References and further reading
The following documents are ordered alphabetically by author, then by date, with accompanying commentary.
A librarian can easily obtain most of the items in this list. For those more difficult to access, supplemental information is given on their availability.
Abbott S, Caughley B, Scott G. 1998. Evaluation of Enterolert®
for the enumeration of enterococci in the marine environment. New
Zealand Journal of Marine and Freshwater Research 32: 505–13.
Reports comparative evaluation of Enterolert® versus membrane filtration
on 343 marine samples from the Wellington area. Found sensitivity of
99.8% and specificity of 97% (2.4% false positives and 0.3% false negatives).
Alexander LM, Heaven A, Morris R. 1992. Symptomatology of children
in contact with sea water contaminated with sewage. Journal
of Epidemiology and Community Health 46: 340–4.
A prospective study of parents of children between 6 and 11 years was
conducted at Blackpool beach (UK) in 1990, resulting in 703 cases of
matched data. Concluded that “children who came into contact with
contaminated sea water are likely to develop symptoms as a result”.
Anderson SA, Turner SJ, Lewis GD. 1997. Enterococci in the New Zealand
environment: implications for water quality monitoring. Water
Science and Technology 35(11–12): 325–31.
A considerable part of the enterococci load in urban and rural catchments
and waterways (typically 102–103 cfu/100 mL) comes from non-human
sources. They may multiply within some non-faecal environments (e.g.
on degrading seaweed).
Ashbolt NJ, Grohmann GS, Kueh CSW. 1993. Significance of specific
bacterial pathogens in the assessment of polluted receiving waters of
Sydney, Australia. Water Science and Technology
27(3–4): 449–52.
Primary sewage released from Sydney’s ocean outfalls and tertiary
chlorinated sewage discharged to rivers were studied for two years.
Diverting the ocean discharge from a cliff-edge release to deepwater
ocean release 3 km offshore resulted in significant reductions of bacteria
in water, but not in near-shore sediments. Campylobacters
were found in rivers but not in effluents or seawater, being associated
with rural land.
Balarajan R, Soni Raleigh V, Yuen P, Wheeler D, Machin D, Cartwright
R. 1989. Health risks associated with bathing in sea water. British
Medical Journal 303: 1444–5.
Reports a three-week prospective cohort study at Ramsgate Beach (Kent,
UK) using 1,883 persons, including 839 non-bathers as a control. The
waters occasionally failed EC standards (but this is not quantified).
Relative risk of gastrointestinal symptoms (age- and gender-adjusted)
was elevated among the bathers (i.e. swimmers and waders). Relative
risks of eye/ear/nose/throat and respiratory illness among surfers and
divers were statistically significant.
Bandaranayake DR, Salmond CE, Cooper AB, McBride GB, Lewis GD, Hatton
C, Turner SJ, Till DG. 1993. Health Effects from
Sea Bathing: A report on the preliminary study carried out at two Auckland
beaches over the 1992/93 summer. Ministry for the Environment,
Wellington.
Reports on the New Zealand 1992/93 preliminary trials. Includes the
paper, the questionnaire, and a sample size calculation (power analysis)
for the planned final study.
Barron RC, Murphy F, Greenberg HB, Davis CE, Bregman DJ, Gary GW,
Hughes JM, Schonberger LB. 1982. Norwalk gastrointestinal illness: an
outbreak associated with swimming in a recreational lake and secondary
person-to-person transmission. American Journal
of Epidemiology 115(2): 163–72.
Incubation period for 121 first-in-their-household persons becoming
ill at a Michigan recreational park was 4–77 hours. A history
of swimming in the park’s lake was elicited with significantly
greater frequency of illness compared to those who did not swim (odds
ratio 4.8, 95% CI = 1.8–12.7). Serological studies identified
Norwalk virus as the aetiological agent. Water appeared to meet current
bacterial guidelines.
Baylor ER, Baylor MB, Blanchard DC, Syzdek LD, Appel C. 1977. Virus
transfer from surf to wind. Science 198:
575–80.
Documents this mode of pathogen transfer.
Brieseman MA. 1987. Town water supply as the cause of an outbreak
of Campylobacter infection. New
Zealand Medical Journal 100: 212–13.
An outbreak of 19 cases in Ashburton was attributed to the local water
supply being contaminated after heavy rain during a period in which
water treatment was temporarily not operating.
Brown JM, Campbell EA, Rickards AD, Wheeler D. 1987. Sewage pollution
of bathing water. The Lancet (21 November):
1208–9.
Reports a Greenpeace study on two southern England resorts, one polluted
the other not, interviewing 190 people. Found that “bathers who
immersed their heads in seawater polluted by sewage were more likely
to complain of gastrointestinal symptoms than those who did not immerse
their heads or those who bathed at a non-polluted resort”.
Bryan JA, Lehmann JD, Setiady IF, Hatch MH. 1974. An outbreak of Hepatitis-A
associated with recreational lake water. American
Journal of Epidemiology 99(2): 145–54.
In a 15-day period in September 1969, 14 cases of viral hepatitis-A
developed in members of a boy scout troop who had been camping on an
island in a lake recreation area about four weeks earlier. Exposure
to contaminated lake water was indicated.
Cabelli VJ, Levin MA, Dufour AP, McCabe LJ. 1975. The development
of criteria for recreational waters. In: ALH Gameson (ed). Discharge
of Sewage from Sea Outfalls. Oxford and New York, Pergamon Press,
63–73.
Foreshadows the full trials reported in Cabelli (1983a). Explains how
the design was aimed at improving perceived shortcomings in the 1940s
study reported by Stevenson (1953), including: ‘swimming’
to require head-immersion, multiple exposures to be avoided, non-bather
controls to be beach attenders, include more candidate indicators. Notes
that studies need to be large enough to obtain “significant results”.
Cabelli VJ. 1977. Indicators of recreational water quality. In: AW
Hoadley and BJ Dukta (eds) Bacterial Indicators/Health
Hazards Associated with Water. ASTM STP 635, American Society
for Testing and Materials, Washington: 222–38.
An early review of Cabelli’s approach. Points to the need to develop
a scientific basis for standards applicable to waters containing faecal
wastes of lower animals (from waterfowl, wild animals, farm run-off
and urban stormwater). Reports results from New York component of the
full study reported by Cabelli (1983a).
Cabelli VJ. 1978. New standards for enteric bacteria. In: R Mitchell
(ed) Water Pollution Microbiology, Vol 2.
Wiley, New York: 233–71.
Covers risk assessment, drinking water, swimming pool water, recreational
waters and shellfish-growing waters. Reviews each area up to the mid-1970s.
Cabelli VJ. 1979. Evaluation of recreational water quality, the EPA
approach. In: A James and L Evison (eds) Biological
Indicators of Water Quality. Wiley, Chichester, 14-1–14-23.
Discusses EPA’s use of “criteria”, “guidelines”
and “standards”: a criterion is a relationship (e.g. between
indicator density and illness risk); a guideline is a suggested upper
limit, derived from the criterion; and a standard is a guideline with
the force of law. The beach studies underway were designed to provide
criteria.
Cabelli VJ, Dufour AP, Levin MA, McCabe LJ, Haberman PW. 1979. Relationship
of microbiological indicators to health effects at marine bathing beaches.
American Journal of Public Health 69(7):
690–6.
Reports results of second year for the New York part of the full study
reported by Cabelli (1983a).
Cabelli VJ, Dufour AP, McCabe LJ, Levin MA. 1982. Swimming-associated
gastroenteritis and water quality. American Journal
of Epidemiology 115: 606–16.
Reports main results of Cabelli (1983a). Concludes that “swimming
in even marginally polluted marine bathing water is a significant route
of transmission for the observed gastroenteritis”.
Cabelli VJ. 1983a. Health Effects Criteria for
Marine Recreational Waters. Report EPA 600/1-80-031, USEPA Cincinnati,
OH (first published 1980). NTIS access #: PB 83-259994.
Major prospective epidemiological study at coastal beaches in New York
and Boston, and a brackish beach at Lake Ponchartrain (Louisiana), involving
26,686 persons. Beaches were impacted by (mostly) chlorinated effluents.
Most notable result was a relationship between swimming-associated illness
risk and (the logarithm of) enterococci concentration. The illness was
HCGI (highly credible gastro-intestinal illness, essentially vomiting
or GI accompanied by fever). Analysis methods used data grouping followed
by linear regression, rather than the more modern “generalized
linear models” (e.g. logistic regression); appropriate software
was not then available. Also includes a 1976–78 study in Alexandria,
Egypt. Some beaches were very polluted (enterococci up to 104 per 100
mL). Egyptian participants included 12,532 locals and 10,707 visitors
(from Cairo). Only E. coli and enterococci
were measured, both showing strong associations with highly credible
gastrointestinal illness. For equivalent enterococci concentrations
illness risks were lower than found in the US studies, attributed to
local immunity (Cairo visitors appeared to be less immune). Four cases
of typhoid were found among swimmers at the polluted beach.
Cabelli VJ. 1983b. Public health and water quality significance of
viral diseases transmitted by drinking water and recreational water.
Water Science & Technology 15(5):1–15.
Presents predictions of gastrointestinal illness at beaches using the
relationships derived in Cabelli (1983a). Notes the inapplicability
of the model to beaches with small immediate waste sources, and local
outbreaks.
Cabelli VJ, Dufour AP, McCabe LJ, Levin MA. 1983. A marine recreational
water quality criterion consistent with indicator concepts and risk
analysis. Journal of the Water Pollution Control
Federation 55: 1306–14.
Presents the health effects enterococci indicator relationship derived
in Cabelli (1983a). Companion paper to Cabelli et al (1982).
Cabelli VJ. 1989. Swimming-associated illness and recreational water
quality criteria. Water Science and Technology
21(2): 13–21.
Presents the application of results in Cabelli (1983a) by USEPA (1986b).
Contains an error in the intercept term (‘0.02’ in Table
E1 should be ‘0.2’). States the expectation that contamination
of water with faecal wastes from lower animals would carry a much lower
risk of illness than from humans.
Calderon RL, Mood EW. 1982. An epidemiological assessment of water
quality and ‘swimmer’s ear’. Archives
of Environmental Health 37(5): 300–5.
A retrospective study of otitis externa in 1980 on 29 cases and controls
finding that swimming and length of time spent in the water were associated
positively with cases of otitis externa. No significant correlation
of the illness with water quality was found (faecal coliforms, enterococci,
Pseudomonas aeruginosa).
Calderon RL, Mood EW, Dufour AP. 1991. Health effects of swimmers
and nonpoint sources of contaminated water. International
Journal of Environmental Health Research 1: 21–31.
Reports a diary illness study of users of freshwater ponds impacted
only by animal wastes. Gastrointestinal illness was related to the number
of swimmers and to staphylococcal counts. “Swimmer illness was
not associated with high densities of common faecal indicator bacteria
...”.
Carrie MS. 1973. Coliforms and water quality legislation. Soil
and Water 10(2): 20–3.
Gives some explanation of how the standards in the 1971 Water and Soil
Conservation Amendment Act (No. 2) came to pass.
Cheung WHS, Chang KCK, Hung RPS, Kleevens JWL. 1990. Health effects
of beach water pollution in Hong Kong. Epidemiology
and Infection 105: 139–62.
Reports on a 1987 prospective study at nine Hong Kong beaches using
18,741 useable responses. E. coli was
found to be the best indicator of health effects (gastrointesteritis
and skin symptom rates) among swimmers. Overall symptom rates for gastrointestinal,
ear, eye, skin, respiratory, fever and total illness was (statistically)
significantly higher for swimmers than for non-swimmers. Low gastrointestinal
illness rates were observed at the two beaches impacted by animal wastes.
Concludes that illness associated with swimming is a public health problem
in Hong Kong. While this study reported low gastro-intestinal swimming-associated
rates at the two beaches influenced by livestock (pig) wastes, respiratory
illness and skin infections rates were elevated such that the total
illness rate was very similar to the other beaches.
Cheung WHS, Chang KCK, Hung RPS. 1991. Variations in microbial indicator
densities in beach waters and health-related assessment of bathing water
quality. Epidemiology and Infection 106:
329–44.
Describes daily and hourly variations in microbial indicators. E.
coli was influenced by tide, by staphylococci and by the number
of bathers. Average staphylococci: E. coli
ratio was 0.04:3. Staphylococci serve as an indicator of bather density
and risk of cross-contamination between bathers. Recommends weekend
sampling for compliance assessment.
Chung H, Jaykus L-A, Lovelace G, Sobsey MD. 1998. Bacteriophages and
bacteria as indicators of enteric viruses in oysters and their harvest
waters. Water Science and Technology 38(12):
37–44.
Concentrations of male-specific (F+) coliphages, Bacteroides
fragilis phages, Salmonella phages
and several indicator bacteria in wastewater, estuarine receiving water
and its oysters were examined at 2–4-week intervals for 14 months.
The levels of most indicators were higher in oysters and water when
oysters were virus-positive. F+ coliphages and C.
perfringens were the only indicators significantly associated
with the presence of enteric viruses in oysters.
Conover WJ. 1980. Practical Nonparametric Statistics.
2nd ed. Wiley, New York.
The best introduction to this class of methods, whereby data ranks are
used in place of their actual magnitudes (e.g. medians and percentiles).
Corbett SJ, Rubin GL, Curry GK, Kleinbaum DG, et al 1993. The health
effects of swimming at Sydney beaches. American
Journal of Public Health 83(12): 1701–6.
Reports follow-up study of 2,839 beach-goers in 1989/90; 683 reported
experiencing symptoms in the 10 days following initial interview, of
whom 435 reported respiratory symptoms. A linear relationship between
water pollution and all reported symptoms (except gastrointestinal)
was shown.
Cornax R, Morinigo MA, Balebona C, Castro D, Borrego JJ. 1991. Significance
of several bacteriophage groups as indicators of sewage pollution in
marine waters. Water Research 25: 673–8.
From a two-beach study this documents a poor correlation between FRNA
phages and pathogen occurrence and persistence. Concludes that faecal
streptococci and E. coli “C bacteriophages” are the most
appropriate indicators of remote pollution in marine waters.
Dadswell JV. 1993. Microbiological quality of coastal water and its
health effects. International Journal of Environmental
Health Research 3: 32–46.
Reviews health-related marine microbiology, both natural and pollution-related
organisms.
D’Alessio D, Minot TE, Allen CI, Tsiatis AA, Nelson DB. 1981.
A study of the proportions of swimmers among well controls and children
with enterovirus-like illness shedding or not shedding an enterovirus.
American Journal of Epidemiology 113(5):
533–41.
A retrospective study of children visiting a paediatric clinic in Madison,
Wisconsin, in 1977: 679 well children and 296 with enteroviral-like
symptoms. Exclusive beach swimmers had significantly (p < 0.0005)
relative risk (odds ratio estimate 3.41) of enterovirus illness. The
highest relative risk (10.63) of enterovirus illness occurred in children
less than four years old who were exclusive beach swimmers.
Davies-Colley RJ, Bell RG, Donnison AM. 1994. Sunlight inactivation
of enterococci and fecal coliforms in sewage effluent diluted in seawater.
Applied and Environmental Microbiology 60:
2049–58.
Two parameters are required to describe the inactivation (loss of culturability):
a shoulder constant and a rate constant. Depth-dependent inactivation
rate for both indicators matched the attenuation profile of UV-A radiation
at about 360 nm (attributable to inactivation maxima in the 318–340
and > 400 nm ranges, Sinton et al 1994). Inactivation by UV-B (290–320
nm, which penetrates less into seawater) is of lesser importance.
Davies-Colley RJ, Donnison AM, Speed DJ. 1997. Sunlight wavelengths
inactivating faecal indicator micro-organisms in waste stabilisation
ponds. Water Science and Technology 35(11–12):
219–25.
UVB, UVA and blue-green (< 550 nm) radiation all contributed to inactivation
of enterococci and (possibly) FRNA phage, consistent with a photo-oxidation
mechanism. In contrast, E. coli and
(possibly) FDNA phage were inactivated mainly by UVB in these freshwaters.
Results suggest E. coli may be a better
freshwater indicator than enterococci.
Davies-Colley RJ, Donnison AM, Speed DJ, Ross CM, Nagels JW. 1999.
Inactivation of faecal indicator microorganisms in waste stabilisation
ponds: Interactions of environmental factors with sunlight. Water
Res 33: 1220–30.
Sunlight exposure is considered to be the most important cause of “natural”
disinfection in waste stabilisation ponds (WSPs). The influence of dissolved
oxygen (DO), pH, and particulate and dissolved constituents in WSP effluent,
on sunlight inactivation of faecal micro-organisms, using small reactors
operated under controlled physico-chemical conditions was examined.
Inactivation of both enterococci and F-RNA phages increased strongly
as DO was increased, and also depended on light-absorbing pond-water
constituents, but pH was not influential over the range investigated
(7.5 to 10). Inactivation of E. coli increased strongly when pH increased
above 8.5, as well as being strongly dependent on DO. Inactivation of
F-DNA phage was independent of the factors investigated. These results
are consistent with the F-DNA phages being inactivated as a result of
direct DNA damage by UVB in sunlight, whereas the other three microbiological
indicators are inactivated as a result of photo-oxidative damage, although
the target of damage is apparently different. Our findings of diverse
influences of physico-chemical conditions suggest difficulties in interpreting
data for a single micro-organism to indicate WSP effluent quality. However,
sunlight remains the factor of overriding importance, and disinfection
in WSPs may be enhanced by increasing sunlight exposure.
Deely J, Hodges S, McIntosh J, Bassett D. 1997. Enterococcal numbers
measured in waters of marine, lake, and river swimming sites of the
Bay of Plenty, New Zealand. New Zealand Journal
of Marine and Freshwater Research 31: 89–101.
Reports enterococci numbers for 32 coastal beaches, 23 lake beaches
and 31 river swimming holes, using medians of five samples. Most marine,
lake and up-river sites had low enterococci counts, complying with current
guidelines, but mid-river and lowland river reaches tended to breach
those guidelines.
Department of Health. 1992. Provisional Microbiological
Water Quality Guidelines for Recreational and Shellfish-gathering Waters
in New Zealand. Department of Health, Public Health Services,
Wellington.
Previous guidelines, issued in response to a number of authorities beginning
to use the USEPA (1986b) criteria. These guidelines attempted to interpret
those criteria in terms of New Zealand conditions.
Disinfection Review Group. 2002. Pilot Study:
Pilot plant investigations, surrogate study results and recommendations.
Final report to Watercare Services Ltd, Auckland, June.
Reports on an extensive set of trials examining inactivation rates of
a number of faecal indicators and pathogens in a pilot plant mimicking
the processes to be used in the upgraded Mangere Wastewater Treatment
Plant. Demonstrates decreasing correlations between indicators and pathogens
(enteroviruses) as the level of treatment is increased.
Donnison AM, Cooper RN. 1990. Enumeration of faecal coliforms and
Escherichia coli in New Zealand receiving
waters and effluents. Environmental Technology
11: 1123–7.
Describes mTEC membrane filtration method for enumeration of faecal
coliforms and E. coli (as a subsequent
step). Compares the method favourably to alternatives (MPN and mFC).
Donnison AM. 1992. Enumeration of enterococci in New Zealand waters
and effluents. Environmental Technology 13:
771–8.
Compares an in-house MPN method to the USEPA Membrane Filter Method,
suggesting it as a desirable method for enumerating enterococci in effluents
(particularly if they are minimally treated).
Donnison AM, Ross CM. 1995. Somatic and F-specific coliphages in New
Zealand waste treatment lagoons. Water Research
29(4):
1105–10.
Concludes that the FRNA:FDNA coliphage ratio may distinguish between
animal and human faecal material.
Donnison AM, Ross CM. 1999. Animal and human faecal pollution in New
Zealand. New Zealand Journal of Marine and Freshwater Research 33: 119–28.
Sentinel freshwater mussels were placed in rivers impacted by faecal
pollution. E. coli were recovered from
all sites (including a forest control site) but were highest at sites
impacted by treated sewage, meat-processing wastes or dairy farm inputs.
The pathogens measured (Campylobacter jejuni,
E. coli, Salmonella
typhimurium, Yersinia enterocolitica)
were recovered from mussels – except at the control site. Untreated
wastewaters (sheep, beef, human sewage) all indicated the presence of
these pathogens, mostly in more than half the samples. Thermophilic
Campylobacters “are likely to
remain after secondary treatment of either meat plant waste water or
sewage”.
Dufour AP. 1984. Health Effects Criteria for Fresh
Recreational Waters. Report EPA 600/1-84.004, USEPA Cincinnati,
OH. NTIS access #: PB 85-150878.
Major prospective epidemiological study at lake beaches in Tulsa, Oklahoma,
and Erie, Pennsylvania, involving 34,598 persons. Most notable result
was a relationship between “swimming-associated pollution-related
illness risk” and (the logarithm of) E.
coli and enterococci concentrations. The association with E.
coli was the stronger of the two. The illness was HCGI (highly
credible gastro-intestinal illness, being GI accompanied by fever).
Analysis methods used data grouping followed by linear regression, rather
than the more modern “generalized linear models” (e.g. logistic
regression); appropriate software was not available. Also reports results
of Egyptian studies, but these were not included in their final analysis.
Dutka BJ. 1979. Microbiological indicators, problems and potential
of new microbial indicators of water quality. In: A James and L Evison
(eds) Biological Indicators of Water Quality.
Wiley and Sons, London.
Reviews alternatives, each of which may signal contamination.
Eberhart-Phillips J, Walker N, Garrett N, Bell D, Sinclair D, Rainger
W, Bates M. 1997. Campylobacteriosis in New Zealand: results of a case-control
study. Journal of Epidemiology and Community Health
51: 686–91.
Reports a study on 621 people with notified illness between June 1994
and February 1995 in Auckland, Hamilton, Wellington and Christchurch.
Found undercooked chicken to be a strong risk factor. Rainwater as a
source at home was a lesser factor. Recreational water use appears not
to have been in the questionnaire.
EEC. 1976. Council Directive of 8 December 1975 concerning the quality
of bathing water (76/160/EEC). Official Journal
of the European Communities. No. L31/1–7. Available at:
http://europa.eu.int/water/water-bathing/directiv.html.
Documents the EEC bathing water directive. Imperative standards require
95% of fortnightly samples to not exceed 10,000 total coliforms per
100 mL or 2000 faecal coliforms per 100 mL. If inspection shows that
other substances may be present, or that water quality has deteriorated,
then there should be zero Salmonella
per litre and zero enterovirus per 10 litres in 95% of samples (sampling
frequency unspecified). Guideline values require 80% of fortnightly
samples to not exceed 500 total coliforms per 100 mL or 100 faecal coliforms
per 100 mL. If inspection shows that the substances may be present,
or that water quality has deteriorated, then 80% of samples should not
exceed 100 faecal streptococci per 100 mL (sampling frequency unspecified).
There are other limits on pH, colour, mineral oils, surface-active substances,
phenols, transparency, dissolved oxygen, tarry residues and floatables
(fortnightly sampling being required for colour, mineral oils, surface-active
substances, phenols, transparency, tarry residues and floatables). The
following should be checked if there is a tendency toward eutrophication:
ammonia and Kjeldahl nitrogen. If inspection shows that other substances
may be present, or that water quality has deteriorated, then sampling
is required for pesticides, heavy metals, cyanides, nitrates and phosphates.
EEC. 1979. Council Directive of 30 October 1979 on the quality required
of shellfish waters. Official Journal of the European
Communities. No. L 281/47–49 plus annex. Details, with
amendment 391L0692, at:
http://europa.eu.int/smartapi/cgi/sga_doc?smartapi!celexapi!prod!
CELEXnumdoc&lg=en&numdoc=31991L0692&model=guichett.
EHD. 1980. A Study of Disease Incidence and Recreational
Water Quality in the Great Lakes. Phase I. Report 81-EHD-67.
Environmental Health Directorate, Health Protection Branch, Health and
Welfare, Ottawa, Canada (prepared by The University of Toronto).
A prospective study using 6,166 interviews, of whom 65% were swimmers
at lake beaches. Swimmers were found to have higher morbidity risks.
Main feature was evidence of bather-to-bather transmission of infections
(strongest association was with Staphylococci).
El-Sharkawi F, Hassan MNER. 1979. The relation between the state of
pollution in Alexandria swimming beaches and the occurrence of typhoid
among bathers. Bulletin of the High Institute of
Public Health of Alexandria IX:
337–51. (Reprinted by the Alexandria University Press, 1980.)
Report obtainable from G McBride, NIWA, Hamilton, New Zealand.
Reports on a 1976 retrospective study of hospital inpatients. Concludes
that “there is a significant risk of contracting Typhoid from
bathing in the polluted water and the mostly affected were the young
age group”. Sewer outfalls discharged raw material directly to
some beaches.
Elliot EL, Colwell RR. 1985. Indicator organisms for estuarine and
marine waters. FEMS Microbiology Reviews
32: 61–79.
Documents finding the presence of pathogens in waters and shellfish
when faecal coliforms are either absent or in low numbers.
Elliott AH. 1998. Prediction of illness risk near ocean outfalls using
frequency distributions of bacterial concentrations. Water
Research 32(10): 3182–7.
Presents a method for combining temporal concentration frequency distribution
with a concentration–response relation to obtain an averaged illness
rate, applied to North Shore (Auckland).
Ellis JC, Lacey RF. 1980. Sampling: defining the task and planning
the scheme. Water Pollution Control 79: 452–67;
discussion: 482–4.
Wide review of sampling programme design. Discusses statistics of assessing
compliance with percentile standards, where the percentile refers to
a percentage of time (not of samples).
EU. 1994. Proposal for a Council Directive concerning the quality
of bathing water. Official Journal of the European
Communities. No. C 112/3–10. Available at:
http://europa.eu.int/smartapi/cgi/sga_doc?smartapi!celexapi!prod!
CELEXnumdoc&lg=en&numdoc=51994PC0036&model=guichett.
Clarifies method of compliance assessment and proposes revised quality
requirements based on E. coli, faecal
streptococci, enteroviruses (bacteriophages mentioned, but no limits
are proposed). Compliance is to be assessed using look-up tables (e.g.
for an imperative standard, 95% percentile are assessed by allowing
no exceedances in 19 samples, one exceedance in between 20 and 39 samples,
etc). The imperative 95% percentile limits for E.
coli and faecal streptococci are 2000 and 400 per 100 mL respectively,
and for enteroviruses it remains at 0 pfu/10 L.
Fattal B, Vasl RJ, Katzenelson E, Shuval HI. 1983. Survival of bacterial
indicator organisms and enteric viruses in the Mediterranean coastal
waters off Tel-Aviv. Water Research 17: 397–402.
Reports ‘die-away’ studies on coliforms and enteric viruses
offshore from Tel Aviv. Concentrations of total coliforms, faecal coliforms
and faecal streptococci were correlated with enterovirus concentrations
(though not all correlations were statistically significant). Faecal
streptococci displayed a similar die-away rate to enteroviruses; the
other bacteria reduced more quickly. About 76% of positive enterovirus
samples were found at beaches within ‘safe’ levels, as indicated.
Fattal B, Peleg-Olevsky E, Yoshpe-Purer Y, Shuval HI. 1986. The association
between morbidity among bathers and microbial quality of seawater. Water
Science and Technology 18(11): 59–69.
Reports a prospective epidemiological study at three Tel Aviv coastal
beaches in 1983, comprising 2,231 persons (23% below four years of age).
Strongest finding was symptoms of enteric morbidity among swimmers,
particularly the 0–4-year-olds, related to elevated levels of
enterococci, E. coli and staphylococci
(not faecal coliforms). Swimmers had more morbidity of all types of
symptoms (enteric, respiratory, others) than non-swimmers.
Fattal B, Peleg-Olevsky E, Agursky T, Shuval HI. 1987. The association
between seawater pollution as measured by bacterial indicators and morbidity
among bathers at Mediterranean bathing beaches of Israel. Chemosphere
16(2/3): 565–70.
A briefer description of the 1983 study than that given by Fattal et
al (1986).
Fattal B, Peleg-Olevsky E, Cabelli VJ. 1991. Bathers as a possible
source of contamination for swimming-associated illness at marine bathing
beaches. International Journal of Environmental
Health Research 1: 204–14.
Further analysis of the 1983 study. Notes that the best association
between an indicator and swimmers’ illness is with Staphylococcus
aureus (rather than enterococcus or E.
coli), suggesting bather-to-bather contamination as a dominant
mechanism.
Favero MS. 1985. Microbiological indicators of health risks associated
with swimming. American Journal of Public Health
75(9): 1051–3.
Reviews the history of this topic up to 1985 (Seyfried et al’s
papers were in this issue). Notes that faecal coliforms may now be regarded
as “relatively useless for judging the safety of natural bathing
waters”. Notes also the USEPA promulgated a proposal that the
criteria be set at 20 enterococci per 100 mL or 77 E.
coli per 100 mL for freshwaters or only three enterococci per
100 mL for marine waters (Federal Register
May 1984, 49(102): 21987–8). These limits were revised upward
after feedback from professionals, many of whom suggested that the proposed
limits were too stringent (Federal Register
February 1986, 51(45): 8012–16).
Fayer R, Graczyk TK, Lewis EJ, Trout JM, Farley CA. 1998. Survival
of infectious Cryptosporidium parvum oocysts in seawater and Eastern
oysters (Crassostrea viginica) in the Chesapeake Bay. Applied
and Environmental Microbiology 64(3): 1070–4.
Oocysts placed in artificial seawater were infectious for up to 12 weeks.
Oysters sampled from natural waters contained infectious oocysts and
can serve as mechanical vectors of this organism.
Ferguson CM, Coote BG, Ashbolt NJ, Stevenson AM. 1996. Relationships
between indicators, pathogens and water quality in an estuarine system.
Water Research 30(9): 2045–54.
Water and sediment sampling for a range of indicators and pathogens
is reported for an urban estuary in Sydney, Australia. Significant increases
of faecal coliforms, faecal streptococci, Clostridium
perfringens spores, F-RNA bacteriophage, Aeromonas
spp., Giardia and Cryptosporidium
spp. occurred in the water after rain, but only faecal coliforms showed
significant increases in the sediments. Isolations of enteric viruses
were sporadic and not exclusively related to wet weather events. C.
perfringens was identified as the most useful indicator of faecal
pollution.
Ferley JP, Zmirou D, Balducci F, Baleux B, Fera P, Larbaigt G, Jacq
E, Moissonnier B, Blineau A, Boudot J. 1989. Epidemiological significance
of microbiological pollution criteria for river recreational waters.
International Journal of Epidemiology 18:
198–205.
Reports a retrospective 1986 follow-up study in the Ardèche basin
using 5737 tourists in eight holiday camps. Found a relative risk of
2.3 (95% CI = 1.7–3.2) for “objective” gastrointestinal
cases (requires vomiting or diarrhoea). Faecal streptococci were best
correlated to morbidity, with threshold 20 per 100 mL.
Fewtrell L, Godfree AF, Jones F, Kay D, Salmon RL, Wyer MD. 1992.
Health effects of white-water canoeing. The Lancet
339: 1587–9.
Reports a prospective cohort study using 516 canoeists on two channels
with different degrees of pollution: arithmetic mean enterovirus 198
and 0 pfu/L and geometric mean faecal coliforms 285 and 22/dL for streams
A and B. Between five and seven days after exposure canoeists using
stream A had significantly higher incidences of gastrointestinal and
upper respiratory symptoms than either canoeists using stream B or non-exposed
controls (spectators).
Fewtrell L, Kay D, Salmon RL, Wyer MD, Newman G, Bowering G. 1994.
The health effects of low-contact water activities in fresh and estuarine
waters. Journal of the Institution of Water and
Environmental Management 8: 97–101.
Four studies were carried out at separate locations (two freshwater
and two estuarine) using about 1000 participants in marathons and canoeing.
Geometric mean faecal coliforms ranged from 62 to 4613 per 100 mL. Comparison
of exposed and unexposed groups five – seven days after exposure
showed minimal health effects for the low water-contact sports.
Figueras MJ, Polo F, Inza I, Guarro J. 1997. Past, present and future
perspectives of the EU bathing water directive. Marine
Pollution Bulletin 34(3): 148–56.
Reviews reasons put forward for changes to the 1976 standards (EEC 1976)
and recent proposals.
Figueras MJ, Robertson W, Pike EB, Ashbolt NJ, Borrego JJ. 2000. Sanitary inspection and microbiological water quality. In: J Bartram, G Rees (eds). Monitoring Bathing Waters: A practical guide to the design and implementation of assessments and monitoring programmes. London, E & FN Spons, 113–67. Published on behalf of the World Health Organization, Commission of the European Communities and US Environmental Protection Agency.
Fleisher JM, McFadden RT. 1980. Obtaining precise estimates in coliform
enumeration. Water Research 14: 477–83.
Argues for increasing precision in coliform enumerations by replication
of sampling.
Fleisher JM. 1985. Implications of coliform variability in the assessment
of the sanitary quality of recreational waters. Journal
of Hygiene (Cambridge) 94: 193–200.
Reanalysed New York coliform compliance data, showing the impact of
lack of precision. Within-day variations were identified.
Fleisher JM. 1990a. Conducting recreational water quality surveys:
Some problems and suggested remedies. Marine Pollution
Bulletin 21(2): 562–7.
Discusses need to account for measurement error and temporal within-day
variability of microbiological examinations. Argues it is better to
maximise replications instead of sample dates.
Fleisher JM. 1990b. The effects of measurement error on previously
reported mathematical relationships between indicator organism density
and swimming associated illness: a quantitative estimate of the resulting
bias. International Journal of Epidemiology
19(4): 1100–6.
Uses computer simulations to demonstrate the effect of measurement error
on indicator–health risk relationships. Underestimation of health
risks was shown. Recommendations for future study designs were made.
Fleisher JM. 1991. A re-analysis of data supporting US federal bacteriological
water quality criteria governing marine recreational waters. Research
Journal WPCF 63(3): 259–65.
Criticises the USEPA criteria for including brackish water (Lake Ponchartrain,
Louisiana), and reanalyses the data using logistic regression. Some
aspects of the reanalysis are also open to question in our opinion (especially
the weight put on Boston data beyond their range).
Fleisher JM. 1992. US Federal bacteriological water quality standards:
a re-analysis. In: D Kay (ed) Recreational Water
Quality Management. Vol. 1, Coastal Waters. New York, Ellis Horwood,
113–28.
Criticises the USEPA criterion’s basis for incorporating three
different relationships (for the three beaches) developed by the author,
using logistic regression.
Fleisher JM, Jones F, Kay D, Morano R. 1993. Setting recreational
water quality criteria. In: D Kay and R Hanbury (eds). Recreational
Water Quality Management. Vol. 2. Fresh Water. New York, Ellis
Horwood, 123–36.
Identifies sources of bias probably incorporated in previous epidemiological
studies, and promotes methods to minimise them.
Fleisher JM, Jones F, Kay D, Stanwell-Smith R, Wyer MD, Morano R.
1993. Water and non-water related risk factors for gastroenteritis among
bathers exposed to sewage contaminated marine waters. International
Journal of Epidemiology 22: 698–708.
Finds three faults in previous epidemiological studies, being failures
to: account for within-day and spatial variability at beaches, relate
indicator concentration to an individual bather, and rigorously control
non-water-related risk factors. Results of two “intervention follow-up
studies” (controlled-cohort trials) are reported. These were at
Langland Bay (109 bathers and 124 non-bathers) and Moreton Beach (97
bathers and 154 non-bathers). Faecal streptococci (and not faecal coliforms)
were associated with bathers’ gastrointestinal illness, and only
for chest-depth samples (two shallower sampling depths were used): “excess
risk among bathers did not occur until exposure to waters containing
40–59 faecal streptococci/100 mL”.
Fleisher JM, Kay D, Salmon RL, Jones F, Wyer MD, Godfree AF. 1996.
Marine waters contaminated with domestic sewage, non-enteric illnesses
associated with bather exposure in the United Kingdom. American
Journal of Public Health 86(9): 1228–34.
Reports on results from all four UK controlled-cohort studies using
1216 healthy adult volunteers (average age about 32 years). Intensive
water-quality monitoring was used to assign possible health-risk indicators
(all bacteria) to individual bathers. Faecal streptococci exposure (threshold
60 per 100 mL) was predictive of acute febrile respiratory illness (which
must include fever), while faecal coliform exposure (threshold 100 per
100 mL) was predictive of ear ailments. Bathers were at higher risk
for eye ailments.
Fleisher JM, Kay D, Wyer MD, Merrett H. 1996. The enterovirus test
in the assessment of recreational water-associated gastroenteritis.
Water Research 30(10): 2341–6.
Uses polychotomous logistic regression on 2066 parallel faecal streptococci
and enterovirus enumerations from 416 UK locations. Found that the actual
viruses enumerated by the assay are not aetiologically related to recreational
water-associated gastroenteritis. Suggest that enterovirus assay may
be of limited use in assessing marine recreational water quality.
Fleisher JM, Kay D, Wyer MD, Godfree AF. 1998. Estimates of the severity
of illnesses associated with bathing in marine recreational waters contaminated
with domestic sewage. International Journal of Epidemiology
27: 722–6.
Reviews findings of the four UK controlled-cohort trials. Concludes
that “illness associated with bathing in marine waters contaminated
with domestic sewage can no longer be viewed as minor, and indeed can
have a substantial impact on the public health”.
Foulon G, Maurin J, Quoi N, Martin-Boyer G. 1983. Relationship between
the microbial quality of water and health effects. Revue
Francaise des Sciences de L’Eau 2: 127–43.
Beach interviews of 4,921 persons at five coastal beaches were followed
by an answer card (only 1532 persons did so). The study indicates that
an answer card system should be avoided. See also the review by Shuval
(1986).
Fraser GG, Cooke KR. 1991. Epidemic giardiasis and municipal water
supply. American Journal of Public Health
81(6): 760–2.
Compares reported rates of giardiasis in Dunedin (New Zealand) for two
10-month periods. The city had two water supplies, one “unfiltered”
(microstrained, 23 mm) and the other a modern plant with dual filters
(anthracite and silica sand). Found incidence rate-ratio of 3.3 (90%
CI = 1.1, 10.1, 49 cases). A parallel case-control study found an odds
ratio of 1.8 (90% CI = 0.5, 6.5). These results do not achieve “statistical
significance” at the 95% level, but are suggestive of transmission
of Giardia via water.
Furfari SA. 1968. History of the 70 MPN/100 mL
standard. Memo, Northeast Marine Health Services Laboratory,
USA.
Documents the history of the 70 MPN per 100 mL shellfish-gathering water
standard, as used by the US Public Health Service. The calculation was
based on a requirement that no more than 50% of 1 mL portions were positive
for coliforms, equivalent to an MPN of about 70 per 100 mL. (Available
only from G McBride, NIWA, Hamilton, New Zealand.)
Gameson ALH, Gould DJ. 1975. Effects of solar radiation on the mortality
of some terrestrial bacteria in sea water. In: ALH Gameson (ed) Discharge
of Sewage from Sea Outfalls. Pergamon Press, Oxford and New York,
209–19.
Rate of die-off of coliforms in water is much greater in daylight than
in the dark. Die-off of E. coli was
slower than that of total coliforms. Reports seminal work on this topic.
Gameson ALH. 1979. EEC directive on quality of bathing water. Water
Pollution Control 78(2): 206–14.
Notes some practical difficulties in implementing the EEC Directive
(EEC 1976).
Geldreich EE. 1978. Bacterial populations and indicator concepts in
feces, sewage, stormwater and solid wastes. In: G Berg (ed) Indicators
of Viruses in Water and Food. Ann Arbor Science, Ann Arbor, Mich.,
51–97.
Substantial review of literature up to the late 1970s.
Gibson CJ, Stadterman KL, States S, Sykora J. 1998. Combined sewer
overflows: a source of Cryptosporidium
and Giardia. Water
Science and Technology 38(12): 67–72.
Combined overflows were found to contribute both parasites in dry and
(particularly) wet weather.
Gilbert RO. 1987. Statistical Methods for Environmental
Pollution Monitoring. Van Nostrand Reinhold, New York.
This is an excellent book on many aspects of statistical interpretation
of pollution data. Particularly strong on the log-normal distribution,
which is often followed by microbiological particles.
Godfree A, Jones F, Kay D. 1990. Recreational water quality: the management
of environmental health risks associated with sewage discharges. Marine
Pollution Bulletin 9: 414–22.
Reviews past studies and claims the 1986 USEPA “standards”
do not have a firm scientific foundation.
Goodman SN. 1993. p values, hypothesis tests, and likelihood: implications
for epidemiology of a neglected historical debate. American
Journal of Epidemiology 137(5): 485–96.
Discusses valid and invalid conclusions from significance tests and
hypothesis tests.
Grabow WOK, Idema GK, Coubrough P, Bateman BW. 1989. Selection of
indicator systems for human viruses in polluted seawater and shellfish.
Water Science and Technology 21(3): 111–17.
Analysed 610 samples of sewage, polluted seawater and shellfish. Ratios
of indicators:viruses varied considerably. Recommends sample medians
of 100 faecal coliforms per 100 mL, 40 faecal streptococci per 100 mL,
50 coliphages per 100 mL, 0 human viruses per 10 L.
Green DH, Lewis GD. 1999. Comparative detection of enteric viruses
in wastewaters, sediments and oysters by reverse transcription-PCR and
cell culture. Water Research 33(5): 1195–200.
Reports results from eight occasions over a 12-month period around Auckland’s
Mangere treatment plant. Enteroviruses were found up to 276 pfu per
L in the final effluent, being highest in winter and spring (four samples
were less than detection limit). They were also present in most sediment
samples and in three oyster samples. Rotavirus was present in most final
effluent and oyster samples, and in one sediment sample. Hepatitis A
virus was confirmed in seven sediment samples, but not in any final
effluent or oyster samples.
Grimes DJ. 1991. Ecology of estuarine bacteria capable of causing
human disease: a review. Estuaries 14(4):
345–60.
Reviews current knowledge concerning A. cinetobacter, Aeromonas, Clostridium,
Enterobacter, Flavobacterium, Legionella, Listeria, Pleisiomonas, Pseudomonas
and Vibrio.
Grimont F, Grimont PAD, Richard C. 1992. The genus Klebsiella.
In: A Balows et al (eds) The Prokaryotes,
2nd ed. Springer-Verlag, New York, 2673–4.
Discusses Klebsiella species as infectious
particles.
Grohmann GS, Ashbolt NJ, Genova MS, Logan G, Cox P, Kueh CSW. 1993.
Detection of viruses in coastal and river water systems in Sydney, Australia.
Water Science and Technology 27(3–4): 457–61.
Isolated enteroviruses, adenoviruses and reoviruses. Data suggest “long-term
survival of viruses in sediments and/or contamination from other sources
such as storm water discharge”. Since the use of deep ocean outfalls
there was a decrease in the number of positive seawater samples close
to the beaches, whereas in stormwater drains viral presence remained
constant.
Haas CN, Rose JB, Gerba CP. 1999. Quantitative
Microbial Risk Assessment. Wiley, New York.
Authoritative reference for this new field of risk modelling, and associated
techniques.
Haile RW, Alamillo J, Barrett K, Cressey R, Dermond J, Ervin C, Glasser
A, Harawa N, Harmon P, Harper J, McGee C, Millikan RC, Nides M, Witte
JS. 1996. An Epidemiological Study of Possible Adverse
Health Effects of Swimming in Santa Monica Bay. Santa Monica
Bay Restoration Project. Final Report, 7 May (summary dated October
1996).
Reports a large-scale epidemiological study of head-immersing bathers
aimed at evaluating the possible adverse health effects of urban run-off.
Some 11,793 successful follow-up interviews were completed with beach
attenders, and daily ankle-depth water samples were analysed for faecal
coliforms, enterococci and E. coli.
Findings include: (i) an increased risk of illness (about 1%) associated
with swimming near flowing storm drain outlets (based on groups swimming
at and 400 yards from drains); (ii) an increased risk of illness associated
with swimming in areas with high densities of bacterial indicators;
(iii) the total coliform to faecal coliform ratio was one of the better
indicators for predicting health risk; (iv) illnesses were reported
more often on days when samples were positive for enteric viruses.
Hall AJ, Rodrigues LC. 1992. Health risks associated with bathing
in sea water. British Medical Journal 302:
572.
A letter to the editor faulting Balarajan et al (1991) for lack of detail
on a number of issues (pre-publicity, influence of non-ownership of
telephones, forms of immersion, accounting for possible confounders).
In reply (same page) the authors clarified aspects of these questions
(e.g. explaining how they minimised pre-publicity so as to avoid enhanced
self-reporting of symptoms). They noted that their main finding was
a “dose-response effect of different forms of contact with sea
water: those bathing activities that entailed more immersion usually
resulted in more symptoms being reported”.
Harrington JF, Wilcox DN, Giles PS, Ashbolt NJ, Evans JC, Kirton HC.
1993. The health of Sydney surfers: an epidemiological study. Water
Science and Technology 27(3–4): 175–81.
Reports a 90-day, six-beach study wherein 2003 recruits returned 4011
questionnaires incorporating 43,175 swimming events. Overall, swimmers
reported illness 1.63 times more often than non-swimmers. Relative risks
for total illness in males rose from 1.79 in high-frequency beach swimmers,
to 2.26 when their swims at non-ocean sites were included. No firm health-based
risk threshold was reported.
Henshilwood K, Green J, Lees DN. 1993. Monitoring the marine environment
for small round structured viruses (SRSVs): a new approach to combating
the transmission of these viruses by molluscan shellfish. Water
Science and Technology 38(12): 51–6.
Shellfish were measured every 1–2 weeks over a 14-month period
for SRSVs. Concentrations were highest in winter, when oyster-associated
gastrointestinal illness is at its peak. Sequence analysis identified
11 SRSV strains. Virus monitoring of shellfish is now possible.
Holmes PR. 1989. Research into health risks at bathing beaches in
Hong Kong. Journal of the Institution of Water and
Environmental Management 3: 488–95.
Partial presentation of results of the 1987 Hong Kong study (see Cheung
et al 1990).
Horwitz MS. 1990. Adenoviruses. In: BN Fields et al (eds) Virology,
2nd ed. Raven Press, New York, 1723–43.
Describes this virus, which can cause significant respiratory illness.
IAWPRC. 1991. Bacteriophages as model viruses in water quality control.
In: AH Havelaar (ed) Study Group on Health Related Water Microbiology.
Water Research 25: 529–45.
Reviews possible use of F-specific RNA phages and phages of Bacteroides
fragilis as virus surrogates. Usefulness of somatic coliphages
is compromised by their ability to multiply in freshwater.
Ikram R, Chambers S, Mitchell P, Brieseman MA, Ikram OH. 1994. A case
control study to determine risk factors for Campylobacter
infection in Christchurch in the summer of 1992–93. New
Zealand Medical Journal 107: 430–2.
A study aimed at determining the risk factors for acquiring Campylobacter
infection in Christchurch in the 1992/93 summer found eating undercooked
chicken away from home is a major factor, but also drinking water from
a non-urban supply.
Jones F, Kay D. 1989. Bathing waters and health studies. Water
Services 93: 87–9.
Raises questions about the Cabelli studies (between-site range of illness
rates, use of telephone survey rather than medical follow-up, lack of
control of length of swim, lack of information on alternative modes
of infection). Opined that USA results may not be transferable to UK.
Jones F, Kay D, Stanwell-Smith R, Wyer M. 1990. An appraisal of the
potential health impacts of sewage disposal to UK coastal waters. Journal
of the Institution of Water and Environmental Management 4: 295–303.
Claims that North American epidemiological studies are not scientifically
robust, leaving a “research vacuum”, such that UK studies
should proceed (pilot controlled cohort studies had been carried out
in 1989 at Langland Bay in Wales).
Jones F, Kay D, Stanwell-Smith R, Wyer M. 1991. Results of the first
pilot-scale controlled cohort epidemiological investigation into possible
health effects of bathing in sea water at Langland Bay, Swansea. Journal
of the Institution of Water and Environmental Management 5: 91–8.
Reviews the 1989 controlled-cohort pilot study. Notes that responses
to their detailed medical questionnaire resulted in higher reported
attack rates of perceived illness for both bathers and non-bathers.
Some statistically significant results were reported for perceived illness,
which were not confirmed by clinical tests. Concludes full-scale studies
are desirable.
Jones N, Graham J. 1995. Outbreak of gastroenteritis associated with
oysters: a Norwalk-like virus most likely cause. The
New Zealand Public Health Report 2(3): 25–7.
Thirty-six of 95 people attending a Christmas party in December 1994
developed a gastrointestinal illness. Epidemiological and microbiological
investigation indicated that oysters contaminated with a Norwalk-like
virus were the most likely cause of infection. The oysters were all
probably from a Bay of Islands farm.
Kay D. 1988. Coastal bathing water: the application of water quality
standards to Welsh beaches. Applied Geography
8: 117–34.
Compares relative utility of European and North American standards to
Welsh beach data. Equates faecal coliforms to E.
coli.
Kay D, McDonald A. 1986a. Coastal bathing water quality. Journal
of Shoreline Management 2: 259–83.
Notes the need for very large samples to identify statistically significant
relationships. Criticises the PHLS (1959) and MRC (1959) findings as
inferences going far beyond the data gathered (which was for two severe
notifiable illnesses).
Kay D, McDonald A. 1986b. The relevance of epidemiological research
in the British context. European Water and Sewage
90: 321–8.
Documents the UK shift away from the views expressed by MRC (1959) and
PHLS (1959). Notes that statistically significant transmission of minor
illnesses could be expected even at beaches that comply with the EEC
standards.
Kay D, Wyer M, McDonald A, Woods N. 1990. The application of water-quality
standards to UK bathing waters. Journal of the Institute
of Water and Environmental Management 4: 436–41.
Analyses data for 425 sampling locations. Ranks EEC, US EPA and Canadian
standards for stringency. Equates faecal coliforms to E.
coli.
Kay D, Fleisher JM, Jones F, Salmon RL, Wyer MD, Godfree AF, Zelenauch-Jacquotte
Z, Shore R. 1994. Predicting the likelihood of gastro-enteritis from
sea bathing: results from randomised exposure. Lancet
344: 905–9.
Reports controlled-cohort trials at four UK beaches with 1216 adults,
including 548 who entered the water, immersing the head three times.
Adverse (gastrointestinal) health effects were identified when faecal
streptococci (at chest depth) exceeded 32 per 100 mL (being the median
of the highest faecal streptococci band which failed to attain statistical
significance). Equation used is Logn odd (of gastroenteritis) = √(FS-32)
– 2.3561. Medical follow-up was included. Some 65.7% of gastrointestinal
cases had onset dates 7–21 days after exposure. Non-bather gastrointestinal
illness rate was 9.7%.
Kay D, Fleisher J, Wyer MD, Salmon RL. 2001. Re-analysis of the seabathing data from the UK randomised trials. A report to DETR, Aberystwyth, University of Wales, Centre for Research into Environment and Health.
Koenraad PMF, Rombouts FM, Notermans SHW. 1997. Epidemiological aspects
of thermophilic Campylobacter in water-related
environments: a review. Water Environment Research
69(1): 52–63.
Risk analysis indicates that the contribution of contaminated recreational
water to human infections may be greater than previously assumed. “The
contribution of viable but non-culturable Campylobacter
cells in the contamination cycle has been found to be negligible.”
Kueh CS, Tam T-Y, Lee T, Wong SL, Lloyd OL, Yu ITS, Wong TW, Tam JS,
Bassett DCJ. 1995. Epidemiological study of swimming-associated illnesses
relating to bathing-beach water quality. Water Science
and Technology 31(5–6): 1–4.
Reports results from a 1992 study at two beaches with 18,122 swimmers,
following on from that in 1987 (Cheung et al 1990). Only swimmer’s
gastrointestinal symptoms were found to be associated with pollution
level, not with faecal coliforms or E. coli,
but with Clostridium perfringens, Aeromonas spp. and Vibrio cholerae
(non-O1). The study did not measure faecal streptococci or enterococci.
Lacey RF, Pike EB. 1989. Water recreation and risk. Journal
of the Institution of Water and Environmental Management 3: 13–18.
Discusses the role of society in regulating voluntary risks, difficulties
of measuring risks via epidemiological studies, questionable predictive
power of bacterial indicators, and identifying a satisfactory rationale
for standards for recreational waters. Concludes that there is no completely
satisfactory way of providing guidance on recreational risk.
Lacey RF, Gunby A, Hay SV. 1995. Methods of Assessing
Compliance with Standards for the Quality of Bathing Waters.
Final report to the Department of the Environment. Report No. DoE 3837/1,
Water Research Centre, Medmenham, Marlow, Bucks, England.
Addresses statistical issues in deciding whether bathing sites conform
to the imperative (I) values in EU Directive (which are based on 95%
of samples).
Lee JV, Dawson SR, Ward S, Surman SB, Neal KR. 1997. Bacteriophages
are a better indicator of illness rates than bacteria amongst users
of a white water course fed by a lowland river. Water
Science and Technology 35(11–12): 165–70.
Reports results from 473 questionnaires from canoeists and rafters.
Logistic regression identified F-specific RNA bacteriophages as the
best microbiological parameter associated with the risk of gastrointestinal
illness. No pattern was found with other illnesses (including respiratory).
Regular users of the course had lower risks of illness. The level of
contamination was very high (median enterococci = 102 per 100 mL).
Leeming R, Ball A, Ashbolt N, Nichols P. 1996. Using faecal sterols
from humans and animals to distinguish faecal pollution in receiving
waters. Water Research 30(12): 2893–900.
Analysed up to seven replicates for faecal samples: hen, seagull, duck,
magpie, Rosella, swan, pig, human. Species chosen from those common
to both urban and rural catchments. Cats and pigs were the only animals
with similar faecal sterol profiles to humans. Sterol fingerprints are
sufficiently distinctive to be of diagnostic value in determining the
origin of faecal pollution.
Le Guyader F, Miossec L, Haugarreau L, Dubois E, Kopecka H, Pommepuy
M. 1998. RT-PCR evaluation of viral contamination in five shellfish
beds over a 12-month period. Water Science and Technology
38(12): 45–50.
Five shellfish beds were surveyed for 12 months. Of the 104 samples,
66% contained at least one virus. The two sites regularly contaminated
by faecal coliforms had the highest percentage of viruses, but HAV was
detected at only one site. Sampling sites meeting the criteria for commercialisation
showed occasional viral contamination and viruses were detected in sites
with no faecal coliform contamination.
Lewis GD, Loutit MW, Austin FJ. 1985. Human enteroviruses in marine
sediments near a sewage outfall on the Otago coast. New
Zealand Journal of Marine and Freshwater Research 19: 187–92.
Sediment and beach sand samples were collected from around a sewer outfall
and tested for presence of enteroviruses and faecal coliforms. Enteroviruses
were recovered from five of 14 samples collected on three occasions
and were recovered from two samples in which faecal coliforms were low.
Lewis GD, Austin FJ, Loutit MW, Sharples K. 1986. Enterovirus removal
from sewage: the effectiveness of four different treatment plants. Water
Research 20: 1291–7.
Human enterovirus removal from four sewage plants (oxidation pond, two
trickling filters, sedimentation/chlorination) showed insignificant
removal through the plants and poor correlation with faecal coliforms,
suspended solids, pH or conductivity. More viruses were present in summer.
Maximum concentration was 2570 pfu per L.
Lewis GD, Loutit MW, Austin FJ. 1986. Enteroviruses in mussels and
marine sediments and deputation of naturally accumulated viruses by
green-lipped mussels (Perna canaliculus). New Zealand
Journal of Marine and Freshwater Research 20: 431–7.
A 16-month survey assessing the distribution of human enteroviruses
in sediments and mussels near two sewage outfalls on the North Taranaki
coast. Enteroviruses were present in high numbers near the New Plymouth
outfall (maximum 32,000 pfu (100 g)–1 of wet mussel tissue and
59 pfu (100 g)–1 of wet sediment material). Viruses were recovered
occasionally from sediments and mussels near the Waitara Borough outfall.
Attempts to depurate the New Plymouth mussels over eight days were unsuccessful.
Lewis GD. 1995. F-specific bacteriophage as an indicator of human
viruses in natural waters and sewage effluents in northern New Zealand.
Water Science and Technology 31(5–6):
231–4.
While F-phage matched pathogen behaviour in several respects, its low
abundance in marine waters, uncertainty as to source and detection irregularities
pose problems for its use as an indicator.
Lightfoot NE. 1989. A prospective study of swimming
related illness at six freshwater beaches in Southern Ontario.
Unpublished PhD thesis, University of Toronto.
A Cabelli-type study, but “highly credible” gastrointestinal
illness was not included in the analysis (the author disagreed with
the inclusion of fever in its definition). It was concluded that there
was “no evidence to suggest that bacterial count contributed to
the prediction of illness in swimmers” (abstract) and that “only
tenuous correlations exist, at best” (p. 141). A logistic regression
model was fitted to the data, finding that interviewer and contact person
were significant confounders.
Liston J. 1994. Association of Vibrionaceae, natural toxins and parasites
with fecal indicators. In: CR Hackney and MD Pearson (eds) Environmental
Indicators and Shellfish Safety. Chapman & Hall, New York.
Notes strong evidence for vibrios being indigenous to estuaries. No
useful correlation between vibrios or Plesiomonas and faecal indicators
has been found for shellfish. Natural toxins are, and should be, completely
independent of testing for faecal contamination. Association between
parasites (Giardia and Cryptosporidium)
is “moot until there is substantial evidence of actual parasite
infection by one of these organisms or any other (e.g. Entamoeba
histolytica) parasite where the vehicle is molluscan shellfish”.
Loutit M. 1985. The fate of certain bacteria and heavy metals in sewage
discharged through an ocean outfall. Proceedings
of the Australasian Conference on Coastal and Ocean Engineering,
Vol. 1, Christchurch, December, pp. 211–19. Sponsored by Institution
of Engineers, Australia, Institution of Professional Engineers, New
Zealand, National Water and Soil Conservation Organisation.
Bacteria could be detected in sediments up to 8 km from Dunedin’s
Lawyer’s Head outfall. On occasion E.
coli could be detected in the sediments but not in the water.
Mariño FJ, Moiñigo MA, Martinez-Manzanares E, Borrego
JJ. 1995a. Microbiological epidemiological study of selected marine
beaches in Malaga (Spain). Water Science and Technology
31(5–6): 5–9.
Reports a three-year study at two beaches. Skin infections were found
to be associated with levels of Pseudomonas
aeruginosa, Candida albicans
and Aeromonas hydrophilia. The study
had very small numbers of non-exposed individuals, making the attainment
of statistical significance difficult.
Mariño FJ, Moiñigo MA, Martinez-Manzanares E, Borrego
JJ. 1995b. Application of the recreational water quality standard guidelines.
Water Science and Technology 31(5–6):
27–31.
Examines applicability of WHO/UNEP and EC bathing water directive using
data from their epidemiological study. Concludes the best indicators
are faecal coliforms, E. coli and coliphages
(at low pollution level) and faecal streptococci and coliphages (at
high pollution level).
McBride GB. 1990. Background Notes for the Development
of Guidelines for Microbiological Receiving Water Standards for New
Zealand. Water Quality Centre Publication No. 18. DSIR, Hamilton.
Report available from the librarian, NIWA, Hamilton.
Documents historical development of microbiological standards for New
Zealand, and issues to be addressed in the forthcoming Resource Management
Act’s implementation.
McBride GB. 1993. Discussion of ‘Health effects of swimmers
and nonpoint sources of contaminated water’, by Calderon et al.
International Journal of Environmental Health Research
3: 115–16.
Disagrees with the claim by Calderon et al (1991) that there was “no
association” between swimmers’ health risk and the concentration
of animal faecal material. Notes that reported rates appear to be in
fact rather high.
McBride GB, Bandaranayake DR, Salmond CE, Turner SJ, Lewis GD, Till
D, Hatton C, Cooper AB. 1993. Faecal indicator density and illness risk
to swimmers in coastal waters: a preliminary study for New Zealand.
Proceedings of the Annual Conference of the New
Zealand Water and Wastes Association, Havelock North, 1–3
September 1993.
Reports results of preliminary trials (1992/93) carried out at Auckland
beaches only. Enterococci emerged as a statistically significant indicator
for HCGI (highly credible gastrointestinal illness). Sample size was
too small to reach firm conclusions about how this might have related
to pollution levels. Minor corrections (hand-annotated on the original)
have been made in the version of this paper appearing in Bandaranayake
et al 1993.
McBride GB, Loftis JC, Adkins NC. 1993. What do significance tests
really tell us about the environment? Environmental
Management 17(4): 423–32. Errata in 18: 317.
Notes that an individual p-value may not be instructive about patterns
and associations in the environment, particularly because one seldom
has confidence that a null hypothesis could in fact be true.
McBride GB, Salmond CE, Bandaranayake DR, Turner SJ, Lewis GD, Till
DG. 1998. Health effects of marine bathing in New Zealand. International
Journal of Environmental Health Research 8: 173–89.
Reports New Zealand national prospective study performed at seven beaches
in the 1995 summer using 1577 beach-users who entered the water, and
2307 who did not. On each of the 107 interview days multiple samples
of the beach water were examined for three faecal indicators (faecal
coliforms, E. coli, enterococci). Log-linear
modelling showed that enterococci was most strongly and consistently
associated with illness risk for the exposed groups, particularly for
respiratory illness among paddlers and long-duration swimmers. Crude
risk differences for these two groups were 7 and 33 per 1000 individuals,
rising to 62 and 87 per 1000 individuals for the highest enterococci
quartile. No substantial differences in illness risks were found between
the human and animal waste impacted beaches, though both were markedly
different from the control beaches.
McBride GB, Thorn C, Salmond C. 1996. Feasibility
of Bathing-health Effects Study for New Zealand Freshwaters.
Ministry for the Environment Report No. 202.
Examines patterns of freshwater recreation at lower North Island sites.
Concluded that an epidemiological study was feasible only if of the
controlled type.
McBride GB, Till DG, Salmond CE. 1998. National study of health effects
of marine bathing and implications for new guidelines. Proceedings
of the 40th Annual Conference and Expo of the New Zealand Water &
Wastes Association, Museum of New Zealand, Wellington, 23–25
September, 251–5.
Implications of the national study (McBride, Salmond et al 1998) for
the review of microbiological water quality guidelines are discussed,
particularly in terms of the ‘single-sample maxima’ and
sampling depth.
McBride G, Till D, Ryan T, Ball A, Lewis G, Palmer S, Weinstein P.
2002. Freshwater
Microbiological Research Programme: Pathogen Occurrence and Human Health
Risk Assessment Analysis. Ministry for the Environment.
A study of New Zealand freshwater recreational sites. The main outcomes
were that: (i) Campylobacter and human adenoviruses are the pathogens
most likely to cause human waterborne illness; (ii) an estimated 4%
of notified campylobacteriosis in New Zealand could be attributable
to water contact recreation; (iii) E. coli
as an indicator of increased Campylobacter infection is in the range
of 200–500 E. coli per 100 mL;
(iv) other pathogens examined could not be related to E.
coli concentrations in fresh waters; (v) pathogens are more likely
to be present and in greater numbers in turbid waters. The report can
be downloaded from www.mfe.govt.nz.
Medema GJ, Asperen IA van, Havelaar AH. 1997. Assessment of the exposure
of swimmers to microbiological contaminants in fresh waters. Water
Science and Technology 35(11–12): 157–63.
Reports on a follow-up study using 1,313 participants in seven triathlons
in 1993/94. All sites were influenced by sewage effluents and most by
agricultural run-off. The risk of gastrointestinal infection correlated
well with concentration of thermotolerant coliforms and E.
coli, but not with other variables (faecal enterococci, Staphylococcus
aureus, F-specific RNA phages, enteroviruses , thermophilic Campylobacter,
Salmonella, Aeromonas,
Pleisiomonas shigelloides, Pseudomonas
aeruginosa). Note that the abstract says more than the paper
on epidemiological parts, but an accompanying poster paper reported
illness results from 827 of the triathletes, with 773 non-swimming controls
(in a run-bike-run event). Thresholds of 220 cfp per 100 mL (thermotolerant
coliforms) and 355 cfp per 100 mL (E. coli)
were reported.
Medema GJ, Asperen IA van, Klokman-Houweling JM, Nooitgedagt A, de
Laar MJW van, Havelaar AH. 1995. The relationship between health effects
in triathletes and microbiological quality of freshwater. Water
Science and Technology 31(5–6): 19–26.
Reports on a follow-up pilot study of 314 triathletes and 81 run-bike-run
controls. The triathletes showed elevated illness rates, indicating
that a full study is feasible. Geometric mean E.
coli and enterococci were 170 and 13 per 100 mL, respectively.
Medema GJ, Teunis PFM, Havelaar AH, Haas CN. 1996. Assessment of dose-response
relationship of Campylobacter jejuni.
International Journal of Food Microbiology
30: 101–11.
Reports the best-fit beta-Poisson dose response model for a common strain
of Campylobacter jejuni (Penner serotype
27).
Melnick JL. 1990. Enteroviruses: polioviruses, coxsackieviruses, echoviruses,
and newer enteroviruses. In: BN Fields et al (eds) Virology,
2nd ed. Raven Press, New York, 549–606.
Good review of virology.
Miles MA. 1973. An investigation into the possible relationship between
bathing and ear complaints in Taupo. New Zealand
Sanitarian 28(2): 75.
Propose that further examination be made into ear complaints among swimmers
at Taupo.
Ministry for the Environment. 1992. ME91. Water
Quality Guidelines No. 1. Ministry for the Environment, Wellington.
Guidelines for the control of undesirable biological growths in water.
Ministry for the Environment. 1994. ME142. Water
Quality Guidelines No. 2. Ministry for the Environment, Wellington.
Guidelines for management of water colour and clarity.
Ministry for the Environment. 1996. Feasibility
of Bathing-health Effects Study for New Zealand Freshwaters.
Prepared by GB McBride, C Thorn and C Salmond. Ministry for the Environment,
Wellington.
Considers possibilities for freshwater epidemiological study of swimmers’
health risk, and concludes that only a controlled-cohort design is likely
to be fruitful. Includes a survey of the degree of recreational use
of freshwaters at sites in Hawke’s Bay, Wairarapa and Manawatu.
Implies that hundreds of thousands of New Zealanders swim at freshwater
sites annually, but in a very dispersed manner (there are seldom more
than 100 people at a ‘site’).
Ministry for the Environment. 1999. Environmental
Education: A guide for programme providers – how to develop, implement
and evaluate strategies and programmes. Ministry for the Environment,
Wellington.
A guide to assist with preparing and implementing effective environmental
education programmes, tailored to meet the needs of individual organisations.
Ministry of Agriculture and Forestry. 1995. Shellfish Quality Assurance Circular. Ministry of Agriculture, Wellington.
Moore B. 1975. The case against microbial standards for bathing beaches.
In: ALH Gameson (ed) Discharge of Sewage from Sea
Outfalls. Pergamon Press, Oxford and New York, 103–9.
Argues against standards, noting that a health-effects versus indicator
relationship had not yet been developed, and that total or faecal coliforms
are not appropriate.
Moore B. 1977. The EEC bathing water directive. Marine
Pollution Bulletin 8: 269–72.
Expresses dissatisfaction with the 1976 EEC Directive (EU 1976), with
concern about competition for public funds. Notes the effect of the
Directive is to give high priority to “epidemiological studies
that will provide a quantitative dimension to the postulated health
risks of bathing in sewage contaminated seawater”.
Moriñgo MA, Wheeler D, Berry C, Jones C, Muñoz MA, Cornax
R, Borrego JJ. 1992. Evaluation of different bacteriophage groups as
faecal indicators in contaminated natural waters in southern England.
Water Research 26(3): 267–71.
River and seawater affected by faecal discharges were analysed to evaluate
the reliability of coliphages and F-specific RNA bacteriophages as indicators
of the microbiological quality of waters. FRNA phages showed no direct
relationship with levels of faecal pollution and were never detected
in samples with few enteroviruses, whereas coliphages were detected.
Coliphages could be considered an optimal indicator.
Morris R. 1991. The EC bathing water virological standard: is it realistic?
Water Science and Technology 24(2): 49–52.
Notes that only culturable enteroviruses and rotaviruses have available
enumeration methods, and that sampling frequency is generally not sufficient
to give effect to the requirement that 95% of samples be free of enteroviruses.
Nevertheless concludes that the present imperative standard should remain.
MRC. 1959. Sewage Contamination of Bathing Beaches
in England and Wales. Medical Research Council Memorandum (UK)
No. 37.
Interpreted the PHLS (1959) study results as: “With the exception
of a few aesthetically revolting beaches around the coast of England
and Wales, the risk to health of bathing in sewage-contaminated sea-water
can, for all practical purposes, be ignored.”
Mujeriego R, Bravo JM, Feliu MT. 1982. Recreation in coastal waters:
public health implications. Vier Journée
Études Pollutions. Cannes, Centre Internationale d’Exploration
Scientifique de la Mer (CIESM): 585–94.
Reports on a follow-up epidemiological study of 24 beaches at Málaga
and Tarragona, using 20,219 responses. Ailments found were skin infections
(2%), ear and eye infections (1.5%) and intestinal infection (< 1%).
According to Shuval (1986) the study does supply “some suggestive
evidence as to the value of enterococci as an indicator of marine pollution”,
but suffers from a lack of controls and appropriate water quality data.
New Jersey Department of Health. 1989. Ocean Health
Study: A study of the relationship between illness and ocean beach water
quality in New Jersey.
A 1988 prospective study using 16,089 (10% under age 10) at nine coastal
and two lake beaches impacted by chlorinated effluents. Swimmers consistently
reported higher symptom rates than non-swimmers (excess of 12.2 cases
per 1000). Water quality was very good and attempts to relate the excess
illness rates with pollution levels failed.
NTAC. 1968. Water Quality Criteria. Report
of the National Technical Advisory Committee to the Federal Water Pollution
Control Administration.
The first federal compilation of quality ‘criteria’, sometimes
called the “Green Book”. It was compiled by five separate
committees, which each recommended different definitions of how one
would judge compliance.
Nuzzi R, Burhans R. 1997. The use of enterococcus and coliform in
characterising bathing-beach waters. Environmental
Health (July/August): 16–21.
Reports water quality studies at New York beaches for total and faecal
coliforms (still used in New York for bathing waters) and enterococci.
Found that enterococcus correlated well with both sets of coliforms,
but would result in more beach closures.
Philip R. 1991. Risk Assessment and Microbiological Hazards Associated with Recreational Water Sports. Reviews in Medical Microbiology 2: 208–14.
PHLS. 1959. Sewage contamination of coastal bathing waters in England
and Wales: a bacteriological and epidemiological study. Journal
of Hygiene (Cambridge) 57: 435–72.
Reports on a retrospective study of enteric fever and poliomyelitis
(both notifiable). Concludes “that bathing in sewage polluted
sea water carries only a negligible risk to health, even on beaches
that are aesthetically very unsatisfactory ...”. This is sometimes
quoted as Moore (1959); Dr Brendan Moore was the main author.
Pike EB. 1993. Recreational use of coastal waters: development of
health-related standards. Journal of the Institution
of Water and Environmental Management: 163–69.
Compares USA/UK/EU approaches to setting standards, noting that all
are primarily directed at bathing. Statistical issues in defining central
and extreme values of indicator variables are discussed, in particular
the use of single sample maxima is problematical. Notes that only the
USEPA criteria had been developed from epidemiological studies (up to
1993).
Pike EB. 1994. Health effects of sea bathing (WMI
9021) – Phase III. Final Report to the Department of the
Environment. Report No. DoE 3412/2, Water Research Centre, Medmenham,
England. Available from Water Research Centre.
Summarises results from the two sets of UK studies in the early 1990s.
These were on 16,569 holidaymakers at 10 beaches using an uncontrolled
prospective cohort design, and on 1112 healthy adult volunteers at four
beaches, using a controlled cohort design. Holidaymakers entering the
sea perceived all symptoms more frequently than those who did not, the
relative increases being related to degree of water contact and age,
being greatest in surfers and in 15–24-year-olds. Relative increases
in frequencies of eye, ear nose and throat, respiratory and skin symptoms
were not strongly related to microbiological water quality. Relative
increases in diarrhoea in those entering the water were related to total
coliform counts and enteroviruses. In the volunteer study, the incidence
in bathers of symptoms suggesting gastroenteritis was related to counts
of faecal streptococci at chest depth. No relationship was evident between
self-recording of symptoms and results of clinical examinations. Overall
conclusions from both types of study are in agreement with the results
of earlier studies.
Prüss A. 1998. Review of epidemiological studies on health effects
from exposure to recreational water. International
Journal of Epidemiology 27: 1–9.
Reviews 22 epidemiological studies conducted for freshwater and coastal
water. Most reported a dose-related increase of health risk in swimmers
with an increase in indicator bacteria count in recreational waters.
Relative risks for swimmers versus non-swimmers are typically in the
range 1.0 to 3.0. Enterococci and faecal streptococci were opined to
be the best indicators for seawater and E.
coli for freshwater. Reviews Bradford Hill’s nine criteria
for causation in environmental studies, as applied to gastrointestinal
symptoms. Passes seven of them: strength of association (yes), consistency
(yes), specificity of association (no), temporality (yes), biological
gradient (yes), plausibility (yes), coherence (yes), experiment (no),
analogy (yes).
Robertson WJ. 1993. Guidelines for the protection of human health
on bathing beaches. Journal of the Canadian Institute
of Public Health Inspectors (Spring): 14–17.
Reviews national recreational water data and proposes that E.
coli and the enterococcus group are currently the best available
indicators for fresh and marine waters respectively. Proposed limits
similar to those of USEPA 1986a.
Robson WLM, Leung AKC. 1990. Swimming and ear infection. Journal
of the Royal Society of Health 199–200.
Reviews the association of ear infection with swimming. Chlorinated
water or stagnant ponds may pose a risk for otitis media or otitis externa.
Rosenberg ML, Hazlet KK, Schaefer J, Wells JG, Pruneda RC. 1976. Shigellosis
from swimming. Journal of the American Medical Association
236(16): 1849–52.
In August 1974, 31 of 45 cases of Shigella
sonnei infection in Dubuque (Iowa) were traced to swimming in
the Mississippi River (in an eight-mile stretch). Significant associations
between illness and swimming were also reported by a retrospective survey
of 60 families who had camped at a park beside the river. The attack
rate for swimmers was 18%. Mean faecal coliform content was 17,500 per
100 mL.
Salas HJ. 1986. History and application of microbiological water quality
standards in the marine environment. Water Science
& Technology 18: 47–57.
Reviews many countries standards up to the mid-1980s. Proposes that
standards are best expressed as an average concentration, and a ‘maximum
value’ that is not to be exceeded for more than a high percentage
of the time (e.g. 90%).
Seyfried PL, Tobin RS, Brown NE, Ness PF. 1985a. A prospective study
of swimming-related illness. I. Swimming-associated health risk. American
Journal of Public Health 75(9): 1068–70.
Reports on a 1980 prospective study on 10 Ontario river and lake beaches
(see EHD 1980), using 4537 interviews. Crude morbidity rates were 69.6
per 1000 swimmers and 29.5 per 1000 non-swimmers. Swimmers experienced
respiratory ailments most frequently, followed by gastrointestinal,
eye, ear, skin and allergenic symptoms.
Seyfried PL, Tobin RS, Brown NE, Ness PF. 1985b. A prospective study
of swimming-related illness. II. Morbidity and the microbiological quality
of water. American Journal of Public Health
75(9): 1071–6.
Reports results for faecal coliforms, faecal streptococci, heterotrophic
bacteria, Pseudomonas aeruginosa, and
total staphylococci. Logistic modelling showed morbidity among swimmers
to be related to staphylococcal counts, faecal coliforms and, less strongly,
to faecal streptococci.
Shuval HI. 1986. Thalassogenic diseases. UNEP
Regional Seas Reports and Studies No. 79, UNEP.
(Greek: thalass = sea, genesis = source.) Comprehensive review of many
studies. Concludes that after years of debate there is now firm evidence
that bathing in sewage-polluted waters causes an excess of gastrointestinal
disease, the rates of which correlate generally with enterococci or
E. coli concentrations.
Simmonds RS, Loutit MW, Austin FJ. 1983. Enteric viruses in New Zealand
wastewaters. New Zealand Journal of Science
26: 437–41.
Forty-seven samples from three treatment plants were tested for human
enteroviruses. Nine different viruses were detected in 36 samples ranging
up to 4000 pfu/L. Chlorine reduced numbers, but they were still detectable
in 11 of 16 chlorinated samples.
Sinton LW, Davies-Colley RJ, Bell RG. 1994. Inactivation of enterococci
and fecal coliforms from sewage and meatworks effluents in seawater
chambers. Applied and Environmental Microbiology
60: 2040–8.
Inactivation of faecal coliforms (FC) and enterococci (Ent) from sewage
and meatworks effluents was measured in experiments (meatworks FC >
sewage FC > meatworks Ent > sewage Ent). Decay coefficient (1st-order)
for FC was two to four times that for Ent, and was slower at lower temperatures.
Factors other than insolation were implicated (by between-experiment
variations). Most inactivation appeared to be in the 318–340 nm
and > 400 nm ranges.
Sinton LW, Donnison AM, Hastie CM. 1993a. Faecal streptococci as faecal
pollution indicators: a review. Part I: Taxonomy and enumeration. New
Zealand Journal of Marine and Freshwater Research 27: 101–15.
Notes that there is no universally accepted method for isolating faecal
streptococci.
Sinton LW, Donnison AM, Hastie CM. 1993b. Faecal streptococci as faecal
pollution indicators: a review. Part II: Sanitary significance, survival,
and use. New Zealand Journal of Marine and Freshwater
Research 27: 117–37.
Faecal streptococci (or the subset enterococci) are more resistant to
sunlight-induced inactivation than faecal coliforms. Notes adoption
of USEPA criteria, using enterococci for marine and freshwaters (and
E. coli for freshwaters) should be adopted
with caution in New Zealand. Also notes the general failure of the faecal
streptococci:faecal coliform ratio as a measure of human:animal contributions
to a faecal load.
Sinton LW, Finlay RK, Hannah DJ. 1998. Distinguishing human from animal
faecal contamination: a review. New Zealand Journal
of Marine and Freshwater Research 32: 323–48.
Notes that reliable evidence is lacking on the relative health risks
posed by exposure to either human or animal faeces. Notes that New Zealand’s
high grazing animal:human ratio makes “it seem prudent to assume
that human and animal faecal pollution both constitute a risk to human
health”. Reviews methods for distinguishing animal and human faecal
residues, noting that DNA-based techniques (e.g. PCR) may assist.
Sinton LW, Finlay RK, Lynch PA. 1999. Sunlight inactivation of fecal
bacteriophages and bacteria in sewage-polluted seawater. Applied
and Environmental Microbiology.
Sunlight inactivation in seawater water of faecal indicators from sewage
was measured in outdoor experiments over a two-year period. The ranking
(from the greatest to least inactivation) was faecal coliforms >
F-RNA phages > somatic coliphages. These results suggest that, in
seawater, somatic coliphages are likely to be the best enteric virus
indicators. This inactivation ranking was also evident in a two-day
experiment, which included enterococci. Although enterococci were initially
more sunlight resistant than faecal coliforms, the two indicators fell
to counts of < 1/100 mL at around the same time on day two.
Sinton LW, Hall CH, Lynch PA, Davies-Colley RJ. 2002. Sunlight inactivation
of fecal indicator bacteria and bacteriophages from waste stabilization
pond effluent in fresh and saline water. Applied
and Environmental Microbiology 68: 3.
An important paper on the topic of receiving waters affected by pond
discharges. Experiments demonstrate that enterococci survive longer
than faecal coliforms in freshwater / raw sewage mixtures, but the opposite
pattern was observed for pond effluents. Enterococci appear to suffer
photo-oxidative damage in ponds, rendering them susceptible to further
such damage after discharge, suggesting that they are unsuitable as
indicators of pond effluents to natural waters.
Sorvillo FJ, Fujioka F, Nahlen B, Tormey P, Kebebjian RS, Mascola
L. 1992. Swimming-associated Cryptosporidiosis. American
Journal of Public Health 82(5): 742–44.
An example of a swimming-pool outbreak of this disease.
Stehr-Green JK, Nicholls C, McEwan S, Payne A, Mitchell P. 1991. Waterborne
outbreak of Campylobacter jejuni in Christchurch: the importance of
a combined epidemiologic and microbiologic investigation. New
Zealand Medical Journal 104: 356–8.
Two cases at a camp and convention centre near Christchurch had water
supply strongly suggested as the source of infection.
Stevenson AH. 1953. Studies of bathing water quality and health. American
Journal of Public Health 43: 529–38.
Reports findings from US Public Health Service studies in 1948–50
at freshwater sites on lake Michigan at Chicago, the Ohio River at Dayton
Ohio (and Tacoma Park pool at Dayton), and New York tidal waters (New
Rochelle and Mamaroneck). Used prospective study with 22,164 persons.
‘Swimming’ didn’t require head immersion. Found illness
in swimmers was appreciably higher than in non-swimmers. Also found
two statistically significant results for illness related to degree
of pollution (assessed using total coliforms), between low and high
contamination days at one of the Chicago beaches and between the Ohio
swimmers.
Streeter HW. 1951. Bacterial Quality Objectives
for the Ohio River: A guide for the evaluation of sanitary conditions
of waters used for potable supplies and recreational uses. Ohio
River Valley Water Sanitation Commission, Cincinnati, OH.
Presents calculations on the risk of contracting typhoid fever for someone
who bathes every day for 90 days in water containing 1000 total coliforms
per 100 mL. This gave a risk of 1:950, or 1:50 for “diarrhea-enteritis”.
This result was used in early standards (Waters Pollution Regulations
1963).
Telford SR. 1996. Annotation: marine waters and non-enteric illness:
matching the degree of analytical rigour to the biology of the infection
process. American Journal of Public Health
86(9): 1203–04.
A comment on the article by Fleisher and others appearing in the same
issue. Notes that their paper represents a “vast methodological
improvement over previous studies”, particularly that of Stevenson
(1953). Notes that causation studies are now desirable.
Teunis PFM, Havelaar AH. 2000. The beta Poisson dose-response model
is not a single-hit model. Risk Analysis
20(4): 513–20.
Cogent account of the validity of a standard dose response model at
low doses, and methods for accounting for uncertainty in that model
(via Bayesian posterior intervals).
Teunis PFM, Nagelkerke NJD, Haas CN 1999. Dose response models for
infectious gastroenteritis. Risk Analysis
19(6): 1251–60.
Identifies some difficulties in modelling the probability of illness
given infection for a range of doses – much less straightforward
than modelling infection given dose.
Teunis PFM, van der Heijden OG, van der Giessen JWB, Havelaar AH.
1996. The Dose-response Relation in Human Volunteers
for Gastro-intestinal Pathogens. RIVM Report No. 284 550 002.
Antonie van Leeuwenhoeklaan 9, PO Box 1, NL-3720 BA Bilthoven, The Netherlands.
In-depth review of the available data on clinical trials for a range
of gastro-intestinal pathogens. Identifies the most satisfactory models
(exponential or beta-Poisson) for each case.
Turner SJ, Lewis GD. 1995. Comparison of F-specific bacteriophage,
enterococci, and faecal coliform densities through a wastewater treatment
plant employing oxidation ponds. Water Science and
Technology 31(5–6): 85–9.
A 12-month study suggests that enterococci may be the best indicator
for oxidation pond systems. Did not include E.
coli.
Turner SJ, Lewis GD, Bellamy AR. 1997. Detection of sewage-derived
Escherichia coli in a rural stream using multiplex PCR and automated
DNA detection. Water Science and Technology
35(11–12): 85–9.
A DNA marker shows promise in identifying E.
coli isolates of human origin. Field trials upstream and downstream
of sewage ponds appear to confirm this.
Tyler KL, Fields BN. 1990. Pathogenesis of viral infections. In: BN
Fields et al (eds) Virology, 2nd ed. Raven
Press, New York, 191–240.
Includes discussion of inhalation of aerosols as a means of acquiring
infectious viral disease.
Tyrrell SA, Rippey SR, Watkins WD. 1995. Inactivation of bacterial
and viral indicators in secondary sewage effluents, using chlorine and
ozone. Water Science and Technology 29(11):
2483–90.
Chlorine reduced faecal coliforms and enterococci > 100-fold, but
for bacteriophages < 10-fold. In contrast, ozonation gave > 100-fold
reduction of the phages, but not so much for vegetative bacteria. Concludes
faecal coliforms are inadequate for predicting viral response to chlorine
or ozone.
USEPA. 1985. Test Methods for Escherichia
coli and Enterococci
in Water by the Membrane Filtration Procedure. Report EPA 600/4-85-076.
United States Environmental Protection Agency, Cincinnati, OH.
Details the test methods to be used at that time when applying the EPA
guidelines to recreational waters.
USEPA. 1986a. Ambient Water Quality for Bacteria
1986. Report EPA 440/5-84-002. USEPA Office of Water Regulations and
Standards, Washington, DC 20460.
Gives explanatory material about the derivation of the criteria, using
the results of Cabelli (1983a) and Dufour (1984).
USEPA. 1986b. Quality Criteria for Water 1986:
Bacteria. Report EPA 440/5-86-001. USEPA Office of Water Regulations
and Standards, Washington, DC 20460.
Promulgates “criteria” (i.e. recommended state standards)
based on the work of Cabelli (1983a) and Dufour (1984).
USEPA. Standard Methods for the Examination of Water and Waste Water. 20th ed, American Public Health Association.
Von Schirnding YER, Kfir R, Cabelli VJ, Franklin L, Joubert G. 1992.
Morbidity among bathers exposed to polluted seawater. South
African Medical Journal 81(6): 543–6.
Reports on the first phase of a 1990/91 prospective follow-up study
at two beaches in Cape Town, using 733 people. Found an excess of gastrointestinal,
respiratory and skin symptoms among swimmers, relative to non-swimmers.
Results were suggestive of a relationship between swimmers’ illness
and water quality.
Von Schirnding YER, Strauss N, Robertson P, Kfir R, Fattal B, Mathee
A, Franck M, Cabelli VJ. 1993. Bather morbidity from recreational exposure
to sea water. Water Science and Technology
27(3–4): 183–6.
Reports on the full study carried out at two Cape Town beaches in the
early 1990s, using 5551 people. Symptom rates for gastrointestinal,
respiratory and skin effects were substantially higher at the polluted
beach, although they did not reach statistical significance. Does not
use the more advanced statistical methods.
Ward RC, Loftis JC, McBride GB. 1990. Design of
Water Quality Monitoring Systems. Van Nostrand Reinhold, New
York.
Documents important features of design. Includes case studies.
Ware JH. 1990. The role of epidemiology in the assessment of societal
risk: a statistician’s perspective. Chance:
New Directions for Statistics and Computing: 41–7.
Tracks the development of new statistical methods for design and analysis
of chronic diseases. Argues that, in spite of inherent uncertainties,
epidemiology plays an essential role in risk assessment.
Wheeler D, Alexander LM. 1992. Assessing the health risks of sea bathing.
Journal of the Institution of Water and Environmental
Management 6: 459–67 (with discussion).
Reviews the UK-controlled cohort and uncontrolled cohort studies. Questions
the effect of necessary pre-publicity of possible self-reporting of
health effects in healthy-adult controlled-cohort trials. Concludes
that using “captive volunteer” populations of healthy adults
has technical merit, but that “there is no epidemiologically defensible
way of linking the output of such methods to the results of more conventional
techniques for assessing risks in marine waters”. Notes that the
Langland Bay pilot controlled cohort study volunteers’ rate of
self-reporting of symptoms was very high and correlated poorly with
clinical examinations.
WHO. 1986. Correlation between Coastal Water Quality
and Health Effects. Report ICP/CEH OO1 m06. World Health Organization,
Copenhagen.
Reviews known information, and proposes protocol for carrying out prospective
epidemiological studies (with input from Prof. Cabelli, and Drs Fattal
and Geldreich). Updated in (uncited) documents ICP/CEH 083/10 (1989)
and EUR/ICP/CEH/103(S) (1991).
WHO. 1998. Guidelines for Safe Recreational-water
Environments: Coastal and fresh-waters. Draft. Report EOS/DRAFT/98.14.
World Health Organization, Geneva.
Proposes 95 percentile guideline values for faecal streptococci (per
100 mL): 10 – NOAEL (No Observed Adverse Effect Level); 50 –
LOAEL (Lowest Observed Adverse Effect Level); 200 – value is above
threshold and LOAEL in most studies; 1000 – derived from limited
evidence concerning typhoid fever.
WHO. 1999. Health-Based Monitoring of Recreational Waters: The feasibility of a new approach (The ‘Annapolis Protocol’). World Health Organization, Geneva.
WHO. 2001. Bathing Water Quality and Human Health:
Protection of the human environment water, sanitation and health.
Report WHO/SDE/WSH/01.2. World Health Organization, Geneva.
Details of the application of the Annapolis Approach. Percentile values
of enterococci for risk based on exposure conditions.
WHO. 2003. Guidelines for Safe Recreational Water
Environments: Volume 1 Coastal and Freshwaters. World Health
Organization, Geneva.
Provides a review and assessment of the health hazards encountered during
recreational use of coastal and freshwater environments. A wide range
of hazards are addressed, including water quality.
Wilkinson J, Jenkins A, Wyer M, Kay D. 1995. Modelling faecal coliform
dynamics in streams and rivers. Water Research
29(3): 847–55.
Field experiments and modelling have been used to account for sediment
entrainment and release of bacteria, as governed by stream flow.
Wittman RJ, Flick GJ. 1995. Microbial contamination of shellfish:
prevalence, risk to human health, and control strategies. Annual
Review of Public Health 16: 123–40.
In the US the largest number of disease cases are of unknown aetiology.
The greatest percentage of known death (95%) is caused by non-cholera
vibrio. People with underlying health conditions are the group most
at risk.
Wyer MD, Fleisher JM, Gough J, Kay D, Merrett H. 1995. An investigation
into parametric relationships between enterovirus and faecal indicator
organisms in the coastal waters of England and Wales. Water
Research 29(8): 1863–8.
Examined a large combined dataset. The amount of variance in enterovirus
concentration explained by bacterial concentrations was only 15–16%.
Wyer MD, Kay D, Fleisher JM, Salmon RL, Jones F, Godfree AF, Jackson
G, Rogers A. 1999. An experimental health-related classification for
marine waters. Water Research 33(3): 715–22.
Proposes a health-related bathing water standard system (based on gastrointestinal
illness avoidance) using faecal streptococci in units per 100 mL. Water
quality is: ‘good’ if more than 50% of the FS distribution
above 32 is below 73; ‘moderate’ if more than 50% of the
FS distribution above 32 is above 73; ‘poor’ if more than
50% of the FS distribution above 32 is above 137; ‘very poor’
if more than 75% of the FS distribution above 32 is above 137.
