In January 1991, epidem ic cholera appeared in Peru and quickly spread to m any o the r Latin Am erican countries. Because reporting o f cholera cases was often delayed in som e areas, the scope o f the epidem ic was unclear. An assessment o f the conduct o f surveillance fo r cholera in several countries identifie d som e recurrent problem s invo lvin g surveillance case definitions, laboratory surveillance, surveillance methods, national coordination, and data m anagem ent. A key conclusion is that a simple, w ell-com m unicated cholera surveillance system in place during an epidem ic w ill facilitate prevention and treatm ent efforts. We recom m end the fo llo w in g measures: a) s im p lify case d efin itio ns fo r cholera; b) focus on laboratory surveillance o f patients w ith diarrhea p rim a rily in the in itia l stage o f the epidem ic; c) use p re do m in an tly the "su s p e ct" case defin itio n when the n um ber o f " co nfirm e d " cases rises; d) tran sm it w eekly the num bers o f cases, hospitalized patients, and deaths to regional and central levels; e) analyze data frequently and d istribute a weekly or biw eekly sum m ary; and f) report the n um ber o f cholera cases p ro m p tly to the W orld Health Organization.# INTRODUCTION Background
Cholera is a highly preventable and treatable disease. C hlorinating w ater supplies and im plem enting other emergency measures can prevent transm ission, and p ro vid ing ready access to oral and intravenous rehydration therapy can dram atically low er death rates. Prevention and treatm ent efforts can function o ptim ally when there is cooperation between regional and central public health offices, as w ell as at national and international levels. The m ovem ent o f the cholera epidem ic, the need fo r supplies, and the effectiveness o f control measures are better assessed w ith a clear and representative picture o f the epidemic. A sim ple, w ide ly accepted, w ell-described surveillance system is the best means o f obtaining that epidem ic picture.
A fter January 1991, when epidem ic cholera firs t appeared in Peru, the disease quickly spread to m any other Latin Am erican countries (7,2). Because this epidem ic was unexpected, some countries had little tim e to prepare fo r it. However, many countries had already drafted and im plem ented preparedness plans fo r the control of cholera.
An ideal plan fo r cholera control has several essential components, including health education, environm ental sanitation, clinical managem ent, laboratory diagno sis, epidem iologic investigation, and surveillance (3). During a cholera epidemic, surveillance is essential to estimate the incidence and the fa ta lity rate, to assess the m ovem ent o f the epidem ic, to plan the d istribution o f supplies fo r treatm ent and prevention, to plan tim e ly epidem iologic investigations, and to determ ine the effec tiveness o f control measures.
During investigations o f the cholera epidem ic in m any countries, epidem iologists from CDC have identified several recurrent problem s w ith cholera surveillance, including d ifficulties w ith collection, transm ission, and analysis o f data. These problem s often have caused delays and obscured the scope o f the epidem ic regionally, nationally, and internationally. In addition, some national surveillance systems fo r cholera use elaborate, com plex case definitions that hinder sm ooth, rapid reporting o f cases. This report outlines selected problem s that characterize cholera surveillance systems in some Latin Am erican countries and includes recom m enda tions to facilitate cholera surveillance both nationally and internationally.

# SURVEILLANCE ISSUES AND RECOMMENDATIONS

# Case Definitions
One com m on problem w ith cholera surveillance is the case definition. A case d efinition is a set o f objective criteria (sym ptom s, signs, and laboratory data) that lead to a reliable, reproducible report o f the disease. In defining cases, m any countries use tw o main categories of cases o f cholera -"su sp e ct" and "c o n firm e d ." Often, w ithin each main category, m ultiple case definitions are used. One country, fo r example, uses three definitions fo r a "su sp e ct" case o f cholera: a) profuse diarrhea, w ith severe dehydration, affecting a person years o f age; b) acute diarrhea in an area w ith confirm ed cholera; and c) acute diarrhea affecting a person w ho traveled th rough an infected area w ith in 5 days before onset o f illness. In another country, only one definition is used fo r a "su sp e ct" cholera case: acute diarrhea affecting a person &5 years o f age; however, this country also uses the additional category o f "p ro b a b le " cholera case, defined as dehydrating diarrhea, vo m itin g , cramps, and malaise affecting a person e pidem iologically associated w ith other cholera cases. M ultiple d efinitions such as these increase the d ifficu lty o f reporting and are likely to confuse the analysis o f surveillance data.
M ost countries use 5 years as the low er age lim it fo r cholera surveillance. A lthough the W orld Health Organization (WHO) has previously recom m ended 10 years as the low er age lim it fo r initial identification o f cholera (3), changes to low er this age are in progress (Dr. J. Tulloch, Director, Division o f Diarrhoeal and Acute Respiratory Disease Control, WHO, personal com m unication). Five years is a useful low er age lim it since it corresponds w ith the transition from preschool to school age; school children m ay be m ore likely to be exposed to some com m unicable diseases, including cholera, than are younger children. For m ost countries, much o f the m o rb id ity from all causes o f diarrhea occurs in the <5-year age group (4). Using 5 years as the low er age lim it in a cholera case d efinition excludes m ore o f the cases of diarrhea that are not cholera and, in effect, renders the d efinition m ore specific.
The other main category, the confirm ed case, is usually defined as Vibrio cholerae 01 infection verified by laboratory m ethods. The m ost com m only used m ethod is stool culture, w ith confirm ation that the isolate is 01 V. cholerae. W here infection is extrem ely rare, it can be helpful to dem onstrate that the isolate produces cholera toxin, because some nontoxigenic 01 strains o f V. cholerae have been documented (5). Serologic diagnosis, based on measurem ent o f acute-and convalescent-phase titers o f vibriocidal or antitoxin antibodies, is available, although rarely used. Sim ply counting laboratory isolates as cases may obscure the true picture o f the epidem ic. In one country, fo r instance, routine culturing o f specimens from fa m ily m em bers and close contacts o f patients w ith previously confirm ed cholera identified some persons w ith asym ptom atic infections. These asym ptom atic persons were then reported as having confirm ed cholera cases. In fact, asym ptom atic cholera Infections are num er ous in epidem ics, but cannot be Identified as cases by clinical signs and sym ptom s alone. Reporting persons w ith o u t diarrhea as confirm ed cholera case-patients can distort surveillance data.
The m ajor d ifficu lty w ith sim ple case definitions fo r cholera lies in the broad spectrum o f illness associated w ith this infection. Over 70% o f infected persons are asym ptom atic, and an additional 15%-23% o f infected persons have m ild or m oder ate nonbloody diarrhea sim ilar to diarrhea from other causes. Some persons w ho meet a " suspect" case definition may not have cholera, although they are likely to represent only a small proportion o f the reported cases in the epidem ic setting. A case d efinition based solely on an adult cholera patient's having dehydrating diarrhea (approxim ately 2%-5% o f those Infected) w ill be more specific than a case definition based on patients w ith any type o f diarrhea, but w ill also miss m any infected persons. In the context o f public health action, an accurate report o f the num ber o f sym pto m atic infections is a more useful measure. No single case definition is perfect; a balance is needed between sensitivity and specificity to provide a representative picture o f the epidem ic in any given area.

# Recommendations
For surveillance in a cholera epidemic, a case definition should be brief and simple to facilitate uniform and rapid reporting of cases. To simplify case reporting, cholera case definitions should be limited to tw o categories, the "confirmed" case and the "suspect" case. A confirmed cholera case is laboratory-confirmed V. cholerae 01 infection of any person who has diarrhea. In the epidemic setting, w e suggest that a suspect case of cholera be defined as acute, watery diarrhea affecting a person 3=5 Years of age.

# Laboratory Confirmation and Environmental Surveillance
The laboratory is a central com ponent o f cholera surveillance. It is essential fo r confirm ing that V. cholerae 01 has arrived in an area and is infecting humans, fo r M onitoring its continued presence or docum enting its disappearance, fo r determ in ing its antim icrobial susceptibilities, and fo r identifying its presence in the e nviron ment. Prelim inary isolation and confirm ation o f V. cholerae 01 require trained Personnel using thiosulfate-citrate-bile salts-sucrose (TCBS) agar and polyvalent antisera (6). In the current cholera epidem ic in Latin Am erica, m ost countries were able to staff some laboratories w ith trained personnel and m inim al supplies shortly after the firs t fe w cholera cases had been confirm ed. However, as epidem ic cholera advanced, m any laboratories w ere quickly overwhelm ed w ith dem ands fo r confirm a tion o f num erous suspect cholera patients. Reporting o f laboratory results slowed because o f this increased am ount o f work.

# Recommendations
In regional laboratories, trained personnel are needed to confirm V. cholerae 01 infection using TCBS agar and polyvalent antisera. At the central laboratory, trained personnel are also needed to confirm field isolates.
Initially, fo r an area threatened w ith cholera, a sample of persons w ith suspect cases should have specimens taken fo r culture. A fter a sufficient num ber of suspect cases have been confirm ed to indicate that cholera is epidem ic in that area (e.g., 10-20), the local or regional laboratory may then reduce the frequency o f perform ing cholera stool cultures from that area (e.g., 10 specim ens/m onth) to confirm the continuing presence o f V. cholerae 01 and to m on itor its a ntibiotic susceptibility. Every laboratory that identifies V. cholerae 01 should provide weekly reports o f the total num ber o f patient Isolates to designated regional and central offices.
In locations where cholera has not been confirm ed, especially those bordering areas w ith cholera, M oore swabs ( 7) can be placed In the sewage effluents o f a lim ited num ber o f sentinel tow ns and cities every 1-3 weeks. If V. cholerae 01 is isolated from sewage or from a person In a given area, the presence o f the organism in the area has been established, and the surveillance w ith M oore swabs can be discontinued. Thereafter, laboratory-based surveillance in that area should focus on patients w ith diarrhea.
When V. cholerae 01 is identified in a country fo r the first tim e, the isolate should be referred to an international reference laboratory fo r confirm ation and further characterization (e.g., using m olecular biological techniques), w hich may be helpful in determ ining Its origin.

# Stages of Surveillance
When epidem ic cholera appears in a region, tw o stages o f surveillance are observed: an early stage, when cultures are obtained from m any patients w ith diarrhea to diagnose cholera, and a later stage, when cholera Is firm ly established in the region and larger num bers o f people are ill. In the early stage, the num ber of persons w ith confirm ed cases may be small and may represent a m in or proportion of the persons w ith suspect cases. M ost countries report only culture-confirm ed cases at this stage. However, as the cholera epidem ic grows, m ore cases are confirm ed, and the num ber o f patients w ith suspect cases m ore accurately reflects the cholera situation in that area. M any countries, nonetheless, continue to report only cultureconfirm ed cases in this later stage o f cholera surveillance, because o f concerns about public response and adverse econom ic consequences if the larger num ber o f suspect cases is reported.

# Recommendations
In a cholera-threatened area, available diarrhea surveillance data can be reviewed to detect trends suggesting early cholera outbreaks. Any report of acute dehydrating diarrhea affecting a person 3 5 years of age should immediately alert local public health workers to investigate for possible cholera. Early in a cholera epidemic when small numbers of cases are being confirmed, a region may report only cultureconfirmed cases. However, when the number of confirmed cases becomes suffi ciently high, surveillance should shift to using the "suspect" case definition because it allows simpler, more timely, and more accurate reporting, and because it avoids overburdening laboratory resources. For a region in this later stage of cholera surveillance, it may be appropriate to limit culturing to a sample of the suspect cases that should continue to be reported. The decision as to when the number of confirmed cases becomes sufficiently high to change from reporting only confirmed cases to reporting cases in both "suspect" and "confirmed" categories should be made promptly on an individual basis after all implications have been assessed. Since most cholera outbreaks are large and often well established when confirmed, early shifting to reporting suspect cases may be more appropriate.
When the cholera epidem ic wanes and the num ber o f infections decreases to the level o f the early stage o f the epidem ic, some countries may revert to reporting only confirm ed cases. However, in m any areas, cholera appears seasonally, w ith num bers of cases Increasing in w arm m onths and decreasing in cold m onths. Therefore, it may be useful to report suspect cases fo r at least a year after the epidem ic wanes, until it is clearly shown that cholera is controlled in an area. A t that tim e, it is reasonable to return to reporting only confirm ed cases fo r that area.

# Information from Patients with Cholera
Some countries have adm inistered lengthy, detailed questionnaires to every patient w ith cholera. In one country, the inform a tion about the patient on the questionnaire included dem ographic data, clinical signs and sym ptom s, laboratory results, characteristics o f the feces and vom itus, travel history, food history, contact history, and additional com m ents by the person fillin g out the questionnaire. A lthough detailed inform ation m ay be helpful in describing a sample o f cholera cases clinically, it is o f epidem iologic interest only in the earliest phase of an epidem ic. Thereafter, as the num ber o f cholera cases increases, the form s may be incom plete or ignored, and much o f the data w ill be unm anageable and unanalyzed unless data-handling resources are diverted from other w o rth w h ile program s. Exposure inform ation collected from patients alone w ill not determ ine the m odes o f transm is sion, because cholera m ay be transm itted by com m on foods or beverages or by m ultiple sources th a t vary from place to place. W ell-designed and w ell-adm inistered case-control investigations in affected areas are a more effective approach to identify vehicles o f transm ission. In sum m ary, lengthy surveillance questionnaires waste scarce hum an resources and im pede handling o f surveillance data.

# Recommendations
For cholera, exposure histories are best reserved for investigations. Surveillance should be streamlined, using simple case definitions and concentrating on timely and accurate reporting of data. At the local level, including all treatm ent centers, information gathered about patients who meet the cholera surveillance case defini tion should be basic, including age, gender, date treated, and home address. The information transmitted to regional and central levels may include age, gender, and location, but it should primarily focus on the numbers of cases, hospitalized patients, and deaths.

# Communication, Analysis, and Timely Reporting of Surveillance Data
Surveillance and laboratory inform ation is o f little value unless it is com m unicated clearly and prom ptly. Tim ely reporting o f laboratory results to a regional epide m io l o g y office w ill allo w early identification o f cholera-affected areas and perm it im m e diate investigations; tim e ly reporting to the central laboratory w ill allo w early confirm ation o f the isolates; and, to com plete the inform a tion loop, tim e ly feedback to the o riginal su bm itter of the isolates w ill help validate diagnoses and im prove patient care. S im ilarly, tim e ly reporting o f the total num ber o f cases and basic analysis results from a central e pidem iology office back to the laboratories and regional e pidem iology offices is essential to allo w the epidem ic to be characterized and to ensure continued cooperation at all levels. In some locations, inform ation dissem ination am ong these m ajor com ponents in the surveillance process som e tim es has not been tim e ly and com plete. Early In the cholera epidem ic in Latin Am erica, fo r example, some countries instituted emergency daily reporting o f the num ber o f cases to a central office, yet did not com m unicate the total and cum ulative num ber o f cases by region to th e ir constituents until m onths later. The suitable form o f inform ation flo w am ong local and central levels m ust be w orked out country by country.

# Recommendations
A proposed communication system includes both reporting to a central office and feedback to regional offices (Figure 1).
Initially, treatm ent centers and regional offices may w ish to report to the central office daily by a rapid m ethod (e.g., radio, telephone, telegram ) the num ber o f suspect cases, the num ber o f confirm ed cases, the num ber o f patients w ho w ere hospitalized, and the num ber w ho died. A rapid sw itch to weekly reporting w ill often reduce the burden o f w ork created by dally reporting w ith o u t com prom ising the main goals of surveillance. The adm inistrative level to w hich each treatm ent center's report should be sent m ust be clearly identified.
Surveillance data should be analyzed p ro m p tly and frequently. Basic tabulation and com parison o f data should be perform ed at the local and regional level If trained personnel are available. A t the central level, epidem iologists should analyze reports o f suspect and confirm ed cholera cases by region and by week to track the spread of the epidem ic, to determ ine w hether unexpectedly large num bers o f cases are occurring In any region, and to evaluate the im pact o f interventions. The results should be dissem inated to all levels and used to estim ate resources needed at local levels and to decide w hether epidem iologic investigations are needed. W hen survell-

# FIGURE 1.
lance data suggest an increase in the num ber o f cases in an area, an epidem iologic investigation should be conducted to determ ine the m odes o f transm ission and identify fu rth e r prevention measures. The results o f these investigations should be reported to all categories o f participants in the surveillance system.

# International Reporting
Cholera is one o f three internationally notifiable diseases, and countries are requested to report cases to WHO prom ptly. Some governm ents m ay be concerned that reporting a large num ber o f cases could have a detrim ental im pact on econom ic factors such as tourism and food exportation. Prom pt and accurate reporting, however, w ill Im prove national and International efforts to allocate resources to control cholera m orbid ity and m ortality.

# Recommendations
The number of cholera cases should be reported to WHO in a timely manner.

# Summary of Recommendations
Case definitions for cholera - In a cholera epidem ic, use on ly tw o categories, "su sp e ct" and "c o n firm e d ."
- Define a suspect case as acute, w a te ry diarrhea affecting a person  5 years o f age.
- Define a confirm ed case as la boratory-confirm ed Vibrio cholerae 01 infection o f any person w h o has diarrhea.

# Laboratory confirmation and environmental surveillance
- Use trained personnel in regional and central laboratories to isolate and confirm V. cholerae 01.
- Confirm the diagnosis bacteriologically o f several suspect cases in new ly threatened areas. - A fte r cholera has become established in an area, use stool cultures o n ly to confirm the continuing presence o f V. cholerae 01 and to m o n ito r its a n tibiotic susceptibility.
- Consider using M oore swabs to id en tify V. cholerae 01 in sewage In cholera-threatened areas where cholera has not been confirm ed.

# Stages of surveillance
- In a cholera-threatened area, investigate cases o f acute dehydrating diarrhea affecting persons 5=5 years o f age. - W hen the num ber o f "c o n firm e d " cases rises, shift to using p rim a rily the "su sp e ct" case definition. - Continue to report suspect cases fo r at least 1 year after the epidem ic wanes.

# Information from patients w ith cholera
- Refrain from using lengthy surveillance questionnaires.
- Collect basic in fo rm a tio n on patients at the local level.
- T ransm it sum m ary data (prim arily the num ber o f cases, hospitalizations, and deaths) to the central level.

# Communication, analysis, and tim ely reporting of surveillance data
- Report surveillance results to a central office w eekly by a rapid m ethod.
- Analyze surveillance data and dissem inate surveillance reports to all com ponents o f the surveillance system quickly and frequently. - Conduct ep id em io log ic investigations in areas w ith increasing num bers o f cases.

# International reporting
- Accurately report the cou ntry's cholera situation to WHO in a tim e ly manner.