Relationship between Trachoma and Chronic and Acute Malnutrition in Children in Rural Ethiopia
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Relationship between Trachoma and Chronic and Acute Malnutrition in Children in Rural Ethiopia by Andrew G. Smith,a Aimee T. Broman,b Wondu Alemayehu,c Beatriz E. Munoz,b Sheila K. West,b and Emily W. Gowerb a Department of Pediatrics, School of Medicine, University of Utah, Salt Lake City, UT b Dana Center for Preventive Ophthalmology, Johns Hopkins University School of Medicine, Baltimore, Maryland, and c ORBIS International, Addis Ababa, Ethiopia Downloaded from http://tropej.oxfordjournals.org at Johns Hopkins University on June 1, 2010 Summary Trachoma is the leading infectious cause of blindness in the world. Areas where it is most prevalent also have some of the highest rates of childhood malnutrition. We examined the relationship between both acute and chronic malnutrition and clinical trachoma. We also explored whether malnutrition alters the clinical manifestations of the disease. Children with chronic malnutrition, but not acute malnutrition, were more likely to have clinical trachoma. Stunted children are 1.96 times more likely to have clinical trachoma than nonstunted children (95% CI: 1.12–3.43), even after controlling for age, gender and infection status of other household members. Host factors including malnutrition may play a role in determining disease manifestations. Introduction the question becomes relevant if there is any relation- Anthropomorphic measures have been used as ship between nutrition and trachoma. markers of malnutrition in numerous studies char- Our literature review found two studies examining acterizing the relationship between nutrition and this question. Both studies focused specifically on infection with malnutrition being a risk factor for acute malnutrition; neither reported acute malnutri- morbidity and mortality in common childhood tion as a risk factor for developing trachoma. Using illnesses like diarrhea and acute respiratory infections 80% of the norm for weight-to-height as a marker, [1–3]. Regions struggling with malnutrition often Resnikoff and Cornand [4] found no relationship between severe clinical trachoma and nutrition when tend to be the same areas where trachoma is a public controlling for age and refugee status. Fine and West health problem. [10] found similar results when comparing mid-upper Trachoma is a chronic infectious eye disease arm circumference (MUAC) with clinical trachoma caused by Chlamydia trachomatis. Typically in status. Neither study examined the relationship trachoma endemic areas infection and clinical signs between trachoma and indices of chronic malnutri- of active trachoma occur in young children; these tion, nor did they examine the interaction between clinical signs on the upper tarsal plate include ocular chlamydial infection and nutritional status. presence of follicles on the conjunctiva (TF) and The aim of this study was to further investigate the inflammation which obscures 50% of the tarsal relationship between malnutrition, infection with vessels (TI). Repeated infection can lead to scarring C. trachomatis, and clinical presentation of tra- of the tarsal plate and ultimately in later life to the choma. Specifically, we examined whether children potentially blinding complication of trichiasis where with signs of chronic or acute malnutrition were eyelashes turned inwards cause corneal abrasion. more or less likely to have clinical signs of trachoma Trachoma is the leading infectious cause of blindness and/or infection with C. trachomatis. Additionally, worldwide [4]. Multiple factors are associated with we investigated whether clinical manifestations of the epidemiology of trachoma, including access to disease (TF or TI) differed among children with signs water, hygiene behaviors, presence of latrines and of malnutrition. markers of socioeconomic status [5–9]. Such factors also are associated with nutrition in children; thus, Material and Methods This study was nested within the Surgery for Trichiasis, Antibiotics to prevent Recurrence Correspondence: Emily W. Gower, PhD, 600 N. Wolfe (STAR) clinical trial conducted in the Wolayta Street, 116 Wilmer Building, Baltimore, MD 21287, USA. district of Ethiopia [11]. In the STAR trial, trichiasis E-mail: . patients who presented for corrective surgery were ß The Author [2007]. Published by Oxford University Press. All rights reserved. For Permissions, please email: journals.permissions@oxfordjournals.org 308 doi:10.1093/tropej/fmm039
A. G. SMITH ET AL. randomized to one of three antibiotic treatment were noted for each eye. A swab of the upper regimens. conjunctiva of the right lid was collected from each One year following surgery, the household mem- subject, using standard field techniques to avoid bers of all participants were evaluated for trachoma contamination. Specimens were stored dry, on ice in and provided antibiotic treatment with oral azithro- the field, and then frozen at –20 C until shipped to mycin against infection with ocular C. trachomatis. Johns Hopkins University International Chlamydia Subjects for this substudy were those household Lab for processing. The Amplicor C. trachomatis members aged 6–59 months who resided in homes qualitative Polymerase Chain Reaction (PCR) assay where one family member was enrolled as a STAR was performed to identify eluted samples positive for trial participant and completing follow up between organism plasmid (Roche Molecular Systems, September and November 2004. Indianapolis, IN). Infection was defined as present The population of the Wolayta district is largely if the swab was positive. Downloaded from http://tropej.oxfordjournals.org at Johns Hopkins University on June 1, 2010 homogenous. Families’ primary source of income is We conducted bivariate analyses comparing infec- through subsistence farming. Most live in dirt dwell- tion status, any active trachoma (TF or TI) and ings where both animals and people sleep, and they severe trachoma (TI) vs. each anthropometric mea- often do not have ready access to water or basic sure. Logistic regressions were used to evaluate the latrines. association between each anthropomorphic measure Parents reported the age of their children in and the outcomes of interest, after adjusting for months, or years and months. When necessary, gender, age and infection status in other household seasons and holidays were used to aid in estimating members. Household infection status adjustment was age. A pediatrician (A.S.) collected anthropometric included since clustering of trachoma occurs within measurements. Infants were weighed in a hanging households, and we wanted to tease apart the scale precise to 0.1 kg increments. For children difference in this clustering vs. malnutrition. weighing >10 kg and able to stand on their own, Infection among household members was considered weight was measured on an electronic standing scale positive if at least one other member of the household precise to the nearest 0.2 kg or a mechanical standing had an ocular swab positive for C. trachomatis. scale with precision to 0.5 kg. Scales were calibrated each morning. A masked comparison of 50 subjects showed that the electronic scale trended 0.55 kg Results heavier than the mechanical. Sixty-one children Analyses included a total of 257 subjects aged were measured using the mechanical scale; their 59 months or younger, who resided with one of 185 weights were adjusted by 0.5 kg upwards to match surgical cases. Subjects were roughly evenly divided those children weighed using the electronic scale. The between genders. The majority (78%) of children was electronic scale was deemed more accurate based on between 36 and 59 months of age (Table 1). standardized weights measured on each scale. Height Clinical manifestations of trachoma were common was collected precise to 0.1 cm increments. Children among study children, with 75% having some form less than 2 years were measured in the supine of active disease (Table 2). Only one child was position. MUAC also was gathered using a cloth positive for ocular C. trachomatis among those tape to 0.1 cm precision. children without active trachoma, compared to Weight for height (WHZ), weight for age (WAZ), 59% positivity among children with TI. Overall, and height for age (HAZ) z-scores were calculated 33% of children were positive for C. trachomatis. using National Center for Health Statistics 2000 Data on anthropometric measures are shown in reference data [12]. MUAC for height (MHZ) Table 3. Study children were significantly smaller measurements were converted to z-scores using than reference populations with regard to all reference data previously reported by others [13]. measurements. Nearly half of all children were Different anthropometric measures represent stunted and underweight. Almost a quarter of varied aspects of malnutrition. Low WHZ (wasting children were wasted. when
A. G. SMITH ET AL. TABLE 1 TABLE 3 Characteristics of study population Mean z-score (SD) for each measure of malnutrition Characteristic N (%) Mean Percentage with Z-score(SD) Z-score
A. G. SMITH ET AL. TABLE 4 Mean z-scores according to nutritional status and trachoma status Clinical trachoma C. trachomatis infectiona No disease Active disease Difference 95% CI of None Present Difference 95% CI of (TF and/or TI) difference difference Chronic malnutrition markers Height/Age 1.34 2.22 0.88 [0.39, 1.38] 1.84 2.31 0.47 [0.0006, 0.95] Weight/Age 1.83 2.29 0.46 [0.05, 0.87] 2.19 2.16 0.03 [0.42, 0.36] Acute malnutrition markers Weight/Height 1.27 1.15 0.12 [0.52, 0.29] 1.30 0.97 0.33 [0.70, 0.05] MUAC/Height 1.35 1.38 0.03 [0.24, 0.31] 1.41 1.27 0.14 [0.40, 0.12] Downloaded from http://tropej.oxfordjournals.org at Johns Hopkins University on June 1, 2010 a Measured using Roche Amplicor PCR. TABLE 5 Adjusted associations between individual anthropomorphic measures and active trachoma (TF and/or TI) Chronic malnutrition Acute malnutrition Height/Age Weight/Age Weight/Height MUAC/Age OR 95% CI OR 95% CI OR 95% CI OR 95% CI Female 1.36 0.77–2.44 1.01 0.66–2.06 1.25 0.70–2.23 1.62 0.78–3.37 Age (months) 1.01 1.00–1.03 1.01 1.00–1.03 1.01 1.00–1.03 1.02 1.00–1.05 Any chlamydial infection 3.66 1.84–7.31 3.59 1.75–7.37 4.33 2.05–9.16 5.62 2.11–14.97 among household members Anthropomorphic measure 0.74 0.61–0.91 0.73 0.58–0.94 0.98 0.76–1.26 1.02 0.70–1.48 (e.g. Height/Age) results from the high rates of exposure to chlamydia immunological disruption may play a role in the in this hyper-endemic area. clinical presentation of trachoma, and ability to Regardless of nutritional status, children acquire convert a severe inflammatory response to a folli- infection. However, disease manifestation appears to cular presentation. Less is understood about the differ with chronic malnutrition. We found that effects of chronic vs. acute malnutrition. Other among children with active disease, children with studies, notably in malaria, have found higher rates markers of chronic malnutrition were more likely to of clinical disease in those with chronic malnutrition have TI than TF. This relationship was found among as compared to acute malnutrition [22, 23]. both the subgroups with and without infection. This Our study is cross–sectional; longitudinal data will relationship suggests that chronically malnourished be important to verify our suggestions that the children are more likely to manifest TI when they presentation as TI with infection and longer pre- have infection, and once infection is cleared, to sentation as TI following clearance of infection are continue to present with TI rather than either TF or more likely in chronically malnourished children. no signs. The study could have been strengthened by evenly A large majority of children (75%) in the current distributed age groups, with more children under the study had clinical trachoma. This finding is consis- age of 3, since stunting is most pronounced during tent with previous research which has shown that the first 3 years of life. Finally, our population is not trachoma is hyperendemic in many areas of Ethiopia a randomly selected sample of the community. All [16–18]. Anthropometric results presented here are children come from households where at least one similar to others conducted in Ethiopia with the member has already developed trichiasis. If there is a exception that we found a greater percentage of genetic component to trachoma, we may have wasting in children (20% vs. 9%) [19, 20]. selected children more likely to have a maladaptive The interaction between nutrition, infection and response to C. trachomatis. immunity is well documented. Both protein-energy This study points to the role of host factors in and micronutrient deficiencies play a role. Humoral clinical trachoma, but not necessarily in infection and cellular components of a host’s immune system acquisition where trachoma is hyper-endemic. are adversely affected by malnutrition [21]. Such Further research exploring the impact of chronic Journal of Tropical Pediatrics Vol. 53, No. 5 311
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