by chemoluminescence using

direct reading nitric oxide monitor (NIOX; Aerocrine AB,

Solna, Sweden), according to the 2005 American Thoracic

Society (ATS) guidelines [ATS/ERS recommendations for

standardized procedures for the online and offline mea-

surement of exhaled lower respiratory nitric oxide and na-

sal nitric oxide, 2005] and expressed in parts per billion

(ppb). Subjects exhaled fully, and then inhaled ambient air

through a nitric oxide scrubber to total lung capacity. Sub-

jects then exhaled against an automatically adjusted resis-

tance to achieve a constant exhalation flow rate of

50 ml s�1. Resistance was also adjusted so that an

upper airway pressure of at least 5 cm H2O was main-

tained throughout exhalation, sufficient to close the velum

and exclude nasal air. FENO measurements were taken

from a stable plateau in exhaled nitric oxide concentration

of at least 3 s during an exhalation. Any exhalation not

meeting ATS/ERS requirements was rejected by the NIOX

system.

Statistical Analysis

Normally distributed data are presented as means

(standard deviation); non-normally as geometric means

(range) and categorical variables as numbers (percent).

Single variable analyses were performed with indepen-

dent-samples t-test, Mann–Whitney U-test or Pearson

Respiratory Health of Seamen 973

Chi-square test. A multivariable logistic regression was

applied to estimate odds ratios (95%CI) of general and

work-related respiratory symptoms. Adjustment was made

for age (<35, 36–45, 46–55, >56), smoking (never/

former/current smokers) and education. A multivariable

linear regression was used for analysis of spirometric vari-

ables. Multivariable logistic regression model was also

used to test the difference between subpopulations in

terms of reduced lung function (FEV1 and FVC less than

80% of predicted, and FEV1/FVC below the 5th percentile

of the predicted values) used as dichotomous variables.

Those subjects who reported doctor-diagnosed asthma

(n ¼ 5) were analyzed separately. Data were analyzed

with SPSS software package (version 18.0 for Windows,

Chicago, IL). All tests were two-sided, P values <0.05

were considered to be statistical significant.

RESULTS

Characteristics of the Study Population

The study population comprised 245 seamen (127

trawler fishermen and 118 merchant seafarers), who were

all males aged from 21 to 67 years old (Table I). Trawler

fishermen were older, with a higher percentage of current

smokers and lower education than the merchant seamen.

Trawler seamen have been somewhat longer employed in

the fleet than the merchant seafarers, but the difference

did not reach significance. Body mass index (BMI, kg/m2)

indicated that both groups of workers were slightly

overweight (BMI > 25 kg/m2). Habitual fish consumption

was reported by almost all participants. Asthma was

reported only by trawler seamen (P < 0.05, Pearson Chi-

square test). Slightly higher percentage of trawler fisher-

men than merchant seafarers reported doctor-diagnosed al-

lergy. The prevalence of eczema was low in both groups

of workers.

General and Work-RelatedRespiratory Symptoms

The prevalence of respiratory symptoms in trawler

fishermen ranged from 3.3% for shortness of breath with

wheezing to 31.9% for daily morning cough, and in mer-

chant seafarers from 0.8% for prolonged cough to 28.8%

for running nose, respectively. All symptoms were

reported more often by trawler fishermen except for work-

related wheezing and chest tightness which were reported

equally frequently by the two groups (Table II).

The crude ORs of all general respiratory symptoms

were increased in trawler fishermen compared to merchant

seafarers, and remained increased after adjustment for po-

tential confounders. Significant results were found for dai-

ly morning cough, while daily morning phlegm and

prolonged cough showed borderline significance. Analysis

of work-related respiratory symptoms showed increased

crude ORs of all upper respiratory symptoms, dry cough,

cough with phlegm and shortness of breath. ORs of these

symptoms remained increased and not significant after ad-

justment. Adjusted ORs of work-related wheezing and

chest tightness showed no difference between merchant

and trawler seamen.

Lung Functions

As demonstrated in Table III, trawler fishermen had

overall lower spirometric values compared to merchant

fleet workers. Significant results were found for absolute

values of FEV1 and FVC, and for FEV1 and FVC % of

predicted values (analyzed as continuous variables). A

multivariable logistic regression analysis was applied to

estimate reduced lung functions in the study subjects

(FEV1 and FVC < 80% of predicted values, and FEV1/

FVC < 5th percentile of predicted values; analyzed as di-

chotomous variables). Significant results were found for

FVC < 80% of predicted values in trawler seafarers. P

value for OR of FEV1 < 80% of predicted values was

borderline.

TABLE I. Characteristics of the Study Population

Trawlerfishermen,n ¼ 127

Merchantseafarers,n ¼ 118 P-Valuea

Age,yearsMean (SD) 45.9 (9.9) 42.2 (12.0) <0.05<35,n (%) 19 (15.0) 35 (29.6)

<0.0536^45,n (%) 33 (26.0) 29 (24.6)46^55,n (%) 53 (41.7) 38(32.2)>56,n (%) 22 (17.3) 16 (13.6)

Smoking,n (%)Currentsmokers 55 (43.3) 34(28.8)

<0.05Formersmokers 25 (19.7) 25(21.2)Never-smokers 47 (37.0) 59(50.0)

BMI,mean (SD) 26.1 (4.1) 25.3 (3.1) n.s.Education,years

Mean (SD) 12.9 (2.5) 14.5 (3.8) <0.05Duration ofemployment

Mean (SD) 23.1 (10.2) 20.7 (11.2) n.s.Asthmab,n (%) 5 (3.9) � <0.05Allergyb,n (%) 15 (11.8) 10 (8.5) n.s.Eczemab,n (%) 1 (0.79) 1 (0.84) n.s.

BMI, bodymass index; n.s., not significant.aP value for Pearson Chi-square test (categorical variables), for independent-samplest-test (continuous variables).bSelf-reported, doctor-diagnosed.

974 Shiryaeva et al.

Fractional Exhaled Nitric Oxide(FENO) Levels

The levels of FENO were stratified by allergy

(self-reported doctor-diagnosed) and smoking status

since it was confirmed previously that these factors

significantly affect FENO levels [Travers et al., 2007],

asthmatic subjects were excluded from this analysis.

Highest FENO levels were seen in allergic study

subjects who never smoked (Table IV). FENO levels did

not differ significantly between the two categories of

seamen.

TABLE II. Prevalence, n (%) of General andWork-Related Respiratory Symptoms in the Study Population

Trawler fishermen,n ¼ 122a

Merchant seafarers,n ¼ 118

Crude,OR (95%CI)

Adjusted,OR (95%CI)b

General respiratorysymptomsWheezing 12 (9.8) 7 (5.9) 1.7 (0.6^4.5) 1.2 (0.4^3.3)Shortness ofbreathwithwheezing 4 (3.3) 2 (1.7) 1.96 (0.3^10.9) 5.2 (0.7^15.2)Dailymorningcough 39(31.9) 15 (12.7) 3.2 (1.6^6.2)z 2.7 (1.3^5.5)z

Dailymorningphlegm 26(21.3) 12 (10.1) 2.4 (1.1̂ 5.0)y 2.1 (0.9^4.6)‰

Prolongedcoughc 6 (4.9) 1 (0.8) 6.0 (0.9^23.9)‰ 10.3 (0.9^56.6)‰

Work-relatedrespiratorysymptomsUpperFrequentsneezing 13 (10.7) 10 (8.5) 1.3 (0.5^3.0) 1.1 (0.4^1.9)Runningnose 37 (30.3) 34 (28.8) 1.1 (0.6^1.9) 1.1 (0.6^1.9)Sore throat 8 (6.6) 5 (4.2) 1.6 (0.5^4.9) 1.5 (0.4^5.1)

LowerDry cough 16 (13.1) 10 (8.5) 1.6 (0.7^3.7) 1.3 (0.5^3.4)Coughwithphlegm 11 (9.0) 7 (5.9) 1.7 (0.6^4.2) 1.1 (0.4^3.4)Wheezing 3 (2.4) 3 (2.5) 0.9 (0.1̂ 4.8) 1.0 (0.1̂ 4.1)Shortnessofbreath 4 (3.3) 3 (2.5) 1.2 (0.3^3.6) 1.1 (0.1̂ 2.6)Chest tightness 3 (2.4) 3 (2.5) 0.9 (0.1̂ 3.1) 1.0 (0.1̂ 2.9)

Crude and adjusted odds ratio (95%CI) of the symptoms for trawler fishermen.aAsthmatic subjects (n ¼ 5)were excluded from the analyses.bOdds ratio (95%CI) of the symptoms adjusted for age, smoking, education, bymultivariable logistic regression.Merchant seafarers formed the reference category (OR ¼ 1.0).cDaily cough lastingmore than 3months in the last12months.yP < 0.05.zP < 0.01.‰0.05 < P < 0.08.

TABLE III. Lung Function Parameters of Trawler Fishermen� Compared toMerchant Seafarers

bRegressioncoefficient (95%CI) Odds ratio (95%CI)a P-Value

FEV1,Lb �0.31 (�0.52 to (�0.06)) � 0.004

FVC,Lb �0.32 (�0.57 to (�0.07)) � 0.01FEV1/FVC%

b �0.29 (�2.70^2.17) � 0.81FEV1%ofpredicted

c �5.28 (�9.28 to (�1.27)) � 0.01FVC%ofpredictedc �5.21 (�9.25 to (�1.17)) � 0.01FEV1 < 80%ofpredicted � 4.12 (0.86^19.7) 0.07FVC < 80%ofpredicted � 5.65(1.9^21.7) 0.005FEV1/FVC < 5thpercentile ofpredicted � 1.94 (0.3^11.1) 0.45

�Asthmatic subjects (n ¼ 5) were excluded from the analyses.aOdds ratio OR (95%CI) of reduced lung function (dichotomous scale) adjusted for age, smoking, education, bymultivariable logistic regression analysis,merchant seafarers formedthe reference category (OR ¼ 1.0).bRegression coefficientb (95%CI) of spirometric variables (continuous scale) adjusted for age, height, smoking, education.cRegression coefficientb (95%CI) of spirometric variables (continuous) adjusted for age, smoking, and education; by multivariable linear regression analyses.Merchant seafarersformed the reference category.

Respiratory Health of Seamen 975

Specific Work Tasks and Work-RelatedRespiratory Symptoms in TrawlerFishermen

Additional statistical analyses were applied to exam-

ine associations between specific work tasks and work-

related respiratory symptoms experienced by trawler

fishermen.

Increased ORs of the symptoms were found for those

workers whose main work task was described as filleting

of fish. The following work-related respiratory symptoms

were found to be significantly associated with filleting of

fish: cough with phlegm (OR: 6.6, 95%CI (1.8–21.9),

P < 0.01), running nose (OR: 3.0, 95%CI (1.2–7.7),

P < 0.05), frequent sneezing (OR: 3.4, 95%CI (1.0–12.7),

P < 0.05). Odds ratios were adjusted for age and smoking

by multivariable logistic regression analyses; asthmatic

workers (n ¼ 5) were excluded from the analyses (data

not shown).

Characteristics of Asthmatic Subjects

Separate analyses were performed for trawler fisher-

men who reported in the questionnaire that they had

doctor-diagnosed asthma. Asthmatic workers were mid-

dle-aged, prevalently former smokers (60%) and were

employed at trawl fleet for more than 20 years (Table V).

Asthmatics were found to have impaired lung functions.

40–80% of the asthmatic subjects reported general and

work-related respiratory symptoms. FENO levels ranged up

to 108 ppb. Most asthmatic workers reported filleting of

fish as main work task they were involved in at trawler

factory. All asthmatics reported cod as main fish specie

processed on board, three of five reported also haddock

and flounder.

DISCUSSION

The study was performed as a response to general

concerns regarding harmful work environment and nega-

tive health effects for employees in trawl and merchant

fleets. The results of our study showed that trawler fisher-

men were more likely to have asthma and respiratory

symptoms, and exhibit impaired lung function more often

compared to merchant seafarers. Those trawler fishermen

who were engaged in filleting of fish were found to have

increased odds ratios of work-related cough with phlegm,

running nose, and frequent sneezing. Therefore, the envi-

ronment in which fishermen work while filleting fish in

onboard factories is suggested to be a risk factor for

experiencing work-related respiratory symptoms.

It has been published that workers in the seafood

industry, especially those engaged in either manual or

automated processing of seafood are exposed to bioaero-

sols, of which inhalation occur primarily during degutting,

cutting, scrubbing, filleting, and cleaning [Jeebhay and

Cartier, 2010]. Processes leading to aerosolization of

the seafood have been identified as a potential high risk

activity for respiratory symptoms, non-specific bronchial

TABLE IV. Nitric Oxide Concentration (Expressed in Parts Per Billion)Stratified byAllergy and Smoking

Trawlerfishermen(n ¼ 122)a

Merchantseafarers(n ¼ 118)

NoallergyNever-smokers 15.4 (5.0^47.0) 14.3 (5.0^61.0)Ever-smokersb 11.0 (5.0^84.0) 13.8 (5.0^56.0)

AllergyNever-smokers 23.6 (16.0^35.0) 22.9 (5.0^180.0)Ever-smokersb 12.9 (6.0^48.0) 16.9 (11.0^34.0)

Data are presented as geometric mean (range).aAsthmatic subjects (n ¼ 5) were excluded from the analyses.bCurrent smokers and former smokers.

TABLE V. Main Characteristics ofAsthmaticTrawler Fishermen (n ¼ 5)

CharacteristicsAge,yearsMean (SD) 48.8 (7.0)

Smoking,n (%)Never-smokers 1 (20)

Formersmokers 3 (60)Currentsmokers 1 (20)

Durationofemployment,yearsMean (range) 25.6 (24^30)

Spirometric values,mean (SD)FEV1%ofpredicted 81.2 (23.7)FVC%ofpredicted 101.0 (20.43)FEV1/FVC 69.4 (24.9)

Impairedspirometric values,n (%)FEV1 < 80%ofpredicted 2 (40)FVC < 80%ofpredicted 1 (20)FEV1/FVC < 5thpercentile ofpredicted 2 (40)

FENO levels,ppbGM(range) 28.1 (17.0^108.0)

Work tasks,n (%)Slaughtering 2 (40)Filleting 4 (80)Bagging 1 (20)

Typeof fishprocessing,n (%)Cod 5 (100)Haddock 3 (60)Flounder 3 (60)

GM, geometricmean.

976 Shiryaeva et al.

hyperresponsiveness, and work-related asthma [Gaddie

et al., 1980; Desjardins et al., 1995; Jeebhay et al., 2001].

Our own previous research work showed that produc-

tion workers who were engaged in seafood processing

were exposed to endotoxins, seafood allergens, proteins,

microorganisms and have high prevalence of airways

symptoms [Bang et al., 2005a]. We also observed that

cold indoor working environment may increase the risk of

symptoms in seafood industry workers [Bang et al.,

2005b]. In addition, in our recently conducted study we

found that salmon-processing workers have impaired re-

spiratory health status compared to controls [Shiryaeva

et al., 2010]. The results of the previous works and the

present study allow us to suggest that seafood-processing

workers are at high risk of experiencing respiratory symp-

toms and reduced lung function parameters. The main

causal agent of the respiratory impairment among this

type of the workers is suggested to be exposure to bioaer-

osol in the working environment of the production area.

Physical factors are also considered to contribute to respi-

ratory symptoms, including the wet environment, strenu-

ous physical activity and low temperatures.

The approach in the present study did not allow us to

include exposure measurements. To be able to evaluate

exposure, we grouped the workers according to the work

tasks performed. Analysis of these questionnaire data

yielded that most fishermen with work-related respiratory

symptoms reported that they were involved in filleting of

fish. This finding implies that production workers at trawl-

er factories are exposed in different ways according to the

various tasks they perform. Concentrations of aerosolized

particles from the processed material may vary between

different processing. According to the studies published

previously, it has been suggested that wet processes such

as fish gutting and filleting produce higher concentrations

of respirable particulate than dry processes such as fish

packing or storage [Jeebhay et al., 2004]. In one Swedish

study among workers processing salmon, exposure to air-

borne salmon antigen were highest around the filleting

compared to the packing area [Dahlman-Høglund et al.,

2002]. Our study on Norwegian salmon-processing work-

ers revealed similar results (unpublished data). One may

expect that exposure to aerosolized fish allergens are

higher among those workers who are exposed to muscular

tissue of fish compared to workers engaged in other tasks,

as the main allergen in fish is a muscle protein. Local ven-

tilation and work intensity are also factors that could vary

between workers and may play a role in the development

of respiratory symptoms. It would thus be of interest to

conduct further studies with comprehensive exposure char-

acterization of workers involved in seafood processing in

onboard factories.

The results from the questionnaire part of the study

were compatible with the objective lung function tests,

showing trawler fishermen to have significantly decreased

lung function values compared to merchant seafarers. This

finding is in agreement with our previous study where

salmon-processing workers were found to have significant-

ly lower values of respiratory variables compared to con-

trols who were not involved in fish processing [Shiryaeva

et al., 2010].

Only trawler fishermen reported doctor-diagnosed

asthma in our study. The working environment onboard

trawler vessels is thought to be more challenging and

the work is more intensive compared to the situation in

merchant vessels. Therefore, theoretically, subjects with

asthma may be expected to leave the harsh environment

in which they worked. Analysis showed that asthmatics

were employed in trawl fleet for more than 20 years,

however, the time when diagnosis of asthma was stated by

a doctor was not specified. The asthmatic status of the

workers reported in the questionnaire was in agreement

with the physiological tests performed, showing impaired

lung function and increased nitric oxide levels in

exhaled air in these subjects. Interestingly, most asthmatic

subjects reported that they were involved in filleting of

fish, and all of them reported cod as the main fish

species processed on board. Previously, seafood-derived

agents have been reported to be involved in asthma

development in trout processors [Sherson et al., 1989],

deep-sea fishermen [Tomaszunas et al., 1988], and

salmon workers [Douglas et al., 1995] and a specific role

of fish exposure was suggested. Lack of exposure meas-

urements and the cross-sectional design prevent us to

make conclusions on causal relationships in the present

study.

Measurements of nitric oxide concentrations in ex-

haled air were performed among all participants of the

study. FENO is known as a noninvasive marker of eosino-

philic airway inflammation. It has been published previ-

ously that raised levels of FENO may occur with a number

of airway or lung disorders, but the most important con-

text in which the measurement of FENO is clinically useful

is that of allergic airways disease [Taylor et al., 2006].

The results of the tests were stratified by allergic and

smoking statuses, as it was observed earlier that these two

factors significantly affect FENO levels [Travers et al.,

2007]. We found compatible results with other studies in

terms of high FENO levels among subjects with allergy

and asthma and low levels in smokers [Bommarito et al.,

2008]. In the present study we did not find striking differ-

ences in FENO levels between the two categories of sea-

men in spite of highlighted impaired respiratory health

status in trawler fishermen. However, interpretation of

FENO results is difficult due to many interfering factors

which influence FENO levels, and currently little is known

about interactions between these factors. Therefore, it is

complicated to draw firm conclusions regarding this aspect

Respiratory Health of Seamen 977

of the study, since more thorough examinations with

multiple FENO testing are needed.

Limitations

As a cross-sectional study, this investigation cannot

make strong conclusion regarding causal relationships be-

tween exposure and health outcomes. The information

about symptoms is self reported, therefore prone to recall

bias. Some of the workers might also have underreported

symptoms they experienced, especially since the survey

was conducted during the regular health examination

aimed to obtain the obligatory health certificate. In spite

of the guarantee of confidentiality, we can not completely

be sure that the workers reported all disorders experi-

enced. The ‘‘healthy worker effect’’ could cause underesti-

mation of the actual risk of respiratory symptoms. Since

two groups of workers were statistically different in terms

of age, smoking, and education, we applied multivariable

regression models (logistic and linear) to correct these

imbalances. Asthmatics were treated separately in the sta-

tistical analyses since asthmatic status may distort the ef-

fect estimate of respiratory outcome variables studied in

the rest of the group. The study is strengthened by objec-

tive lung function test and measurements of nitric oxide

concentration in exhaled air.

CONCLUSION

In conclusion, the study demonstrates that trawler

fishermen have impaired respiratory health status com-

pared to merchant seafarers. The role of bioaerosol expo-

sure during fish processing is implied. Filleting of fish as a

work task is suggested as a risk factor for respiratory

symptoms among trawler fishermen in our study.

According to the available information, the number of

people engaged in sea-related occupations is increasing

steadily, especially in the fishing industry. Such informa-

tion confirms the necessity of maintaining efficient health

services systems, with the active introduction of preven-

tive measures.

Control of bioaerosol exposure at workplaces on on-

board fish processing factories needs to be implemented.

Health examinations should be offered as preventive regu-

lar measures to all workers more often and, in particular,

to workers expressing health problems in order to impede

development of long-term illnesses. Fishermen may also

benefit from health promotion and education programs.

ACKNOWLEDGMENTS

We would like to thank Lidia Pukanova, MD, PhD,

Anastasia Bagretsova, MD, PhD and Elena Kazakevich,

MD, Professor from Northern Medical Clinical Centre

named after N.A. Semashko for their assistance with vari-

ous aspects of the project.

REFERENCES

Agterberg G, Passchier J. 1998. Stress among seamen. Psychol Rep83(2):708–710.

ATS/ERS recommendations for standardized procedures for theonline and offline measurement of exhaled lower respiratory nitricoxide and nasal nitric oxide. 2005. Am J Respir Crit Care Med171(8):912–930.

Bang B, Aasmoe L, Aamodt BH, Aardal L, Andorsen GS, Bolle R,Boe R, Van Do T, Evans R, Florvag E, Gram IT, Huser PO, KramvikE, Lochen ML, Pedersen B, Rasmussen T. 2005a. Exposure andairway effects of seafood industry workers in northern Norway.J Occup Environ Med 47(5):482–492.

Bang BE, Aasmoe L, Aardal L, Andorsen GS, Bjornbakk AK,Egeness C, Espejord I, Kramvik E. 2005b. Feeling cold at workincreases the risk of symptoms from muscles, skin, and airways inseafood industry workers. Am J Ind Med 47(1):65–71.

Bommarito L, Migliore E, Bugiani M, Heffler E, Guida G, Bucca C,de Marco R, Rolla G. 2008. Exhaled nitric oxide in a populationsample of adults. Respiration 75(4):386–392.

Castellsague J, Burgos F, Sunyer J, Barbera JA, Roca J. 1998.Prediction equations for forced spirometry from European originpopulations. Barcelona Collaborative Group on Reference Values forPulmonary Function Testing and the Spanish Group of the EuropeanCommunity Respiratory Health Survey. Respir Med 92(3):401–407.

Dahlman-Høglund ALP, Renstrøm A, Elsayed S. 2002. ‘‘Levels ofsalmon antigen in the air among workers in a salmon industry.’’ In5th International Congress of the International Occupational HygieneAssociation, Bergen, Norway.

Desjardins A, Malo JL, L’Archeveque J, Cartier A, McCants M,Lehrer SB. 1995. Occupational IgE-mediated sensitization and asth-ma caused by clam and shrimp. J Allergy Clin Immunol 96(5 Pt 1):608–617.

Douglas JD, McSharry C, Blaikie L, Morrow T, Miles S, Franklin D.1995. Occupational asthma caused by automated salmon processing.Lancet 346(8977):737–740.

Filikowski J. 1977. Health condition of seamen of ocean-going trans-port vessels. Bull Inst Marit Trop Med Gdynia 28(3–4):107–118.

Filikowski J. 1987. Main health problems of seafarers. Bull InstMarit Trop Med Gdynia 38(3–4):157–163.

Filikowski J. 1989. Changes in the state of health of seamen inducedby their working environment. Bull Inst Marit Trop Med Gdynia40(1–2):41–49.

Filikowski J, Rzepiak M, Renke W. 1998. Health problems of deepsea fishermen. Bull Inst Marit Trop Med Gdynia 49(1–4):45–51.

Gaddie J, Legge JS, Friend JA, Reid TM. 1980. Pulmonary hyper-sensitivity in prawn workers. Lancet 2(8208–8209):1350–1353.

Hansen JE, Sun XG, Wasserman K. 2007. Spirometric criteria forairway obstruction: Use percentage of FEV1/FVC ratio below thefifth percentile, not<70%. Chest 131(2):349–355.

Jeebhay MF, Cartier A. 2010. Seafood workers and respiratory dis-ease: An update. Curr Opin Allergy Clin Immunol 2010(10):104–113.

978 Shiryaeva et al.

Jeebhay MF, Robins TG, Lehrer SB, Lopata AL. 2001. Occupationalseafood allergy: A review. Occup Environ Med 58(9):553–562.

Jeebhay MF, Robins TG, Lopata AL. 2004. World at work: Fishprocessing workers. Occup Environ Med 61(5):471–474.

Jeebhay MF, Robins TG, Seixas N, Baatjies R, George DA,Rusford E, Lehrer SB, Lopata AL. 2005. Environmental exposurecharacterization of fish processing workers. Ann Occup Hyg 49(5):423–437.

Jensen OC, Sorensen JF, Thomas M, Canals ML, Nikolic N, Hu Y.2006. Working conditions in international seafaring. Occup Med(Lond) 56(6):393–397.

Lawrie T, Matheson C, Ritchie L, Murphy E, Bond C. 2004. Thehealth and lifestyle of Scottish fishermen: A need for health promo-tion. Health Educ Res 19(4):373–379.

Lindstrom CD, van Do T, Hordvik I, Endresen C, Elsayed S. 1996.Cloning of two distinct cDNAs encoding parvalbumin, the major al-lergen of Atlantic salmon (Salmo salar). Scand J Immunol 44(4):335–344.

Lodde B, Jegaden D, Lucas D, Feraud M, Eusen Y, Dewitte JD.2008. Stress in seamen and non seamen employed by the samecompany. Int Marit Health 59(1–4):53–60.

Lucas D, Jegaden D, Lodde B, Arvieux C, Dewitte JD. 2006. Occu-pational asthma in maritime environment. Int Marit Health 57(1–4):177–187.

Neutel CI. 1990. Mortality in fishermen: An unusual age distribution.Br J Ind Med 47(8):528–532.

Oldenburg M, Jensen HJ, Latza U, Baur X. 2009. Seafaring stressorsaboard merchant and passenger ships. Int J Public Health 54(2):96–105.

Oldenburg M, Baur X, Schlaich C. 2010. Occupational risks andchallenges of seafaring. J Occup Health 52(5):249–256.

Pellegrino R, Viegi G, Brusasco V, Crapo RO, Burgos F, Casaburi R,Coates A, van der Grinten CP, Gustafsson P, Hankinson J, Jensen R,Johnson DC, MacIntyre N, McKay R, Miller MR, Navajas D,Pedersen OF, Wanger J. 2005. Interpretative strategies for lung func-tion tests. Eur Respir J 26(5):948–968.

Roberts SE. 2002. Hazardous occupations in Great Britain. Lancet360(9332):543–544.

Roberts SE. 2010. Britain’s most hazardous occupation: Commercialfishing. Accid Anal Prev 42(1):44–49.

Schilling RS. 1966. Trawler fishing: An extreme occupation. Proc RSoc Med 59(5):405–410.

Schilling RS. 1971. Hazards of deep-sea fishing. Br J Ind Med28(1):27–35.

Sherson D, Hansen I, Sigsgaard T. 1989. Occupationally related re-spiratory symptoms in trout-processing workers. Allergy 44(5):336–341.

Shiryaeva O, Aasmoe L, Straume B, Bang BE. 2010. Respiratoryimpairment in Norwegian salmon industry workers: A cross-section-al study. J Occup Environ Med 52(12):1167–1172.

Standardization of Spirometry. 1994. Update. American ThoracicSociety. 1995. Am J Respir Crit Care Med 152(3):1107–1136.

Taylor DR, Pijnenburg MW, Smith AD, De Jongste JC. 2006.Exhaled nitric oxide measurements: Clinical application and inter-pretation. Thorax 61(9):817–827.

Tomaszunas S, Weclawik Z, Lewinski M. 1988. Allergic reac-tions to cuttlefish in deep-sea fishermen. Lancet 1(8594):1116–1117.

Travers J, Marsh S, Aldington S, Williams M, Shirtcliffe P, PritchardA, Weatherall M, Beasley R. 2007. Reference ranges for exhalednitric oxide derived from a random community survey of adults.Am J Respir Crit Care Med 176(3):238–242.

Respiratory Health of Seamen 979