Enteric diseases, such as cholera, typhoid fever and shigellosis, still produce a significant burden, especially among the poor in countries where these illnesses are endemic. Older-generation, parenteral, whole-cell vaccines against cholera and typhoid fever were abandoned in many countries as public health tools because of problems with insufficient protection and/or inadequate safety profiles. Modern-generation licensed vaccines are available for cholera and typhoid fever, but are not widely used by those in greatest need. A number of experimental candidates exist for all three diseases. Future research should focus on generating the evidence necessary to obtain a consensus on the deployment of existing vaccines against cholera and typhoid fever, and on clinical evaluation of pipeline vaccine candidates against all three diseases

Acosta, CJ

Carbis, R

Clemens, JD

Deen, JL

Galindo, CM

Lee, HJ

Ochiai, RL

von Seidlein, L

English

LSHTM Research Online

Ochiai, RL; Wang, X; von Seidlein, L; Yang, J; Bhutta, ZA; Bhat-tacharya, SK; Agtini, M; Deen, JL; Wain, J; Kim, DR; Ali, M; Acosta,CJ; Jodar, L; Clemens, JD (2005) Salmonella paratyphi A rates, Asia.Emerging infectious diseases, 11 (11). pp. 1764-6. ISSN 1080-6040Downloaded from: http://researchonline.lshtm.ac.uk/10269/Usage GuidelinesPlease refer to usage guidelines at http://researchonline.lshtm.ac.uk/policies.html or alterna-tively contact researchonline@lshtm.ac.uk.Available under license: Creative Commons Attribution Non-commercial No Derivativeshttp://creativecommons.org/licenses/by-nc-nd/2.5/SalmonellaParatyphi A Rates,AsiaR. Leon Ochiai,* XuanYi Wang,* Lorenz von Seidlein,* Jin Yang,† Zulfiqar A. Bhutta,‡ Sujit K. Bhattacharya,§Magdarina Agtini,¶ Jacqueline L. Deen,* John Wain,# Deok Ryun Kim,* Mohammad Ali,*Camilo J. Acosta,* Luis Jodar,* and John D. Clemens*Little is known about the causes of enteric fever inAsia. Most cases are believed to be caused by Salmonellaenterica serovar Typhi and the remainder by S. ParatyphiA. We compared their incidences by using standardizedmethods from population-based studies in China,Indonesia, India, and Pakistan. Enteric fever still causes substantial illness and death inmany parts of the world, especially in poorer nations.Salmonella enterica serovar Typhi is believed to causemost enteric fever episodes, and a smaller portion arecaused by S. Paratyphi (1–3). This assumption, however,may no longer be true. Since 1999, more S. Paratyphi Athan S. Typhi strains have been isolated in the province ofGuangxi, southeastern China (4). Increasing isolation ratesof S. Paratyphi A has also been reported from India (5).This finding has 2 major implications for the prevention ofenteric fever. First, licensed typhoid fever vaccines (Vipolysaccharide and live oral Ty21a) do not protect againstinfections caused by S. Paratyphi A, and they may becomeless useful in controlling enteric fever in regions of Asia.Second, transmission and risk factors for S. Typhi and S.Paratyphi are different in Indonesia (6), so reductionstrategies effective against S. Typhi may not protectagainst S. Paratyphi. Since little is known about the currentcause of enteric fever in Asia, we compared S. Typhi andS. Paratyphi A incidence from study sites in China,Indonesia, India, and Pakistan by using standardized epi-demiologic and laboratory methods (7).The StudyAfter a baseline census, surveillance was conducted instudy sites in Karachi, Pakistan; Calcutta, India; NorthJakarta, Indonesia; and Hechi City, China, for 12 monthsto identify typhoid and paratyphoid cases from specificpopulations at high risk (Table). None of the sites had spe-cific enteric fever control programs in the past. Hechi City,China, is located in Guangxi Zhuang Autonomous Regionwhere Vi vaccines had been used in the past (8,9); howev-er, no such intervention had taken place in Hechi City. Theclosest county with a vaccination program was ≈80 kmaway and vaccinated only students (29,000 doses in 2001).During the surveillance period, persons with fever wholived in each study area were requested to visit participat-ing healthcare providers. We collected 5–10 mL bloodfrom adults with fever >3 days’ duration into Bactec bot-tles (Becton Dickinson, Franklin Lakes, NJ, USA). Wecollected 3–8 mL from children with fever >3 days’ dura-tion into Pediatric Bactec bottles. The bottles were incu-bated at 37°C for 7–10 days and visually checked forgrowth every day. Bottles were subcultured onMacConkey agar on days 1, 2, 4, and 7 or when turbiditywas detected. Suspected colonies were screened by usingKligler iron agar, sulfide-indole-motility medium, ureaagar, and citrate. Colonies that showed biochemical reac-tions suggestive of salmonellae were confirmed serologi-cally by Felix-Widal tube agglutination test with specificO and H antisera (Becton Dickinson). All Salmonella iso-lates were confirmed at a reference laboratory (Universityof Oxford, Wellcome Trust Clinical Research Unit, Ho ChiMinh City, Vietnam).Incidence rates were calculated by using age-specificdenominators of the population living in the catchmentarea based on the study census. We assumed that each per-son living in the study area contributed 12 months of per-son-time to the denominator. The number of diseaseepisodes in eligible individuals was used as the numerator. Each study received individual approval from the localethical committees, the institutional review board of theInternational Vaccine Institute (Seoul, Korea), and theSecretariat Committee for Research Involving HumanSubjects, World Health Organization (Geneva,Switzerland).During the surveillance period, 285 S. Typhi episodesand 84 S. Paratyphi A episodes were detected at the 4 sites(Table). In Indonesia, 14% of enteric fever episodes werecaused by S. Paratyphi A, in Pakistan 15%, in India 24%,and in China 64% (Figure). The highest S. Typhi incidencewas observed in Pakistan (394/100,000/year), and the low-est S. Typhi incidence was found in China(15.2/100,000/year). The highest S. Paratyphi A incidencewas also seen in Pakistan (72/100,000/year), and the low-est S. Paratyphi A incidence was seen in Indonesia(13.7/100,000/year).DISPATCHES1764 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 11, No. 11, November 2005*International Vaccine Institute, Seoul, Korea; †Guangxi Centersfor Disease Control and Prevention, Nanning, People’s Republicof China; ‡Aga Khan University, Karachi, Pakistan; §NationalInstitute of Cholera and Enteric Diseases, Kolkata, India;¶National Institute of Health, Research and Development, Jakarta,Indonesia; and #Sanger Institute, Cambridge, United KingdomConclusionsThe perception that a small proportion of enteric fevercases are caused by S. Paratyphi A is probably no longertrue in many regions of Asia, especially in southeast China,where S. Paratyphi A is already more frequently isolatedthan is S. Typhi. This finding could be signaling the emer-gence of S. Paratyphi A as a pathogen in Asia. Comparisonof S. Paratyphi A incidence during the last decade is need-ed to prove this hypothesis. However, none of the siteshave comparable surveillance data on S. Paratyphi A overtime. An alternative explanation is that the incidence of S.Typhi is decreasing. Previous reports from vaccine trialshave shown successful control of S. Typhi but no changesin the incidence of S. Paratyphi A (8,10,11). Nonetheless,the reversal of the proportion of S. Typhi and S. ParatyphiA infections in Hechi City, China, is unlikely to be theresult of typhoid fever control in other counties, consider-ing the distance and oral-fecal transmission route of S.Typhi and S. Paratyphi A. Economic growth in Asia has also resulted in improvedwater supply, sanitation, and hygiene; however, we haveno reason to assume selective reduction only for transmis-sion of S. Typhi. The incidence of typhoid fever per100,000 in the different countries follows the same patternas mean gross national income (2003) and the mortalityranking for children <5 years (12). The sensitivity of blood culture for S. Typhi is welldescribed, but little is known about S. Paratyphi A.Bacterial loads during infection are probably similar forboth S. Typhi and S. Paratyphi A (J. Wain, unpub. data).Furthermore, S. Paratyphi A had been rarely isolated inthese regions, which suggests that the increase in isolationrate of S. Paratyphi A is possibly caused by an increase inthe number of cases of enteric fever caused by S.Paratyphi A rather than any bias toward blood culture–positive disease.Besides the limitation that our studies only describe a12-month period, the population varied between sites. InPakistan, only children 2–16 years of age were included.As S. Paratyphi A infections are more frequently observedin adults, including older patients in surveillance mayincrease S. Paratyphi A incidence rates reported fromPakistan.In China and India, countries with the largest popula-tions in the world, S. Paratyphi A is the causal agent for asubstantial proportion of enteric fever episodes that can-not be distinguished clinically from typhoid feverepisodes. While similar treatment strategies may work forboth organisms, future enteric fever prevention strategiesin Asia must focus on S. Paratyphi A as well as on S.Typhi, especially when considering the emergence ofdrug-resistant strains (13–15). Future vaccination strate-gies should include bivalent vaccines that protect againstS. Typhi as well as S. Paratyphi A. Otherwise, the protec-tive effectiveness of typhoid fever vaccines (Vi, Ty21a)against enteric fever may diminish, which could result ina loss of public confidence and decrease public willing-ness to be vaccinated.AcknowledgmentsWe are grateful for the support for this work received fromC.M. Galindo, A.L. Page, M.C. Danovaro-Holliday, and J. Farrar.We acknowledge the hard work from the laboratory personnelfrom each site, M.L. Wang, D. Alam, S. Dutta, and Murad. Wethank an anonymous reviewer for valuable suggestions. This work was supported by the Diseases of the MostImpoverished Program, funded by the Bill and Melinda GatesFoundation and coordinated by the International VaccineInstitute.Mr Ochiai is associate research scientist at the InternationalVaccine Institute, coordinating the Diseases of the MostImpoverished Typhoid Fever Program. His specialty is epidemi-ology and international health, and his current area of interest isvaccine-preventable disease epidemiology.Salmonella Paratyphi A Rates, AsiaEmerging Infectious Diseases • www.cdc.gov/eid • Vol. 11, No. 11, November 2005 1765Figure. Incidence of Salmonella enterica serovar Typhi and S.Paratyphi A in 4 Asian countries.References1. Herikstad H, Motarjemi Y, Tauxe RV. Salmonella surveillance: aglobal survey of public health serotyping. Epidemiol Infect.2002;129:1–8. 2. Crump JA, Youssef FG, Luby SP, Wasfy MO, Rangel JM, Taalat M,et al. 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Vaccines against cholera, typhoid fever and shigellosis for developing countries.

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