Associations between Household-Level Exposures and All-Cause Diarrhea and Pathogen-Specific Enteric Infections in Children Enrolled in Five Sentinel Surveillance Studies
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Population
2.2. Outcome Variable
2.3. Covariates
- Drinking water: whether or not the subject resided in a household with access to an improved drinking water source (with potential to deliver safe water by nature of its design and construction such as piped water or protected tubewells, boreholes, dug wells, or springs) [34].
- Sanitation: whether or not the subject resided in a household with access to an improved, non-shared sanitation facility (“improved” meaning designed to hygienically separate excreta from human contact) [34].
- Flooring material: whether or not the subject resided in a household that had a covered (“improved”—rudimentary or finished) as opposed to natural (“unimproved”—earth or sand) floor [35].
- Caregiver education: a binary variable indicating whether or not the subject’s caregiver had completed primary education (≥6 completed years of schooling [25]).
- Household crowding: a binary variable indicating whether or not the subject resided in a household with 3 or more residents per bedroom [22].
- Site: a categorical variable indicating at which of the 22 study sites the subject was enrolled, included to adjust both for between-site differences in background pathogen transmission levels and for potential confounding engendered by differences in surveillance methods between the 5 studies.
- Sample type: whether the stool sample was collected during a diarrheal episode (cases of diarrhea in GEMS and RECODISA, diarrheal collections in MAL-ED, Novel Biomarkers and SHINE) or while the subject was asymptomatic (controls in GEMS and RECODISA, surveillance samples in MAL-ED, Novel Biomarkers and SHINE).
- Age: the subjects’ age in continuous months at the time of stool sample collection, modeled using linear, quadratic, and cubic terms to account for non-linearity of association with enteric pathogen presence.
- Feeding status: a categorical variable indicating whether the child was being exclusively breastfed, partially breastfed or had been fully weaned (no longer receiving any breastmilk) at the time of sample collection.
- Nutritional status: two binary variables indicating whether or not the child was moderately or severely stunted or underweight (respectively, a length-for-age and weight-for-age Z-score of ≤−2.0) to adjust for both the impact of nutritional status on susceptibility to infections [36] and potential unobserved confounding by socio-economic status.
2.4. Statistical Methods
3. Results
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
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Adenovirus 40/41 | Astrovirus | Norovirus | Rotavirus | Sapovirus | Aeromonas spp. | Campylo-bacter spp. | EAEC | |
---|---|---|---|---|---|---|---|---|
Bamako, Mali | 460 (26.3) | 136 (7.7) | 351 (19.9) | 216 (12.3) | 238 (13.5) | 41 (2.3) | 899 (50.8) | 1151 (65.1) |
Basse, The Gambia | 373 (25.4) | 98 (6.4) | 250 (16.3) | 227 (14.8) | 201 (13.1) | 19 (1.3) | 787 (52.2) | 873 (58.7) |
Bhaktapur, Nepal | 348 (5.9) | 301 (5.1) | 714 (12.0) | 249 (4.2) | 651 (11.1) | 149 (2.5) | 1256 (22.3) | 2690 (47.0) |
Cajazeiras, Brazil | 1 (0.5) | 9 (4.5) | 8 (4.0) | 12 (6.0) | 9 (4.5) | 6 (3.0) | 6 (3.0) | 68 (34.0) |
Crato, Brazil | 5 (2.5) | 4 (2.0) | 2 (1.0) | 46 (23.0) | 6 (3.0) | 12 (6.0) | 26 (13.0) | 83 (41.5) |
Dhaka, Bangladesh | 1306 (23.5) | 1142 (20.3) | 1086 (19.0) | 578 (10.2) | 1054 (18.8) | 162 (2.8) | 1730 (33.8) | 2245 (41.1) |
Fortaleza, Brazil | 137 (4.7) | 52 (1.8) | 187 (6.4) | 40 (1.5) | 132 (4.5) | 40 (1.4) | 401 (13.8) | 883 (30.1) |
Haydom, Tanzania | 365 (8.3) | 282 (6.4) | 735 (16.6) | 227 (5.2) | 482 (11.0) | 131 (3.0) | 1818 (45.9) | 2843 (65.1) |
Karachi, Pakistan | 366 (22.4) | 191 (11.6) | 393 (23.8) | 161 (9.8) | 306 (18.5) | 122 (7.5) | 1023 (62.9) | 1132 (68.9) |
Kolkota, India | 734 (41.5) | 101 (5.8) | 316 (18.0) | 321 (18.3) | 201 (11.4) | 193 (10.9) | 824 (46.6) | 1028 (58.1) |
Loreto, Peru | 1380 (21.0) | 1049 (15.7) | 1230 (18.0) | 261 (4.0) | 975 (14.9) | 177 (2.6) | 1293 (20.3) | 3174 (55.6) |
Manhiça, Mozambique | 377 (36.3) | 41 (4.0) | 151 (14.7) | 202 (19.7) | 120 (11.7) | 50 (4.8) | 462 (44.5) | 817 (78.7) |
Midlands, Zimbabwe | 198 (8.3) | 66 (2.8) | 277 (11.7) | 122 (5.1) | 155 (6.5) | 36 (1.5) | 602 (25.5) | 1361 (57.6) |
Mirzapur, Bangladesh | 443 (24.7) | 89 (5.0) | 243 (13.6) | 392 (21.9) | 183 (10.2) | 59 (3.3) | 434 (24.2) | 992 (55.3) |
N. Feroze, Pakistan | 823 (12.8) | 930 (14.6) | 1388 (21.4) | 274 (4.2) | 1063 (16.6) | 35 (0.5) | 1667 (27.0) | 2288 (36.5) |
Nyanza, Kenya | 165 (9.1) | 61 (3.4) | 250 (13.9) | 160 (9.0) | 179 (10.0) | 109 (6.0) | 662 (36.5) | 952 (53.1) |
Ouricuri, Brazil | 7 (3.5) | 9 (4.5) | 12 (6.0) | 5 (2.5) | 6 (3.0) | 11 (5.5) | 17 (8.5) | 52 (26.1) |
Patos, Brazil | 6 (3.0) | 0 (0.0) | 4 (2.0) | 6 (3.0) | 1 (0.5) | 3 (1.5) | 10 (5.0) | 194 (97.0) |
Picos, Brazil | 3 (1.8) | 0 (0.0) | 0 (0.0) | 14 (8.5) | 8 (4.9) | 2 (1.0) | 15 (7.5) | 92 (46.0) |
Souza, Brazil | 2 (1.0) | 0 (0.0) | 10 (5.1) | 3 (1.5) | 5 (2.5) | 2 (1.1) | 12 (6.3) | 161 (83.9) |
Vellore, India | 921 (17.1) | 622 (11.6) | 822 (15.2) | 434 (8.1) | 789 (14.7) | 275 (5.1) | 1144 (22.0) | 3283 (62.5) |
Venda, South Africa | 503 (10.7) | 332 (7.1) | 529 (11.2) | 92 (2.1) | 517 (11.0) | 24 (0.5) | 535 (11.4) | 1698 (36.0) |
Total positive | 8923 (15.7) | 5515 (9.7) | 8958 (15.6) | 4042 (7.2) | 7281 (12.8) | 1658 (2.9) | 15,623 (28.4) | 28,060 (50.8) |
Total stools | 56,704 | 56,828 | 57,350 | 56,168 | 56,668 | 57,185 | 54,923 | 55,280 |
Atypical EPEC | Typical EPEC | LT-ETEC | ST-ETEC | Salmonella spp. | Shigella spp./EIEC | Crypto-sporidium spp. | Giardia spp. | |
Bamako, Mali | 382 (21.6) | 588 (33.2) | 511 (29.0) | 319 (18.1) | 52 (2.9) | 567 (32.1) | 522 (29.5) | 1233 (70.8) |
Basse, The Gambia | 330 (22.0) | 461 (30.8) | 370 (24.8) | 289 (19.3) | 82 (5.5) | 480 (32.7) | 279 (18.5) | 630 (42.4) |
Bhaktapur, Nepal | 1673 (28.5) | 403 (6.8) | 575 (9.7) | 620 (10.5) | 55 (0.9) | 376 (6.3) | 272 (4.6) | 545 (10.3) |
Cajazeiras, Brazil | 34 (17.0) | 3 (1.5) | 7 (3.5) | 0 (0.0) | 7 (3.5) | 10 (5.1) | 24 (12.1) | 66 (33.3) |
Crato, Brazil | 66 (33.0) | 13 (6.5) | 33 (16.5) | 0 (0.0) | 78 (39.0) | 76 (38.0) | 13 (6.5) | 55 (27.5) |
Dhaka, Bangladesh | 1328 (23.6) | 1075 (19.1) | 849 (15.0) | 1799 (32.6) | 57 (1.0) | 865 (15.4) | 380 (6.8) | 661 (12.8) |
Fortaleza, Brazil | 764 (25.9) | 100 (3.4) | 129 (4.4) | 73 (2.5) | 27 (0.9) | 158 (5.4) | 37 (1.3) | 266 (9.7) |
Haydom, Tanzania | 1266 (28.6) | 821 (18.6) | 1141 (26.1) | 1242 (28.3) | 19 (0.4) | 790 (17.9) | 514 (12.0) | 931 (27.3) |
Karachi, Pakistan | 358 (21.8) | 545 (33.2) | 404 (24.7) | 356 (21.8) | 22 (1.3) | 543 (32.9) | 383 (23.4) | 931 (57.0) |
Kolkota, India | 519 (29.4) | 367 (20.8) | 392 (22.2) | 293 (16.6) | 23 (1.3) | 533 (30.1) | 275 (15.6) | 1076 (62.2) |
Loreto, Peru | 1548 (24.1) | 807 (12.1) | 1137 (17.2) | 763 (11.4) | 85 (1.3) | 786 (11.8) | 633 (9.6) | 1415 (26.1) |
Manhiça, Mozambique | 279 (26.9) | 318 (30.7) | 280 (27.0) | 329 (31.7) | 41 (4.0) | 328 (31.6) | 323 (31.2) | 726 (70.9) |
Midlands, Zimbabwe | 608 (25.7) | 219 (9.2) | 464 (19.6) | 231 (9.7) | 42 (1.8) | 93 (3.9) | 210 (8.9) | 348 (15.1) |
Mirzapur, Bangladesh | 430 (24.0) | 209 (11.6) | 337 (18.8) | 95 (5.3) | 22 (1.2) | 648 (36.1) | 80 (4.5) | 377 (21.1) |
N. Feroze, Pakistan | 869 (13.4) | 683 (10.6) | 578 (8.9) | 605 (9.4) | 4 (0.1) | 445 (6.9) | 402 (6.3) | 1585 (34.4) |
Nyanza, Kenya | 453 (25.0) | 440 (24.3) | 555 (31.0) | 278 (15.3) | 39 (2.1) | 421 (23.2) | 336 (18.5) | 735 (40.8) |
Ouricuri, Brazil | 27 (13.6) | 1 (0.5) | 6 (3.0) | 0 (0.0) | 28 (14.0) | 22 (11.0) | 1 (0.5) | 22 (11.0) |
Patos, Brazil | 76 (38.0) | 4 (2.0) | 17 (8.5) | 7 (3.5) | 13 (6.5) | 8 (4.0) | 10 (5.0) | 21 (10.6) |
Picos, Brazil | 21 (10.5) | 5 (2.5) | 5 (2.5) | 0 (0.0) | 26 (13.0) | 21 (10.5) | 11 (5.5) | 58 (29.0) |
Souza, Brazil | 86 (44.8) | 3 (1.6) | 12 (6.3) | 5 (2.6) | 17 (8.9) | 10 (5.3) | 17 (8.9) | 30 (15.8) |
Vellore, India | 1440 (26.7) | 870 (16.2) | 877 (16.4) | 717 (13.4) | 67 (1.2) | 701 (13.0) | 278 (5.2) | 1039 (23.2) |
Venda, South Africa | 945 (20.1) | 212 (4.5) | 346 (7.4) | 194 (4.2) | 14 (0.3) | 337 (7.2) | 226 (4.9) | 704 (16.2) |
Total positive | 13,502 (23.8) | 8147 (14.3) | 9025 (15.9) | 8215 (14.5) | 820 (1.4) | 8218 (14.4) | 5226 (9.3) | 13,454 (26.8) |
Total stools | 56,713 | 56,943 | 56,832 | 56,842 | 57,154 | 56,930 | 56,485 | 50,177 |
Improved Water Source | Improved Sanitation | Improved Flooring | Caregiver Education | Household Crowding | Total Subjects | |
---|---|---|---|---|---|---|
Bamako, Mali | 5872 (87.5) | 127 (1.9) | 5253 (98.5) | 1242 (31.4) | 3119 (58.5) | 6711 |
Basse, The Gambia | 4087 (86.3) | 82 (1.7) | 2837 (85.0) | 1029 (42.4) | 2987 (89.5) | 4738 |
Bhaktapur, Nepal | 232 (98.3) | 131 (55.5) | 104 (44.1) | 152 (64.4) | 47 (19.9) | 240 |
Cajazeiras, Brazil | 172 (86.0) | 197 (98.5) | 198 (99.0) | 137 (68.5) | - | 200 |
Crato, Brazil | 189 (94.5) | 181 (90.5) | 170 (87.2) | 169 (84.9) | - | 200 |
Dhaka, Bangladesh | 242 (100.0) | 28 (11.6) | 226 (93.4) | 57 (23.6) | 3 (1.2) | 265 |
Fortaleza, Brazil | 142 (67.6) | 201 (95.7) | 208 (99.0) | 146 (69.5) | 6 (2.9) | 233 |
Haydom, Tanzania | 79 (31.6) | 0 (0.0) | 17 (6.8) | 6 (2.4) | 23 (9.2) | 262 |
Karachi, Pakistan | 3274 (62.6) | 2428 (46.4) | 2881 (75.6) | 1120 (37.8) | 443 (11.6) | 5231 |
Kolkata, India | 5147 (98.7) | 635 (12.2) | 3877 (95.9) | 1880 (64.2) | 160 (4.0) | 5214 |
Loreto, Peru | 309 (89.6) | 70 (20.3) | 98 (28.4) | 192 (56.3) | 45 (13.0) | 378 |
Manhiça, Mozambique | 2745 (85.1) | 219 (6.8) | 1691 (70.1) | 454 (24.7) | 417 (17.4) | 3227 |
Midlands, Zimbabwe | 611 (61.8) | 619 (61.2) | 547 (55.2) | 844 (82.6) | - | 1046 |
Mirzapur, Bangladesh | 5907 (99.8) | 2830 (47.8) | 887 (20.8) | 2662 (75.3) | 769 (18.0) | 5916 |
Naushahro Feroze, Pakistan | 265 (100.0) | 9 (3.4) | 74 (27.9) | 41 (15.5) | 55 (20.8) | 277 |
Nyanza, Kenya | 2549 (64.5) | 169 (4.3) | 659 (19.5) | 1630 (52.9) | 34 (1.0) | 3951 |
Ouricuri, Brazil | 193 (96.5) | 195 (97.5) | 195 (98.0) | 142 (71.0) | - | 200 |
Patos, Brazil | 199 (100.0) | 197 (98.5) | 198 (99.5) | 139 (70.6) | - | 200 |
Picos, Brazil | 198 (99.5) | 193 (96.5) | 192 (96.5) | 129 (64.5) | - | 200 |
Souza, Brazil | 200 (100.0) | 181 (90.5) | 198 (99.0) | 125 (62.5) | - | 200 |
Vellore, India | 235 (100.0) | 12 (5.1) | 220 (93.6) | 123 (52.3) | 1 (0.4) | 251 |
Venda, South Africa | 216 (85.4) | 3 (1.2) | 233 (92.1) | 207 (81.8) | 62 (24.5) | 314 |
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Colston, J.M.; Faruque, A.S.G.; Hossain, M.J.; Saha, D.; Kanungo, S.; Mandomando, I.; Nisar, M.I.; Zaidi, A.K.M.; Omore, R.; Breiman, R.F.; et al. Associations between Household-Level Exposures and All-Cause Diarrhea and Pathogen-Specific Enteric Infections in Children Enrolled in Five Sentinel Surveillance Studies. Int. J. Environ. Res. Public Health 2020, 17, 8078. https://doi.org/10.3390/ijerph17218078
Colston JM, Faruque ASG, Hossain MJ, Saha D, Kanungo S, Mandomando I, Nisar MI, Zaidi AKM, Omore R, Breiman RF, et al. Associations between Household-Level Exposures and All-Cause Diarrhea and Pathogen-Specific Enteric Infections in Children Enrolled in Five Sentinel Surveillance Studies. International Journal of Environmental Research and Public Health. 2020; 17(21):8078. https://doi.org/10.3390/ijerph17218078
Chicago/Turabian StyleColston, Josh M., Abu S. G. Faruque, M. Jahangir Hossain, Debasish Saha, Suman Kanungo, Inácio Mandomando, M. Imran Nisar, Anita K. M. Zaidi, Richard Omore, Robert F. Breiman, and et al. 2020. "Associations between Household-Level Exposures and All-Cause Diarrhea and Pathogen-Specific Enteric Infections in Children Enrolled in Five Sentinel Surveillance Studies" International Journal of Environmental Research and Public Health 17, no. 21: 8078. https://doi.org/10.3390/ijerph17218078