Epidemiology of Enteric Viral Infections

Epidemiology of Enteric Viral Infections V. J. Cabelli Department of Microbiology, University of Rhode Island, Kingston, RI 02881, USA

ABSTRACT Information obtained from a multi-year, multiple location epidemiological program conducted by the United States Environmental Protection Agency to develop health effects recreational water quality criteria provided some insights as to the eti­ ology of the observed swimming-associated, pollution-related gastroenteritis. A number of factors suggest the human rotavirus or the parvo-like viruses as the etiologic agents, probably the former. Included are the infectivity, prevalence, and/ or survival properties of the agent as seen from the illness-indicator relation­ ships and the effect of pollution sources on them, the role of immunity as obtaiiEd from the comparison of the data from united States and Egyptian studies and from Cairo visitors and Alexandria residents in the Egyptian study, the age distribution of symptomatology, and the incubation period, severity and duration of the gastro­ intestinal symptoms.

KEYWORDS Swimming-associated disease, gastroenteritis, water quality, epidemiology, rota­ virus .

INTRODUCTION This report will present some circumstartLal evidence that the human rotavirus and/ or the Norwalk virus are the etiologic agents for the most common illness associ­ ated with the recreational use of sewage-polluted marine waters, a relatively mild gastroenteritis. The evidence comes from the findings of a multi-year, multiple location, prospective epidemiological study conducted by the United States Environ­ mental Protection Agency (USEPA) and its grantees (Cabelli, 1980)· Moreover, the mathematical relationship obtained between the incidence of swimming-associated gastroenteritis and the quality of the bathing water (as indexed by its mean enterococcus density) suggests that this may also be true of the drinking water and shellfish-consumption routes as well. In fact, a non-specific gastroenteritis is the most commonly reported illness associated with these two routes (McCabe, 1977; Verber, 1965). Until 1979, the only viral disease for which there was unequivocal evidence from VWWT - υ

291

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V. J. Cabelli

case and outbreak reports of transmission via the recreational, drinking water or shellfish routes was infectious hepatitis (McCabe, 1977; Verber, 1965). There have been three reports of waterborne disease outbreaks attributed to enteroviruses, a poliomyelitis outbreak from drinking water (Mosely, 1965) and Coxsackie virus A andB outbreaks associated with recreational use (Denis and others, 1974; Hawley and others, 1973). However, in all three instances, the association to the particular waterborne route was questionable. This was also true of the single outbreak of infectious hepatitis associated with recreational swimming (Bryan and others, 1974). In 1979, however, there were two reports of "waterborne" gastroenteritis. The first clearly showed the Norwalk virus as the etiologic agent for some 2,000 cases of gastroenteritis associated with the consumption of oysters (Murphy and others, 1979); and the second suggested that the same agent was responsible for some 200 cases of swimming-associated gastro­ enteritis (Center for Disease Control, 1979). There also have been several out­ breaks of gasteroenteritis associated with the consumption of shellfish in which a small (about 29nm) round virus was consistently demonstrated in the feces of the affected individuals (Appleton, 1981). The output from the USEPA program clearly showed a relationship of swimmingassociated gastroenteritis to the quality of the bathing water and provided a recreational water quality criterion (Cabelli, 1980). The relationships obtained will be considered herein only insofar as they provide insights as to the nature of the etiological agent. Emphasis will be placed on the incubation period, durat­ ion and severity of the reported symptomatology, its age distribution, and comparisons which suggest an important role of immunity in the epidemiology cf the disease. STUDY DESIGN The details of the prospective design used in the USEPA epidemiological program have been presented elsewhere (Cabelli, 1980; Cabelli and others, 1974; Cabelli and others, 1979). Potential participants in family groups were recruited at the beach at which time they were queried as to swimming activity and demography. They were "followed-up" some 7-10 days later by phone or personal interview for further demographic information and their responses to information concerning symptomato­ logy and its severity. Information was requested for a range of symptoms, including gastrointestinal, upper respiratory, ear, eye and skin, fever, headache etc. Thereby, no prejudgement was made as to which symptoms or groups of symptoms were swimming-associated and which were both swimming-associated and sewage polution related. In addition, samples of the bathing water were assayed for a number of fecal indicators, opportunistic pathogens, and one enteric pathogen (Salmonella). Thereby, the "best" indicator could be designated as the one whose densities were best correlated to the incidence of those symptoms which were both swimming-associated and pollution-related. Pollution relatedness could be examin­ ed in the New York City study independent of fecal indicator densities because two beaches were used, one at Coney Island and the other at the Rockaways (Cabelli, and others, 1976). The former was considerably closer to the known source of sewage pollution, the Hudson River. Studies were conducted at four locations, three in the United States and one in Egypt. The locations, years (summers) during which trials were conducted, and the number of useable responses are given in Table 1. In the Egyptian study, both Alexandria residents and Cairo visitors were recruited. An altered study design was required with the latter group. Because tourists at seashore beaches tend to swim daily, weekend trials, in which individuals who swam in the midweeks before and after the weekend in question were eliminated from the study, could not be used with the Cairo visitors. The altered design did allow more day to day variability in the pollution levels. However, it also permitted inquiries for diseases with longer incubation periods, notably infectious hepatitis.

293

Epidemiology of Enteric Viral Infections TABLE 1.

Number of Useable Responses by Beach and Year for Studies Conducted Under the ÜSEPA Program

Location

Beaches

Number of Usable Responses During Year

New York City, NY

Coney Island Rockaways Levee Fountainbleau Revere Nahant Maamoura 4 Ibrahemia^

641 681 3432

Lake Pontchartrain, LA Boston Harbor, MA Alexandria, Egypt

1824 2229 819 823

4

Mandara"^ Sporting 4

3146 4923 2768 551

6491

1492 1695 1117 1159

1786 2173 2050 1820

1257 1243

2025 2457

1163

Coney Island, Rockaways, 1973-1975; Levee, 1977-1978; fontainbleau, 1978; Revere, Nahant, 1978; Maamoura, Ibrahemia, 1975-1977; Mandara, 1975; Sporting 1976, 1977. 2

q

Included with Levee; ^ Alexandria residents;

4

Cairo visitors,

RESULTS Most of the symptoms were found to be swimming-associated. That is, the rates for swimmers (defined as exposure of the upper body orifices to the water) were higher than those for the nonswimming but beachgoing controls. However, only gastroin­ testinal (GI) symptoms (vomiting, diarrhea, nausea or stomachache) were consis­ tently both swimming-associated and pollution-related (Cabelli, 1980). Moreover, this was also true of the "highly credible" portion (HCGI). It included all cases of vomiting, diarrhea with a fever or a disabling response (remained home, remained in bed or sought medical assistance) or nausea or stomachache with a fever (Cabelli, 1980; Cabelli and others, 1979). Swimming-associated infectious hepatitis was not observed in the Egyptian study. Enterococcus and, to a much lesser extent, Escherichia coli densities in the water provided the best correlation to the incidence of total GI and HCGI symptoms of those indicators examined (enterococci, E. coli, total coliforms, fecal coliforms, Klebsiella, Enterobacter-Citrobacter, Clostridium perfringens, Pseudomonas aeru­ ginosa, and Aeromonas hydrophila. Of special note, were the poor correlations ob­ tained with both total and fecal coliforms (Cabelli, 1980). Implications of Illness-Indicator Relationship The Y on X regression lines obtained for the rates of swimming - associated (swimmer minus nonswimmer) gastrointestinal symptoms (Y) against the mean enter­ ococcus and E. coli densities in the water (X) for trials clustered by similar in­ dicator densTties (1) are shown in Figure Í. It can be seen that appreciable swiiaming-associated rates for total and highly credible GI symptoms (about 1 and 2%, respectively) were associated with mean bathing water densities of about 10 enter­ ococci per 100 ml. Although the E. coli regression lines were much less correlated

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V. J. Cabelli

and had shallower slopes, the swimming-associated rates for an E. coli density of about 10 per 100 ml were similar to those for the enterococcus Tndicator system. However, the X axis intercepts for the two indicators were markedly different. One explanation for the differences is that enterococci more closely resemble the etiologic agent for the observed symptmatology with regard to its survival proper­ ties in marine waters than does E. coli. This is consistant with what is known about the relative survival prope'rties of the two indicator systems (Hanes and Fragella, 1967; Shuval and others, 1981)

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The indicator illness-relationships observed, especially when the estimated in­ gestion of water during a swimming experience (10-50 ml) is considered, would sug­ gest that the etiologic agent is highly infectious, is present in extremely large numbers in the water (and, hence, in sewage) and/or survives extremely well in the marine environn:ent.

Effect of Pollution Source The source of sewage pollution to the beaches in the New York City (NYC) study was that carried through the Verrazano Narrows from the Upper Hudson Bay. It con­ sisted of a mixture of raw, treated, and disinfected sewage (New York City Dept. of

Epidemiology of Enteric Viral Infections

295

Health, 1975). Moreover, the raw discharges were decreased in 1975 as opposed to 1973 and 1974. The sources of pollution to the beaches in the Alexandria, Egypt study were raw sewage discharged through a series of short (about 50 meters) out­ falls. The sources in the Lake Pontchartrain and Boston Harbor studies were much less defined and assumed to be at greater distances from the study beaches. The better survival of the etiological agent of the swimming-associated GI symp­ toms relative to E. coli and even the enterococci is suggested from the examina­ tion of the correTation coefficients, slopes, and X axis intercepts of the ill­ ness-indicator regression lines for NYC 1973-1974, NYC 1973-1975, the NYC and Lake Pontchartrain studies, all the U.S. studies, and the Egyptian study (Table 2). The best correlations, especially for E. coli, were obtained from the 1973-1974 New York City data and the Egyptian study. TABLE 2. Comparison of Correlation Coefficients, slopes and Log^^ X asix inter­ cepts for the Regression Swimming-Associated Gastrointestinal Symptoms (Y) on Enterococcus and E. coli Densities (X) in the Bathing Water.

Symp

Total Gil

Stat

Indicator

Entero. Ε. coli Entero. slope^ Ε. coli Entero. Ε. coli inter HCGI^ r Entero· Ε. coli slope Entero. Ε. coli log ,0 X Entero. inter E. coli

NYC^ 73-4 .90 .95 31.5 32.6 • 50 .63 .98 .95 18.7 13.8 .49 .21

NYC 73-5 .81 .56 22.2 14.1 .31 .13 .96 .51 20.9 6.79 .63 -.26

NYC + Pont'

.83 .16 24.9 5.04 .27 -4.40 .82 .46 13.4 5.64 .18 1.33

All U.S.^ .82 .28 24.2 8.42 .21 -1.60 .75 .51 12.2 6.23 -.0069 -.89

Cairo Visit ^

•88 .89 20.3 17.4 1.83 1.54

Alex. Res 10

.68 .76 5.48 5.10 .88 .48

Total gastrointestinal symptoms 2 Highly credible GI symptoms; vomiting or diarrhea, Egyptian study. 3 Correlation coefficient for linear regression. 4 5 Slope of regression line; iogm ^ ^^^^ intercept. 6 7 8 9 New York City study; Lake Pontchartrain study; All U^S. studies; Cairo visitors to Alexandria beaches; ^^Alexandria residents. In general, the correlation coefficients (r) were higher, the slopes of the linear regression lines were steeper, and the X axis intercepts were greater for entero­ cocci than for E. coli. The exceptions were obtained from the analyses of the data from the fTrst two years of the New York City study and from the Egyptian study; and, in both, there were relatively close sources of raw sewage. Further­ more, the successive inclusion of the data from the third year of the New York City, the Lake Pontchartrain, and the Boston Harbor studies general reduced r, decreased the slope, and reduced the value of the X axis intercept. By 1975, a major and relatively close source of raw sewage to the NYC beaches (lower Manhat­ tan) had been eliminated, and the sewage sources in the Lake Pontchartrain study were relatively distant. These findings suggest that enterococci better mimic the survival characteristics of the etiological agent than does E, coli. They

296

V. J. Cabelli

also suggest that, with sewage disinfection and/or protracted transport times bet­ ween the source (outfall) and the target (beach), even enterococcus densities tend to underestimate the potential for gastrointestinal symptomatology. There was considerable day to day variability in the enterococcus and E^. coli den­ sities at the Lake Pontchartrain beach (Levee) during 1977. In fact, there were days with very high E. coli and only moderate enterococcus densities and days with relatively low E. coli and relatively high enteroccus densities. The former situations were associated with heavy rainfall and were presumed to be due to stonnwater run-off. We believe that the latter was due to a pollution source(s) which was discharging near the base of a bayou (St. John) which is immediately ad­ jacent to the beach. It can be seen from Table 3 that the rates of swimmingassociated symptoms were higher during the former than latter situations. This is turn suggests that stormwater run-off was not the major source of the etiologic agent and that there was protracted transport time between the source (in the Bayou?) and the beach. TABLE 3 Analysis of 1977 Lake Pontchartrain Data by Rainfall (Dry Versus Wet periods? Characteristic

Relatively "Dry" Period

Relatively "Wet" Period

Number of trials Period Rainfall

4 7/9 - 7/24 .128 in/day

9 7/30 - 8/28 .433 in/day

Densities/lOOml Levee Beach Mouth of Bayou Total

Enterococcus 253 363 301

GI Symptom Rates Total Highly Credible

Swim 123.2 46.8

E.coli 76.1 149.0 107.0

Nonswim 56.8 17.0

Δ. 66.4*** 29.7**

Enterococcus 22.7 66.3 38.8 Swim 86.6 32.2

E. coli 2074 2219 2145

Nonswim Δ 60.7 25.9 9.8 22.4**

^Total rainfall for the interval starting 6 days before the first trial and ending with the trial date., divided by the number of days in the interval. 2 Geometric mean for all samples collected on the trial dates. ^N - 1282; V 5 2 8 ; V 9 9 3 ; V5IL ** *** Ρ .01; Ρ .001

Comparison of findings from U.S. and Egyptian Studies Initially, it was thought that the Egyptian data might be combined with the U,S. data to provide a single illness-indicator relationship. By the end of the first year of the Egyptian study, it was obvious that the data from the Alexandria resi­ dents could not be so used; and, by the end of the third year, it was concluded that this was also true of the data from the Cairo visitors. The regression lines for the rates of swimming-associated vomiting and diarrhea from these two groups along with those for total GI and HCGI symptoms from the U.S. studies against the corresponding mean enterococcus densities are presented in Figure 2 . It can be seen that, in the U.S. studies, gastrointestinal illness rates comparable to those obtained in the Egyptian study were associated with bathing in waters with much lower enterococcus densities. Part of the dissimilarity is probably due to dif­ ferences in the survival characteristics of the fecal indicator relative to those of the etiologic agent and in the nature (raw vs. treated) and proximity of the

297

Epidemiology of Enteric Viral Infections

pollution sources in the U.S. and Egyptian studies. However, disparities in the immune state of the three populations to the etiolojgic agent(s) probably accounts for many of the differences in the indicator-illness relationships. The plateaus shown in the regression lines for the Alexandria residents and the Cairo visitors also suggest the role of immunity. The assumption is that, in general, the Cairo visitors are more affluent individuals (they can afford a holiday at the seashore) who probably live under better conditions of environmental sanitation. Hence, they are less likely to be immune to the etiologic agent by the time they reach swim­ ming age than are the Alexandria residents.

VOMITING OR DIARRHEA CAIRO VISITERS HIGHLY C R E D I B L E GI U.S. S T U D I E S y ^ /

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Plateaus in the Illness-Indicator Relationship Animal infectivity studies conducted with most infectious agents yield sigmoid dose-response curves. At the inception of the Environmental Protection Agency program, the relationship of illness among swimmers to indicator densities in the bathing waters was also expected to be sigmoid in nature. However, when the swim­ ming-associated rates for gastrointestinal symptoms from the NYC study were plotted in percentages on a scale that was not expanded to show differences, the slopes of the lines were quite shallow relative to those seen in most dose-response curves. They may have represented the first parts of sigmoid curves, from which the expec-

298

V. J. Cabelli

tation was accelerated increases in the symptom rates with further increases in the indicator densities at the beaches. An equally plausible explanation is that the regression lines obtained were the linear portions of basically sigmoid relation­ ships (i) in which a measurable response was associated with the ingestion of very low enterococcus or E.coli densities because of the differential survival of the indicators relative to the etiologic agent(s) over the travel time between the beaches and the sources of pollution (ii) in which the shallow slopes of the regre­ ssion lines were due to high levels of immunity to the infective agent(s) in the swimming populations and (iii) from which the expectation was that the rates for the specific illness(es) involved would not accelerate with increasing levels of pollution as seen from the indicator densities. The results of the Egyptian study argue against the first explanation and for the second.

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Epidemiology of Enteric Viral Infections

299

transformed indicator densities fit the data for total GI and HCGI symptoms for the New York City study and for total GI symptoms for the Lake Pontchartrain-Boston Harbor data. This was not as true for HCGI symptoms from the Lake PontchartrainBoston Harbor studies. Moreover, whereas the slopes of the two "linear" regress­ ion lines for total GI symptoms were not significantly different, those for HCGI symptoms were. One explanation for these differences is that at least a portion of the population in the Lake Pontchartrain study population was partically immune, resulting in continued increases in mild (total GI) but not more "severe" (HCGI) symptoms. This may also have been observed in the New York City study had higher pollution levels been obtained. Age distribution In each study in which the age distribution of the swimming-associated, gastro­ intestinal symptomatology was examined, it was found that these symptoms were much more prevalent among children (10 years of age) than adults. This can be seen from the 1974 data from New York City (Table 4 ) , the 1977 data from Lake Pontchartrain (Table 4) and the data from the Egyptian study (Figure 4 ) . This also suggests the importance of immunity in the epidemiology of the observed swim­ ming-associated gastroenteritis. TABLE 4

Study

Age Distribution of Gastrointestinal Symptomatology.

Beach

Year

Symptoms

Symptom Rate per 1000 Persons for Children 1 Other than Children Swim

NYC"^ 4 Pont,

Coney Isl.

1974

Total GI^ HCGI 6

Levee

1977

Total GI HCGI

57 24 123 61

Nonswim

Swim

14 43* 4.5 19.5* 50 28

33*,v

Nonswim

Λ

37 13

29 11

8 2

94 33

61 12

33** 21**

1 NYC, ^ 10 years of age; Lake Pontchartrain, < 10 years of age; 3 . 4 . 5 New York City; Lake Pontchartrain; Total gastrointestinal

2

Difference

Highly credible GI S3niiptom (see text for definition). ** Ρ 0.05; Ρ 0.01. Nature, Onset and Duration of Symptomatology *

The gastrointestinal "illnesses" as described in the four studies can be character­ ized as relatively benign since no cases of hospitalization, much less death, were reported. Fever accompanied the GI symptoms in some : instances, and diarrhoea occured more frequently than vomiting. Highly credible GI symptoms were substantial enough to be designated gastroenteritis. As seen from the U.S.data (Figure 1) and especially the 1974 New York City trials (Table 4 ) , the trends for total GI symptoms and those for the highly credible portion were similar, suggesting that the former may have included a milder form of the latter, possibly in partially immune individuals. The duration of GI sjnnptoms was about three days, a little longer for the "disabling" portion (remain home, remain in bed, seek medical advice) and on the average a little shorter for total GI symptoms (Table 5 ) . One of the more strik­ ing characteristics of the swimming-associated gastroenteritis was its very short incubation period. It can be seen from figure 5 that symptoms developed within one day and that the number of new cases among swimmers decreased markedly by the second day post-swimming. There was also a slight peak for nonswimmers between

300

V. J. Cabelli

the second and third days following a weekend trial suggesting that, among beechgoers , routes of transmission at the beach other than immersion of the head in the water may have been responsible for some cases of illness. This reaffirms the importance of having a nonswimming control population that is at the beach.

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ALEXANDRIA

RESIDENTS

Age-specific, swimming-associated rates for vomiting or diarrhoea by beach and study population for the 1977 Egyptian trials. The agespecific rates for the non-swimming Alexandria residents and Cairo visitors are shown as an insert.

Epidemiology of Enteric Viral Infections TABLE 5

Duration of Gastrointestinal Symptomatology:

301

New York City, 1975 trials

Duration of Symptoms in Days for Swimmers Nonswimmers Average Number Average Number Duration Reporting Duration Reporting

Symptoms

Total Vomiting Diarrhoea Stomachache Nausea

30 73 101 64

2.8 2.6 2.7 2.7

10 26 36 18

2.6 2.7 2.4 2.8

Disabling* Vomiting Diarrhoea Stomachache Nausea

17 22 36 24

3.7 3.0 3.5 2.6

5 11 12 8

2.6 3.2 3.0 3.2

* Individual remained home, remained in bed or sought medical advice

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Fig.5. Day of onset of GI symptoms as obtained from the 1975 New York City trials

V. J. Cabelli

302 DISCUSSION

Two viral agents or groups of agents, the human rotavirus and the parvo-like viruses, are suggested as the etiological agents for the swimming-associated gastro­ enteritis observed in the epidemiological program. Those characteristics observed or implied by its findings along with those reported for the human rotavirus and the Norwalk virus (one of the parvo-like viruses) are presented in Table 6. TABLE 6

Comparison of Clinical, Epidemiological and Etiological Characteristics for the Swimming-Associated Gastroenteritis in the USEPA Program to those Reported for the Human Rotavirus and Norwalk Agent

2

Characteristic

Swimming-Associated

Human Rotavirus

Distribution Incubation period 4 Symptoms Vomiting

Worldwide^ 1 - 3 days

Worldwide 15 - 72 hrs

Worldwide 18 - 48 hrs

Diarrhoea Nausea Abdominal cramps Fever Severity Duration of illness Age Distribution

Variable Frequent Frequent Frequent Variable Benign 2 - 4 days Mostly children

Very frequent Frequent Very frequent Frequent Variable Benign 1 - 2 days All ages

Density of agent in feces Infectivity of agent Stability of agent

High High High

Variable Frequent Frequent Variable Variable Benign 4 - 8 days Mostly infants & children 10 11 . lO^^-lO^Vgm presumed high presumed high

7

Norwalk Virus

3

^8 10 -10 /gm low to moderate ?

1

2 3 4 Reference 1; References, 16 - 19; References, 20 - 22; In children; Tentative conclusion from USEPA epidemiological program; Some mortality in 7 8 infants; Inferred from the illness-indicator relationships; From human volunteer studies. The role of immunity, the age of distribution, and the very short incubation period favor the human rotavirus as the etiological agent. On the other hand, the Norwalk agent was shown (Murphy and others, 1979) or suspected to be (Center for Disease Control, 1979) the etiological agent in two recent outbreaks of "waterborne" gastroenteritis. With reference to waterborne disease, the finding of Norwalk gastroenteritis in outbreak situations and rotavirus gastroenteritis as "sporadic" cases would not be unlikely in view of what is known concerning the age distributions for the two disease and serologic responses. Moreover, this line of reasoning would suggest that the rotavirus is more infective or more prevalent in sewage than the Norwalk agent. Now that methods are available for performing serological epidemiology for both agents and are becoming available for quantifying the rotavirus (or, at least, the production of viral protein) in tissue cultures, this hypothysis can be tested. One last point deserves to be mentioned. At gram, it was thought that swimming in sewage minor route of tranmission for the illnesses individuals of swimming age as seen from the

the onset of the epidemiological pro­ polluted waters would be a relatively involved. In fact, this is not so for ratios of rather than the difference

Epidemiology of Enteric Viral Infections between the swimmer and density in the water of nonswimmers. Moreover, credible GI symptoms at

303

nonswimmer rates (Cabelli, 1980). At a mean enterococcus 10/100 ml, the HCGI symptom rate was about twice that for the ratio approached unity for both total and highly an enterococcus density of about 1/100 ml.

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