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Home , Campylobacteriosis, Campylobacter jejuni, Dysentery

Journal of and Public Health (2011) 4, 12—21

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A comparison of disease caused by and species: 24 months community based surveillance in 4 slums of Karachi, Pakistan

Sajid Bashir Soofi a,∗, Muhammad Atif Habib a, Lorenz von Seidlein c, Muhammad Jawed Khan a, Shah Muhammad a, Naveed Bhutto a, Mohammad Imran Khan a, Shahid Rasool a, Afia Zafar b, John D. Clemens c, Qamaruddin Nizami a, Zulfiqar A. Bhutta a

a Department of Paediatrics & Child Health, Aga Khan University, Pakistan b Department of Microbiology, Aga Khan University, Pakistan c International Vaccine Institute, Seoul, Republic of Korea

Received 26 March 2009; received in revised form 10 October 2010; accepted 15 October 2010

KEYWORDS Summary Despite the efforts of the international community diarrheal dis- ; eases still pose a major threat to children in children less than five years of ; age. Bacterial diarrhea has also emerged as a public health concern due to the ; proliferation of drug resistant species in many parts of the world. There is a Children; paucity of population-based data about the incidence of shigellosis and Campy- Epidemiology lobacter in Pakistan. We report country specific results for Shigella diarrhea that were derived from a multicenter study conducted in six Asian coun- tries. Disease surveillance was conducted over a 24 month period in urban slums of Karachi, Pakistan, a city with a population of 59,584. Cases were detected through passive detection in study treatment centers. Stool specimens or rectal swabs were collected from all consenting patients. Between January 2002 and December 2003 10,540 enteric infection cases were detected. The incidence rate of treated diarrhea in children under 5 was 488/1000/year. In children, 5 years and older, the diarrhea rate was 22/1000/year. 576 (7%) Campylobacter isolates were detected. The pre-dominant Campylobacter species was C. jenuni with an increase of 29/1000 year in children under 5 years. Shigella species were iso- lated from 394 of 8032 children under 5 years of age. Shigella flexneri was the dominant species (10/1000/year in children under 5 years) followed by (3.9/1000/year), (2.0/1000/year) and (1.3/1000/year). Shigellosis and Campylobacter infection rates peaked during the

∗ Corresponding author at: Department of Pediatrics & Child Health, Aga Khan University, P.O. Box 3500, Stadium Road, Karachi 74800, Pakistan. Tel.: +92 21 4864798. E-mail address: sajid.soofi@aku.edu (S.B. Soofi).

1876-0341/$ — see front matter © 2010 King Saud Bin Abdulaziz University for Health Sciences. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.jiph.2010.10.001 A comparison of disease caused by Shigella and Campylobacter species 13

second year of life. The incidence rate of shigellosis increased in old age but such a trend was not observed in Campylobacter infections. Of 394 shigellosis patients 123 (31%) presented with in contrast to only 54 (9%) of 576 patients with Campylobacter infections (p < 0.001). Both Campylobacter infections and shigellosis are common in community settings of Pakistan but shigellosis presented more fre- quently with and dysentery than Campylobacter infections indicating that shigellosis may be a more severe illness than Campylobacter infections. Due to the increased and disease severity, drug resistant shigella have become a significant health problem; moreover it is a disease of poor and impoverished people who do not have the access to standard water and sanitary conditions, health care services or optimal treatment. In the face of these facts it is empirically important to develop a low cost effective vaccine that can protect these populations for a longer duration. © 2010 King Saud Bin Abdulaziz University for Health Sciences. Published by Elsevier Ltd. All rights reserved.

Introduction and mishandling of [11,12]. Based on the Despite efforts of the global community to control studies from Thailand and Mexico the incidence and prevent the diarrheal diseases, they still remain rates are estimated to be 40,000 per 100,000 for a major cause of morbidity and mortality in children children younger than five years [11]. In develop- especially in impoverished areas of South East Asia ing countries, Campylobacter infections in children [1,2] moreover the incidence of dysentery (which commonly occur under the age of two years and can is an aggravated diarrheal condition characterized sometimes leads to death and other complications by frequent passage of stool containing and [12]. In several community-based surveys Campy- ) has also increased. Much of the dysentery lobacter jejuni was the most commonly isolated is considered to be of bacillary origin species of enteropathogen in diarrheal stools from children Shigella (S. flexneri, S. sonnei, S. dysenteriae, and aged less than 5 years [13]. S. boydii) and Shigellosis has become a public health Like shigellosis Campylobacter infections are issue [3]. also wide spread and C. jejuni is considered to be On a global level, it is estimated that about 165 a common cause of acute bacterial million cases of diarrhea due to Shigella occurs globally. The organism becomes more serious annually, 99% occur in developing countries, and due to its association with serious post-infection in developing countries 69% of episodes occur in neurological complications. A study conducted children under five years of age. About 1.1 mil- by Clarence et al. reveals a much increased lion deaths are attributed to Shigella infections in risk of Gullien Barre Syndrome (GBS) among developing countries, 60% of which occur in the Campylobacter patients compared with under-five age group [3]. A multicenter study con- previously reported studies [14]. Campylobacter ducted in six Asian countries illustrates incidence are widespread in both developed and developing rates of Shigellosis up to 13% [4]. A combination of countries but due to increasing incidence and disease severity and resistance is posing much attention is required to address a real dilemma especially in young children [5,6]. the problem in developing countries [15]. The recognition of extended range beta lactamases Drug resistance is also an important factor while in Shigella strains may jeopardize the effec- addressing Campylobacter infections. Addressing tiveness of including third-generation these infections in many developed countries is a cephalosporins [7—9]. The appearance of resistance priority due to the emergence of increased levels against the majority of antimicrobials has added of resistance [16]. Further the infections urgency to the development of vaccines which portray the same situation of drug resistance even can protect against shigellosis while to date only in the developing countries which is evident from a single vaccine to protect against shigellosis is the studies conducted in Thailand by Serichanta- accredited worldwide [10]. lergs and colleagues [17]. Campylobacter infection is also a common cause The Campylobacter disease burden is also quite of acute gastroenteritis both in the developed and high in the south Asian region. Studies from developing countries and like other bacterial infec- Bangladesh, and Pakistan reveals that it tions incidence is much higher in the developing is one of the most frequent organisms causing nations due to poor water and sanitary conditions gastroenteritis [18]. In Pakistan the presence of 14 S.B. Soofi et al.

Campylobacter organisms are quite high in food The quackery medical practice was common and commodities which are usually used by the common Quacks or ‘‘village doctors’’ who have no for- man [19], which in turn results in an increased inci- mal training or degree used to prescribe allopathic dence of Campylobacter infections (12%) in all age medications even antibiotics. Untrained pharmacy groups [20]. Another study conducted at Rawalpindi shopkeepers and registered pharmacists provide reveals that C. jejuni is the most frequent cause medication based on the description of the signs of childhood diarrhea and dysentery in that setting and symptoms of the patient over the counter. In [21]. addition, a variety of traditional healers (Hakims) Due to its epidemiological spread, Pakistan is a and homoeopaths practiced in the study areas. potential site for future vaccine trial and in ground- Once these primary health care providers have been ing of future vaccine trial sites it is crucial to exhausted the residents of the study areas can seek recognize the shigellosis incidence as shigellosis is treatment from hospitals. A study clinic was estab- much more notorious than the other enteric organ- lished in each of the 4 slums for more than a year isms. Our study is the foremost community based before the surveillance started, these clinics were study to estimate the factual incidence of shigel- equipped with trained doctors, medicines and rel- losis on a population level. Earlier hospital based evant laboratory equipment. The clinics provided studies do not provide a denominator essential for free medical services for residents. The availabil- incidence estimates [22—29]. Not only is it signif- ity of free healthcare in the study clinics had been icant to appreciate the shigellosis incidence in a announced during community meetings when resi- study area it is evenly imperative to understand dents were asked to attend the study clinics in case the distribution of Shigella serogroups, types, and of diarrhea. The presence of the study clinics was subtypes because the knowledge about cross pro- further publicized during the census. tection between Shigella serotypes and subtypes We estimated the burden of enteric diseases is very limited at best [30]. We have consequently through a population-based, surveillance system. A conducted shigellosis surveillance in 4 urban slums passive case detection system was used which cap- of Karachi over a 24 months period. The unexpect- tured patients when they visited the study clinics. edly high detection rates of Campylobacter species Each household was visited weekly and the house- have allowed us to evaluate and contrast the epi- hold head or a representative was asked about demiology as well as the clinical presentation of diarrhea cases in the preceding 7 days. If a diarrhea shigellosis and Campylobacter infections. case was reported the patient was asked to come to the study clinic. The study followed a generic pro- tocol, which was adapted to local needs by staff Methods and collaborating centers [32]. Verbal consent was obtained from each participant (parent or guardian This study was done as a part of the Multicenter for children) following an explanation of the pur- study for Shigella diarrhea in six Asian countries pose of the study. [4] to compare shigellosis with campylobacterio- Consenting patients of all age groups with diar- sis in four slum communities, in Karachi, Pakistan rhea or dysentery presenting to the study clinics (Rehri Goth, Sherpao Colony, Sultanabad and Hijrat were eligible to participate in the study. Diarrhea Colony). Pashto and Hazara migrants from the was defined as three or more loose bowel move- NWFP Province of Pakistan are the major population ments during a 24-h period, dysentery as one or groups in the impoverished slum areas of Sherpao more loose bowel movements with visible blood, colony, Hijrat colony and Sultanabad. Rehri Goth is and as an axillary temperature of 37.5 ◦Cor a much older fishing community mainly consisting of higher. Diarrhea following three days or more of Sindhi speaking settlers. A census was conducted in normal bowel movements was considered a new each of the communities prior to the surveillance diarrhea episode. For every patient presenting with that demonstrated a population of 59,584 indi- diarrhea, a case report form (CRF), describing viduals including 8381 children less than 5 years. demographics and medical history & examination Karachi is a tropical area with hot summers last- was completed and two rectal/stool swabs or a ing from April through October and more moderate stool specimens were obtained. All the cases were temperatures for the rest of the year, rains are provided with the standard treatments as outlined expected during the second half of each summer in the protocols. All consenting patients with a but can skip one or more years. history of dysentery or diarrhea for three days or The health care system of these slums con- more were eligible to participate in the study. The sisted of 79 private practitioners, among them 32 study received approval from the Aga Khan Univer- were the graduates from medical colleges [31]. sity Ethics Review Committee and the Secretariat A comparison of disease caused by Shigella and Campylobacter species 15

Committee for Research Involving Subjects, 10540 Diarrhea Patients presented * WHO, Geneva, Switzerland. 90 Revisits 70 Not eligible† To isolate the exact organism we set up a stan- 2339 didn’t provide a specimen dard laboratory at every clinic. We obtained three 8032 patients enrolles rectal swabs one for buffered glycerol saline (BGS), 576 campylobacter Isolates¶ 547 C. Jejuni one for alkaline peptone water APW and one for 24 C.Coli phosphate buffered saline PBS and along with that 5 C. Larid 394 Shigella Isolates‡ we ask the patient to bring a stool sample in a con- 242 S. Flexerni tainer for stool culture. All these medias were used 72 S. Sonnei for the enrichment and transport of the isolates to 42 S. Boydii 37 S. dysenteriae the Central Lab at Aga Khan University, Karachi, 340 Other Isolates§ Pakistan. The collected stool samples were also 129 V. Cholerae 56 E.Coli plated immediately onto XLD-, SS-, MacConkey’s- 98 Spp. ◦ agar and incubated at 37 C for 18—24 h before 57 Aeromonas Spp. transport at the center. All swabs and stool samples 6756 No organism Isolated were stored refrigerated and transported daily in a *During the study period 1/1/2002 to 12/31/03 cool box to the Central Laboratory at Aga Khan Uni- †Didn’t fulfill the inclusion criteria ‡From 22 patients more than one organism was isolated versity, Karachi following the standard protocols. ¶From 25 patients more than one organism was isolated The Central Laboratory at Aga Khan University is §From 21 patients more than one organism was isolated one of the state of the art laboratories in the South Asian region. To ensure the robust implementation Figure 1 Case assembly. *During the study period 1/1/2002 to 12/31/03. †Did not fulfill the inclusion cri- of laboratory procedures, the doctors of the health ‡ centers received an extensive training for all labo- teria. From 22 patients more than one organism was isolated. ¶From 25 patients more than one organism was ratory procedures. § isolated. From 21 patients more than one organism was On arrival specimens in BGS were plated on isolated. MacConkey’s agar and Salmonella-Shigella agar. Biochemical reactions of lactose negative colonies software (SAS Institute Inc., Cary, NC, USA) and were evaluated with Triple Iron agar and Stata/SE 8 (Stata Corp., Texas, USA). A p-value less Lysine Indole Motility medium isolates producing than 0.05 (2-tailed) was considered significant. Inci- reactions consistent with shigella were sero- dence rates were calculated by using age-specific logically confirmed by slide agglutination with denominators of the population residing in the appropriate group-specific polyvalent antisera, catchment area in 2001. We calculated 95% CI for followed by type-specific monovalent antisera the incidence rates by the Wilson score method (Denka-Seiken, Tokyo, Japan). In cases where no [33]. As the observation period was 24 months, agglutination occurred with live , the test we assumed that each person residing in the study was repeated with boiled suspensions of bacteria. area contributed 24 months of person time to the Campylobacter was identified after 48 h by colony denominator. The number of age-specific disease morphology, , Gram staining, and motil- episodes was used as numerator. For the compar- ity. The organisms were identified to species level ison of clinical presentations only patients were by a positive test, a negative urease test, included from whom a single organism was isolated. failure to produce H2S, and non-fermentation in Patients with multiple infections (co-infections) TSI, resistance to cephalotin, nitrate reaction and were excluded. hippurate hydrolysis. Although in the main study of Through out the surveillance period, the senior Shigella diarrhea the investigators look for Shigella level staff did regular ongoing monitoring and eval- using PCR but that was not done in Pakistan. All PCR uation of various process and outcome indicators. studies were conducted at the USAFRIMS, Bangkok, The data management unit produced an indicator Thailand [4]. report on weekly basis that reflected the flow of the All Case Record Forms were archived serially project activities. To ensure the proper implemen- in the box files and then were double entered tations of the project, regular refresher trainings into a custom-made data entry programs (FoxPro, were provided to the staff involved in the project. Microsoft, Redmond, WA, USA). The data manage- ment programs included error as well as consistency and range check programs. Chi-square tests were Results used for binary data analysis. For the analysis of non-normally distributed data, Wilcoxon rank sum During the 24 month study period, which started test was applied. Data were analyzed with SAS 1st January 2002 and ended on 31st December 16 S.B. Soofi et al.

a 1000 35 Diarrhea 900 Dysentery Temp (°C) 30 800 Precip (mm)

700 25

600 20

500 Celsius 15 o no. of cases 400 mm of precipitation

300 10

200 5 100

0 0 Jan-03 Feb-03 Mar-03 Apr-03 May-03 Jun-03 Jul-03 Aug-03 Sep-03 Oct-03 Nov-03 Dec-03

b 90 300 shigellosis 80 campylobacter Precip (mm) 250 70 Temp (°C)

60 200

50 150 Celsius

o 40 no. of cases

30 100 mm of precipitation

20 50 10

0 0 Jan-03 Feb-03 Mar-03 Apr-03 May-03 Jun-03 Jul-03 Aug-03 Sep-03 Oct-03 Nov-03 Dec-03

Figure 2 (a and b) Seasonality of enteric infections in relation to weather changes in Karachi, Pakistan in 2003.

2003 10,540 enteric infection cases were detected serotypes were 2a (38 of 89 isolates; 16%) followed (Fig. 1). The incidence rate of treated diarrhea in by S. flexneri 6 (37 isolates; 15%), S. flexneri 1b (25 children under 5 years was 488/1000/year com- isolates; 10%), and S. flexneri 2b (23 isolates; 10%). pared to 22/1000/year in the older population. This high incidence in young children is a clear evi- dence that the enteric infections still prevail in the younger populations. Enteric infections (diarrhea, dysentery) and specifically Campylobacter infections and shigel- losis increased during the warmer months of the year (Fig. 2a and b). There was no correlation between changes in enteric infections rate and rainfall in 2003. From 8032 stool specimens 394 (5%) Shigella species were isolated. S. flexneri was the dom- inant species (10/1000/year in children under 5 years) followed by S. sonnei (3.9/1000/year), S. boydii (2.0/1000/year) and S. dysenteriae Figure 3 Incidence of children under 5 years presenting (1.3/1000/year). The dominant S. flexneri with dysentery in Karachi, Pakistan. A comparison of disease caused by Shigella and Campylobacter species 17

a 70

60

50 shigellosis campylobacter 40

30

20

incidence rate / 1000 year 10

0 1st 2nd 3rd 4th 5th 6th 7th 8th 9th 10th year of life b 2.5

2 shigellosis

campylobacter 1.5

1

incidence rate / 1000 year 0.5

0 10 to 19 20 to 29 30 to 39 40 to 49 50 to 59 60 to 69 70+ years of life

Figure 4 (a and b) Age distribution of Shigella and Campylobacter infected patients in Karachi, Pakistan.

During the study period 576 (7%) Campylobac- Of 394 shigellosis patients 123 (31.2%) presented ter isolates were detected. The most frequently with dysentery in contrast only 54 (9.3%) of 576 isolated Campylobacter species was C. jejuni patients with Campylobacter infections (Table 1). (29/1000/year in children under 5 years) fol- The percentage of Campylobacter and shigellosis lowed by (1.4/1000/year in patients presenting with dysentery varied with children under 5 years) and Campylobacter lar- the age of the patient and the infecting species idis (0.3/1000/year in children under 5 years) (see (Fig. 5). Of 173 children with S. flexneri infections Fig. 3). 58 (34%) presented with dysentery in contrast to 31 There were significant differences between of 69 (45%) adults (p = 0.05; Fig. 5). The percent- the presentation of Campylobacter infections and ages of Campylobacter infected patients presenting shigellosis. Shigellosis patients were significantly with dysentery were identical to the percentages older (mean age 6.3 years) compared to Campy- patients presenting with dysentery from whom no lobacter patients (mean age 2.8 years, p < 0.001; organism could be isolated. Table 2). As illustrated in Fig. 4a both shigellosis and Campylobacter infections peaked in the 2nd year of life and dropped below 10/1000/year by Discussion the 5th year of life. In contrast to Campylobac- ter infection rates, shigellosis rates increased with Surveillance in impoverished areas of Karachi found increasing age after age 30 (Fig. 4b). relatively high shigellosis and even higher rates of Of the 10,540 enteric infections 1123 (11%) pre- Campylobacter infection. Consistent with previous sented with dysentery. Out of which 123 (11%) were studies the dominant Campylobacter species was Shigella species and 54 (5%) were Campylobac- C. jejuni and the dominant Shigella species was S. ter species respectively. The dysentery incidence flexneri [34]. The infection rates were highest in was highest in S. flexneri patients (3.5/1000/year the extremes of age. Both infections peaked in the in children under 5 years) followed by C. jejuni second year of life. Newborns may be protected (2.5/1000/year; Fig. 5). against shigellosis and Campylobacter infection by 18 S.B. Soofi et al.

90% % of children < 5 years 80% % of individuals 5 years and older

70%

60%

50%

40%

30%

20% % patients presenting with dysentery

10%

0% S.flexneri S.sonnei S.dysentriae S.boydii C.coli C.jejuni C.larid no organism

Figure 5 The percentage of patients with Shigella or Campylobacter infections presenting with dysentery (the 95% confidence intervals are shown as whiskers). *No organism isolated.

Table 1 Total population, number of cases over a 24 months observation period, incidence rates and 95% confidence intervals in Karachi, Pakistan. <60 months ≥60 months Total n = 59,584a n = 8381a n = 51,203a Cases IR/1000/year Cases IR/1000/year Cases IR/1000/year Diarrhea 8174 488 (477—498) 2276 22 (21—24) 10,450 88 (86—90) Dysentery 761 45 (41—50) 362 4 (3—4) 1123 9 (9—10) Campylobacter infections 515 31 (27—35) 61 0.6 (0.4—0.9) 576 5 (4—5) Shigellosis 292 17 (15—21) 102 1 (0.7—1.3) 394 3 (2.9—3.90) Shigellosis dysentery 82 5 (4—7) 41 0.4 (0.2—0.6) 123 1.0 (0.8—1.3) Campylobacter dysentery 45 3 (2—4) 9 0.1 (0.0—0.2) 54 0.5 (0.3—0.7) a Denominator.

Table 2 Patient characteristics. Shigellosis patients % Age Campylobacter patients % Age na 372a 551b Male 207 56% 320 58% Age (mean) 6.3 — 2.8 — Age (median) 2 — 1.5 — Dysentery 119 32% 50 9% Ever watery stools 236 63% 413 75% Mucous stools 95 26% 125 23% Abdominal pain 46 12% 43 8% 1 0.3% 2 0.4% Fever 135 36% 224 41% 46 12% 70 13% 17 5% 27 5% Number of stools in the last 24 h 5 or less 139 37% 201 37% 6—10 118 32% 141 26% 11—30 10 3% 9 2% Too many to count 105 28% 200 36% a 22 patients with co-infections have been excluded. b 25 patients with co-infections have. A comparison of disease caused by Shigella and Campylobacter species 19 trans placental antibodies, breast , and per- bowel movements. These findings are in agreement haps lower exposure rates [35—39]. Following a with findings from Bangladesh as well as other coun- peak in the first years of life the rates for both infec- tries [42,43]. tions dropped by more than an order of magnitude. Shigellosis and Campylobacter infections appear After age 30 a trend for increasing shigellosis rates to have a similar seasonality. Consistent with was observed but not for Campylobacter. This find- previous reports from Karachi, shigellosis and ing may be explained by waning immunity against Campylobacteriosis rates increased in the hot sum- shigellosis with increasing age. There is no apparent mer months and dropped during the colder months waning of immunity against Campylobacter infec- of the year [44]. The notion that ‘‘the seasonal vari- tions. ation of C. jejuni infection appears to be influenced Alternatively of shigellosis may by rainfall’’ was not supported by our findings [45]. increase with increasing age. Shigellosis is thought The increase in all enteric infections including C. to be mostly transmitted from person to person. jejuni started well before the onset of rains in 2003 Flies may in some places play a role in the trans- in Karachi. mission of this disease [40]. The transmission of Several hospital-based studies of enteric infec- Campylobacter is less well understood. It is thought tions have been conducted in Pakistan including that most and many household pets are Karachi. The studies found that from between Campylobacter carriers in Pakistan [41]. The age 3% and 19% of stool specimens were Shigella distribution of C. jejuni infections is very different positive [22—24,26,44]. In hospital based found in the USA where after a peak in the first years of studies Campylobacter was isolated from 17% to life a second peak of infections is observed during 25% of stool specimens [41,42,46—48]. In our study the third decade of life [42]. Not surprisingly the Shigella species were isolated was from 5% of stool age distribution of C. jejuni cases in Bangladesh specimens that is at the lower end of the expected described by Glass and coworkers more than 20 range. Campylobacter species were isolated from years ago was strikingly similar to our findings in 7% of specimens which is below the expected range. Pakistan [43]. Our study differs from previous reports in that Shigellosis and Campylobacter infections were it was community-based and included patients of also significantly different in their presentation. A all ages hence patients with a potentially differ- significantly larger proportion of shigellosis patients ent disease severity and prevalence. Furthermore presented with dysentery compared to patients our study was set up to detect shigellosis cases with Campylobacter infections. Indeed the percent- and methods were optimized to detect Shigella age of Campylobacter infected patients presenting species. Campylobacter unlike Shigella species are with dysentery was similar to the percentage in highly fastidious and may have escaped detection. patients from whom no organism could be iden- A cohort study conducted in Mexico found that tified. It cannot be excluded that co-infection children under 5 years had 2.1 episodes of Campy- with agents responsible for the background rates lobacter infections per year [48]. In a hospital of dysentery also cause dysentery in Campylobac- based study in the US Campylobacter spp. were ter infection patients. Older patients presented isolated from 5% of stool specimens [42]. A study more frequently with dysentery compared to chil- in Bangladesh C. jejuni in 14% of outpatients pre- dren less than 5 years. This finding may be best senting with diarrhea to a research hospital [43]. explained by differences in health care utilization. However C. jejuni was isolated less frequently from Adult patients may only seek care for severe dis- village children with diarrhea (5%). ease including dysentery. Children may be brought The findings of our study were consistent with to health care providers for more trivial disease another done in Peru [49]. The Peruvian study episodes. reveals that C. jejuni was the leading cause of diar- Two thirds of the shigellosis patients had at rhea and is more frequent in malnourished children some stage of their diarrhea episode watery diar- with low socioeconomic background. The partici- rhea. The proportion of patients who had at pants in our study also belonged to a low socio some stage watery diarrhea was even higher in economic stratum of society. The Peruvian study patients with Campylobacter infections. An obser- also found an excess risk of GBS among Campylobac- vation that challenges the notion which associates ter enteritis patients [14]. We followed our cases shigellosis exclusively with dysentery. Abdominal and did not find such trends. pain was more frequently associated with shigel- Our study made use of passive surveillance. losis than with Campylobacter infections. While Patients were captured when they presented to shigellosis appears to cause more pain and dysen- study clinics. This method has the advantage that tery. C. jejuni infections caused more frequent trivial diarrhea cases that usually would not seek 20 S.B. Soofi et al. treatment are not included. Passive surveillance Conflict of interest statement however has the disadvantage that patients who seek care outside the study clinics will escape the Funding: No funding sources. surveillance. Furthermore 23% of diarrhea patients Competing interests: None declared. who were captured by the surveillance did not Ethical approval: Not required. provide a stool specimen. 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