Objective
The objective of the study was to examine the relationship between breastfeeding patterns, markers of maternal human immunodeficiency virus (HIV) disease, and woman’s breast pathology.
Study Design
Secondary data analysis from a randomized breastfeeding trial including 947 HIV-infected women (n = 5982 visits) from breastfeeding initiation until 6 months postpartum; 1 month after breastfeeding cessation; or loss to follow-up or death. Generalized estimating equations assessed the effects of breastfeeding pattern and maternal HIV status on breast pathology.
Results
One hundred ninety women (20.1%) had a breast problem; 86 (9.1%) had mastitis; and 31 (3.3%) had abscess. After confounder adjustment, nonexclusively breastfeeding women had an increased risk of breast problems (odds ratio, 1.98; 95% confidence interval, 1.33–2.95) and mastitis (odds ratio, 2.87, 95% confidence interval, 1.69–4.88) compared with exclusive breastfeeders. Women with a CD4 count less than 200 cells/μL tended to have an increased risk of abscess.
Conclusion
Nonexclusive breastfeeding significantly increased the risk of breast pathology. Exclusive breastfeeding is not only optimal for infant health but it also benefits mothers by reducing breast problems.
Breastfeeding is essential for the survival of children born to human immunodeficiency virus (HIV)-infected mothers in low-resource settings, and the efficacy of antiretroviral drugs in reducing HIV breast milk transmission allows women to protect their infants from both HIV and other infectious diseases that threaten their infants’ lives. Nevertheless, postnatal HIV transmission continues to occur, and improving the safety of breastfeeding for HIV-infected women and their children remains important.
In several studies, postnatal HIV transmission increased in the presence of breast lesions, mastitis, and abscess, although exclusive breastfeeding reduced the risk of HIV transmission. Globally, 10-33% of women experience mastitis, typically occurring in the early days of breastfeeding.
Mastitis and breast pathology are also reasons women cite for early cessation of breastfeeding. In HIV-uninfected populations, milk stasis, because of mixed feeding or rapid weaning, is the predominant cause of mastitis, whereas bacterial infections are relatively infrequent. Other risk factors for mastitis include nipple fissures, prior history of mastitis, use of nipple creams, stress, and fatigue.
Physiologically, mastitis and abscess alter the cellular tight junctions that regulate breast epithelial permeability, resulting in increased sodium and chloride levels in breast milk. These changes have been associated with increases in breast milk HIV and an increased risk of transmission and maternal morbidity, highlighting the need for appropriate interventions.
Little is known about the predictors of breast problems, especially mastitis and abscess, in HIV-infected women. As HIV disease progresses, the risk of opportunistic infections also increases. Theoretically, a weakened immune system could increase the risk of mastitis because of bacterial infections, although reports in the literature are conflicting.
Most studies to date have focused on biochemically defined subclinical mastitis or elevations in breast milk sodium or sodium/potassium ratio. Two studies from sub-Saharan Africa identified HIV infection as a risk factor for subclinical mastitis, but markers of the severity as a function of HIV disease stage were not examined. A microbiological study of subclinical mastitis in HIV-infected women did not find a relationship between HIV plasma viral load and the sodium/potassium ratio. Thus, few data exist identifying either the specific HIV-associated factors or the variations in infant feeding that increase the risk of breast problems, mastitis, and abscess in HIV-infected women. Consequently, we hypothesized that both nonexclusive breastfeeding and advanced HIV disease would be associated with a higher risk of mastitis and abscess.
Materials and Methods
Population and study sample
This analysis includes all randomized mothers (n = 958) enrolled in the Zambia Exclusive Breastfeeding Study (ZEBS), as described previously. Briefly, ZEBS was a randomized trial designed to assess the impact on HIV-free child survival of exclusive breastfeeding for 4 months with abrupt weaning vs exclusive breastfeeding through 6 months with the normal weaning and full duration of breastfeeding based on the mother’s choice. In this analysis, we analyzed breastfeeding behavior, not randomization assignment, on the risk of breast problems. In an unpublished analysis, randomization assignment did not have an impact on the risk of breast problems (data not shown).
Maternal single-dose nevirapine followed by infant dose was given per Zambian guidelines to prevent perinatal HIV transmission. Highly active antiretroviral therapy became available only near the time of study completion. Women and their infants were seen weekly for the first month postpartum, twice a month through 6 months postpartum and every 3 months until 24 months postpartum. The study received ethical approval from all investigators’ institutions; all participants provided written informed consent.
In the cohort of 958 randomized women, 4 women initiated highly active antiretroviral therapy (HAART) during pregnancy and 7 were missing data on infant feeding patterns. Therefore, the analysis was limited to 947 women. Women are at risk for mastitis or abscess during the breastfeeding period and for 1 month beyond breastfeeding cessation; thus, we included women from breastfeeding initiation (delivery) through 6 months postpartum (n = 467) or until the mother-child pair: (1) completed a visit through 1 month after complete cessation of breastfeeding (n = 292), (2) was lost to follow-up (n = 113), (3) initiated HAART (n = 9), or (4) the mother or child died (n = 66). Data were censored at 6 months postpartum, the duration currently recommended for exclusive breastfeeding.
Assessment of exposures
Breastfeeding pattern
Women were categorized at each visit as 1 of the following: (1) exclusively breastfeeding; (2) mixed feeding; or (3) stopped breastfeeding. At each clinic visit, women were asked, “On how many days in the last week, did the baby consume …” and then each of the following items were asked: breast milk, plain water, nonmilk liquids, nonhuman milk, semisolids/solids, fermented milk/cereal, medicine, or anything else. Women’s responses were categorized into either “not given,” “given 1, 2, 3, 4, 5, 6, 7 (everyday),” or “do not know.” The previous week’s feeding report was used to create the breastfeeding classification for each clinic visit.
Exclusive breastfeeding (EBF) was defined as the provision of breast milk only with allowance of prescription medication. Provision of any other food/liquid, including water, along with breast milk identified the mother as mixed breastfeeding or non-EBF. Women who ceased breastfeeding and reported no provision of breast milk in the 1 week period prior to the visit were categorized as stopped breastfeeding.
To quantify the breastfeeding pattern, a variable defining breastfeeding pattern as full, high, low, or stopped was developed. Women who provided only breast milk (and prescribed medicines) were categorized as full breastfeeding. For non-EBF, the number of days per week when something other than breast milk was given to the child was calculated (minimum of 1 day and a maximum of 7 days per week of mixed feeding). Women who mixed fed 1-4 days in the previous week were defined as high breastfeeding; women who mixed fed 5-7 days in the previous week were defined as low breastfeeding. Finally, women who provided no breast milk were categorized as stopped breastfeeding.
Maternal HIV characteristics
Demographic and maternal health indicators were collected at enrollment. Maternal biological variables included: CD4 count (FacsCount; BD BioSciences, Franklin, NJ), HIV-1 ribonucleic acid (RNA) copies/mL (Amplicor HIV-1 monitor test, version 1.5; Roche, Indianapolis, IN), World Health Organization (WHO) clinical stage, hemoglobin (HemoCue System; HemoCue, Cypress, CA), and body mass index (BMI; kilograms per square meter). Women’s CD4 counts were grouped using standard cutoffs (<200 cells/μL, 200-350 cells/μL, >350 cells/μL). WHO stage III illness was defined as report of any of the following: weight loss in the last 6 months, fever or cough or diarrhea for more than 30 days in the past 6 months, or ever being diagnosed with tuberculosis or thrush. BMI was calculated at 1 month postpartum; women with a BMI less than 18.5 kg/m 2 were considered underweight.
Assessment of outcome
At each clinic visit, data were collected on the occurrence of a clinical breast problem. A standardized checklist guided the study nurse through a breast examination to assess the following: engorgement, red/shiny breast, swollen or sore nipples, cracked/bleeding nipples, blocked duct, white patches/ Candida , abscess, and other problems with the breast/areola/nipple. Women were asked whether they had any problems since the last visit and whether their breasts were currently painful.
Three outcomes were utilized in this analysis: (1) breast complication, (2) mastitis, and (3) abscess. A breast complication was defined as the presence of any of the following: engorgement, red/shiny breast, sore/swollen nipples, blocked duct, cracked/bleeding nipples, white patches/ Candida , or current pain. Mastitis was defined as the presence of engorgement, red/shiny breasts, blocked duct(s), painful breasts, and reported or current fever (38°C or higher). Abscess was specifically assessed by breast palpation at each clinic visit; current or reported fever was not required ( Table 1 ).
| Characteristic | Cohort (n = 947) |
|---|---|
| Maternal demographic characteristics | |
| Mean maternal age, y (SD) | 26.1 (5.1) |
| Married, n (%) | 804 (84.9) |
| Electricity in home, n (%) | 380 (40.1) |
| Maternal education, primary or none, n (%) | 537 (56.7) |
| Full-time employment, n (%) | 70 (7.4) |
| Part-time employment, n (%) | 16 (1.7) |
| Informal sector employment, n (%) | 229 (24.2) |
| Ran out of food more than 1 day in the last 30 days, n (%) | 218 (23.0) |
| BMI, kg/m 2 at 1 month postpartum, mean (SD), median (n = 842) | 21.7 (3.2); 21.4 |
| Parity, mean (SD), median | 2.4 (1.7) |
| History of mastitis in prior breastfeeding experience, n (%) | 103 (10.9) |
| Maternal HIV-specific characteristics | |
| Low CD4 count (<200 cells/μL), n (%) a | 222 (23.5) |
| Mean CD4 count (SD), median (IQR) a | 361 (202), |
| 330 (209–471) | |
| Mean plasma viral load, log 10 copies/mL (SD), median (IQR) a | 4.49 (0.81), |
| 4.59 (3.99–5.11) | |
| Mean hemoglobin, g/dL (SD), median (IQR) b | 10.6 (1.5), |
| 10.6 (9.8–11.5) | |
| WHO stage III or higher, n (%) | 368 (38.9) |
| Child characteristics | |
| Mean child birthweight, g (SD), median (IQR) (n = 926) | 3004 (485), |
| 3000 (2700–3300) | |
| Mean time to breastfeeding initiation, min (n = 895) (SD), median | 42 (75), 30 |
| Male sex in child, n (%) b | 488 (51.6%) |
All study subjects were offered comprehensive health care at the study facilities, minimizing the instances in which care was obtained outside the study. However, standardized questionnaires were not utilized for the sick visits. At the clinic visits, fever was treated as present with maternal temperature recorded at 38°C or higher.
Statistical analysis
For each visit to 6 months, the point prevalence of each breast problem was calculated. Variables analyzed with χ 2 tests, Student t tests, or Kruskal-Wallis tests, as appropriate. Associations between each breast problem and the covariates of interest were investigated using generalized estimating equations, using an unstructured correlation matrix, for bivariate and multivariate logistic regression analysis.
Breastfeeding pattern was first analyzed as a 3 way categorical variable (exclusive vs mixed vs stopped); mixed feeding was then further divided into high (1-4 d/wk mixed feeding) or low (5-7 d/wk mixed feeding) breastfeeding.
Potential confounders included maternal age, parity, gravida, history of mastitis in previous breastfeeding experience, and maternal nutritional status. Using forward selection, confounders that made a 10% difference in the odds ratios were retained in the final models. Maternal health indicators were included in all models. Analyses were completed in SAS version 9.1.3 (SAS Institute, Inc, Cary, NC).
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