Conceived and designed the experiments: HNN BO DRF EDM RFB. Performed the experiments: JBO NW JO. Analyzed the data: HNN LC JW DN. Wrote the paper: HNN.
Worldwide,
Surveillance participants were interviewed in their homes every 2 weeks by community interviewers. Participants also had free access to a designated study clinic in the surveillance area where stool specimens were collected from patients with diarrhea (≥3 loose stools within 24 hours) or dysentery (≥1 stool with visible blood during previous 24 hours). We adjusted crude incidence rates for participants meeting stool collection criteria at household visits who reported visiting another clinic.
More than 1 of every 200 persons experience shigellosis each year in this Kenyan urban slum, yielding rates similar to those in some Asian countries. Provision of safe drinking water, improved sanitation, and hygiene in urban slums are needed to reduce disease burden, in addition to development of effective
Although rates have decreased in middle-income and wealthy nations, shigellosis remains a major public health problem in impoverished settings because of sub-optimal sanitation and hygiene and contaminated water supplies
Symptoms of shigellosis typically include diarrhea and/or bloody stools with abdominal cramps and tenesmus
Previous estimates of the burden of shigellosis in developing countries may have underestimated its magnitude. Studies present varying incidence and prevalence rates, because of divergent methods and intrinsic disparities among the populations studied
Since 2005, the Centers for Disease Control and Prevention (CDC) and the Kenya Medical Research Institute (KEMRI) have maintained population-based infectious disease surveillance (PBIDS) in a geographically defined area within an urban informal settlement in Nairobi, Kenya
The urban PBIDS system is based in Kibera, a large informal settlement (urban slum) in Nairobi, Kenya. Kibera lacks adequate sanitation facilities; human and animal wastes drain into open sewage runoff. Drinking water is often obtained from unregulated vendors using illegal connections to a municipal piped water system, a situation that facilitates contamination of water supplies. Food is traded at unregulated outdoor markets that often lack basic hygiene standards.
The PBIDS procedures have been described previously
From January 1, 2007 through December 31, 2010, we collected stool samples from consenting patients who met the following criteria:
Uncomplicated diarrhea (defined as ≥3 loose stool within a 24-hour period) without signs or symptoms of dehydration or dysentery. (To minimize burden on the laboratory we sampled a maximum of 6 stool specimens from patients with uncomplicated diarrhea per day: 3 from patients <5 years old and 3 from patients ≥5 years old);
Complicated diarrhea based on the presence of symptoms or signs of dehydration, defined as: drinking eagerly or unable to drink or breastfeed, vomiting everything, slow skin pinch return (≥2 seconds), irritability, sunken eyes, lethargy or unconsciousness (all patients);
Dysentery, defined as reported or visible blood in ≥1 stool within 24 hours of clinic visit (all patients).
A case of shigellosis was defined as a patient meeting any of the above criteria who had
We provided each consenting participant meeting the stool collection criteria with a labelled stool container and instructions on how to sample their stool; placing emphasis on including blood or mucus, if present. From May 2008, patients visiting the clinic who were unable to provide a stool sample while at the clinic were sent home with a labelled container to collect a stool specimen. A sample collector was then sent to the patient's home to collect the specimen within 4 hours after the clinic visit. Swabs of whole stool specimens were placed in Cary-Blair transport medium, refrigerated at 4–8 °C then transported to the KEMRI-CDC enteric microbiology laboratory in Kisumu from Jan 2007 to May 2009; thereafter, stool specimens were processed in a microbiology laboratory at the study clinic. More than 80% of specimens were processed within 24–28 hours after collection. Specimens were processed using standard microbiological procedures
Data were analysed using SAS version 9.1 (Cary, NC). We calculated incidence rates as the number of shigellosis cases per 100,000 person-years of observation (PYO), as described previously
In calculating crude incidence rates, we divided the number of
The overall adjusted incidence rate was calculated by summing the adjusted
For characterizing clinical features, drug susceptibility and
Logistic regression analysis was used to determine association of clinical features and shigellosis for patients seen at the clinic. Significant unadjusted clinical features (p<0.05) were then entered into a multivariate model to control for confounding. We also examined household data collected from patients confirmed to have shigellosis for a period of one month after the clinic visit when the diagnosis was made to assess the number of hospitalizations and deaths
We used incidence rates from this study to project the burden of shigellosis among the estimated 4.3 million people living in informal settlement areas in Kenya
The protocol, surveillance questionnaires and consent forms were reviewed and approved by the Ethical Review Committee at the Kenya Medical Research Institute (protocol number 1899) and the Institutional Review Board of CDC- Atlanta (protocol number 4566).
Between 1 May, 2008, and 31 Dec, 2010, 77,939 PYO were contributed by persons enrolled into the surveillance system. Adults 18–34 years of age accounted for 35% of the population under surveillance, followed by young adults 10–17 years who accounted for 16%. Males and females contributed equally. The highest proportion of surveillance participants were from Zone 1; 18% followed by zone 10; 16% (
| Person years of observation (PYO) | Incidence rates | ||
| Crude incidence/100,000 | Adjusted incidence/100,000 | ||
| Age category | |||
| <12 m | 2,369 (3) | 84 | 136 |
| 12– | 2,954 (4) | 203 | 273 |
| 24–59 m | 8,936 (11) | 291 | 369 |
| 5–9 y | 12,070 (15) | 141 | 175 |
| 10–17 y | 12,765 (16) | 212 | 268 |
| 18–34 y | 26,968 (35) | 356 | 559 |
| 35–49 y | 4,207 (5) | 1046 | 1575 |
| 50 y+ | 7,669 (10) | 78 | 108 |
| Sex | |||
| Males | 39,090 (50) | 219 | 306 |
| Females | 38,849 (50) | 356 | 484 |
| Year | |||
| 2008 | 17,658 (23) | 306 | 392 |
| 2009 | 28,892 (37) | 270 | 363 |
| 2010 | 31,388 (40) | 293 | 428 |
| 1 | 13,741 (18) | 393 | |
| 2 | 9,398 (12) | 766 | |
| 3 | 2,467 (3) | 446 | |
| 4 | 2,828 (4) | 601 | |
| 5 | 7,839 (10) | 370 | |
| 6 | 8,852 (11) | 215 | |
| 7 | 5,111 (7) | 274 | |
| 8 | 10,219 (13) | 391 | |
| 9 | 5,379 (7) | 316 | |
| 10 | 12,105 (16) | 256 | |
| Overall | 77,939 | 287 | 408 |
Adjusted incidence rates by zone not shown
Over 80% of enrolled study participants had successful interviews during the biweekly/weekly household visits. By year, this was distributed as follows; 78% in 2007, 74% in 2008, 83% in 2009 and 84% in 2010. During these visits, over 60% of participants who met any of the stool collection criteria and reported visiting any clinic, had visited Tabitha clinic (data not shown). At Tabitha clinic, 7,449 patients met one of the three stool collection criteria (
We isolated 262(24%)
The overall crude incidence rate of shigellosis was 287/100,000 PYO (
Most
Patients with dysentery were more likely to have
| Bivariate analysis | Multivariate analysis | |||||
| Characteristic | N | Shigella positive (%) | OR | CI | OR | CI |
| Age category | ||||||
| <12 m | 72 | 2 (3) | Ref | |||
| 12–23 m | 101 | 7 (7) | 2.13 | 0.52–12.93 | 2.36 | 0.47–11.85 |
| 24–59 m | 216 | 34 (16) | 4.85 | 1.53–27.94 | 5.47 | 1.26–23.68 |
| 5–9 y | 117 | 20 (17) | 5.47 | 1.63–31.88 | 6.10 | 1.36–27.38 |
| 10–17 y | 122 | 29 (24) | 8.16 | 2.52–47.28 | 9.34 | 2.12–41.14 |
| 18–34 y | 297 | 115 (39) | 16.08 | 5.32–91.94 | 17.51 | 4.15–73.89 |
| 35–49 y | 136 | 49 (36) | 14.57 | 4.63–83.91 | 15.84 | 3.66–68.55 |
| 50 y+ | 35 | 6 (17) | 6.12 | 1.38–38.00 | 6.64 | 1.24–35.70 |
| Sex | ||||||
| Male | 526 | 105 (20) | Ref | Ref | ||
| Female | 570 | 157 (28) | 1.52 | 1.15–2.02 | 1.47 | 1.68–2.00 |
| Vomiting | ||||||
| No | 532 | 126 (24) | Ref | |||
| Yes | 168 | 24 (14) | 0.54 | 0.33–0.86 | — | — |
| Reported fever | ||||||
| No | 406 | 87 (21) | Ref | |||
| Yes | 311 | 65 (21) | 0.97 | 0.67–1.39 | — | — |
| Duration of diarrhea | ||||||
| Less than 3 days | 594 | 156 (26) | Ref | |||
| 3–5 days | 398 | 86 (22) | 0.77 | 0.58–1.05 | — | — |
| 6–9 days | 69 | 11 (16) | 0.53 | 0.27–1.04 | — | — |
| 10 days and more | 22 | 4 (18) | 0.62 | 0.21–1.87 | — | — |
| Belly pain | ||||||
| No | 132 | 36 (27) | Ref | |||
| Yes | 542 | 175 (32) | 1.27 | 0.83–1.94 | — | — |
| Headache | ||||||
| No | 265 | 79 (30) | Ref | |||
| Yes | 154 | 43 (28) | 0.91 | 0.59–1.42 | — | — |
| Muscle pain | ||||||
| No | 378 | 104 (28) | Ref | |||
| Yes | 35 | 13 (37) | 1.56 | 0.76–3.20 | — | — |
| Case presentation | ||||||
| Complicated diarrhea with dehydration | 61 | 3 (5) | Ref | Ref | ||
| Uncomplicated diarrhea | 543 | 83 (15) | 3.49 | 1.07–11.39 | 1.73 | 0.51–5.85 |
| Dysentery | 492 | 176 (36) | 10.77 | 3.33–34.87 | 5.32 | 1.59–17.86 |
| HIV status | ||||||
| Negative | 313 | 105 (34) | Ref | |||
| Positive | 100 | 33 (33) | 0.98 | 0.60–1.57 | — | — |
Significant variables on bivariate analysis included into multivariate model
Significant characteristics on bivariate analysis but not significant on multivariate model hence excluded from final multivariate model
One patient was hospitalized within 2 days of being seen at the clinic while one patient died within 3 weeks after being diagnosed with shigellosis at the clinic.
Over 80% of
| Antibiotic class | Antibiotic tested | Number of |
| Penicillins | Ampicillin | 147 (67) |
| Amoxicillin/clavulanic acid | 69 (35) | |
| Cephalosporin | Ceftriaxzone | 3 (1) |
| Quinolone | Nalidixic acid | 7 (3) |
| Fluoroquinolone | Ciprofloxacin | 2 (1) |
| Chloramphenicol | Chloramphenicol | 91 (41) |
| Aminoglycosides | Gentamycin | 5 (2) |
| Streptomycin | 192 (86) | |
| Sulfonamide | Sulfisoxazole | 212 (96) |
| Sulphonamide and trimethoprime | Trimethoprim-sulfamethoxazole | 212 (95) |
| Tetracycline | Tetracycline | 184 (83) |
low denominator due to stock out of Amoxicillin/clavulanic acid disks
`40 isolates did not have drug susceptibility tests done as antibiotics were not available when they were being tested
Our study revealed a high burden of shigellosis within a densely populated urban slum in Kenya. The high crude incidence of shigellosis of 0.29% was slightly higher than that reported in a multicenter population-based study done in six developing countries in Asia; three of the sites were rural/semi rural (in China, Thailand, and Vietnam) and three of the sites were in urban slums (in Bangladesh, Indonesia, and Pakistan), where the overall unadjusted incidence of
In our study, over 20% of all stool samples yielded
As expected, patients presenting with dysentery were more likely to have
Females in the 35–49 year age group had a higher incidence of shigellosis, than males in the same age group. It is not clear why women in this age group were at increased risk of being infected with
Our adjusted rates suggest that over 0.4% of people living in urban slum settings are stricken with shigellosis annually. Like other developing countries, Kenya is experiencing rapid urbanization (>3%/year) and migrants from rural to urban areas tend to settle in slums
As in other developing countries
Many of the
While this study was unique in terms of its active surveillance for shigellosis and for providing reliable basis for rate adjustments, limitations may have led to underestimates or overestimates of the burden of disease. Because of transport requirements to the Kisumu laboratory, some stool specimens were processed >24 hours after collection. Cary-Blair solution preserves viability of
In calculating, adjusted incidence rates, we assumed that persons with diarrhea who reported visiting any clinic had similar shigellosis incidence rates as those seen in the study field clinic. This assumption could be erroneous if there was a systematic bias in which persons with shigellosis tended to go to the designated study clinic at different rates than persons with other causes of diarrhea or dysentery. We believe that use of non-study field clinics occurred primarily because the study clinic was open only Monday-through-Friday during daylight hours; thus, we do not think that there would be intrinsic biases in the way we adjusted the incidence rates. We did not adjust the incidence rates based on the proportion of patients who met the case definition and did not provide a stool specimen. This is because a relatively small proportion of patients meeting our diarrhea case definitions provided stool specimen, which would have made further adjustments imprecise, potentially exaggerating the adjusted incidence rates. On the other hand, opting not to make this adjustment likely led to underestimation of incidence rates. In addition, patients with dysentery were more likely to provide a stool sample for culture and sensitivity studies compared to patients presenting with non-bloody diarrhea. This led to a higher adjustment factor among patients with diarrhea (without dysentery), which may over estimate the burden of shigellosis in this category of patients.
Drinking water, sanitation, and hygiene improvements within the rapidly multiplying and expanding informal settlements in Kenya, and elsewhere in Africa, are needed to reduce the risk of shigellosis and other enteric infections. Health education, including a focus on hand washing with soap, provision of safe drinking water and proper waste disposal are feasible strategies for containing the burden of shigellosis
We thank Lilian Atieno and George Awiti for processing and running laboratory tests, Kariuki Njenga for leading the lab team, Michele Parsons and Cheryl Bopp from CDC Atlanta who provided technical assistance to the laboratory, Maurice Ombok for providing rainfall data, Mark Katz, Brett Archer and George Rutherford for helpful assistance in manuscript preparation.