[advances in applied microbiology] advances in applied microbiology volume 30 volume 30 ||...

Microbiology of Potable Water

BETTY H. OLSON AND LASLO A. NAGY Environmental Analysis,

Program in Social Ecology, University of CaZifornia, Irvine,

Iroine, CaZ$ornia

I. Introduction . . . . . . . . . . . .

11. Source Water . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

111. Treated Water

D. Filamentous Fungi . . . . . . E. Yeasts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

. ...........

. . . . . . . . . . . . ........................

. . . . . . . . . . . .

E. Yeasts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

G . Protozoa . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

H. Other Organisms ...........................

B. Systems Model . . . . . . . . .

V. Distribution System D

73 76 76 79 81 82 86 86 86 87 87 88 88 90

100 101 104 105 107 108 109 109 110 113 117

1. Introduction

The topic of the microbial quality of water and wastewater is one of continuing concern and general interest. In the mid-MOs, the association of waterborne diseases with massive loss of human life in continental Europe and England focused attention on the importance of public health aspects of water quality. As better sanitation methods were employed and water treatment processes were initiated the incidence of waterborne diseases decreased. Perhaps most significant was the introduction of chlorination in water supplies to reduce the number of microbial pathogens. As can be seen in Fig. 1, there was a decrease in the number of waterborne disease outbreaks in the United States toward the middle of the twentieth century. This

73 ADVANCES IN APPLIED MICROBIOLOGY. VOLUME 30

Copyright 0 1984 by Academic Press, Inc. All rights of reproduction in any form reserved.

ISBN 0-12-002630-9

74 BE"Y H. OLSON AND LASLO A. NACY

v) 45 Y

m

25

w > 5

" 20-'25* I 1 26-30 36-40+

1

-50 56-60 66-7( -60

YEARS

Fic. 1. Number of outbreaks of waterborne disease in the United States, 1920-1980.

trend was then reversed by a small but steady increase in waterborne disease outbreaks continuing to the present. Two explanations for this have been developed. One invokes better reporting efforts through the cooperation of the Center for Disease Control, the United States Environmental Protection Agency (USEPA), and state agencies. The other points to increased pressure on water sources through urbanization and extended use of remote areas for recreation. Most likely, both factors are important in explaining the increase.

The number of waterborne disease cases in the United States approxi- mates 20,000 per year. The importance of this figure is difficult to assess because of the uncertainty associated with this reported value. The general sentiment is that 20,000 cases per year may underestimate the actual number by as much as 30%. Given the size of the population of the United States and the expectation of high water quality, many instances of waterborne disease could be attributed to other sources such as food, or could go unrecognized, since symptoms are often transient. Nevertheless, waterborne disease is still a recognizable phenomenon in this country. In develop- ing countries, waterborne diarrheal diseases are often the leading cause of infant and childhood morbidity and mortality, as exemplified by Central and South America (Pan American Health Organization, 1982). The lack of basic sanitation and the lack of access to safe water supplies constitute the major problems for decreasing the incidence of waterborne diseases in these countries. Thus, the majority of the population in the world is still concerned with waterborne diseases in the manner that Europe and North America were in the middle and late nineteenth century. Today, in both Europe and the United States, waterborne diseases are viewed as a minor health concern.

MICROBIOLOGY OF POTABLE WATER 75

The questions that remain unanswered in the United States involve the persistence of pathogens in aquatic environments, their level of pathogenicity after environmental exposure, their ability to survive treatment barriers, and how to predict the possibility of a disease outbreak if those barriers fail. Microbiologists and sanitary engineers grapple with this persistent threat to public health in order to ensure microbially safe water supplies. This requires an approach which underscores the behavior of pathogenic microorganisms, opportunistic pathogens, and nonpathogenic microorganisms, as well as the behavior of indicator organisms throughout the system, from source water to consumer. An ecological approach is needed to understand the microbiology of potable water from its origin to the consumer’s tap. Until recently, few studies in the literature adopted this perspective. Instead the literature has assumed an engineering approach which is designed to look at removal, survival, etc., under controlled conditions or to report observational data collected in the field.

Findings in recent years regarding disinfectant efficiency, ability of injured pathogens to produce disease, and the persistence of unexpected organisms in distribution systems have certainly pointed out the shortcomings of a laboratory strategy for defining what actually occurs in the system (Ridg- way and Olson, 1982; R. R. Colwell. 1983, personal communication).

This review describes the microbiology of potable water from a historical as well as an ecological perspective. The review does not focus directly on methodology, pathogens, or coliform or other indicator organisms in potable water as these subjects have been reviewed recently (Bitton, 1980; Dutka, 1981; Hendricks, 1979; James and Evison, 1979; Mitchell, 1972; Pipes, 1982; Sobsey and Olson, 1983).

The historical perspective reacquaints the reader with the insights and endeavors of investigators who preceded us in the quest for protection and understanding of the microbial quality of water. The ecological perspective is not used in this review as it applies to theoretical ecology, but rather in the sense of applied ecology, which attempts to explain why and how organisms move from one ecosystem to another and the mechanisms which prevent or enhance such movement. “Ecosystem” is defined here as each unique environment, i.e., source waters, treatment plants, or distribution systems. Once this view is adopted, the subject of potable water microbiology becomes a series of discrete yet intimately linked parts. One can imagine the source water, treatment plants, and the distribution system as separate eco- systems linked together by the continuous flow of water from its origin to the consumer. This review tries to identify the critical linkages and how they Eunction in each of these systems. It endeavors to report not only the state of knowledge of microbiology, but also the importance of chemistry and engineering aspects, in each compartment of the potable water system.

76 B E ” Y H. OLSON AND LASLO A. NAGY

EARLY HISTORY

The first microbiological study of drinking water can be traced back to the middle of the nineteenth century. It was conducted on the water supply of London by Hassell, who in 1850 published his findings in a report entitled “A Microscopic Examination of the Water Supplied to the Inhabitants of London and the Suburban Districts” (Rafter, 1892; Whipple et al., 1927). Hassell stressed the importance of microbiological examination of drinking water and outlined a relationship between sanitary quality and microbiological activity. At about the same time, similar conclusions were being reached by Ferdinand Cohn, who in 1853 published a treatise entitled “Liv- ing Organisms in Drinking Water” (Whipple et al., 1927). These works were preceded by studies on the waterborne nature of cholera (Snow, 1855) and typhoid fever (Budd, 1857). The initial observations of Hassell and Cohn were confirmed by other investigators during the second half of the nineteenth century (Rafter, 1892; Whipple et al., 1927). The idea of specific microbial indicators evolved around the 1880s with the work of von Fritsch and Escherich on fecal coliforms, and Miquel on plate count microorganisms as indicators of sanitary quality (Prescott and Winslow, 1904).

The first book dealing with the subject of drinking water microbiology was MacDonalds 1875 “Guide to the Microscopical Examination of Drinking Water.’’ This was followed by a book by Fox (1878) on the sanitary examination of water, a book by Rafter (1892) called “The Microscopical Examination of Potable Water,” and a book by Whipple (1899) entitled “The Microscopy of Drinking Water.” Whipple’s book, with the title unchanged, was reedited in 1905, 1914, and 1927. The last edition was actually completed by Whip- ple’s associates after his death and has become “Whipple et al.” (1927). In 1904 Prescott and Winslow compiled “Elements of Water Bacteriology,” a book that was similarly reedited and expanded over the years. The first edition of “Standard Methods for the Examination of Water and Waste- water,” appearing in 1904, was largely based on the previously formed set of procedures and recommendations of a committee appointed in 1897 by the American Public Health Association (APHA).

II. Source Water

Historically, efforts to designate the quality of source water to be used as a potable supply resulted in two divergent viewpoints. One argues that the best available source in terms of initial quality must be obtained, while the other proposes heavy reliance on treatment processes to improve a water source of initially poor quality. Regardless of the position taken, increasing urbanization and the increased use of recreational facilities have placed ex-


treme pressure on the microbiological quality of both groundwater and remote surface water sources. Further, the location of large populations far from water sources has led to the development of water transport systems that carry water hundreds of miles from its source. These transport systems and storage facilities en route to the customer become the major foci of public health and management concerns. Therefore, no matter what the philosophical background, in reality more reliance is being placed on water treatment to produce finished water of acceptable microbiological quality, regardless of source quality.

The importance of source water quality and our increasing reliance on treatment process is demonstrated by data collected in the United States from 1971 to 1977 which showed that 67% of the largest waterborne disease outbreaks occurred due to source water contamination where treatment was either inadequate or nonexistent (Sobsey and Olson, 1983).

Microbiological quality of source water has been assessed through the use of indicator organisms. In the United States, most often total coliforms have been used to determine the level of treatment required for a source water. Table I shows treatment strategies recommended by the United States Pub- lic Health Service in relation to source water quality. As can be seen, the level of treatment increases as microbial quality decreases. In recent years,

TABLE I

RECOMMENDED SANITARY REQUIREMENTS FOR WATER TREATMENT SYSTEMS RELATED TO THE QUALITY OF THE SOURCE WATER"

Level of Coliform count sanitary (per 100 ml

Designation Treatment required Type of water contamination per month)

Group1 None Protected ground- None 5 1 water

water

tion for turbidity; samples exceeding waters polluted by 5000 sewage

Group I1 Chlorination Ground and surface Low 550

Group 111 Complete Water requiring filtra- Medium ~ ~ 5 0 0 0 and 20% of

Group IV Complete plus auxilia- Polluted High 25000 in more than ry treatment to rapid sand filtration with continuous postchlorination

20% of the samples and

more than 5% of samples

220,000 in not

From Public Health Reports (1927).

78 BETTY H. OLSON AND LASLO A. NAGY

the validity of coliforms as an adequate indicator of source water microbial quality has been increasingly compromised. Newly identified pathogens such as Legionella, or pathogens only recently recognized as causing waterborne disease, e.g., Yersinia, have the ability under certain circumstance to grow in water. Other pathogenic agents have resistant life stages, such as Giardia. These produce a cyst stage that survives for much longer periods in the environment than Escherichia coli or other fecal coliforms. Such factors limit our ability to relate pathogen occurrence to fecal contamination by traditional indicators.

Increasing evidence, mostly in the form of unpublished reports in the United States, suggests that coliforms can regrow under a variety of conditions. E. coli has been shown to survive and grow in a warm (28.5-38°C) monomictic reservoir which receives thermal effluent (Gordon and Flier- mans, 1978). Blooms of E. coli 08 have been reported in Lake Burragorang, the raw water source for Sydney, Australia (MacKay and Ridley, 1983). E. coli blooms occurred at several locations simultaneously in this 2.1 X lo6 M1 lake after spring rainfall and algal blooms. The same serotype of E. coli was found in several areas of the lake, which suggested regrowth as opposed to direct fecal contamination. The authors concluded that E. co2i was able to grow on the organics released from decaying algae. In the summer of 1983, a persistent coliform bloom was observed in an open finished water reservoir in Southern California. The bloom of organisms, identified as Etiterobacter cloacae, lasted for several weeks. The coliform was found to be associated with a concurrent algal bloom and a resident frog population in the reservoir. Addition of chlorine to the reservoir eliminated the problem (E. G. Means, personal communication, 1983). Thus, interpreting the meaning of the presence of coliform bacteria in relation to fecal contamination of a source water continues to be difficult for the water industry.

One might wonder why these indicators, which have been relied upon with great success, are suddenly less valid. There are, of course, many possible explanations. In the United States, the Safe Drinking Water Act of 1974 focused attention and research dollars on the microbial qualtity of drinking water and is a probable link. One has only to look at a comparison of the work produced in Europe and the United States over the last several decades to realize that drinking water microbiology has had a significant resurgence in the United States in the 1970s. This research focused on finished water microbial quality and has led to renewed interest in source water quality and indicator organisms in general.

Further, difficulty in understanding temporal relationships between source water and resultant problems in the distribution system caused these two systems to be viewed as separate and unrelated entities. Focus on isolating the causative agents of waterborne diseases has reinforced the link-


age not only between the source water and the distribution system, but also between treatment practices and efficiency. This linkage is becoming increasingly important as protection comes to rely more implicitly on treatment. One such example of the linkage between systems is the deposition of silt in distribution lines from a surface water source which received only chlorination and fluoridation as treatment. This deposition of sediment in the distribution system gave rise to colonization of the mains by the coliform Klebsiella (Ireland et al., 1983). The problem of how to deal with a water supply in which coliforms are regrowing is faced by an increasing number of water utilities with increasing frequency. For detailed information on source protection the reader is directed to Pojasek (1977).

Ill. Treated Water

Water treatment is the most important and direct means of controlling the microbial quality of drinking water. Treatment schemes consisting of chemical coagulation and flocculation, filtration, and disinfection are usually used for surface waters, although high quality surface waters are sometimes treated by direct filtration and disinfection or just disinfection. Groundwaters, being generally lower in such contaminants as microbial agents, particulates, and organics, often receive no treatment or only disinfection. A number of laboratory and field studies have shown that under optimum conditions, these treatment processes can substantially reduce the levels of microbial agents and other contaminants in water.

A variety of treatment schemes are shown in Fig. 2, depicting storage, pretreatment, coagulation, filtration, and disinfection. Storage is one of the oldest means of treating water. Today, storage of water in reservoirs usually serves to regulate the supply of water available on a short- or long-term basis. However, it is also of value as a form of microbial treatment. Storage serves to reduce not only dissolved and suspended organic matter, but also the numbers of bacteria and pathogenic agents, such as viruses and pathogenic protozoa (Poynter and Stevens, 1975). Several factors act to reduce the numbers of microorganisms and these include flocculation, sedimentation, ultraviolet light, production of bactericidal agents by certain organisms, pre- dation, and competition for nutrients (Hutchinson and Ridgway, 1977).

Storage can also result in the degradation of water quality by pollution from water fowl or sea gulls, and by algal growth which can promote growth of coliform and other bacteria. Products released by decaying algal blooms can promote actinomycete growth, which can result in taste and odor problems. (Geldreich, 1966; Williams and Richards, 1976).

The processes shown in Fig. 2 are the major treatment schemes used today, although specific types may be more common in one country than

Borehole abstraction 2 Chlorination -Supply

Storage on protected : Chlorination _I_C Supply catchments

Storage Micro-st raining

bChlorination - Supply \ Slow sand

Direct abstraction - filtration Storage *

Micro-straining/ Coagulat Ion Rapid sand Dechlarination

filtration Clarification Re-chlorination Rapid sand - Prechlorination- + -filtration = Supply

+ Biological Coagulation Rapid sand Carbon

Mrect >- abstraction

Mrect _I Pretreatment- Prechlorination---t + - f i l t r a t i o o - f i l t e r c Supply abstraction (rapid sand/ Clarification

sediment at ion)

FIG. 2. TyTical wmbinations of watcr treatment pwcsses used in the Unitrri Kingdom (from Hutchinsari and Fiidgway, 1977).


another. Flash chlorination prior to treatment is commonly used in the United States where trihalomethanes are not a problem. This reduces the microbial load and also oxidizes organic matter. It should be noted that enteric viruses and protozoan cysts are less effectively reduced by certain treatment processes than are enteric bacteria. These findings have raised concerns about the possibility of producing drinking water that meets cur- rent bacteriological standards but still contains sufficient viral and protozoan pathogens to pose a health risk to consumers. Such situations are most likely to occur when treatment is minimal or only marginally effective and raw water pathogen levels are high. At the present time there is inadequate epidemiological information available to show that this is a significant or widespread problem.

A. VIRUSES

The topic of virus removal and inactivation by different drinking water treatment processes was first reviewed by Clark and Chang (1959). Since that time a number of subsequent review articles have covered this expand- ing research field (Committee Report, 1979; Hutchinson and Ridgway, 1977; LAWPRC Study Group on Water Virology, 1983; Leong, 1983; Report to Congress, 1978; Roebeck et al . , 1962; Sobsey, 1975; Sobsey and Olson, 1983; Taylor, 1974). It is generally accepted that conventional water treatment practices (composed of coagulation, flocculation, sedimentation, filtration, and disinfection) can reduce viral levels by 6-8 logs in the finished water (Committee Report, 1979; LAWPRC Study group on Water Virology 1983; Leong, 1983; Report to Congress, 1978; Sobsey, 1975).

Coagulation, flocculation, and sedimentation remove approximately 99% (a 2 log reduction) of the viral plaque forming units (PFUs) found in raw water (Clarke and Chang, 1959; Committee Report, 1979; Leong, 1983; Sobsey, 1975; Sobsey and Olson, 1983); however, as would be expected, the type of coagulant, virus, and water can produce wide deviations from this value (Clarke and Chang, 1959; Leong, 1983; Sobsey and Olson, 1983).

Filtration is relatively ineffective in terms of virus removal, especially if the viruses are not associated with large particles (Leong, 1983; Sobsey, 1975; Sobsey and Olson, 1983). However, under correct operating practices and without floc breakthrough, sand filtration can produce a 1-2 log reduction in viral numbers (Clarke and Chang, 1959; Leong 1983; Sobsey, 1975; Sobsey and Olson, 1983).

Disinfection, usually in the form of chlorination, has been the main method of virus inactivation in drinking water, generally resulting in a 4 log reduction in viral levels (Clarke and Chang, 1959; Committee Report, 1979; IAWPRC Study Group on Water Virology, 1983; Leong, 1983; Report to


Congress, 1978; Roebeck et al., 1962; Sobsey, 1975; Sobsey and Olson, 1983; Taylor, 1974). The many laboratory, pilot, and field experiments on the impact of chlorination on a number of different viruses have been recently reviewed by a number of authors (IAWPRC Study Group on Water Viology, 1983; Leong, 1983; Sobsey and Olson, 1983), and are not indi- vidually discussed here. It appears from the information currently available that viruses are considerably more resistant to chlorination than are coliforms, and consequently they require higher chlorine residuals and longer contact times than coliforms (IAWPRC Study Group on Water Virology, 1983; Leong, 1983; Sobsey and Olson, 1981). Ozonation, at least from bench tests, appears to be a relatively good viricidal treatment; however, treatment plant studies with ozone have often recorded viruses in the finished water (Leong, 1983; McDermott, 1974; Taylor, 1974). The use of chloramines for virus disinfection has indicated that in comparison to chlorine, chloramines require higher doses and much longer contact times for satisfactory inactivation (Wolfe et al., 1984).

B. BACTERIA

There are few reports in the literature from the 1920s to the present on the effectiveness of removal of various bacterial pathogens or indicators by treatment processes.

1 . Pretreatment

Generally, three types of pretreatment are used: microstrainers, roughing filters, and biological sedimentation. Microstrainers are not commonly used in the United States. In actuality, microstraining does little to remove bacteria because the smallest mesh size is 23 pm (Boucher, 1967). It does, however, remove larger particles and certain types of algae. Microstrainers can develop bacterial slimes or biofilms which reduce thier efficiency. Therefore, routine maintenance practices often require control of the biofilm by ultraviolet light or disinfection. Roughing filtration utilizes large diameter sand particles to remove larger suspended solids or filamentous algae. Its main benefits are the passage of large volumes of water through the filter in a short period of time and reduction of the need for backwashing during filtration.

Biological sedimentation is sometimes used in Europe, but is not often found in the United States as a pretreatment process. Water is run through horizontal and upflow tanks in a manner which keeps the biofloc (river sand, sand, or alum floc) in suspension. The large surface area of these flocs is excellent for removing ammonia (Millner et al., 1972).


2 . Slow Sand Filtration

Slow sand filtration is not widely practiced in Europe today, but has a long history beginning in the early 1800s. In the United States, rapid sand filtration has always been the favored form of water treatment. Slow sand filtration is the classical form of biological treatment and it was responsible for the identification of water treatment as a means to reduce waterborne outbreaks of typhoid and cholera (Baker, 1949). Water passes through the filter at a slow rate (0.1 mph). The filter is composed of fine sand (0.2-0.4 mm in diameter). A biofilm (Schmutzdecke) is formed on the surface, which removes not only bacteria, protozoa, and viruses, but also organics and nitrogen. Further, the mechanical process of filtration occurs as the water moves through the sand bed, increasing removal of various chemical constituents as well as microorganisms. As with all treatment processes this is not free from problems, including seeding with sporeformers which can result in spores passing through the filter.

3. Coagulation and Filtration

In the United States, coagulation and sedimentation are frequently used to treat surface water sources. Flocculants include ferrous or aluminum sulfate which form positively charged flocs of the respective hydroxide. Treatment plants are designed so that slow mixing enhances floc formation, and water movement down channels allows settling of the floc, which is then discharged to the sewer or to sludge-drying beds.

Coagulation and sedimentation are usually followed by rapid sand filtration. Rapid sand filtration as opposed to slow sand filtration removes the organisms throughout the filter depth, not just at the surface. Rapid sand filtration is purely a physicochemical process, but the filters can become contaminated with microorganisms (Hutchinson and Ridgway, 1977). This condition usually results from ineffective backwashing or the formation of mud balls in stagnant areas of the filter. Dual or mixed media filters are preferred.

Table I1 shows reduction of indicator organisms by coagulation and filtration. Removal rates for E . coli and coliforms by aluminum sulfate range from 75 to 99.4% and closely parallel reductions in turbidity. Slow sand filtration examples shown in Table I1 removed from 41 to 99.5% of the bacteria. These studies do not designate the numbers of bacteria in the source water, but generally a 2-3 log removal appears to be the norm. Thus, disinfection is a critical barrier to bacteria entering the distribution systems if the source water carries greater than 103 bacterialml.

84 B E m H. OLSON AND LASLO A. NACY

TABLE I1

INUICATOH BACTEHIA REDUCTION BY CIIEMICAI. COAGULATION AND FILTHATION"

Coagulationb Type Turbidity Bacterial

of Dose removal removal Agent water (mgfliter) T I C ("/.I is) Reference

Total coliforin River 12.6 14 96 97 Cummins and Nash

Total coliform River 20 8 40 74 Mallman and Kahler

Total coliform River 25 140-255 9699.6 99.4 Chang et al. (1959) E. coli River 10.5 168 90 83 Streeter (1927) E. coli Lake 12.1 40 72 76 Streeter (1927)

(1978)

(1948)

Filtration Aerial

Type of loading Initial Agent filter rate concentration Removal (%) Reference

Total coliform Slow sand 5 m/day Unknown 70-98 Hoekstra (1978) Total coliform Slow sand Unknown Unknown 96.S99.5 Poynter and Slade

Total coliform Slow sand Unknown Unknown 88 (low temp) Burman (1962) Total coliform Slow sand Unknown Unknown SO Robeck et nl.

E. coli Slow sand Unknown Unknown 41 (low temp) Burman (1962)

(1977)

(1962)

0 From Sobsey and Olson (1983). Using Al2(S0&. Initial turbidity units.

4. Disinfection

In Table 111 examples of disinfection efficiency for inorganic chloramines, chlorine, and chlorine dioxide are shown. Chlorine dioxide is the most efficient disinfectant for bacteria, having both the lowest effective dose and the shortest contact time. Unfortunately, human health problems can arise with its use in certain populations (Bercz et d., 1982; Bull, 1982; Lubbers et al., 1982). All reactions listed in Table I11 are pH and temperature dependent. At higher pH values (> 7.0) chlorine becomes less effective because hypochlorite ion is formed; increased pH levels (> 7.5) also shift dichloramines to monochloramines, which are less bactericidal. However, increasing pH increases the bactericidal activity of chlorine dioxide (Hoff and Geldreich, 1981). interestingly dichloramines are less efficient viricides than monochloramines (Esposito, 1974; Dorn, 1974). Increasing the temperature increases the inactivation rate of bacteria for these three disinfectants. For

TABLE I11

INDICATOR AND PATHOGEN REDUCTION BY DISINFECTION^ _ _ _ ~

Contact Concentration time Temp. Reductionb

Agent Disinfectant (mgliter) (minutes) pH ("C) ("/.I Reference

Escherichia coli E . coli E . coZi E . coli E . coli E . coli (ATCC 11229) E . coli E . coli E . coli E . coli E . coli E . coli E . coli (ATCC 11229) Salmonella typhi Pseudonwnas pyocyaneo Pseudomonas pyocyanea Legwnella pneumophh Legwnella pneumophih Campylobacter jejuni Campylohacter jejuni Campylohacter jejuni

HOCl oc1- NHzCl NHzCl NlizCl NHClz oc1- OCI - ClOZ ClOZ ClOZ ClOZ uv2 OCI - OCI - oc1- HOCl HOCl HOCl HOCl HOCl

0.1 1.0 1.0 1.0 1.2 1.0 0.3 0.4 0.25 0.25 0.25 0.25

3 x lo3 W-s/cmZ 0.3 0.75 0.4 3.3

1.W1.5 2.5

0.63 5.0

0.4 0.92

175 64 m.5 5.5

LO 10 1.8 1.3 0.68 0.27

NAC 10 10 10

<1 19 1 30

1

6.0 10.0 9.0 9.0 9.0 4.5

10.0 10.0 6.5 6.5 6.5 6.5 7.0

10.7 10.7 10.0 NRd NR NR NR NR

5 5 5

15 25 15

20-25 20-25

5 10 20 32 20

20-25 2&25 20-25

25 NR NR NR NR

99 99 99 99 9Y 99

100 100 99 99 99 99 99.9

100 100 100 99.9 99

100 100 100

Scarpino et nl. (1974) Scarpino et d. (1974: Siders et al. (1973) Siders el al. (1973) Siders et d. (1973) Esposito (1974) Butterfield (1948) Butterfield (1948) Cronier et d. (1978) Cronier et al. (1978) Cronier et al. (1978) Cronier et d. (1978) Rice and Hoff (1981) Butterfield (1948) Butterfield (1M8) Butterfield (1948) Skaliy et d. (1980) Skaliy et ul. (1980) Wang et al. (1982) {Vng et ul. (1982) Wang et 01. (1982)

4 From Sobsey and Olson (1983). b Calculated, in many instances.

NA, Not applicable. NR, Not reported


more detail the reader is referred to the National Research Council (NHC) Report (1980) on disinfection of drinking water.

C. ACTINOMYCETES

The impact of water treatment practices on actinomycete numbers has been reviewed by Burman (1973). This review, and a number of other papers, indicated that filtration results in a comparatively small reduction (approximately 50-90%) in actinomycete colony forming units (CFU) (Bays et al., 1970; Niemi et al., 1982); this is attributed to the presence of actinomycetes in the natural flora of the filters (Burman, 1973). Actinomycetes in the vegetative or the spore form are considerably more resistant to chlorination than are coliform bacteria, such that under commonly employed chlorination practices, actinomycete CFU/ml may be reduced by only 20- 90% (Bays et al., 1970; Burman, 1973). Chloramines are even less effective against actinomycetes, and may even be used to enhance their recovery (Burman, 1973).

D. FILAMENTOUS FUNGI

The influence of different water treatment practices on filamentous fungi has not been investigated in detail. However, it appears that water treatment generally results in a 2 log reduction in filamentous fungal CFUs (Bays et al., 1970; Niemi et al . , 1982). As stated in Standard Methods for the Examination of Water and Wastewater (APHA, 1980), the chlorine resistance of filamentous fungi is relatively unknown. However, a number of recent papers have provided some information on this topic (Ah0 and Hirn, 1981; McLaughlin et al., 1983; Rosenzweig et aZ., 1983) and it appears that filamentous fungi are morc chlorine tolerant than are coliforms. Similar results have been observed with respect to ozone (Brewer and Carmichael, 1979; Haufele and Sprockhoff, 1973).

E. YEASTS

Although the passage of yeasts through wastewater treatment plants has received considerable attention (Cooke, 1970), corresponding studies have not been conducted for water treatment plants.

Several studies have compared the chlorine and ozone resistance of yeasts with that of coliforms (Haufele and Sprockhoff, 1973; Jones and Schmitt, 1978; Rosenzweig et al., 1983; Farooq and Akhlayue, 1983) and have found that yeasts are generally more resistant to these two disinfectants than are coliforms.


F. ALGAE

The occurrence of algae in drinking water treatment plants has been reviewed for different sections of the United States by Palmer (1958, 1960, 1961) and by Palmer and Poston (1958). These articles provide a detailed review of the historical literature from the last century on algae in drinking water treatment plants as well as an analysis of more recent information.

Algae are important in surface water treatment because they frequently clog both slow and rapid sand filters (Palmer, 1958). Consequently they can reduce the duration of filter runs from 100 to 5 hours (Palmer, 1961). These problems are usually highly seasonal, with the greatest clogging in the late summer months (Baylis, 1922). Diatoms are frequently problem organisms, mainly because their silica shells clog filters even though the protoplasm inside has been inactivated. Algae are also important because they can cause taste and odor problems (Izaguirre et al., 1982; Palmer 1958, 1960, 1961; Palmer and Poston, 1958; Smith, 1972; Task Group Report, 1966), as well as an increase in trihalomethane (THM) precursors (Briley et al., 1978; Oliver and Shindler, 1980; Veenstra and Schnoor, 1980). The chlorination of these precursors results in chlorinated organics that may be carcinogenic (Jolley, 1978; Jolley et al., 1978, 1980), and consequently are limited to 100 pg/liter by the USEPA. Although coagulation and filtration, depending upon operating conditions, will remove varying levels of algae from raw water (Palmer, 1958, 1960, 1961; Palmer and Poston, 1958), copper sulfate (Joint Discus- sion, 1954; Flentje, 1952; Muchmore, 1978), chlorine (Joint Discussion, 1954; Kay et al., 1980), and chlorine dioxide (Ringer and Campbell, 1955) have been relatively effective in controlling algal levels in raw and in finished waters. Unfortunately, the chlorination of large numbers of algal blooms in finished drinking water increases THM levels and releases nutrients which may be utilized by aftergrowth bacteria.

G . PROTOZOA

Over the years, several investigators have tried to determine the impact of different water treatment practices on protozoa numbers in finished drinking water (Sobsey and Olson, 1983). Initially, work centered on removal or inactivation of Entamoeba, whereas more recently investigations of Giardia have become more frequent (Logsdon et al., 1981). When properly per- formed, coagulation, flocculation, sedimentation, and filtration can remove 90-99% of protozoan cysts in water (Baylis et al., 1936; Jakubowski and Hoff, 1979; Logsdon et al., 1981; Sobsey and Olson, 1983). Outbreaks of waterborne illness caused by protozoa have frequently been attributed to improper operation of treatment plants (Kirner et al., 1978; Lippy, 1978; Shaw

88 B E m H. OLSON A N D LASLO A. NAGY

et aZ., 1977). Chlorination can further reduce levels of protozoa by an additional 90-99% (Chang and Fair, 1941; Cooper and Bowen, 1983; Jarroll et al., 1981; Rice et al., 1982). Other disinfectants such as ozone and chloramines exhibit a similar degree of inactivation (Newton and Jones, 1949; Wolfe et al., 1984). Currently, small utilities are being advised by the USEPA to use slow sand filtration to remove Giardia cysts.

IV. Distribution Systems

Sobsey and Olson (1983) reported that 27% of the waterborne disease outbreaks between 1971 and 1977 occurred due to contamination of the distribution system. This fact indicates that there is a substantial need to better understand the functioning of distribution systems in order to protect the microbiological quality of the water after it leaves the treatment plant.

The possibility of microbial aftergrowth in distribution systems was first suggested in the published literature about 50-60 years ago (Baylis, 1930; Committee on Water Supply, 1930; Powell, 1921; Schaut, 1929; Whipple et a l . , 1977), but the topic has received relatively little attention until the early 1970s. At that time, certain principles from aquatic and terrestrial microbial ecology were adapted and applied to drinking water distribution systems. This microbial ecosystem approach has provided valuable explanations and raised some important public health and system management questions.

A. VIRUSES

There is some controversy about the presence of viruses in drinking water distribution systems. Most investigators agree that viruses can be isolated from drinking water that has been improperly treated or subjected to contamination (Cookson, 1974; Dennis, 1959; Hejkal et al., 1982; IAWPRC Study Group on Water Virology, 1983; Mahdy, 1979; Rao et al., 1981; Roy and Tittlebaum, 1982; Roy et al., 1981b; Sobsey, 1975; Sobsey and Olson, 1983), but there is disagreement about the presence of viruses in properly treated and maintained distribution system waters. Although other microbial groups are discussed in terms of their presence in drinking water and on distribution system wall/pipe surfaces, this separation is impractical for viruses, as all the work thus far has involved possible isolations from the actual drinking water.

I. Viruses in Drinking Water

Several French investigators reported in 1966 and 1967 the presence of viruses in 8-9% of drinking water samples analyzed from Nancy and Paris (Taylor, 1974). Partly as a result of these findings, ozone levels were in-


creased in France, and subsequent surveys have not been able to recover viruses from drinking water (McDermott, 1974; Taylor, 1974). In 1972 the USEPA reported the results of a preliminary survey of viruses in two Mas- sachusetts communities, in which 9% of the samples were positive for viruses (McDermott, 1974). Another USEPA-funded study reported poliovirus in effluent from a supposedly functioning water treatment plant (Hoehn et al., 1977). Partly as a result of the above findings, the USEPA conducted a more detailed survey in which all possible external sources of viral contamination were reduced or controlled. This study examined 255 drinking water samples from 56 communities and found no viruses in any of these waters (Clarke et al., 1975; Committee Report, 1979; Report to Con- gress, 1978). However, more recently, investigators have isolated viruses from apparently well-functioning treatment plants (Payment, 1981; ShaEer et al., 1980; Sekla et al., 1980) These studies suggest that naturally occurring viruses have a significantly lower chlorine inactivation rate than their laboratory cultured counterparts (Payment, 1981; ShaRer et al., 1980).

It may not be possible to provide definite answers about the occurrence of viruses in drinking water until some standardized sampling techniques are developed. Several researchers have investigated viral recovery techniques (Berman et al., 1980; Farrah et al., 1976; Fenters and Reed, 1977; Guttman- Bass and Armon, 1983; Rao et al., 1968, 1981; Sobsey and Glass, 1980; Sobsey et aE., 1981). The fourteenth edition of Standard Methods for the Examination of Water and Wastewater (APHA, 1976) contained a tentative prodedure. This procedure has been evaluated (Sobsey et al., 1980a) and some additional changes have been suggested (Sobsey et al., 1980b) as a result of the evaluation.

2 . Importance of Viruses in Drinking Water Environments

The public health importance of viruses in drinking water has been reviewed by a number of authors (Cookson, 1974; Hutchinson and Ridgway, 1977; Sobsey, 1975; Sobsey and Olson, 1983). Where viruses are present in drinking water due to improper treatment or distribution, serious outbreaks can result (Clarke and Chang, 1959; Dennis, 1959; Hejkal et al., 1982; Mayr, 1980).

The inactivation of viruses by various disinfectants was recently reviewed by Leong (1983) and by Sobsey and Olson (1983). A considerable amount of research has been conducted on this topic and apart from investigating the impact of chlorine, researchers have tried to assess the viricidal efficiency of a number of other disinfectants, including chlorine dioxide (Alvarez and O’Brien, 1982), bromine chloride (Keswick et al., 1981), chloramine (Gowda et al., 1981), ammonia (Craemer et al., 1983), iodine (Alvarez and O’Brien,


1982), sodium fluoride (Eubanks and Farrah, 1981), and ozone (Roy et a l . , 1981b, 1982). Although results are influenced by disinfectant concentration, water quality, pH, and a variety of other factors, it appears that viruses generally are slightly more resistant to disinfection than are coliform bacteria.

With the currently available information, it is not possible to accurately judge the ecological or system management importance of viruses in drinking water distribution systems. However, unlike the other groups of microorganisms discussed in this review, it is highly improbable that in a well- hnctioning distribution system virus levels would increase as the water moved from treatment plant to the consumer.

H. BACTERIA

1. Bacteria in Drinking Water

By the early 1920s it was well established that bacterial levels in drinking water increase due to passage through a distribution system (Powell, 1921). This was further substantiated by Schaut (1929), Baylis (1930), and the Com- mittee on Water Supply (1930). Powell (1921) in a survey of 32 municipal water plants indicated that 92% experienced aftergrowth in their treated water. Schaut (1929) found higher bacterial levels in winter months when chlorination was less effective. Baylis (1930, 1938) pointed out that under certain conditions aftergrowths occur in distribution systems, probably when chlorine residuals are lost, or when a chlorine-free zone develops in pipe sediments or at the pipe surface. Furthermore, he demonstrated a log increase in bacterial numbers as a result of passage through a distribution system, and he demonstrated a log increase in bacterial numbers as a result of passage through the distribution system, and he showed a possible association between bacterial and coliform numbers in distribution pipe sediments. Bushwell (1938) described various food sources that microorganisms in drinking water may be utilizing, and indicated that bacteria may be deriv- ing their energy from the oxidation of ammonia. At about the same time, Howard (1940) observed that there is a greater tendency for bacterial aftergrowth in the summer months. This was the opposite of what had been observed by Schaut (1929), but Howard suggested that higher summer numbers would be due to faster bacterial multiplication, more frequent loss of a chlorine residual, or greater introduction of bacteria from the pipe surface into the water as a result of greater variations in water pressure. He also stated that the possibility of properly treated water degrading to unsafe levels as a result of bacterial aftergrowth was extremely unlikely, and thus


ruled out any public health importance assignable to microorganisms in drinking water distribution systems.

The above-mentioned assumption was soon questioned by some of the findings of Shannon and Wallace (1941, 1944). These researchers were the first to carry out a comprehensive bacteriological analysis of drinking water consisting of isolation, enumeration, and identification techniques (Shannon and Wallace, 1944). They examined drinking water from various dead ends in the Detroit distribution system and observed numerous coliforms as well as members of the genus Salmonella. Shannon and Wallace (1941, 1944) also isolated several other genera including Flavobacterium, Achromobacter, Pseudomonas, Alcaligenes and Proteus. They were also the first to use lower incubation temperatures (20 instead of 37°C) and extended incubation times (96 instead of 48 hours). Howard’s (1940) assumption about the lack of public health importance of microorganisms in properly treated water was further questioned by investigators who found coliforms surviving chlorination, or reinfecting distribution systems once chlorine levels decreased (Charlton, 1933; Levine et al . , 1939, 1942; Mellman and Fontes, 1955).

The research generated since the early 1970s can be divided by environment, into investigations of bacteria isolated from drinking water and those isolated from drinking water distribution system wall/pipe surfaces. It is generally accepted that bacterial aftergrowth occurs on surfaces; however, as a result of problems of ready access to such surfaces and the lack of established techniques of sampling them, the majority of studies have examined bacteria in the actual water. This approach is not entirely unjustified as microbial aftergrowths on pipe surfaces generally would only become a problem once they reenter the passing water. Since the early 1970s a large number of studies have observed, enumerated, and in some cases identified bacteria in drinking water; and a number have reviewed the general topic [Allen, 1978, 1979, 1980, 1981, 1982, Anon, 1981; Bonde, 1977; En- glebrecht, 1983; Geldreich et d., 1972; Greenberg, 1983; Herman, 1978; Hutchinson and Ridgway, 1977; National Academy of Sciences-National Research Council (NAS-NRC) 1982; NATO, 1982; Olivieri, 1983; Pipes, 1983; Reasoner, 1983; Seidler and Evans, 1983; Sobsey and Olson, 19831. Studies conducted in the 1970s were based on a better understanding of the need to integrate physical, chemical, and engineering data into the evaluation process. Therefore, more complete information was gathered on treatment of the water prior to entering the system and on the chlorine residuals maintained than in earlier published reports. A survey of the literature also indicates that most studies conducted outside of Europe (specifically Ger- many) contain little or no information on the chemical properties of the associated water. The importance of chemical information is well docu-


TABLE IV

RELATIONSIIIP BETWEEN TOTAL ORGANIC CARBON (TOC) I N A WATER SOURCE AND BACTERIAL N U M B E M U

Geometric Dissolved oxygen TOC mean (% change in

Source (mdliter) (CFU/ml) distribution system)

Well 0.2-0.3 1 4 0 to -2 River 1.7 32 0 Moorland reservoir 1.0-1.1 18 0 to -5 Impounding reservoir 1 .0 100 -9 Lowland impounding reservoir 4.6 347 -5 Stored river water 2.4-2.9 4075 -9 to -11 Direct river abstraction 3.13.8 4OOO51,OOo -15 to -25

Adapted from Ainsworth et al. (1980)

mented in corrosion and disinfection field studies, but has generally obtained less visability in studies of the microbial quality of distribution systems. The role of pH, total organic matter, and dissolved oxygen in promoting bacterial growth is frequently not addressed in field studies and when addressed appears to make little sense.

The data in Table IV suggest a direct relationship between the amount of total organic carbon (TOC) in a water supply and the colony forming units of bacteria recovered per milliliter. Further, dissolved oxygen in the distribution system of waters generally decreases as organic content and bacterial numbers increase. It appears that bacterial numbers have a greater effect on reducing oxygen than does TOC. A decrease in dissolved oxygen also suggests an increase in chlorine demand, making it more difficult to maintain a chlorine residual.

Data in Table V have been extracted from a number of studies to provide information on the types of bacteria that occur in water supply systems. Table VI shows the numbers of microorganisms likely to be present in various treated water as that water moves from the source to the consumer. None of the studies reported here followed the same sample of water as it moved through the system, but rather, in the best cases, relied upon numerous samplings to provide representative data at the two points within the system. In Tables V and VI four types ofwater are denoted: river, aqueduct, lake, and well/ground. Investigators now make a distinction between samples collected at the well and those collected directly from a groundwater aquifer. Because of the difficulty in sampling aquifers, the literature contains few reports on bacteria in these waters. In the southwestern United States water is often transported hundreds of miles from its source through open or

TABLE V

OCCURRENCE OF BACTERIAL GENERA IN WATER SUPPLY SYSTEMS RECEIVING TREATED OR UNTREATED WATER FROM 1‘.4RiOUS SOURCES

Water source“

River ~ Lake

Aqueduct Cincinnati, Well dead end Lake Michigan,

Aqueduct Triinklirie \ Dis. rys.? hydrant. Hhinc, dis. sys., Artificial Treated Well” Dis. sys. Customer wallk hydrmt hydrant dis. 5ys. dis. sys. hydrants lakcd sy\. tap Welid hydrant” tap

Orgariisni - - - - - I

+ + + + Achrmrwbacter - - -

Acinetobacteri + + + + + + +

- + + + + + Aeromonasi - -

+ - - -

A. calcoaceticus

Aeromonas hydrophila

- - - t

Alcaligenes + + + + + + + - + + Arthrobacter - - + - + Actinom ycetes - - - - Bacilll4.S Chromobacterium - - -

Citmbucfer -

Corynefurm + - Cytophaga + Enterobacter cloacael -

- - + + + +

- - - + + - - + - + -

- - - - - - - - - - - + - + + +

+ + + - + ‘t

- - - - -

I - - -

- - - - - - + +

+ + +

+ - - - - - - - - -

+ + + + + + + + + + - E . aerogenes, E . agglonlerans

Xanthonwnas

- lknbacterium spp.! t’ -I- + + + + + t +

Grarii-positivc imknuwn (I + + f + + t -

Gram-negative uinknclrm a + + + - Kiebsiella spp. - Leptothrirf + +

-

- - - -

- + + + + + + +

- - - + + - - - - - - - -

(continued)

Water sourcea

River Lake

Aqueduct Cincinnati, Well dead end Lake hf ichigan,

Aqueduct Trunkline”, Dis. SYS.~. hydrant. Rhine. dis. sys.. Artificial Treated Wellell” Dis. sys. Customer wi l lb hydrant hydrant dis. ys. di5. sys. hydrants laked dis. sys. tap Welld hydrantd tap

Organism - - - - - + Lactobacillus - .t - - + Micrococcus + + +

+ Moraxeh + + - f

P[anctomyccd + I -

Pseudomonas + + + + + + + + + + + + - + + + - - + + + + + + Sewatia

Staphylococcus - - - Sarcina

- - - - - + 4 - + -

+ + - - + - - - - - - - - - - I

- - - - - - - - + - - - - - - - - - +

+ - -

- - - - - - - - - - g Salmonello -

Incubation characteristic# RT 35°C 35°C 35°C W C W C 20°C NR S C 3 8 C 35°C 35°C

Mediumh R2A YSPC MSPC SPC v TGE NSM SPC MSPC MSPC MSPC NR Method‘ SP SP SP MF M F SP YF NR SP SP SP NR Reference N w et Olson and Olson and Nash and Dott and Shannon and Dott and Reilly Olson Olwn Olson Lamke el

ol. 1:1952) Hanami Hanami Geldreich Schoenen Wallace (1944) Tampisch and and and and d. (1980)

5days ds hours 48 hours 48 hours 3 days 3G72 hours 55 days 48 hours 48 hours 48 hours 48 hours

11980) (1980) (1980) (1981) (1981. Kippin Hanami Hanami Hanami 1983) (19831 ilW@ <l%qi (1980)

Treated, imless otherwise indicated. ’2 Chlorination only. L‘ DistrihutioIh systetn.

e Category not used. I Observed via scanning eledron microscope studies. g RT, Room temperature; NR, not reported. h MA, Low nutrient [Reasoner and Geldrich, 1984); MSPC, bl standard plate count (Taylor and Geldrich, 1W1: SPC, standard plate count (Difco); V,

Untreated.

various media; TGE, tq-ptose glucose extract (Difco); NSM, nonselective media; NR not reported. SP, Spread plate: MF, membrane filtration; NR, not reported.

TABLE VI

BACTERIAL NUMBERS RECOVERED FROM SOURCE AND DISTRIBUTION SYSTEM LOCAT~ONS OF VARIOUS WATERS

Clz residual Source water System Location CFU/mP Treatment (mgAiter)

Ground Ground Ground WelUspring Rhine River

Rhine River

River Aqueduct water

~ Aqueduct water O7 Aqueduct water

Aqueduct water Aqueduct water

Aqueduct water

Aqueduct water

Lake

Lake, reservoir

Well Well Distrib. system Distrib. system Finished water

Finished water

Distrib. system Trunkline Distrib. system Trunkline Distrib. fiystem Open finished

reservoir

clearwell

water reservoir

Open finished

Open finished

Distrib. system

water reservoir

water reservoir

Uistritr. systetn

Polyamid pipe Well water Hydrant Customer tap Surface water

Wall column

Dead end hydrant Hydrant Hydrant Pressure vdve Customer tap

TOP Middle Bottom Water column

5 meters below

Dead end hydrant sudace

Middle and dead end

1-50 60-8 X 102 40-4 X 103

5-1.9 X lob 106 103 2.2 x 109

102-104 70

35-170 102- 103 1@~-1W 105 103-106 0-350b

3.2 X 102

104

5-48 X 18 (37"C)b, 40-80 x 18 (U)"C)b <3->500

None None None None? Complete Complete CompIete?

C,Fl,S,F,Cld C, F1, S, F,CI C, Fl,S, F,CI C1 CI c, H,S, F, c1

C, F1, S, F,CI

C, Fl ,S , F,CI

C1

C,FI, S, F,CI

0.15 0 0 NRC 0.15 0.15 0.3

NR 0.5-0.1) 0.28-0.85 1.32 1.0 0

0

0

0.15-0.33

0->I.O

Reference

Schoener~ and Dott (1982) Olson et al. (1980) Olson et al. (1950) Lamka et al. (1980) Schmnen and Dott (1982)

Scboenen and Dott (1977)

Nash and Geldreich (1980) Olson et al. (1980) Olson et al. (1980) McCoy et al. (19s) McCoy et d. (1983) Olson et al. (1980)

Silverman et al. (1983)

Ward et al. (1982)

Shannon and Wallace (1944)

Reilly and Kippin (198.3)

Mean values. Forty-eight-hour incubation. NH, Not reported. C, Coagulation; GI, chlorination; S, settling: F, filtration; FI, flocculation.

96 BETIT H . OLSON AND LASLO A. NAGY

closed cement-lined canals to where it is treated and delivered. The long distance in transport sufficiently changes the characteristics of the water to reflect those of the transport system, necessitating the source of these waters to be classified as aqueduct and not as the site of origin.

Of the 12 studies reported on in Table V, Acinetobacter and Alcakgenes were isolated from 73% of the systems, while Flauobacterium and Pseudomonas occurred in YO and 100% of the systems, respectively. Gram- positive or gram-variable genera were found to occur less frequently, but were present in 27 and 36% of the systems sampled, respectively. Coliforins isolated from nonselective media were frequently identified in 58 and 83% of the systems examined, and were represented respectively by Klebsiella spp. and Entwobacter spp. Stuph ylococcus saprophyticus was found in several supplies (Nash and Geldreich, 1980) and Staphylococcus aureus has been reported by Lamka et al. (1980) and LeChevallier and Seidler (1980). Aero- monos spp. were isolated from all groundwater systems and one river supply system. Generally, these data indicate a remarkable concurrence in the types of organisms isolated even though a variety of incubation temperatures, durations, media, and isolation techniques were employed. Iden- tification schemes also employed various techniques, with the German con- tributions using the most sophisticated of these (numerical taxonomy) (Dott and Schoenen, 1981).

The data in Table VI indicate that bacterial numbers are highly variable at both source and distribution locations regardless of the nature of the water supply. Groundwater counts ranged from 1 to lo3 CFU/ml. Generally, numbers were lower if a chlorine residual was reported. Surface waters (river, aquaduct, and lake) contained greater numbers of organisms even in the presence of a chlorine residual. The highest reported value, lo9 CFU/ml, came from the surface of a clear well (Schoenen et al., 1979). As will be discussed later, surface colonization of distribution systems or source water supply facilities can lead to the introduction of organisms into the system in a unpredictable manner. Even at free residual chlorine levels of greater than 1 mg/liter bacterial numbers can exceed lo2 CFU/ml. Howev- er, in general, highest values are reported for supplies with low chlorine residuals.

2. Bacteria on Drinking Water Distribution System WalllPipe Surfaces

By the early 1970s aftergrowth in distribution systems was thought to be largely a result of microbial growth on pipe surfaces in the distribution system and its subsequent reentry into the passing water (Baylis, 1938; Ewing and Hopkins, 1930; Howard, 1940; Larson et al., 1960; Shannon and Wallace, 1944). The ability of various microorganisms, and in some cases


macroorganisms, to grow and survive on the surface of drinking water pipes was relatively well established by the turn of the century (Whipple et al., 1927). As early as 1876, Hartwig Petersen described minute animals inhabit- ing the water pipes of the city of Hamburg (Whipple et al . , 1927). These findings were substantiated around the turn of the century by other investigators in several other water distribution systems (E. G. Smith, 1903; 0. T. Smith, 1904; Whipple, 1899; Whipple et al., 1927). During the next 60-70 years, the ability of pipe surface microorganisms to influence water quality was most clearly demonstrated by iron and maganese bacteria. Numerous investigators observed these organisms in the water andlor on cast iron pipe surfaces (Alexander, 1974; Berry, 1932; Brown, 1934; Clark et al., 1967; Grainge and Lund, 1969; Hasselbarth and Ludemann, 1972; Leuschow and Mackenthun, 1962; McMillan and Stout, 1977; Tenny, 1939; Myers, 1961; Wilson, 1945), resulting in considerable corrosion and water coloration.

These growths are usually not a public health hazard, however, colored water invariably reduces consumers’ confidence in their water utility, and may encourage the use of aesthetically more pleasing but microbiologically inferior alternatives.

Although iron and manganese bacteria provided the best example of a relationship between events at the pipe surface and subsequent water quality, in the early 1970s it was strongly believed that other microorganisms could also survive and multiply at the pipe surface, or within sediment at the bottom of such pipes, and at a later time reenter the water column (Baylis, 1930, 1938; Ewing and Hopkins, 1930; Howard, 1940; Larson et al., 1960; Shannon and Wallace, 1944; Shindala and Chisholm, 1970; Victoreen, 1969).

The resurgence of activity in drinking water microbiology in the 1970s was largely a result of increased availability of research tools such as scanning electron microscopes, vital stains, and a wider range of media. Also, investigators found that coliforms and total count bacteria were surviving chlorination, or were protected once within the distribution system. The complexity of the issues facing researchers caused them to place greater emphasis on understanding the microbial ecology of distribution systems. In addition, increased interest in drinking water quality came about as a result of the United States Safe Drinking Water Act of 1974. Two critical papers of this period were by Victoreen (1969) and Geldreich et al. (1972). The former presented the pipe-water interface as a highly heterogeneous microbial ecosystem, often removed from the direct influence of disinfectants, whereas the latter paper reaffirmed the public health and management significance of bacterial aftergrowth in drinking water distribution systems.

Several investigators have observed the occurrence of coliforms on the surface of reservoirs (Ellgas and Lee, 1980; Seidler et al., 1977), on pipe surfaces from dead ends (Earnhardt, 1980), and in finished water reservoir

98 BElTY H. OLSON AND LASLO A. NAGY

sediments (Olson et al., 1980). The growth of coliforms has been found to be stimulated by tubercle deposits from drinking water pipes (Victoreen, 1980), and Salmonella species have been isolated from such pipe sediments (Muller, 1979).

Burman and Colbourne (1977) and Colbourne and Brown (1979) have developed extensive procedures to determine the abilities of various materials used in drinking water systems to support microbiological growth. Sim- ilar research has been conducted for materials used in finished water reservoirs (Dott et al . , 1979; Schoenen, 1980; Schoenen and Dott, 1979, 1982; Schoenen and Hotter, 1981; Schoenen and Thofern, 1981a,b; Schoenen et al . , 1978; Thofern et al., 1978). Drinking water pipe surfaces have been examined by a number of investigators using a variety of microbiological media (Bigham and Tuovinen, 1983; Lee et al., 1980; Olson et al . , 1981; Tuovinen and Hsu, 1982; Tuovinen et a l p , 1980) as well as scanning electron microscopy (Allen et al., 1980; Olson et al., 1981; Ridgway and Olson, 1982; Ridgway et al., 1981; Tuovinen et al., 1980).

It is difficult to arrive at a comparison of bacterial numbers on the surface of walls and reservoirs, since results have been expressed in terms of CFUlmilliliter of biofilm (Dott et al . , 1979; Thofern et al., 19781, CFWlmilli- liter of sediment (Olson et al . , 1981), or CFU/gram of sediment (Tuovinen and Hsu, 1982). When recalculated in terms of surface area, bacterial levels are usually in the loo-lo6 CFU/cm2 range on drinking water wall/pipe surfaces. Although relatively few investigations have identified heterotrophic bacteria on drinking water surfaces (Dott et al . , 1979; Nagy, 1984; Olson et al., 1981), the organisms isolated have been found to be basically the same as those isolated from the actual water (Table V).

3. lmportance of Bacteria in Drinking Water Environments

a . Public Health. Investigators have also isolated from well-functioning drinking water systems bacteria of definite public health importance such as Legionella (Brown et al . , 1982; Tison and Seidler, 1983; Yee and Wadowsky, 1982; Wadowsky et al . , 1982), Klebsiella pneumoniae (Ptak et al . , 1973; Reilly and Kippin, 1983; Seidler et al . , 1977), Yersinia enterocolitica (Weber et al., 1981a,b), S. aureus (Lamka et al., 1980; LeChevallier and Seidler, 1980), and Salmonella (Mendis et al., 1976; Muller, 1979; Schubert and Scheiber, 1979; Sinegre et al., 1975). In addition to these organisms a number of bacterial genera (see Table V) which are classified as opportunistic pathogens have been routinely encountered. These include Pseudomonas, Aeromonas hydrophila, Edwardsiella tarda, Flavobacterium, Klebsiella, Enterobacter, Serratia, Proteus, Providencia, Citrobacter, and Acinetobacter. These organisms usually only produce infections in indi-


viduals who are in some manner compromised (postoperative or immu- nosuppressed patients, the elderly, and newborn babies). The fact that many of these organisms are found in water supplies, and that they are capable of growth in water (as in the case of Pseudomonas aeruginosa) (Favero et al., 1971; Carson et al., 1972) indicate a need to understand their pathogenicity for high risk groups in the population. This is especially true for certain institutions such as convalescent and nursing homes, and acute care hospitals. Routine analysis of new hospital water supplies has revealed as many as 3000 to 4000 CFU/ml (Eichorn et al., 1977).

b. Disinfection in Relation to Coli&orms. A number of studies have identified and/or enumerated coliforms in drinking waters, usually with respect to chlorine levels (Allen et al., 1976; Armstrong et al., 1981; Clark and Pagel, 1977; Clark et al., 1982; Earnhardt, 1980; Goshko et al., 1981, 1983; Haas et al., 1983; LeChevallier et al., 1980; Lister, 1979; Martin et al., 1982; Mossel et al., 1977; Ptak et al., 1973; Seidler et al., 1977; Talbot et al., 1979; Tracy et al., 1966; Victoreen, 1980), or high recoveries (Evans et al., 1981a,b,c; Feng and Hartman, 1982; Fujioka and Narikawa, 1982; Hsu and Williams, 1982; LeChevallier et al., 1983a,b; McDaniels and Bordner, 1983; McFeters et al., 1982; Nash and Geldreich, 1980; Seidler et al., 1981; Standridge and Delfino, 1982). The most frequently isolated coliforms appear to be Entero- bacter (Clark and Pagel, 1977; Clark et al., 1982; LeChevallier et al., 1983a) and Citrobacter (Evans et al., 1981b). As pointed out by Seidler et al. (1981), the isolation of these two genera is just as important from the public health and system management viewpoint as is the isolation of Escherichia or Kleb- siella species.

c. Systems Management. Microorganisms not only represent potential health threats, but they also serve as excellent tools to evaluate how well a system is functioning. Recent investigations have illuminated the inade- quacies of the coliform. test. The standard plate count (SPC) (APHA, 1980) will be modified in the sixteenth edition of Standard Methods. This modification changes the name of SPC to the heterotrophic plate count (HPC), because several new methods have been introduced. These methods should allow utilities the option to select a medium and enumeration technique suitable to the individualities of each system. Although bacterial numbers fluctuate seasonally, a pattern is soon established for a system if samples are processed on a regular basis and are representative of the system. As opposed to the coliform test which is mandated by law, the HPC is currently proposed as a guideline. The object of this latter method is not to achieve zero or any particular value but rather to be able to follow trends throughout a system. If values suddenly deviate in an upward manner from the norm,


this can provide an important clue as to the location and magnitude of the problem. Although most outbreaks occur due to major problems, i.e., cross- connections, a number are not easily explained, especially in the distribution system. Again, an understanding the system as a whole is necessary; this is best achieved by an ecological approach.

C. ACTINOMYCETES

Actinomycetes are frequently found in aquatic environments (Cross, 1981) and consequently in drinking water distribution systems (Burman, 1973; Dott and Waschko-Dransmann, 1981). As in the section on bacteria, the discussion below encompasses the occurrence of actinomycetes in drinking water, and on drinking water distribution system walllpipe surfaces; followed by a description of their importance in drinking water environments.

1. Actinomycetes in Drinking Water

Numerous studies examining the occurrence of bacteria in drinking water have reported the isolation of actinomycetes, even though no special isolation techniques were used for the latter group (Armstrong et al., 1981; Lamka et al., 1980; Olson and Hanami, 1980; Reilly and Kippin, 1983). Other studies have attempted to isolate and enumerate actinomycetes specifically, usually using membrane filtration and selective media (Bays et al . , 1970; Burman, 1965; Burman et al., 1969; Donlan, 1983; Hsu and Lock- wood, 1975; Niemi et al . , 1982). Media employed include chitin agar (Bays et al., 1970; Burman, 1965; Burman et at., 1969; Donlan, 1983), nutrient and actinomycete isolation agar (Niemi et al., 1982), and starch-casein agar (Donlan, 1983); incubation temperatures and durations have usually been 20-22°C and 7-14 days, respectively. Donlan (1983) found that starch- casein agar recovered higher levels of actinomycete CFU than chitin agar, with no significant difference between 7 and 14 days incubation. Standard Methods for the Examination of Water and Wastewater (fifteenth edition, APHA, 1980) suggests the use of starch-casein agar with a pour overlay technique, although on this medium, membrane filtration may be superior to both the pour overlay and spread plate procedure (Donlan, 1983). Levels of actinomycetes in drinking water are usually in the 1O0-1@ CFU/100 ml range (Bays et al., 1970; Burman, 1965, 1973; Niemi et al . , 1982) although numbers as high as 103 CFUllOO ml have been reported (Bays et al., 1970). Representatives of the genus Streptomyces are probably the most frequently isolated actinomycetes from drinking water (Burman, 1973) although Nocar- dia and Micronwnospora species have also been reported (Bays et al., 1970; Burman, 1965, 1973).


2 . Actinomycetes on Drinking Water Distribution System WalllPipe Surfaces

Actinomycetes have been observed microscopically in biofilm on the surface of a drinking water reservoir (Dott et al., 1979), as well as in drinking water pipe encrustations in several different systems (Allen et aZ., 1980). Furthermore, they have been isolated from reservoir biofilm (Schoenen et al., 1979) and from rubber joints used to seal drinking water pipes (Hookey et aZ., 1980; Leeflang, 1963, 1968). No quantitative assessments are available to indicate the possible levels of actinomycetes per given area of surface, and it is doubtful if such assessments will be feasible; however, both Strep- tomyces (Hookey et al., 1980; Leeflang, 1963, 1968) and Nocardia (Hookey et al., 1980; Schoenen et al., 1979) have been isolated from drinking water surfaces. As indicated earlier, these genera are also the frequently found actinomycete genera in the actual drinking water.

3. lmportance of Actinomycetes in Drinking Water Environments

As far as can be ascertained, actinomycetes in drinking water systems are of no public health importance. However, in terms of distribution system ecology and management they require considerable attention. Ac- tinomycetes are the microorganisms primarily responsible for taste and odor problems in drinking water (Bays et al., 1970; Larson, 1966; Lewis, 1966; Silvey and Roach, 1953, 1959). Most of these actinomycete taste and odor problems are attributable to certain members of the Streptomyces (Bays et al., 1970; Lewis, 1966; Raschke et al., 1975; Rosen et al., 1970; Silvey, 1966), although some Micromonospora (Morris, 1962) have also been implicated.

In addition to contributing to a degradation in water quality, actinomycetes in drinking water distribution systems may also contribute to the degradation of the physical system. Because they are able to grow on or in rubber used for sealing pipe joints (Leeflang, 1963, 1968) they may produce economic problems due to earlier replacement and higher water loss through faulty pipe joints.

D. FILAMENTOUS FUNGI

Studies of filamentous fungi in drinking water distribution systems have been considerably less numerous than those on bacteria. However, even the limited currently available information indicates that filamentous fungi can be isolated from most drinking water environments. As in the previous section, studies on these fungi can be divided into those addressing occurrence in drinking water or on drinking water distribution system surfaces.

102 BETIT H . OLSON AND LASLO A. NAGY

1 . Filamentous Fungi in Drinking Water

A number of studies have made reference to the occurrence of filamentous fungi in drinking waters (Burman et al., 1969; de Malignon, 1976; Mack- enthun and Keup, 1970; O’Connor et al., 1975; Rae, 1981). In most of these instances filamentous fungi were observed in hydrant flushings or water taken from dead ends.

Several investigations have also enumerated, and in some cases identified, filamentous fungi from drinking water (Bays et al., 1970; Burman, 1965; Nagy and Olson, 1982; Niemi et aZ., 1982). These enumerations have generally used membrane filtration (Qureshi and Dutka, 1976; Sherry and Quereshi, 1981) and subsequent incubation at room temperature for 7-10 days on media such as Martin’s (Burman, 1965), Czapek (Nagy and Olson, 1982) or malt extract (Niemi et al . , 1982). Standard Methods for the Exam- ination of Water and Wastewater (APHA, 1980) recommends either neopep- tone-glucose (similar to Martin’s), Czapek, or yeast extract-malt extract agar for the isolation of filamentous fungi from water. Results of fungal enumerations are usually expressed in CFU1100 ml of water, with typical levels in the loo-102 CFU1100 ml range.

Filamentous fungi isolated from drinking water generally belong to the Deuteromycotina, or imperfect fungi, with genera such as Ceyhalosporium, Verticillium, Tr i chodem, Penicillium, Sporocybe, Acremonium, Fusar- ium, Alternark, and Epicoccum commonly observed (Bays et al., 1970; Burman et aE., 1969; Nagy and Olson, 1982). With respect to filamentous fungi, great care should be taken in assigning relative ecological importance to different genera based upon the levels of spores or CFU recovered. There is considerable variation in the spore-forming ability of different genera, and the number of spores enumerated may not be an accurate representation of that organism’s true occurrence and environmental importance in drinking water distribution systems (Bays et al., 1970).

2 . Filawntous Fungi on Drinking Water Distribution System WallIPipe Surjiaces

Filamentous fungi have been noted on, or isolated from, the surface of drinking water reservoirs (Dott et al., 1979; Dott and Thofern, 1980; Schoenen and Dott, 1977; Schoenen et al., 1979, 1981; Thofern et al . , 1978), drinking water tanks (Seidler et al., 1977), drinking water pipes (Nagy and Olson, 1984), and pipe joints (Roesch and Leong, 1983). Some of these studies have also enumerated and identified these organisms, using media such as Sabouraud dextrose, Czapek, and nutrient agars. Results have been expressed as CFU/milliliter of slime (Thofern et al., 1978), CFU/gram of slime (Schoenen et al., 1979), or CFU/100 cm2 of surface (Nagy and Olson,


1984). Levels of filamentous fungi in reservoir biofilm or slime have been in the l@-105 CFU/g range (Schoenen et al., 1979), whereas on pipe surfaces the observed numbers were 10°-104 CFU/100 om2 (Nagy and Olson, 1984). Genera identified have usually included members of the Deuteromycotina such as Penicillium, Cladosporium, Cephalosporium, Verticillium, Tri- c h o d e m , Fusarium, Alternaria, and Epicoccum (Nagy and Olson, 1984; Schoenen et al., 1979; Thofern et al., 1978). These genera are the same as those isolated from drinking water (Bays et al . , 1970; Burman, 1965; Nagy and Olson, 1982) and this result substantiates a similar relationship as noted for bacteria in regard to the presence on surfaces and in the distribution water itself.

3. Importance of Filamentous Fungi in Drinking Water Environments

The possible public health importance of filamentous fungi in drinking water has been indicated by the isolation of a pathogenic fungus, Pe- triellidium boydii, from drinking water pipe joints (Roesch and Leong, 1983), and by the observation that some fungi in aquatic environments produce humic substances (Day and Felbeck, 1974) which may subsequently act in the presence of chlorine as precursors for trihalomethanes (THM). THMs are formed in the presence of chlorine, and because many of this class of compounds are suspected human carcinogens their levels in drinking water are limited to 100 pglliter in the United States. Furthermore, a number of filmentous fungi isolated from drinking water have been found to be positive for mycotoxin production, at least under laboratory conditions (Rosenzweig et al., 1983).

As stated in Standard Methods for the Examination of Water and Waste- water (APHA, 1980), the “amount of chlorine or other disinfectant required for fungal control is essentially unknown.” However, several recent studies have indicated that filamentous fungi, in both the vegetative and spore form, are somewhat more resistant to chlorination than are coliforms (Ah0 and Hirn, 1981; Rosenzweig et al . , 1983). Fungi growing in pipe joints may be particularly well protected from the effects of chorination, as a 350-400 ppm initial dose over a 3-day contact period was insufficient to inactivate the previously mentioned pathogenic fungus in core samples taken from caulk in pipe joints (Roesch and Leong, 1983). Consequently, the pipeline had to be abandoned. From the limited information available, the resistance of filamentous fungi to ozone appears to be similar to that of bacteria such as E . coli and P . aeruginosa (Haufele and Sprockhoff, 1973).

With the currently available information, it is not possible to accurately judge the ecological and management importance of filamentous fungi in drinking water distribution systems. However, it is clear that some filamen-

104 I3El-N H. OLSON AND LASLO A. NAGY

tous fungi can grow actively in such environments, as indicated by observations of fungal mycelia in biofilm on the surface of drinking water reservoirs (Schoenen and Dott, 1977; Schoenen et al . , 1981), drinking water storage tanks (Seidler et al . , 1977), and drinking water pipe joints (Roesch and Leong, 1983).

Filamentous fungi have also been found to increase in number as water moves from the treatment plant to the consumer (Bays et al . , 1970), contribute to taste and odor problems (Burman, 1965), and frequently appear in hydrant washings from dead ends (OConnor et al . , 1975; Rae, 1981).

E. YEASTS

Yeasts, or nonfilamentous fungi, have received even less attention in drinking water systems than their filamentous counterparts. Although a number of studies have observed yeasts in drinking water systems, very few have identified and even fewer have enumerated these organisms in the water or on surfaces.

1. Yeusts in Drinking Wuter

Yeasts have been isolated from hydrant washings (O’Connor et al . , 1975), tap washings (Reilly and Kippin, 1983), and from regular drinking water (LeChevallier et a l . , 1980). They were found to number 2.3% of the bacterial population (LeChevallier et al., 1980) on media formulated for bacterial isolation and enumeration. Rosenzweig et ul. (1983) isolated and identified three species from drinking water (Cryptococcus luurentii, Rhodotorulu glutinis, and Rhodotorula rubra), which they subsequently used in chlorine resistance experiments. Stantlard Methods for the Examination of Water and Wastewater suggests the use of Diamalt agar or quantitative enrichment agar for isolating yeast from water, although Sabouraud dextrose (supple- mented with 33.3 mg/ml rose bengal and 80 mg/ml streptomycin) has also been used effectively (Rosenzweig et al . , 1983). Membrane filtration on a suitable medium would probably provide the most acceptable results (Buck and Bubucis, 1978). The accurate enumeration of yeasts in drinking water is complicated by their nonfilamentous growth pattern, which makes their colonies difficult to distinguish from the usually more numerous but similar looking bacterial colonies. Only microscopic examination for cell size (at x400 or X1000) allows differentiation of the two groups.

2 . Yeasts on Drinking Water Distribution System WalllPipe Surfaces

Only one investigation so far has reported on the occurrence of yeasts on the surface of drinking water pipes (Nagy and Olson, 1984). In this study


yeasts were enumerated on Czapek, nutrient, and Sabouraud dextrose agars (using microscopy to differentiate between yeast and bacterial colonies) and then identified using the AP1-2OE system. Frequently occurring yeasts were Cryptococcus albidus, C . laurentii, Rhodotorula minuta, R . glutinis, R. rubra, and Sporobolomyces salmonicolor, some of which have also been isolated from drinking water (Rosenzwieg et al . , 1983).

3. lmportance of Yeasts in Drinking Water Environments

It is difficult to evaluate the public health or ecological/management importance of yeasts in drinking water distribution systems. There is relatively little information from drinking water environments on this group of microorganisms; however, the topic would probably be a promising area of research, especially since one yeast, Candida albicans, has been suggested as a possible indicator organism in water quality analysis (Buck and Bubucis, 1978; Sherry et al . , 1979; Svorcova, 1982).

Yeasts thus far isolated and identified from drinking water are of some public health importance, but are not actual pathogens. The chlorine resistance of yeasts from drinking water is slightly higher than that of bacteria (Rosenzweig et al . , 1983) but their ozone resistance is approximately the same (Farooq and Akhlaque, 1983; Haufele and Sprockhoff, 1973).

F. ALGAE

Algae can be observed in most aquatic environments, and consequently are present in drinking water environments, particularly if a light source is present. In a survey of water supplies (Mackenthun and Keup, 1970), algae were the organisms creating the greatest number of reported problems, affecting about three times as many supplies as iron bacteria, the next highest category. (For the purposes of this discussion blue-green algae will be regarded as part of the algae group.)

1 . Algae in Drinking Water

Numerous studies and reports have pointed out the widespread occurrence of algae in drinking water (Baylis, 1930; Berry, 1932; Committee Report 1953, 1983; Committee on Water Supply 1930; Kay et al., 1980; Mackenthun and Keup 1970; Palmer, 1960, 1961; Rae, 1981; Silverman et al., 1983; Task Group Report, 1966). Most of this widespread occurrence results from the use of uncovered finished water reservoirs within the distribution system (Baylis, 1930; Committee Report, 1983; Committee on Water Supply, 1930; Palmer, 1960, 1961; Silverman et al., 1983). Several investigators have attempted to enumerate and in some cases identify algae in such finished drinking water reservoirs (Kay et al . , 1980). These enumera-

106 BE" H. OLSON AND LASLO A. NAGY

tion procedures rely on light microscopy, with a number of different techniques available in Standard Methods for the Examination of Water and Wastewater (APHA, 1980). These techniques usually express their results in terms of algae cellslmilliliter with average numbers for finished drinking water reservoirs in the 10'-10$ cells/ml range (Kay et at., 1980; Silverman et a l . , 1983; Sykora et al., 1980). The water entering these reservoirs is usually of relatively high quality with very low leyels of algae. However, during the time period of detention, water quality decreases and algal numbers increase (Committee Report, 1953, 1983; Committee on Water Supply, 1930). This increase can be relatively dramatic (Kay et al., 1980; Silverman et al., 1983) and usually occurs in the warmer months. One of the main parameters influencing algae numbers in such finished drinking water reservoirs is temperature, however reservoir flow-through rate may also be critical (Kay et al., 1980; Silverman et al . , 1983). Frequently observed algal genera are green algae such as Chlorella, Ankistrodesmus, and Scenedesmus; the blue- green, Schizothrix, and the diatom, Glenodinium (Kay et al., 1980). Of these, Chlorella appears to be particularly widely distributed and adapted to finished drinking water reservoirs (Kay et al., 1980; Silverman et al., 1983). Water from reservoirs frequently carries with it an algal load, and despite chlorination practices, the algae frequently survive passage through the distribution system (Kay et al., 1980).

2. Algae on Drinking Water Distribution System WalllPipe Surfaces

Algae, usually diatoms, have often been observed in encrustations on the surface of drinking water pipes (Allen et al . , 1980). Organisms associated with these walls are usually of the same genera as those found in high numbers in the water (Kay et al., 1980; Smith, 1972) once again reinforcing the previously noted similarities between microorganisms in the water and those attached to surfaces.

3. Importance of Algae in Drinking Water Environments

Although algae themselves have minimal public health significance in drinking water systems, their presence in such systems could result in some secondary public health concerns. The tastes and odors that algae may add to water could cause a loss of public confidence in the water supplier (Palmer, 1960) and the utilization of alternative, perhaps less wholesome, sources. Furthermore, the chlorination of water leaving finished drinking water reservoirs could substantially increase the THM content of those waters (Hoehn et al . , 1980; Kay et al . , 1980; Veenstra and Schnoor, 1980; Oliver and Schindler, 1980). As stated above, THMs are suspected human carcinogens, and their levels are strictly regulated by the USEPA.

With the exception of copper in reservoirs, the impact of various disinfec-


tants upon the different algal populations in drinking water is relatively uninvestigated. Chlorine appears to be highly algicidal for Chlorella (Kay et al., 1980) and it is probably also relatively effective against other green algae. Chlorination can be a useful control measure for reducing algal blooms in finished drinking reservoirs although copper is probably more widely utilized (Committee Report, 1953, 1983; Committee on Water Supply, 1930; Flentje, 1952; Muchmore, 1978; Palmer, 1961).

Most of the ecological or management problems caused by algae in drinking water systems originate in uncovered finished water reservoirs and would be dramatically reduced if the reservoirs were covered. This solution has been long obvious to the drinking water industry (Committee Water Supply, 1930); however, its implementation has been considerably more difficult.

G . PROTOZOA

Apart from a few pathogenic species, protozoa have not been investigated in detail in drinking water distribution systems. However, several reports have pointed out their frequent occurrence in such systems (Chang, 1960, 1961; Cooper and Brown, 1983; Ingram and Bartsch, 1960) and since most protozoa feed on detritus and bacteria, their presence in drinking water is not unexpected.

1 . Protozoa in Drinking Water

Protozoa in both the ciliate and amoeboid form are commonly observed in uncovered finished water reservoirs (Ingram and Bartsch, 1960). Amoebae have also been observed, during regular monitoring, in uncontaminated distribution systems (Chang, 1960; Cooper and Bowen, 1983). A number of different isolation and enumeration techniques, usually developed for pathogenic protozoa, are available (APHA, 1980).

Approximately half of the treated potable water samples from one distribution system were positive for free-living amoebae (Cooper and Bowen, 1983). Numbers of amoeba ranged from <1 to 17 per 1000 ml with older parts and dead ends of the distribution system representing a disproportion- ately greater share (Cooper and Bowen 1983). The most frequently isolated genus in treated waters is Hartmannella (Chang, 1960; Cooper and Bowen, 1983), although Naegleria, Echinarnoeba, and Acanthamoeba have also been recorded (Cooper and Bowen, 1983).

2. Protozoa on Drinking Water Distribution System WalllPipe Surfaces

Protozoa have been reported in slime or biofilm on the surface of finished water reservoirs (Dott et al., 1979; Schoenen and Dott, 1977; Schoenen et

108 BETIY H. OLSON AND LASLO A. NAGY

al., 1981; Thofern et al., 1978). Ciliate as well as flagellate forms have been observed (Dott et al., 1979; Schoenen et al., 1981), with numbers in one instance in the range of 105/ml of biofilm (Schoenen et al., 1981). The genera Bodo, Vorticella, Uronemu, and Euplotes have been observed in such environments (Schoenen et al., 1981).

3. Importance of Protozoa in Drinking Water Environments

Most protozoa have little or no public health importance in drinking water environments. However, Giardia lamblia, Entamoeba histolytica, Balan- tidium coli, Naegleria floweri, and the genus Acanthamoeba are regarded as protozoan pathogens that can be acquired from known drinking water supplies (Sobsey and Olson, 1983). However, these pathogens usually are present only as a result of some gross contamination, or negligence. Relatively little is known about the impact of various disinfectants on the different protozoan groups. However with some pathogenic protozoa, such as Giar- dia, the cyst form is apparently more resistant to chlorine than are coliforms or viruses (Jarroll et al., 1981; Rice and Hoff, 1981; Rice et al., 1982). Additionally, cyst-forming amoebae are generally resistant to chlorine residuals greater than 0.3 mg/liter (Cooper and Bowen, 1983).

The ecological or system management importance of protozoa in drinking water environments is difficult to evaluate. High protozoan numbers probably indicate high levels of bacteria or soluble organics in the system. The presence of non-cyst-formers signifies low to absent chlorine residuals. But both of these parameters (bacterial levels and free chlorine residuals) could be assessed directly, without a need to determine protozoan levels. Ex- tremely high or sudden increases in protozoan levels should act as a warning to system operators, however, and the cause of the increase should be investigated in detail.

H. OTHER ORGANISMS

Although this review is specifically concerned with microorganisms, it should be mentioned that numerous other larger organisms can also occur in drinking water distribution systems (APHA, 1980; Ingram and Bartsch, 1960; Mackenthun and Keup, 1970). These include sponges (Ingram and Bartsch, 1960), water lice (Phillips, 1968), cyclops (Crabill, 1956), nematodes (Chang, 1960, 1961; Chang et al . , 1959, 1960; Schonen et al., 1981; Thofern et al., 1978), and bloodworms (Silvey, 1956), as well as snails, clams, and insects (Ingram, 1956, Ingram and Bartsch, 1960).

MICROBIOLOGY O F P O T A B L E W A T E R 109

V. Distribution System Dynamics

A. ECOLOCXCAL PROCESSES

A solid object such as a pipe surface in contact with flowing water will undergo a series of physical-chemical and biological modifications at the solid-liquid interface (Characklis, 1973a,b, 1981; Marshall, 1976). These modifications consist of four main stages (Characklis, 1981) which are sum- marized as follows: (1) absorption of organic molecules onto solid surface; (2) adhesion of microorganisms to this “conditioned” surface: (3) continued adhesion and/or multiplication of microorganisms forming biofilm at the solid- liquid interface; and (4) dynamic equilibrium of biofilm with film growth and film destruction in relative balance.

The overall process can be regarded as a microbiological succession start- ing with a conditioned surface that supports a primary, then a secondary, and finally a climax community of microorganisms (Alexander, 1971; Hud- son, 1968; Webster, 1970). A distribution system pipe surface can thus be viewed as a microbial ecosystem increasing in complexity over time until the development of the dynamic equilibrium/climax state. From investigations of microbial successions at solid-liquid interfaces it appears that the primary colonizers are invariably bacteria with certain physiological characteristics. These characteristics allow the bacteria to produce sticky extracellular slime covers, generally composed of polysaccharides and water (Characklis, 1973a). Such slime coats would have obvious ecological advantages in drinking water systems as they would facilitate adhesion to surfaces and afford better protection against chlorine (Reilly and Kippin, 1983). Scanning electron microscope studies have in fact revealed the presence of bacteria with possible extracellular slime layers on distribution pipe surfaces (Ridgway and Olson, 1981).

Once slime-producing bacteria colonize a pipe surface, inorganic and organic particles as well as cells of other microorganisms can become en- trapped in the matrix (Characklis 1973a, 1981). The new arrivals can be bacteria or other microorganisms and they may grow and become part of the biofilm, or die and together with other dead cells add to the biochemical/nutritional diversity of the matrix.

Microbial successions range in duration from a few months (Harper and Webster, 1964; Nagy and Harrower, 1979, 1980) to a number of decades (Rayner, 1977a, b). Generally, their duration is inversely proportional to the range and concentration of available nutrients in the particular ecosystem. In drinking water distribution systems the time required for the microbial succession to reach dynamic equilibrium is unknown, however, the relatively low levels of nutrients probably serve to extend the duration.


A number of papers have suggested rate-limiting factors for microbial successions on distribution system pipe surfaces. These include physical, chemical, and biological parameters such as pH, temperature, redox potential, TOC, chlorine residual, hardness, mineral content, etc. (Geldreich et al., 1972; Goshko et al., 1981; Hutchinson and Ridgway, 1977; LeChevallier et al., 1981; Lee et al., 1980; NAD-NRC, 1982; Olson et al., 1981; Reilly and Kippin, 1983; Shindala and Chisholm, 1970; Tuovinen et al., 1980; Vic- toreen, 1974). There is widespread agreement that free residual chlorine is a critical rate-limiting factor for the microbial succession, as is total organic carbon (Ainsworth et al., 1980).

There is also general agreement concerning the idea of microbial detachment from pipe surfaces. It has been suggested that the flow of water within the pipes enhances the removal particles and attached microorganisms from surfaces (Baylis, 1930, 1938; Geldreich et al., 1972; Goshko et al., 1981; Howard, 1940; Olson et a l . , 1981; Shannon and Wallace, 1944; Shindala and Chisholm, 1970; Tuovinen et al., 1980), which then reenter the water distribution system and are delivered to consumers. Depending upon free chlorine residuals and water utilization, these resuspended microorganisms may or may not be of public health importance. Although it is generally accepted that drinking water pipes act as sites for microbiological successions, that free residual chlorine is important in controlling both attached and detached microbial aftergrowths, and that microorganisms from the pipe surface can reenter the passing water, few studies have evaluated these ideas directly under field conditions.

B. SYSTEMS MODEL

As suggested by previous authors (Anon., 1982; Armstrong et al., 1981; Baylis, 1930, 1938; Ewing and Hopkins, 1930; Goshko et al., 1981; Howard, 1940; Larson et al., 1960; Olson et al., 1981; Shannon and Wallace, 1944; Shindala and Chisholm, 1970; Tuovinen et aZ., 1980), flow rates influence bacterial levels in drinking water at a single site, such that as flow rates increase bacterial levels also increase per unit volume of water (Nagy, 1984). This has important monitoring consequences, as most distribution systems experience considerable flow fluctuations in any 24-hour period (Fig. 3; Walker, 1978). The correlation between flow rates and bacterial levels indicates that the microbiology of distribution systems is highly dynamic. Monitoring efforts often fail because the importance of flow changes on microbial levels is not considered. Disregarding an important component of sample variability may produce confounding results, unless samples are taken at the same time of day and site conditions remain very similar.

An increase in the microbiological levels of drinking water as a result of


400 r

50 t 01 ' I

12 2 4 6 8 10 12P 2P 4P 6P 8P 1OP 12

HOUR OF DAY

FIG. 3. Water flow in a typical distribution system.

passage through the distribution system is often but not always observed (Baylis, 1930, 1938; Geldreich et al . , 1972; Hutchinson and Ridgway, 1977; MacKenthun and Keup, 1970; NATO, 1982; Victoreen, 1969, 1974). Hutchinson and Ridgway (1977) showed a decrease in average free residual chlorine levels (from 0.21 to 0.02 mg/liter) as the water moved from the intermediate to the end sections of the distribution system and a general increase in bacterial numbers per milliliter. Similarly, Reasoner and Geldreich (1979) found a 2 log increase in heterotrophic bacteria in drinking water as a result of passage through 42 km of pipes. However, Nagy (1984) observed a decrease in bacterial levels with distance traveled, as did Haas et al., (1983). A model to explain these contradictory results is presented in Fig. 4. This descriptive model relies on two factors which act as opposite forces on bacterial numbers. These are free chlorine residual (contact time) and detachment of bacteria from pipe surfaces. Most chlorine disinfection analyses indicate that after a contact time of 5-10 minutes very little additional change in bacterial numbers is observed (Safe Drinking Water Com- mittee, 1980) at free residual levels of approximately 1 mg/liter. However, most disinfection studies have been conducted under laboratory conditions and it is highly probable that bacteria under field conditions would exhibit higher survival if not actual resistance (Safe Drinking Water Committee, 1980). There is evidence to indicate that heterotrophic bacteria recovered from chlorinated drinking water systems have a higher tolerance to chlorine than those isolated from unchlorinated systems (Ridgway and Olson, 1982). High levels of bacteria have on numerous occasions been isolated from drinking water with free residual chlorine levels in the range of 0.4-0.7 mg/liter (Olson et al . , 1981). Laboratory studies for both bacteria and viruses

112

W

g; W A -11

Y o

u w R W

U. a

Laboratory D

BETTY H . OLSON AND LASLO A. NAGY

'\ \

IRerampling Field Studies) Source to Site Studies and fection Studies Chlorine-Bacteria Correlation Studies

FIG. 4. A conceptual model for the relationship between chlorine levels, contact time, and bacterial detachment in a drinking water distribution system.

have suggested increased tolerance after repeated exposure to this disinfectant (Leyval et al., 1983; Schatter et al., 1980). Field studies have shown that Legionella pneumophila, Flavobacterium sp., and nontuberculous mycobac- teria lose their tolerance to chlorine after subculturing under laboratory conditions (Wolfe et al . , 1984; Carson and Favero, 1984; Kutcha et al . , 1984).

At relatively short contact times (0-30 minutes) considerable decreases are observed in bacteria levels due to inactivation. This is followed by a period (probably 1-6 hours), when the more resistant bacteria in the water are gradually inactivated. These bacteria may be biochemically or physically less susceptible to the biocidal effects of chlorination, due to such characteristics as clumping (Reilly and Kippin, 1983) or attachment to particulate materials (Ridgway and Olson, 1981). At these middle contact times, the contribution provided by detachment begins to increase gradually, such that a point is reached where the reduction produced by chlorine is the same as the increase from the pipe surface, as shown in Fig. 4. Beyond this contact time (probably over 8 hours), bacterial levels increase in drinking water as a result of passage down a distribution system, because the contribution from the pipe surface is greater than the reduction due to chlorination.

This descriptive model (Fig. 4) brings together the observations of disin-


fection studies using short contact times and usually high chlorine levels with field experiments that test water with a range of contact times and bacterial levels. Laboratory studies (Butterfield et al., 1943; Haas and En- glebrecht, 1980a,b; Kruse et al., 1970; Morris, 1966; Safe Drinking Water Committee, 1980; Scarpino et al., 1974; Skaliy et al., 1980; Wang et al., 1982) have found dramatic decreases in bacterial levels over time in a given body of water, and because these experiments were carried out under controlled conditions, they could ensure that (1) the same water was resampled over time, (2) the chlorine demand remained stable, and (3) bacteria tested were washed and disaggregated.

Field experiments on the other hand have usually, but not always, found a negative correlation between free residual chlorine and bacterial levels, although the same body of water was not resampled (Goshko et al., 1983; Haas et ul., 1983; Hutchinson and Ridgway, 1977; LeChevallier et al., 1980; Olson et al., 1981; Reasoner and Geldreich, 1979; Shannon and Wallace, 1944). Recent experiments have allowed resampling of the same body of water in the field and have also measured contact times (Nagy, 1984).

Interestingly, the descriptive model predicts that free residual chlorine and bacterial levels will positively correlate in the early sections, not correlate over the middle sections, and show negative correlations in the later sections of the distribution system. This explains the observed results of Nagy (1984), where in field resampling (flow) experiments, there was a simultaneous decrease in both free residual chlorine and bacterial levels in an early section of a distribution system. The model also explains some unusual findings by other investigators (Goshko et ul., 1983) who have noticed significant positive correlations between chlorine levels and coliforms in some, and significant negative correlations in other distribution systems. According to the above model such results are possible if one system has a short and the other a long contact time before water reaches the consumer or the sampling site.

VI. Future Research

As stated in Section I the need to understand how the organisms of interest function in potable water is of great importance. This is likely to be achieved only if an ecological approach is adopted. An incomplete understanding of systems and processes has led to anecdotal and contradictory results. The most obvious of these contradictions are found in the disinfection literature. The vast majority of disinfection work has focused on the use of laboratory or environmental pure culture organisms which are grown under optimal conditions, harvested, washed to remove chlorine demand, disaggregated, and then subjected to the disinfectant in sterile, demand-free

114 BE’ITY H. OLSON AND LASLO A. NAGY

water. Although such a system is excellent in allowing the development of models of disinfection, it is difficult to see how these studies relate to natural environments where bacteria are usually in a static state, aggregated, covered with extracellular polysaccharides, and in a water milieu containing one or more interfering compounds. All of these factors will influence disinfection efficiency. As the model in Fig. 4 indicates, a holistic view of a system often leads to sensible explanations for previously divergent views (in this instance disinfection efficiency) and does not require complete knowledge of all variables. This points to the need to develop methods which are concerned with estimating the survival of microorganisms under natural conditions.

The recent work of Ward et al. (1982) indicated that mixed natural populations of microorganisms had distinctly different die-off curves than pure cultures in the presence of chloramines and free residual chlorine, reflecting differences in susceptibility to each disinfectant. Further, the concept of environmental strains being more “hardy” than culture collection organisms may be inaccurate. Ward et al. (1984) have shown that the phenomenon is not one of environmental versus culture collection, but rather one of strain differences in susceptibility. In the future it is hoped that greater emphasis will be placed on understanding the many competing and complex factors which exist under field conditions and that more techniques will be developed to assess disinfection efficiency under in situ conditions.

Another area of growing concern (and of increasing appreciation of its complexity) is the meaning and validity of the coliform as an indicator organism. This subject seems to be discussed by scientists approximately every 20 years only to reconfirm the conclusion that the best available indicator is the coliform. Yet, with the methodology that exists today, it should be possible for microbiologists interested in potable water to develop more sensitive and specific measures of water quality. The relative conservatism of the water community in demanding foolproof solutions, which have as yet never been attained, inadvertently decreases the possibility for investigators to introduce innovation and perhaps to move the field forward. It strikes us as interesting that since the introduction of the basic coliform test in the late 1800s, little has changed except for the development of membrane filtration and a few modifications in the ingredients of the media. One could, of course, argue that the method was so good that it could not be improved upon, but all that is necessary to dispel this idea is to ask microbiologists what they think of the testing procedure and its relationship to public health. Unfortunately, microbiologists are told that alternative methods are too ex- pensive or too difficult for water treatment personnel to handle. We believe that individuals involved in protecting the safety of drinking water should be required to be well trained and that testing should not be limited to tests which are inexpensive but only partially accurate.


r 0.100

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7

FIG. 5. Relationship between disease risk and viruses, coliforms, and fecal coliforms (after Mechalas et al . , 1972).

The relationship between indicators and incidences of waterborne disease outbreaks has resulted in various models. Figures 5 and 6 show the relationship between coliforms or fecal coliforms, respectively, and the risk of illness of viruses and SaZmonelZa. However, according to a compilation of data presented by Sobsey and Olson (1983), this relationship seldom seems to hold in actual outbreaks. The numbers of coliforms are usually exceed- ingly low if present at all and frequently no records exist on coliform levels. Even in the best documented case for coliform occurrence, the number of coliforms detected was far below the level which would have predicted disease according to these models. This points to the importance in understanding pathogen-indicator relationships and emphasizes, in the absence of such knowledge, the need for small systems to frequently monitor for indicators.

Both microbiologists and engineers need to have a greater understanding of the interactions of the physical, chemical, and microbiological compo- nents of water treatment and distribution. The recent results of Wadowsky


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0 10 20 30 40 50 6 0 7 0 COLIFORM (10’ MPN1100rnl)

I 1 I

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FECAL COLIFORM (lo3 M P N I I O O ~ I ) FIG. 6. Relationship between disease risk and salmonella coliforins, and fecal coliforms (after

Mechalas et al., 1972).

and Lee (1983) showing that LegionelZn’s presence in distribution systems is due to symbiotic relationships with the natural flora in pipe sediment have both public health as well as management implications. However, it is doubtful that such an understanding would have arisen without an applied ecological approach. Too often a report in the literature ignores the chemistry of a water supply or does not adequately describe the physical system. This lack of description leads to an incomplete understanding of the major question being asked, which in turn produces controversial results. In reality these contradictions can often be explained by simple differences of environment. Investigators with an incomplete understanding of an environment or an approach which is solution oriented may resolve a problem for the moment, but too often it recurs with no available explanation. This has produced a field of anecdotal works which contribute only in a minor way to the understanding of broad concepts and solutions toward which the field strives. Hence, as seen in this review, investigators in the 1970s were asking basically the same questions as those in the 1940s. If a clearer understanding of the ecological parameters which promote or decrease disease transmission in water systems is achieved, better design and operation of facilities will be possible which in turn will result in better protection of public health.

The value of microbiology in understanding water treatment management and distribution maintenance has only recently been appreciated. The po-


tential now exists for drinking water microbiology, with its ecological approach, to move the field from a science concerned only with public health hazards into a broader based discipline concerned also with system management through the use of microorganisms. But here again, it is necessary to view the system as an integrated whole. Bacteria may play an important role in one phase of a process, such as corrosion, but they are often ignored in the examination of the problem because historically the process has been viewed to be only chemical or physical. In reality, it is generally accepted that few multicompartment systems function in this manner. The task ahead for potable water microbiologists is to extend their knowledge and training in the fields of chemistry, engineering, and ecology. If this is done many questions currently left unanswered will fall into place as the ecology of microorganisms in the treatment process or the distribution system is finally understood.

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