Waterborne Outbreak Control: Which Disinfectant?

Environmental Health PerspectivesVol. 46, pp. 7-12, 1982

Waterborne Outbreak Control:Which Disinfectant?by Elmer W. Akin,* John C. Hofft and Edwin C. Lippy*

Drinking water disinfection was shown to be an important public health measure around theturn of the century. In the United States, it was perhaps the single most important factor incontrolling typhoid fever, a waterborne disease that was rampant throughout the world duringthe last century. It may also be assumed that disinfection was important in limiting the numberof cases of other diseases known to be capable of waterborne transmission, i.e., cholera,amebiasis, shigellosis, salmonellosis, and hepatitis A.Even though modern treatment has eliminated water as a major vehicle of infectious disease

transmission, outbreaks still occur. In fact, the annual number has been increasing since 1966.Interruption in chlorination or failure to achieve adequate levels of chlorine residual is the mostoften identified deficiency of the involved water supplies. This finding indicates that waterbornemicrobial pathogens remain as a potential health threat and underscores the importance ofdisinfection.From the outset, chlorination has been the drinking water disinfectant of choice in the

country. Numerous studies have demonstrated its ability to inactivate bacterial, viral, andprotozoal pathogens when applied under proper conditions. However, the finding that chlori-nated organics that are potentially carcinogenic are formed has prompted an evaluation ofalternative disinfectants. The viable alternatives to chlorine currently under consideration forwidespread use are ozone, chlorine dioxide, and chloramines. In terms of biocidal efficiency,ozone is the most potent of the three. Chlorine dioxide is about the equivalent of free chlorine inthe hypochlorous acid form but much more efficient than the hypochlorite form of free chlorine.The chloramines are weaker biocides than hypochlorite. Although this general order of rankingof efficiency holds for diverse types of microorganisms, quantitative comparisons vary withdifferent microorganisms and experimental conditions.

Since the turn of the century, the benefits topublic health from the disinfection of drinkingwater have been broadly recognized. The discoverythat water could be a major vehicle of diseasetransmission preceded scientific verification of thegern theory of disease in the late 1800s. In 1854,John Snow made his classic deduction that a watersupply was responsible for a severe cholera epi-demic that was localized in a section of London,

*U.S. Environmental Protection Agency, Health EffectsResearch Laboratory, Cincinnati, Ohio 45268.

tU.S. Environmental Protection Agency, Municipal Envi-ronmental Research Laboratory, Cincinnati, Ohio 45268.

England. The outbreak that had caused 500 deathswas interrupted by removal of the handle on theBroad Street pump. A hint of the importance ofwater disinfection for disease control had actuallybeen reported in 1835. Human Health, published inPhiladelphia, stated that marsh water could bemade potable by the addition of a small quantity ofchlorine (1).Concomitant with the recognition and acceptance

of drinking water as a significant route of infectiousdisease transmission was the introduction of thedisinfection process. In those early years, as now inthis country, disinfection was synonymous withchlorination. In 1888, patents were issued on an

brought to you by COREView metadata, citation and similar papers at core.ac.uk

provided by PubMed Central

8

electrolytic treatment process that generated chlo-rine from chloride of lime. The practice of chlorina-tion of drinking water supplies spread throughoutthe major cities of the U.S. as the chlorine deliveryprocess improved and experience revealed its micro-bial destructive power. It is interesting to note thatthe theory of chlorination chemistry that developedduring the early 1900s indicated that nascent oxy-gen was responsible for the microbicidal action ofthe process. This theory, which also fostered inter-est in ozone as a disinfectant, was held untildisproven in 1944 (1).

Waterborne DiseasesThe most widely recognized achievement of drink-

ing water treatment in the U.S. has been thedramatic reduction in typhoid fever which in largepart is attributed to this single public healthmeasure. The disease caused by an enteric bacte-rium was known to be waterborne with an esti-mated 40% of the cases attributed to this route oftransmission. In 1900, the typhoid death rate in theU.S. had been 36 per 100,000 population, i.e.,25,000 deaths. As water treatment, including disin-fection, became an increasingly common practice,the death rate decreased to 20 and 3 per 100,000 in1910 and 1935, respectively. Perhaps Cincinnati'sexperience was typical. At the turn of the century,the city's water supply was the Ohio River withpotability produced by only natural sedimentationto reduce settleable solids. The average annualtyphoid fever illness rate during this time wasalmost 400 cases/100,000 persons. In 1907, the cityadded coagulation and rapid sand ifitration treat-ment processes, and typhoid fever rates droppedprecipitously. Chlorination, introduced in 1915, wasfollowed by a second major reduction to a level lessthan one-tenth the rate reported for the year priorto introduction of water treatment (2).Success in control of this disease by water

treatment may better be illustrated by the declinein the reported cases of waterborne typhoid in theU.S. over the past 40 years (Fig. 1). In contrast toan annual average of 385 cases reported for theperiod 1940-45, no waterborne cases were reportedduring the 1976-79 period. A single typhoid out-break resulting in 212 cases was responsible forincreasing the annual average for 1971-75 from 2 to44 cases. This outbreak resulted from the ingestionof contaminated ground water at a migrant workcamp in Florida.In addition to typhoid fever, other enteric patho-

gens have been associated with waterborne dis-ease. The most widely recognized waterborne viral

AKIN, HOFF AND LIPPY

FIGURE 1. Average annual number of cases of typhoid fever inU.S. occurring in waterborne outbreaks from 1940 through1979.

disease is hepatitis A. Mosley (3) compiled a list of50 published reports worldwide of infectious hepa-titis outbreaks attributed to contaminated drinkingwater. Epidemiological investigation has clearlyshown this association even though disease mani-festations normally do not appear until approxi-mately 30 days after ingestion of contaminatedwater. Cholera and dysentery were rampant water-borne diseases during the 1800s but became lessimportant in this century. Water disinfection mostassuredly was important in their decline; however,the specific impact is not well documented.

Waterborne OutbreaksAlthough the number of cases of waterborne

infectious disease has been greatly reduced sincethe adoption of a standardized treatment processfor unprotected surface water, outbreaks still occur.Actually, the annual number of reported outbreakshas been increasing since 1966 (Fig. 2). In 1979, thelatest year for which complete data are available,43 outbreaks were reported that resulted in 7,500cases of illness. Preliminary information for 1980shows a further increase in the number of cases.Outbreaks are reported on a voluntary basis to theCenters for Disease Control by state health agen-cies. Generally, there is not a concentrated effort todocument occurrence of outbreaks and significantunder-reporting is suspected. EPA is attempting todetermine the actual occurrence of waterborneoutbreaks through the support of studies in threestates. The objectives are to design, implement,and evaluate a comprehensive surveillance system.

DISINFECTION AND INFECTIOUS WATERBORNE DISEASE

(a 50-

40-U.

0

cc

30-

z

4 2

tD41 10- 11|l|lllll

4C

FIGURE 2. Average annual number of waterborne disease out-

breakis occurring in U.S. from 1920 through 1979.

Investigations in one state uncovered seven out-

breaks in the first 9 months of the study. In the

previous year, only one outbreak had been reported

through the normnal surveillance procedures.

The most commonly occurring syndrome associ-

ated with waterborne illness is gastroenteritis that

may be caused by a variety of microorganisms

including viruses, bacteria, and protozoa. The fre-

quency of each disease entity for outbreaks occur-

ring between 1971 and 1977 is shown in Table 1.

Acute gastrointestinal illness is a nonspecific cate-

gory for which no known pathogens were identified.

A group of viruses which have recently been

observed by electron microscopy in the stools of

outbreak victims is believed to be important in the

etiology of this illness. Infectious hepatitis caused

by hepatitis A virus is the most widely recognized

waterborne virus illness. Epidemiological investiga-

tions have confirmned the waterborne transmission

of this disease on numerous occasions. Since 1977,

the protozoan Giardia lamblia has produced perhaps

Table 1. Etiology of waterborne disease outbreaks in the

U.S., 1971-1977.a

Outbreaks, Cases ofType of illness % illness, %

Acute gastrointestinal illness 57 58Chemical poisoning 12 3Giardiasis 10 18Shigellosis 9 14Hepatitis A 8 1Salmonellosis 2 3Typhoid 2 <1Enterotoxigenic E. coli <1 3

100 100

aData of Craun (6).

the largest number of waterborne disease cases andoutbreaks. Its occurrence in "pristine" mountainstreams contaminated by fecal waste of wild ani-mals (especially beavers) has taken advantage ofless vigorous water treatment procedures normallyrequired for surface water sources (4). Inactivationof Giardia cysts requires more stringent control ofthe disinfection process than normally employed bymany water utilities (5).

Conventional treatment, i.e., coagulation, sedi-mentation, filtration and chlorination, as it is com-monly practiced in this country, coupled with anuncompromised distribution system, appears ade-quate to prevent waterborne infectious disease.However, the integrity of water systems is notassured and outbreaks are associated with breachesof these conditions. Table 2 indicates the causes ofwaterborne outbreaks in municipal and semipublicsystems. Treatment deficiencies were importantcauses in both systems. Failure to maintain uninter-rupted chlorination at an adequate chlorine concen-tration was found to be the single most importanttreatment deficiency (6). This was believed to bethe cause of a recent gastroenteritis outbreakassociated with a groundwater supply in a Texascommunity that affected approximately 8000 resi-dents. The symptoms, i.e., rapid onset of diarrheaand abdominal cramps accompanied by headacheand nausea, were typical of enteric microbial dis-ease. However, no etiological agent has yet beenidentified. About 30 cases of hepatitis A were alsoassociated with this outbreak (Lippy, unpublisheddata).

Water DisinfectionAlthough virus isolations from disinfected drink-

ing water have been reported (7), most healthauthorities believe that chlorination, when prac-

Table 2. Waterborne disease outbreaks in the U.S., 1971-1977:type and deficiencies of water systems.a

Percent of outbreaks

Municipal SemipublicDeficiency systems systemsUntreated surface waterb 14 9Untreated ground water 10 43Treatment deficiencies 28 40Distribution deficiencies 40 2Miscellaneous 8 6

100 100

aData from Craun (6).bIncludes giardiasis outbreaks in chlorinated, but not filtered,

systems.

9

10

ticed under recommended conditions, is adequatefor preventing the transmission ofpathogens throughdrinking water. The current widespread use of freeresidual chlorine for disinfection of drinking waterevolved as a result of developments in our knowl-edge of chlorination chemistry and the biocidalcapabilities of various forms of chlorine. Earlywater chlorination practice was termed simplechlorination or marginal chlorination. It consistedof adding chlorine as a final step after filtration orthe use of chlorine as the only treatment. In theearly 1900s, observations indicating that bacterici-dal action continued even after free chlorine haddisappeared, and the subsequent discovery that thecombined chlorine products formed also had disin-fecting capabilities led to the widespread use ofchloramines. In part, this change was made becausethe use of chloramines eliminated the tastes andodors caused by the reactions of free chlorine withphenols and other organic compounds. Later, rec-ognition of the superior biocidal capabilities of thehypochlorous acid form of free residual chlorine anddevelopment of the "breakpoint" concept resultedin changing to the current predominant practice offree residual chlorination.During this period, a great variety of physical

and chemical agents have been studied regardingtheir potential utility for water disinfection. Some,such as heat, are highly effective, but impracticalbecause of cost. Others may be unsuitable becausetheir effects are selective, e.g., quaternary ammo-nium compounds are effective bactericides, butineffective viricides. Chemical oxidants are themost widely used and potentially usable agents.These include the halogens such as bromine, iodine,and chlorine in various forms, metal salts such asferrate and permanganate, and peroxides such asozone and hydrogen peroxide. Of these, only ozone,chlorine dioxide and chloramines are currentlyconsidered to be immediately viable alternatives tofree residual chlorine for use as primary disinfec-tants for potable water. This consideration is basedmainly on the fact that these agents have been usedsuccessfully in actual treatment practice. The use ofchloramines in some treatment systems has contin-ued, with apparent success, in spite of laboratorydata indicating that they are relatively poor disin-fectants.

Comparative Biocidal EfficiencyThe assessment of the biocidal efficiency of disin-

fectants is based mainly on the results of laboratoryexperiments conducted under controlled conditions.Some of the problems associated with such assess-ments were described by Morris (8) as follows:

AKIN, HOFF AND LIPPY

"Although the bases for the quantitative expression of theeffectiveness of germicidal agents have been known for morethan 60 years, there has been relatively little application tothe systematic tabulation of the relative potencies of disinfec-tants. Only a very small fraction of the total publishedliterature on germicidal action is sufficiently complete or inform suitable for satisfactory quantitative analysis. Moreover,there is no consensus on which method of tabulation is mostconvenient. Probably the most common technique is to list theconcentrations required to give a fixed percentage of kill witha given time of contact, but there is no unanimity with regardto either the percentage or the time."

Inactivation ofmicroorganisms by chemical disinfec-tants can be considered as a first-order chemicalreaction in which the rate of inactivation is depen-dent on the disinfectant type and species, thedisinfectant concentration, and the microorganismsbeing inactivated. Although actual data often showdeviation from first-order kinetics, it is a usefulconcept. Using data in this way, comparativebiocidal efficiency can be expressed as the relativeconcentration of various disinfectants required forequivalent disinfection rates or as the relativeinactivation rates produced by equivalent concen-trations of different agents. Data from laboratoryexperiments conducted at constant disinfectantlevels and with pure cultures of the organism areshown in Figures 3 and 4. The data shown arecomposites of results from studies conducted over aperiod of years in one laboratory using consistentexperimental methods and microorganism strains(9).

100

. 10

-i

E 1.0

0.1

n n1

0.01 0.1 1.0 10 100 1000Time in Minutes for 99% Inactivation

FIGURE 3. Inactivation of E. coli (ATCC 11229) by free andcombined chlorine species and chlorine dioxide at 15°C (9,13).

NH2CI(pH 9)

Water pH has important effects on the efficiencyof free residual chlorine and chlorine dioxide. In thecase of free residual chlorine, increasing the pH

-_ NHCI2 from 6 to 10 alters the disinfectant species present100_ XQ (pH 4.5) from a very efficient nonionized chemical species to

a much less efficient ionized species. In contrast,NH2CI the efficiency of chlorine dioxide increases over a

10_ (pH9) similar pH range. Both E. coli (12) and poliovirus 1s - *HOdI 4 (13) are inactivated more rapidly at pH 9 than at pH

(pH 6) X 7 by chlorine dioxide. In this case it appears to be a1>l.oL *K.\wXA change in the sensitivity of the organisms since< RSoci- chlorine dioxide remains the same chemically over

_ :k *(pH 10) this pH range. Further evidence that differentmicroorganisms are affected differently by disinfec-

0.1 - (C0pH2-)tants is shown in Table 3 (14). This group of sixenteroviruses show widely differing patterns ofresistance to both hypochlorous acid and hypochlo-

.0li I italiti I i. ,,,,,,, rite ion. Relative differences in resistance to.01 a] 1.0 10 100 10° hypochlorous acid and hypochlorite ion range from

Time in Minutes for99% Inctivion 5-fold to 192-fold for different enteroviruses. In the-URE 4. Inactivation of poliovirus 1 by free and combined same study, they showed that the presence of anchlorine species and chlorine dioxide at 150C (9, 13). inorganic salt (KCI) can significantly influence the

rate of inactivation of viruses by both free chlorinespecies. Others have confirmed this observation

Figure 3 shows the times and concentrations of and have shown that similar effects are producedveral disinfectants required to cause inactivation by NaCl and CsCl (15-17). More recently, Haas and99% of a population of Escherichia coli. Free Zapatkin have shown that E. coli is similarlysidual chlorine in the form of hypochlorous acid is affected (18).

somewnat more eiiectlve than cnlorine clioxilae, butin its other form, hypochlorite ion, free residualchlorine is less effective than chlorine dioxide.Dichloramine is somewhat less effective than hypo-chlorite ion and monochloramine is the least effec-tive. The overall pattern shown by results ofstudies of poliovirus 1 inactivation (Fig. 4) issimilar. Note that all of the curves are further tothe right, indicating the generally higher resistancepattern of viruses than E. coli to the disinfectants.Hypochlorous acid and chlorine dioxide are similarin efficiency with hypochlorite ion somewhat lesseffective. Both chloramine species are much lesseffective, but their order of efficiency is reversedfrom that shown for E. coli. Studies similar to thesewith ozone are difficult because the instability andextremely rapid inactivation rates shown by thisdisinfectant make it difficult to obtain reproducibleresults. Studies that have been done indicate thatozone is perhaps two to three orders of magnitudemore efficient than free residual chlorine (10, 11).The overall efficiency rankings indicated in Figures3 and 4 are consistent in general with the disinfec-tion literature for all microorganisms includingbacteria, viruses and protozoan cysts. However,precise quantitative ranking of the disinfectantswith regard to the degree of difference in efficiencyis not possible.

Choosing a DisinfectantThe important considerations in choosing a disin-

fectant appear to be technical rather than economicin nature. Cost comparisons have not been pre-sented here. However, Clark (2) has determinedthat while operating cost of using the disinfectantsunder discussion may vary 3- to 4-fold, when con-sidered in terms of cost-benefit ratios, all threeshow a highly positive net benefit.An important consideration in choosing a disin-

fectant for use in water treatment is the stability ofthe disinfectant species. In general, degree of

Table 3. Comparison of virus inactivation by free residualchlorine at pH 6.0 and 10.0, and 5.0°C ± 0.20C."

Time for 99% inactivation, min

Virus strain pH 6.0 pH 10.0 Ratiob

Coxsackie A9 (Griggs) 0.3 1.5 5Echo 2 (Farouk) 0.5 96.0 192Polio 2 (Lansing) 1.2 64.0 53Echo 5 (Noyce) 1.3 27.0 21Polio 1 (Mahoney) 2.1 21.0 10Coxsackie B5 (Faulkner) 3.4 66.0 19

aData of Engelbrecht et al. (14).bTime required at pH 10.0/time required at pH 6.0.

aE

FiG

se,ofrei

11DISINFECTION AND INFECTIOUS WATERBORNE DISEASE

12 AKIN, HOFF AND LIPPY

Table 4. Summary of disinfectant characteristics relating tobiocidal efficiency.

Rankb pH effects

Biocidal on efficiencyDisinfectant efficiency Stability (pH range 6-9)

Ozone 1 4 Little effectChlorine dioxidec 2 2 pH increase is

beneficialFree chlorinec 3 3 pH increase is

detrimentalChloramines 4 1 Little effect

aData of Hoff and Geldreich (19).bl = best, 4 = worst.cRanking influenced by pH

stability correlates inversely with biocidal efficiency,the more stable the disinfectant, the less efficient.Although chlorine dioxide is similar in disinfectioncapability to hypochlorous acid, it is considered tobe more stable because it does not react withammonia which is frequently present in raw waters.However, disinfectant stability can also be consid-ered beneficial because stable disinfectants such aschloramines, although less efficient, may be veryeffective because of their prolonged persistence.An overall view of some of the characteristics ofozone, chlorine dioxide, and free and combinedchlorine is shown in Table 4. It is clear that none ofthe agents is optimal in all respects. The currentconcern regarding disinfection and the productionof potentially toxic substances, the subject of thissymposium, further complicates this picture. Per-haps the only firm conclusion that can currently bedrawn concerning drinking water disinfection is itsabsolute requirement, by some means, in the treat-ment process if the transmission of waterborneinfectious disease is to be prevented.

REFERENCES

1. White, G. C. Handbook of Chlorination, Van Nostrand-Reinhold, New York, 1972.

2. Clark, R. M. Evaluating costs and benefits of alternativedisinfectants. J. Am. Water Works Assoc. 73: 89-94 (1981).

3. Mosley, J. W. Transmission of viral diseases by drinking

water. Transmission of Viruses by the Water Route,Interscience, New York, 1967, pp. 5-24.

4. Jakubowski, W., and Hoff, J. C. (Eds.). Waterborne Trans-mission of Giardiasis. U.S. EPA, Office of Research andDevelopment, 1979, No. EPA-600/9-79-001.

5. Jarroll, E. L., Bingham, A. K., and Meyer, E. A. Effect ofchlorine on Giardia lamblia cyst viability. Appl. Environ.Microbiol. 41: 483-487 (1981).

6. Craun, G. F. Waterborne disease outbreaks in the UnitedStates. J. Environ. Health 41: 259-265 (1979).

7. Akin, E. W., Berg, G., Clarke, N. A., Culp, R., Engelbrecht,R. S., Lennette, E. H., Metcalf, T., Mosely, J. W., Pearson,H. E., Sullivan, R., and Wolf, H. W. Viruses in drinkingwater-committee report. J. Am. Water Works Assoc. 71:441-444 (1979).

8. Morris, J. C. Aspects of the quantitative assessment ofgermicidal efficiency. In: Disinfection Water and Wastewater,J. D. Johnson (Ed.), Ann Arbor Science Publishers, AnnArbor, Mich., 1975.

9. Esposito, M. P. The inactivation of viruses in water bydichloramine. Master's Thesis, Univ. of Cincinnati, 1974.

10. Laubusch, E. J. Chlorination and other disinfection processes.In: Water Quality and Treatment, McGraw-Hill, New York,1971.

11. Diaper, E. W. J. Disinfection of water and wastewater usingozone. In: Disinfection Water and Wastewater, J. D.Johnson (Ed.). Ann Arbor Science Publishers, Ann Arbor,Mich., 1975.

12. Benarde, M. A., Israel, B. M., Olivieri, V. P., andGranstrom, M. L. Efficiency of chlorine dioxide as a bac-tericide. Appl. Environ. Microbiol. 13: 776-780 (1965).

13. Cronier, S., Scarpino, P. V., and Zink, M. L. Chlorinedioxide destruction of viruses and bacteria in water. In:Water chlorination, Environmental Impact and Health Effects,Vol. 2, R. L. Jolly, H. Gorchev and D. H. Hamilton (Eds.).Ann Arbor Science Publishers, Ann Arbor, Mich., 19t8.

14. Engelbrecht, R. S., Weber, M. J., Salter, B. L., andSchmidt, C. A. Comparative inactivation of viruses bychlorine. Appl. Environ. Microbiol. 40: 249-256 (1980).

15. Sharp, D. G., Young, D. C., Floyd, R., and Johnson, J. D.Effect of ionic environment on the inactivation of poliovirusin water by chlorine. Appl. Environ. Microbiol. 39: 530-534(1980).

16. Sharp, D. G., and Leong, J. Inactivation of poliovirus 1(Brunhilde) single particles by chlorine in water. Appl.Environ. Microbiol. 40: 381-385 (1980).

17. Jensen, H., Thomas, K., and Sharp, D. G. Inactivation ofcoxsackie B3 and B5 viruses in water by chlorine. Appl.Environ. Microbiol. 40: 633-640 (1980).

18. Haas, C. N, and Zapkin, M. A. Effects of various additionson the inactivation ofEscherichia coli by chlorine. Abstractsof the Annual Meeting of the American Society for Micro-biology, p. 209.

19. Hoff, J. C., and Geldreich, E. E. Comparison of the biocidalefficiency of alternative disinfectants. J. Am. Water WorksAssoc. 73: 40-44 (1981).