Efstratiou 2001
Efstratiou 2001
425±432, 2001
Ó 2001 Elsevier Science Ltd. All rights reserved
Printed in Great Britain
PII: S0025-326X(00)00225-3 0025-326X/01 $ - see front matter
Viewpoint
Managing Coastal Bathing Water
Quality: The Contribution of
Microbiology and Epidemiology
MARIA A. EFSTRATIOU*
Department of Marine Sciences, University of the Aegean, 5 Sapphous Street, 81 100 Mytilene, Greece
The EU Bathing Water Directive with a life of 25 years water. Concern has been expressed worldwide and is
(EEC, 1976) has contributed signi®cantly to the im- based on the fact that apart from the populations living
provement of the quality of coastal recreational waters permanently along the coast-line, millions of tourists use
throughout Europe and has successfully protected public the sea for recreation. Domestic and foreign tourism are
health. Improvement of the standards of living and general heavily concentrated during the summer months, in
public demands has made it necessary to consider updat- which period the sea constitutes the main recreational
ing it (EU, 1994) introducing important changes in mi- amenity for locals and visitors alike, who occupy them-
crobiological parameters. Measurement of microbial selves in swimming, sea-skiing, windsur®ng and other
pollution is of primary importance to this new proposal, as activities. As a result many beaches, particularly those
is to the regulatory schemes introduced by the very recent located near the largest urban areas, are heavily over-
`Annapolis Protocol' (WHO/US EPA, 1999). This report crowded and the ill implications to public health from
discusses the microbiological aspects of the health-related swimming in polluted waters aect more individuals.
management of bathing seawater in the context of the A number of symptoms of ill health, mainly aecting
scienti®c information available from epidemiological and the gastrointestinal tract, ear, skin, eye and upper re-
microbiological studies. Ó 2001 Elsevier Science Ltd. All spiratory tract have been associated with direct contact
rights reserved. with such waters (Table 1). Diseases spread by the oral-
faecal route and caused by microorganisms shed in the
Keywords: microbiology; epidemiology; marine; pollution; faeces of ill individuals or carriers could be potentially
bathing; quality. contracted by swimming in sewage polluted waters. So
are diseases spread through inhaling or skin contact.
Microorganisms may cause infection by being forced
into breaks of the skin or into ruptures of delicate
Sea Bathing and Health membranes of the ear or nose resulting from the trauma
The association between water and disease has been associated with diving. Symptoms have been reported to
recognized since ancient times. In situations other than include, amongst others, salmonellosis (typhoid and
drinking water or food contaminated by water the main paratyphoid fever), shigellosis (bacillary dysentery),
channel of human exposure to microorganisms is cholera, gastroenteritis, dermatitis, otitis. In the major-
through contact with polluted bathing water or beach ity of cases the complains are mild upsets rather than life
sand. threatening or serious disease.
With increased demands on recreational water re- The existing regulations have brought a marked im-
sources, problems of microbial contamination of surface provement on bathing water quality, in spite of which
waters have become a matter of growing public aware- the approach to the management of microbial hazards
ness and scienti®c concern. Public attention has centred in recreational waters has been criticized as insucient
in recent years on actual and potential adverse health (WHO/US EPA, 1999). The new development in envi-
eects arising from human exposure to recreational ronmental monitoring is predictive approaches based on
prede®ned surveillance models.
Existing legislation and all models of health moni-
*Fax: +30-251-28187. toring of swimming beaches rely to a greater or lesser
E-mail address: [email protected] (M.A. Efstratiou). extent on microbiological standards: on the concentra-
425
Marine Pollution Bulletin
TABLE 1
Human pathogens commonly isolated from coastal recreational waters.a
tions of faecal pollution indicators in the recreational pathogens is a subject currently under serious consid-
water. This paper discusses the microbiological aspects eration (WHO/US EPA, 1999; Papadakis et al., 1997).
of the sanitary quality management of marine recre-
ational waters in the context of the scienti®c information
available from the relative epidemiological and micro- Monitoring Marine Water Quality Through
biological investigations, which are reviewed. Legislation
To minimize the risks involved in the use of polluted
seawater the solutions available are in two directions: (a)
Sources of Microbial Marine Pollution
the establishment of sewage treatment plants and/or
Microbial marine pollution consists of pathogenic, construction of submarine outfall structures taking the
potentially pathogenic and other terrestrial microor- euent out to sea; and (b) the development and en-
ganisms whose normal habitat is not the sea. Waste- forcement of control measures in the form of quality
water discharges reach the immediate coastal zone very criteria aimed at ensuring, as far as possible, that rec-
often untreated. Results of a survey of pollutants from reational marine areas present no health hazard caused
land-based sources in the Mediterranean Sea estimate by microbial pollution. To protect the users of recre-
that about 33% of the liquid municipal waste is dis- ational waters governments and international bodies
charged into the sea in the raw state (UNEP/WHO, establish water quality standards, integral parts of which
1996). Treatment can only partly reduce the numbers of are the permissible bacteriological (and other) densities.
pathogens. Untreated or inadequately treated discharges The presence of indicator microorganisms is indicative
are disposed into the immediate coastal environment of recent pollution as well as of the probable presence of
through point sources of pollution: sewage works, in- pathogenic organisms.
dustrial euents, urban runo (Godfree, 1997). In many Practically all recreational water microbiological cri-
cases this is done directly on the coast. teria and standards currently in use are based entirely on
Non-point sources of marine microbial pollution have concentrations of bacterial indicator organisms in the
also been pinpointed as causes of deterioration of the aected waters as an index of acceptability or otherwise
quality of marine recreational areas. Agricultural land (Table 2). Bacterial indicator concentrations provide a
run-o, livestock wastes, land wash-o after heavy measure of the degree of total faecal pollution, since
rainfall events, bird droppings, rodents, carry a heavy they `indicate' the presence of the latter. Although it is
load of microbiological pollutants in the watercources the pathogenic microorganisms that may cause ill health
they are discharged into, which almost inevitably reach to swimmers, routine examination of recreational sea-
the sea (Jones and Obiri-Danso, 1999; Jenkins, 1997; water or wastewater is con®ned to the indicator bacte-
Weiskel et al., 1996; Wyer et al., 1995; Gales and Baleux, ria. The search for pathogens is impractical because
1992). Rivers add microbiological pollution, mainly isolation techniques are expensive, time consuming and
from sewage discharged upstream. The swimmers have involve relatively complicated procedures that exceed
been known to shed the microorganisms that inhabit the capabilities of many routine laboratories. Water
their skin (Robinton and Mood, 1966) and there is ev- quality management eorts focused for decades in
idence linking adverse health eects to bathers with establishing acceptable concentrations of bacterial
swimming in highly populated beaches (Reid and Por- indicator organisms. In Geldreich's words: The idealistic
ter, 1981). The contribution of bathers themselves as a aim in establishing microbiological standards for recre-
source of pollution of recreational waters by human ational water has been to develop the `magic number' of
426
Volume 42/Number 6/June 2001
TABLE 2
Microbiological quality requirements for bathing waters in 100 ml.a
organisms that will denote no health risk to the people polluted sea water and lay down bacteriological stan-
using the water (Geldreich, 1970). Microbiological (and dards for bathing beaches. Contrary to the Stevenson
physical and chemical) standards determining the survey conclusions, they reported no dierentiation in
acceptable quality of swimming water exist in most disease incidents between bathers and non-bathers. They
countries. The mechanisms of implementing the stan- concluded that: bathing in sewage polluted seawater
dards are not straightforward everywhere, since re- carries only a negligible risk to health, even on beaches
sponsibilities are spread among a number of authorities that are so fouled as to be aesthetically very unsatisfac-
and agencies. tory. That a minimal risk attending such bathing is
probably associated with chance contact with intact ag-
gregates of faecal material that happen to have come from
Epidemiological ± Biological Surveys
infected persons (PHLS, 1959). This has formed the basis
In order to develop microbiological water quality of the British policy towards the problem of monitoring
guidelines and standards for recreational waters the bathing areas to the early 1980s, when driven by Euro-
legislator ideally would base decisions on sound scien- pean Union regulations the British conformed to the
ti®c evidence. Criteria can be established by determining EEC Directive.
either: Since the mid-1970s several new epidemiological
surveys attempted to de®ne the levels of risk following
A. the relationship between the density of the indicators exposure to dierent concentrations of bacteria in
and occurrence of adverse health eects amongst the recreational waters. The investigations were carried out
swimmers; or in various countries: the United States, the United
B. the relationship between density of indicators and Kingdom, Spain, Egypt, Israel, Canada, France, Aus-
presence of pathogenic microorganisms in the water. tralia, Hong Kong, Italy (Table 3). Two of the major
epidemiological studies exhibit a strong correlation
The ®rst of the above relies on epidemiological evidence, between faecal streptococci and disease incidents. The
the second on microbiological analyses. investigation conducted by Cabelli and his co-workers
in the USA between 1972 and 1978 was a large-scale
Epidemiological studies prospective epidemiological study including both ma-
The principal aim of studies into the adverse health rine and freshwater beaches and involving 26 000 sub-
eects of swimming (epidemiological studies) has been jects. The results showed that the best correlation to
to determine what dierence in illness incidence might total gastrointestinal symptoms was obtained with en-
be expected from swimming in waters containing vari- terococci (Cabelli et al., 1982). The 1986 US Environ-
ous degrees of bacterial pollution. The National Tech- mental Protection Agency standards, based on these
nical Advisory Committee to the Federal Water investigations, recommended the use of enterococci for
Pollution Control Administration in the USA, based on the estimation of marine water pollution (US EPA,
the results of an epidemiological survey conducted by 1986).
A.H.Stevenson for the United States Public Health The second study that showed superiority of faecal
Service (Stevenson, 1953), advised on a limit of 200 streptococci over other indicator microorganisms was a
faecal coliforms per 100 ml (Nat. Tech. Adv. Comm., randomized `trial' of an environmental exposure to
1968). At about the same time the Public Health Lab- measure the health eects produced by this exposure,
oratory Service studies in the UK adopted a retrospec- conducted in the UK (Kay et al., 1994). It measured the
tive approach. They conducted an extensive study to eects of bathing on 1216 adults over a period of four
evaluate the contamination of coastal bathing beaches summers. A signi®cant relation between faecal strepto-
by sewage, assess the risk to health of bathing in sewage- cocci concentrations, as measured at chest depth, and
427
Marine Pollution Bulletin
TABLE 3
Epidemiological studies in seawater.a
gastroenteritis was established. Adverse health eects ronment has been to determine the relationship between
were identi®ed when faecal streptococci concentrations these two groups of microorganisms. The necessity of
exceeded 32 per 100 ml. such investigations has been often recognized. Gallacher
This upgrading of faecal streptococci as indicators of and Spino (1968) were emphasizing that: a correlation
recreational water pollution is re¯ected in the recent between levels of total and faecal coliforms and the
proposal for a Council Directive of the European Union probability of isolating pathogens would be enormously
concerning the quality of bathing waters (EU, 1994) valuable in setting reliable bacteriological standards,
which does not include total coliforms in the microbial particularly for recreation and ®shing uses.
parameters. Instead it suggests the use of faecal strep- Literature search indicates that the ®rst large-scale
tococci. research in this ®eld was carried out by the members of
All other important epidemiological surveys in marine the Committee on Bathing Beach Contamination, of the
waters have produced results diering from the above Public Health Laboratory Services of the United King-
(Table 3). The study of Cheung et al. (1990) in Hong dom, in the ®fties (Table 4). In their report (PHLS,
Kong implicated skin complaints as being the most 1959) they describe a progressive increase of Salmonella
common bathing-related symptoms, and concentrations isolation with increase in presumptive coliform counts.
of staphylococci were associated with statistically sig- Grunnet and Brest Nielsen (1969) found an approxi-
ni®cant morbidity amongst bathers. No signi®cant cor- mately rectilinear relationship between the most prob-
relation between morbidity symptoms amongst bathers able number of Escerichia coli and species of Salmonella
and the concentration of one or more speci®c bacterial they isolated from seawater of a gulf in Denmark which
indicator has been reported by most of the research receives wastewater from local industries and a large
teams (Kueh et al., 1995; Torregrossa et al., 1994; town. Research on these lines was carried out by other
Harrington et al., 1993; Von Schirnding et al., 1993; teams and produced similar results (Slanetz et al., 1968;
Borrego et al., 1991; Foulon et al., 1983; PHLS, 1959). Kaper et al., 1979).
In some cases high correlation was found between dis- Based on ®ndings of numerous fresh water and estu-
ease incidents and non-microbial parameters like water arine pollution studies conducted by Health Authorities
turbidity (Kueh et al., 1995). In most cases it was re- in the US Geldreich (1970) had concluded that 200
ported that bathers experience signi®cantly more illness faecal coliforms per 100 ml is the limit above which a
incidents than non-bathers (Fleisher et al., 1996b; Kueh sharp increase in the frequency of Salmonella detection
et al., 1995; Balarajan et al., 1991; Harrington et al., incidents is expected. Consequently in 1976 the Envi-
1993; Von Schirnding et al., 1993; Torregrossa et al., ronmental Protection Agency of the USA, in the `Cri-
1994; Corbett et al., 1993; Borrego et al., 1991; Foulon teria for Water Quality' it published, based its proposal
et al., 1983; Cabelli et al., 1982; Stevenson, 1953). for 200 faecal coliforms per 100 ml on a rationale based
on the Geldreich publication (US EPA, 1976).
Microbiological studies Further eorts were made to access the eciency of
The principal aim of studies enumerating bacterial total coliforms, faecal coliforms, faecal streptococci as
indicators and human pathogens in the marine envi- indicators of sewage pollution in marine waters by
428
Volume 42/Number 6/June 2001
TABLE 4
Microbiological studies in sea and estuarine water.a
Author and Date Country Water Indicators examined Pathogens examined Indicator/pathogen
correlating
correlating their densities with the presence of Salmo- dictors of the presence of Salmonella and S. aureus,
nella and other pathogens (Table 4). In the Mediterra- faecal coliforms better predicting C. albicans, in mod-
nean Sea Papadakis et al. (1988) recorded, in coastal erately polluted areas. The conclusion was reached that
areas of moderate pollution in Greece, better correla- enumeration of total coliforms is sucient to predict the
tions of the coliform group with Salmonella isolation, presence of Salmonella spp and S. aureus in seawater
compared with the other indicators. Mori~ nigo et al. moderately aected by sewage pollution.
(1990) correlated Salmonella detection percentages to
total coliforms, faecal coliforms, faecal streptococci,
Clostridium perfringens and coliphages in seawater o a
Criticism to Both Approaches
coast in Spain in¯uenced by submarine outfall dis- Drawing conclusions concerning the quality of rec-
charges. Faecal coliforms and C. perfringens were the reational waters based on the ®ndings of epidemiologi-
most closely related to Salmonella spp. Borrego et al. cal studies has been strongly criticized by the scienti®c
(1991) found that in polluted marine areas faecal coli- community over the years.
forms, faecal streptococci and coliphages correlated well Some of the usual problems in conducting epidemio-
with Pseudomonas aeruginosa, Aeromonas hydrophila logical studies are that: the enumeration of bacterial
and Candida albicans. Yoshpe-Purer and Golderman indicators was not always systematic and it did not al-
(1987) showed that total and faecal coliforms correlated ways refer speci®cally to the water the bathers swam in,
well with the presence of P. aeruginosa in bathing bea- but generally to the swimming beach; that measuring of
ß and Krstulovicß (1994) described a moderate
ches. Solic indicators during the period of swimming of an indi-
positive relationship between the three indicators and vidual has shown that the bacterial levels can vary from
the pathogen Staphylococcus aureus in Croatia. Hoi et al. one sampling to the next, even if taken within a very
(1998) demonstrated signi®cant correlation between the small lapse of time or from dierent sampling points at
occurrence of coliform bacteria and faecal streptococci the same time; that most studies did not account for
on the one hand and Vibrio vulni®cus on the other. infection parameters evolving from sources of infection
The ability of indicators to predict the presence of excluding the water like food, sunbathing, etc. (Fleisher
pathogens has been discussed: Polo et al. (1996) ob- et al., 1993). The two epidemiological studies showing
served that the three indicators in the existing standards superiority of streptococci over the other indicators were
of the EEC Directive generally predict the presence of conducted in the USA and the UK where the factors
Salmonella in fresh water reservoirs and in the seawater. aecting the survival of terrestrial microorganisms in the
Efstratiou et al. (1998) assessed the value of total coli- marine environment namely UV radiation, salinity,
forms, faecal coliforms and faecal streptococci in pre- temperature, eutrophication, are dierent than those in
dicting the presence of Salmonella, S. aureus and C. seas, like the Mediterranean, where exposure to sea-
albicans in sewage polluted seawater. Regression anal- water (therefore to pathogens if present) via swimming
ysis demonstrated superiority of total coliforms as pre- and sea sports is practiced for longer periods of time.
429
Marine Pollution Bulletin
Many epidemiological surveys were carried out in Kay et al., 1994; Pike, 1993; Cabelli et al., 1982). Lit-
estuarine (not marine) water. The vast variation in the erature is sadly poor on the topic of associating disease
resistance or immunity to pathogenic microorganisms incidence or indicator densities to viral or phage density.
among the population e.g., locals vs tourists, young vs
older, healthy vs immunocompromised, etc., make it
impossible to calculate accurately the eects of swim- Conclusions
ming in polluted waters. The epidemiological studies Central problem in many environmental matters is
have also been repeatedly criticized for methodological that they trespass traditional scienti®c and academic
and statistical ¯aws (Fleisher, 1990; Kay et al., 1994). borders. Recreational water quality management is a
But above all the epidemiological surveys correlating characteristic example. Most of the early attempts to
disease incidents among bathers to indicator densities de®ne the problem and present solutions are based only
have been found to be not replicable. The ®nding that on one scienti®c point of view. Yet the science impli-
appears consistently in these studies is that there is a cated in the rational management of bathing waters
higher risk of contracting disease in bathers than in non- stretches to various disciplines. Microbiologists, physi-
bathers (Fleisher et al., 1996a,b; Kueh et al., 1995; cians, engineers, legislators are seeking meaningful cri-
Torregrossa et al., 1994; Harrington et al., 1993; Von teria or standards to determine the sanitary quality and
Schirnding et al., 1993; Corbett et al., 1993; Balarajan public health hazard of sewage polluted recreational and
et al., 1991; Borrego et al., 1991; Foulon et al., 1983; shell®sh growing areas. Important scienti®c questions
Cabelli et al., 1982; Stevenson, 1953). remain unanswered and so do consequent practical
On the other hand drawing conclusions concerning problems in planning and implementing policies (EU,
the quality of bathing waters based on microbiological 1997).
criteria, that is on the correlation between indicators and The investigations of Stevenson, the Public Health
pathogenic microorganisms, has its drawbacks. The Laboratory Service of the UK, of Geldreich and of
practice of using guidelines and standards based on in- Cabelli have profoundly eected policy on both sides of
dicator concentrations is based on the assumption that the Atlantic. The European Community Directive con-
under average conditions of illness in the urban popu- cerning the quality of bathing waters (EEC, 1976) has
lation producing the sewage the ratio indicator-patho- already had a life of 25 years and it has been felt that it
gen in the wastewater and receiving waters is relatively ought to be updated. The recent proposal for a new
constant. Such relationships can be satisfactory for European Union Council Directive suggests changes in
waters receiving the discharges from large urban areas. the indicator system used, based on the results of epi-
When smaller number of individuals contribute the demiological surveys. At the same time the latest mi-
faecal wastes the indicator-pathogen ratio will ¯uctuate. crobiological research indicates that the bacteria
Where the population producing the wastes is very small presently used for the monitoring of coastal recreational
the ratio will vary tremendously, depending on the good areas in the countries of the European Union predict in
or otherwise health of even one individual. Therefore a satisfactory manner the presence of some of the most
routine examination for indicator microorganisms of common pathogens in the seawater.
waters receiving faecal pollution from few individuals is Today a massive change of direction is witnessed from
of little value. current regulatory schemes in favour of the concepts of
For dierent reasons many researchers have com- the WHO/US EPA (1999) `Annapolis protocol'. This is
municated their belief that the currently used indicators, the development of a more sophisticated approach that
or some of them, are insucient for the measurement of re¯ects health risk and provides enhanced scope for ef-
the public health dangers imposed by the use of recre- fective management intervention by classifying beaches
ational water contaminated by pathogens. Particular to a ®ve-stage grading scheme. Much interest centres on
attention was given to the use of coliforms as indicators the microbiological standards that might be applied in
of the sanitary quality of marine waters and the coliform future regulations. Under this new regime, and in order
index has received continual criticism due to the non- to make the primary classi®cation of beaches, water
speci®city of this group of indicators of pollution. It has sampling and use of indicator organisms as a measure of
also been argued that, although indicators are always microbial contamination is to be continued for the
detected in sewage-polluted receiving waters, pathogens bene®t of providing a background picture of average
appear only if a portion of the population is ill and that water quality and pollution impact. Selection of indi-
it is conceptually unsound to expect a uniform rela- cators and their permissible density could rely not only
tionship between a faecal indicator and a pathogen that on epidemiological evidence but on the indicator ability
it is not extremely prevalent in the population at large. to predict the presence of bacterial, viral, etc. pathogens,
Additionally more insight is called for in the area of which will, after all, if present cause the ill health eects
correlating numbers of indicators to the presence of vi- to the users of the swimming waters.
ruses. Gastrointestinal infections of viral origin have
been repeatedly considered the principal hazards in Thanks are due to Dr G. Kamizoulis, Senior Scientist, WHO/EURO
sewage polluted bathing waters (Fleisher et al., 1996a; Project oce, UNEP, Athens, Greece for useful comments.
430
Volume 42/Number 6/June 2001
Balarajan, R., Soni Raleigh, V., Yuen, P., Wheeler, D., Machin, D. Godfree, A. F. (1997) Point source discharges to bathing waters. In
and Cartwright, R. (1991) Health risks associated with bathing in Technical Feasibility of an a Priori Measurement Approach for
seawater. British Medical Journal 303, 1444±1445. Managing Bathing Water Quality. Report of a Workshop held in
Borrego, J. J., Romero, P. and Marino, F. (1991) Epidemiological Sitges (Spain) 26±29 April 1997, European Commission Measure-
study of bathers from selected beaches in Malaga. UNEP/WHO: ment and Testing Programme, EUR 17801 EN.
Epidemiological Studies Related to Environmental Quality Criteria Godfree, A. F., Kay, D. and Wyer, M. D. (1997) Faecal streptococci as
for Bathing Waters, Shell®sh-Growing Waters and Edible Marine indicators of faecal contamination in water. Journal of Applied
Organisms (Activity D). MAP Technical Reports Series No 53. Microbiology Symposium Supplement 1997 83, 110S±119S.
United Nations Environment Programme, Athens. Grunnet, K. and Brest Nielsen, B. (1969) Salmonella types isolated
Cabelli, V. J., Dufour, A. P., McCabe, L. J. and Levin, M.A. (1982) from the Gulf of Aarhus compared with types from infected human
Swimming-associated gastroenteritis and water quality. American beings, animals, and feed products in Denmark. Applied Microbi-
Journal of Epidemiology 115, 606±616. ology 18, 985±990.
Cheung, W. H. S., Hung, R. P. S., Chang, K. C. K. and Kleevens, J. Harrington, J. F., Wilcox, D. N., Giles, P. S., Ashbolt, N. J., Evans, J.
W. L. (1990) Epidemiological study of beach water pollution and C. and Kirton, H. C. (1993) The health of Sidney surfers: an
health-related bathing water standards in Hong Kong. Water epidemiological study. Water Science and Technology 27, 175±181.
Science and Technology 23, 243±252. Hoi, L., Larsen, J.L., Dalsgaard, I. and Dalsgaard, A. (1998)
Corbett, S. J., Rubin, G. L., Curry, G. K. and Kleinboum, D. G. Occurrence of Vibrio vulni®cus biotypes in Danish marine environ-
(1993) The health eects of swimming at Sidney beaches. American ments. Applied and Environmental Micribiology 64, 7±13.
Journal of Public Health 83, 1701±1706. Jenkins, A. (1997) A catchment based modelling scheme for prediction
EEC (1976) Council Directive of 8 December 1975 concerning the of bacterial water quality and hazard assessment. In Technical
quality of bathing water (76/160/EEC). Ocial Journal of the Feasibility of an a Priori Measurement Approach for Managing
European Communities L/031, 1±7. Bathing Water Quality. Report of a Workshop held in Sitges (Spain)
El Sharkawi, F. and Hassan, M. N. E. R. (1982) The relation between 26±29 April 1997, European Commission Measurement and Testing
the state of pollution in Alexandria swimming beaches and the Programme, EUR 17801 EN.
occurrence of typhoid among bathers. Bulletin of the High Institute Jones, K. and Obiri-Danso, K. (1999) Non-compliance of beaches with
of Public Health Alexandria 12, 337±351. the EU directives of bathing water quality: evidence of non-point
EU (1997) Technical Feasibility of an a Priori Measurement Approach sources of pollution in Morecambe Bay. Journal of Applied
for Managing Bathing Water Quality. Report of a Workshop held in Microbiology Symposium Supplement 85, 101S±107S.
Sitges (Spain) 26±29 April 1997, European Commission Measure- Kaper, J., Lockman, H., Colwell, R. R. and Joseph, S. W. (1979) Ecology,
ment and Testing Programme, EUR17801EN. serology, and enterotoxin production of Vibrio cholerae in Chesa-
EU (1994) Proposal for a Council Directive concerning the quality of peake Bay. Applied and Environmental Microbiology 37, 91±103.
bathing water. Document COM(94)36 ®nal. Commission of the Kay, D., Fleisher, J. M., Salmon, R. L., Jones, F., Wyer, M. D.,
European Communities. Godfree, A. F., Zelenauch-Jacquotte, Z. and Shore, R. (1994)
Efstratiou, M. A., Mavridou, A., Richardson, S. C. and Papadakis, J. Predicting likelihood of gastroenteritis from sea bathing: results
A. (1998) Correlation of bacterial indicator organisms with Salmo- from randomised exposure. The Lancet 344, 905±909.
nella spp, Staphylococcus aureus and Candida albicans in seawater. Kueh, C. S. W., Tam, T. Y., Lee, T., Wong, S. L., Lloyd, O. L., Yu, I.
Letters in Applied Microbiology 26, 342±346. T. S., Wong, T. W., Tam, J. S. and Bassett, D. C. J. (1995)
Fattal, B., Peleg-Olevsky, T., Agurshy, T. and Shuval, H. I. (1986) The Epidemiological study of swimming associated illness relating to
association between sea-water pollution as measured by bacterial bathing beach water quality. Water Science and Technology 31, 1±4.
indicators and morbidity of bathers at Mediterranean beaches in Larsen, J. L. and Willeberg, P. (1984) The impact of terrestrial and
Israel. Chemosphere 16, 565±570. estuarial factors on the density of environmental bacteria (Vibri-
Fewtrell, L. and Jones, F. (1992) Microbiological aspects and possible onaceae) and faecal coliforms in coastal water. Zentralblatt
health risks of recreational water pollution. In Recreational Water Bacteriologie und Hygiene I. Abt. Orig. 179, 308±323.
Quality Management, vol. 1: Coastal Waters, ed. D. Kay. Ellis Mori~ nigo, M. A., Cornax, R., Mu~ noz, M. A., Romero, P. and
Horwood Ltd., London. Borrego, J. J. (1990) Relationships between Salmonella spp and
Fleisher, J. M. (1990) The eects of measurement error on previously indicator microorganisms in polluted natural waters. Water Re-
reported mathematical relationships between indicator organism search 24, 117±120.
density and swimming associated illness: a quantitative estimate of Mujeriego, R., Bravo, J. M. and Feliu, M. T. (1982) Recreation on
the resulting bias. International Journal of Epidemiology 19, 1100± coastal waters: public health implications. VIth Workshop on
1106. Pollution of the Mediterranean, International Commission for the
Fleisher, J. M., Kay, D., Wyer, M. and Merrett, H. (1996a) The Scienti®c Exploration of the Mediterranean Sea. 2±4 December,
enterovirus test in the assessment of recreational water-associated Cannes, pp. 585±594.
gastroenteritis. Water Research 30, 2341±2346. Nat. Tech. Adv. Comm. (1968) Water Quality Criteria. National
Fleisher, J. M., Kay, D., Salmon, R. L., Jones, F., Wyer, M. D. Technical Advisory Committee. Federal Water Pollution Control
and Godfree, A. F. (1996b) Marine waters contaminated with Administration, Dep. Interior, Washington DC.
domestic sewage: Non-enteric illness associated with bather expo- Papadakis, J., Mavridou, A., Richardson, S. C., Lambiri, M. and
sure in the United Kingdom. American Journal of Public Health 86, Marcelou, U. (1997) Bather-related microbial and yeast populations
1228±1234. in sand and seawater. Water Research 31, 799±804.
Fleisher, J. M., Jones, F., Kay, D., Stanwell-Smith, R., Wyer, M. and Papadakis, J. A., Mavridou, A., Richardson, S. C., Lambiri, M. and
Morano, R. (1993) Water and non-water related risk factors for Velonakis, E. (1988) Relations between densities of indicator
gastroenteritis among bathers exposed to sewage-contaminated organisms and microbial pathogens in seawater. Rapports, Com-
marine waters. International Journal of Epidemiology 22, 698±708. mission Internationale pour l'Exploration Scienti®que de la Mer
Foulon, G., Maurin, J., Nguyen-Noge, Q. and Martin-Bower, G. Mediterranee 31, (2) M-II9, p. 177.
(1983) Relationship between the microbiological quality of bathing PHLS (1959) Sewage contamination of coastal bathing waters in
water and health eects. Revue Francaise des Sciences de l'Eau 2, England and Wales. The committee on bathing beach contamina-
127. tion of the Public Health Laboratory Service. Journal of Hygiene,
Gallacher, T. P. and Spino, D. F. (1968) The signi®cance of numbers Cambridge 57, 435±472.
of coliform bacteria as an indicator of enteric pathogens. Water Pike, E. B. (1993) Recreational use of coastal waters: development of
Research 2, 169±175. health-related standards. Journal of the Institute of Water and
Gales, P. and Baleux, B. (1992) In¯uence of the drainage basin input Environmental Management 7, 162±169.
on a pathogenic bacteria (Salmonella) contamination of a Mediter- Polo, F., Figueras, M. J., Inza, I., Sala, J. and Guarro, J. (1996) Do
ranean lagoon (the Thau Lagoon France) and the survival of this indicator organisms predict the presence of Salmonella? In Pro-
bacteria in brackish water. Water Science and Technology 25, 105± ceedings of the 1996 Symposium on Health-Related Water Microbi-
114. ology. IAWQ, 6±10 October Mallorca, A54, p. 112.
Geldreich, E. E. (1970) Applying bacteriological parameters to Reid, T. M. S. and Porter, I. A. (1981) An outbreak of otitis externa in
recreational water quality. Journal of the American Water Works competitive swimmers due to Pseudomonas aeruginosa. Journal of
Association 62, 113±120. Hygiene, Cambridge 86, 352±362.
431
Marine Pollution Bulletin
Robertson, W. J. and Tobin, R. S. (1983) The relationship between Oce of Water Regulations and Standards Division. Washington
three potential pathogens and pollution indicator organisms in DC.
Nova Scotian coastal waters. Canadian Journal of Microbiology 29, US EPA (1976) United States Environmental Protection Agency.
1261±1269. Quality Criteria for Water 42, US EPA, Washington DC.
Robinton, E. D. and Mood, E. W. (1966) A quantitative and Von Schirnding, Y. E. R., Strauss, N., Robertson, P., K®r, R., Fattal,
qualitative appraisal of microbial pollution of water by swimmers: B., Mathee, A., Franck, M. and Cabelli, V. J. (1993) Bather
a preliminary report. Journal of Hygiene, Cambridge 64, 489±499. morbidity from recreational exposure to seawater. Water Science
Slanetz, L. W., Bartley, C. H. and Stanley, K. W. (1968) Coliforms, and Technology 27, 183±186.
Fecal Streptococci and Salmonella in seawater and shell®sh. Health Weiskel, P. K., Howes, B. L. and Heufelder, G. R. (1996) Coliform
and Laboratory Sciences 28, 66±78. contamination of a coastal embayment: sources and transport
ß, M. and Krstulovicß, N. (1994) Presence and survival of
Solic pathways. Environmental Science and Technology 30, 1872±1881.
Staphylococcus aureus in the coastal area of Split (Adriatic Sea). WHO/US EPA (1999) Health-Based Monitoring of Recreational
Marine Pollution Bulletin 28, 696±700. Waters: the feasibility of a new approach (the Annapolis Protocol)
Stevenson, A. H. (1953) Studies of bathing water quality and health. WHO/SDE/WSH/99.1, Geneva.
Journal of the American Public Health Association 43, 529±538. Wyer, M. D., Kay, D., Jackson, G. F., Dawson, H. M., Yeo, J. and
Torregrossa, M. V., Valentino, L. and Saliba, L. J. (1994) Coastal Tanguy, L. (1995) Indicator organism sources and coastal water
recreational water quality and human health. Travel Medicine quality: a catchment study on he Island of Jersey. Journal of Applied
International 12, 225±229. Bacteriology 78, 290±296.
UNEP/WHO (1996) Survey of Pollutants from Land-Based Sources in Yoshpe-Purer, Y. and Golderman, S. (1987) Occurrence of Staphylo-
the Mediterranean Sea. MAP Technical Reports Series No. 109. coccus aureus and Pseudomonas aeruginosa in Israeli coastal water.
United Nations Environment Programme, Athens. Applied and Environmental Microbiology 53, 1138±1141.
US EPA (1986) United States Environmental Protection Agency.
Ambient Water Quality Criteria for Bacteria-1986. EPA440/5-84-02.
432