Duration of FH
Median (range) duration of FH documented by daily log use during the study was 9.6 weeks (range 1 day to 15.6 weeks); mean (SD) duration of FH during the study was 8.7 (5.3) weeks. Notably, at least 4 women reported FH beyond the period of study follow-up (3 months), 1 of whom continued to do so for an additional 9 months, until her infant was 18 months old. Thus, the reported mean duration of FH during the study is shorter than mean duration of actual use.
In 24-hour recalls, all mothers reported cleansing the utensils. During FH sessions observed by counselors, mothers washed their hands with soap and water 100% of the time. Utensils were washed 95% of the time, with soap and/or boiling water in 78.8% of episodes, and with only running water 16.2% of the time.
During FH observations, milk was expressed into the jar used for heating (as recommended) 21.5% of the time and into a cup or glass during all other episodes. Mean time for expression was 16.7 (7.5) minutes.
The median frequency of milk expression was 3 times daily: daily mean (SD) was 2.6 (0.8) based on log results and 3.3 (1.5) times based on 24-hour recall.
Median milk volume per episode was 120 mL based on daily logs and 24-hour recall and 100 mL during observation. According to recall data, median volumes were higher for fourth and fifth daily expressions (180 mL) than for the first through third expressions (100 mL), that is, women who expressed more frequently also expressed greater volumes. The linear association between total daily milk volume and number of expressions daily was statistically significant, P = 0.006 (Fig. 2). Median (range) total daily volumes were 300 (25–1120) mL from logs and 360 (10–1200) mL from recalls. When controlling for differences between individuals, there was no significant within-individual relationship between age of infant and daily milk volume expressed.
Heating and Feeding Expressed Milk
Mothers heated and fed milk as frequently as they expressed, suggesting milk was not combined from more than 1 expression for heating. Reported time lapse between expressing and heating milk ranged from 10 minutes to 7.5 hours (79% of intervals were measured; 21% estimated).
During FH sessions observed by counselors, kerosene was the most frequently used fuel (42.3%), followed by charcoal. In all but 2 observations, the water in the pan was at the proper level; the milk was removed from the pan before the water boiling in only 1 episode. Observed mean time required for heating was 12.0 (4.6) minutes, and mean peak milk temperature was 79.3 (4.4)°C (range: 68.0–88.8).
Although most often mothers fed the heated milk to the infant immediately (71.6% of reports), heated milk was stored in the jar used for heating (9.9%), a cup (12.3%), or bottle (1.2%) anywhere from 5 minutes to 7.7 hours. Stored milk was reported to be covered 78.6% of the time. Mother reported reusing the water 95% of the time, most often for cooking (50.0%) or bathing (40.8%).
During observed FH sessions, infants were fed the milk with a cup in all cases except once each using a spoon and bottle; water was added to the milk in 3.8% of observations, always after heating the milk.
Bacterial cultures were performed on 105 preheated and postheated samples from 61 mothers. Of the 105 samples collected before heating, 44 (41.9%) samples had bacterial growth with a median colony-forming units (CFU)/mL of 2.4 × 103 (range 80- too many too count). All but 1 of the contaminated samples were positive for coliforms; median coliform count was 2.0 × 103 CFU/mL (range 50- too many too count). Thirty-two samples (30.5%) contained pathogens. Twenty-six samples (24.8%) were positive for S. aureus [median concentration 3.0 × 103 (range: 90–7.8 × 103)]; additional pathogens isolated included Escherichia coli and Klebsiella and Bacillus species. One sample was negative before heating and positive for Staphylococcus epidermedis and coliforms after heating, (total colony count 3.4 × 103 CFU/mL). All other 104 heated samples yielded negative bacterial cultures. Of the 44 mothers who provided more than 1 sample, 3 mothers' samples were contaminated on multiple occasions.
To evaluate the risk for staphylococcal food poisoning if unheated samples were stored before heating, the growth rate of S. aureus was calculated over 6 hours at 37°C. Mean (SD) log CFU/mL of those samples testing positive for S. aureus was 3.22 (0.04) at 0 hours; and at 6 hours, it was 3.44 (0.26), P < 0.003. No samples reached a concentration of 104 CFU/mL.
Mothers reported hiding milk expression in 78.3% of the time and FH in 76.0% of the time; 92.6% of mothers hid these practices at some point—usually from neighbors (78.5% of reports of hiding expression and 65.0% of those hiding FH), with fewer reports of hiding from family (21.5%, 26.6%) or friends (7.7%, 16.7%). Most (71.2%) mothers reported that someone in their family or household knew they were FH; most often this was the infant's father (64.9%) with the most common reactions being “supportive” (41.1%), “neutral” (35.7%), and “curious” (21.4%). Forty-six percent of mothers surveyed explained to others why they FH milk; half of these mothers gave the reason of killing HIV and one-third said it was because of a breast infection or problem. Ten percent of mothers reported newly disclosing their HIV status during the study.
There was no statistically significant difference in number of morbidities (number of days ill with each symptoms as follows: diarrhea, cough, runny nose, fever, vomiting, rash, or ear infection) between 6 and 9 months in infants who received versus those who did not receive flash-heated breastmilk, but there was a trend toward fewer ear infections in those receiving heated breastmilk, P = 0.08. Growth was also not significantly different between the 2 groups of infants.
Breast and Nipple Pain
After 6 months postpartum, there were 4 reports of breast or nipple pain within the past 2 weeks from 3 mothers; 2 who did not flash-heat compared with 1 flash-heater P = 0.58.
Dietary data from 24-hour recalls (n = 217) after 6 months of age for the 34 infants fed heated breastmilk versus the 28 who were not revealed no difference in the mean daily number of servings of meat [0.46 (0.39) vs. 0.45 (0.49), P = 0.56], meat stew [0.05 (0.18) vs. 0.11 (0.27), P = 0.46] or eggs [0.01 (0.09) vs. 0.06 (0.20), P = 0.24]. However, infants not receiving expressed heated breastmilk received a slightly greater mean (SD) number of daily servings of other animal milks than did those receiving human milk, 1.5 (0.9) versus 1.0 (0.7), P = 0.03.
In 3 of 83 (3.6%) surveys of flash-heaters, the infant was fed directly at the breast in the last week, from 2 to 10 times.
This study has several important findings. Foremost, a substantial percent (51.4%) of HIV-infected mothers whose infants tested HIV negative at 5 months were willing to express and flash-heat their breastmilk upon introduction of complementary foods. This was a greater proportion than the 33% we anticipated. It is notable that the percentage of mothers that chose to flash-heat dramatically increased over the course of the study, possibly as a result of the counselors' greater experience. Second, we observed that mothers were able to successfully follow the FH protocol, and the heated milk was bacteriologically safe. Third, the amount of breastmilk provided to these infants substantially contributed to their diet. The mean daily volume of 322 mL constitutes approximately 34% of caloric needs for an average 6 month infant (weight 7.6 kg)14 and increased by 2-fold to 3-fold the mean amount of animal milk they otherwise received (1 serving daily). Fourth, most mothers sustained this practice for at least 2 months, with duration varying widely from 1 day to 1 year. Last, these mothers succeeded in FH with only modest support from trained peer counselors rather than healthcare providers, suggesting this counseling could be sustainable in terms of costs and workforce capacity at a larger scale in resource-limited settings.
In addition to the wide variation in duration of method use, mothers in our study reported a huge range of milk volume expressed daily, from a mean of only 46 mL to nearly a liter. Anti-infective effects of breastmilk are dose responsive, and even partial breastfeeding has been documented to decrease infections in infants.15,16 There may be a threshold effect, however, and the lower amounts of daily breastmilk expressed by some mothers in this study may not provide significant immunoprotection although the greater amounts almost certainly would.15 Of note, this feasibility study was not powered to detect differences in growth and morbidity and should not be used to infer that clinically significant differences would not occur in a larger trial.
Milk volumes at the lower end of the range expressed by mothers in our study likely relate, in part, to relatively infrequent expression (mean 2.3 episodes recorded daily) as milk production declines if the breasts are not emptied regularly and thoroughly.17,18 Accordingly, we expect that mothers with more frequent expression would be better able to maintain a robust milk supply, producing greater mean milk volumes, and sustaining milk production for longer durations. This expectation is supported by our data whereby mean reported volumes of milk expression for the fourth and fifth episodes in the previous day were greater than mean reported volumes for the first through third episodes, that is, women expressing more frequently had both larger volumes per expression and larger daily volumes.
One possible strategy that may enable mothers to express milk more frequently would be for them to “batch heat” milk from 2 or more expressions. This method, involving heating more than 1 jar of milk in a pan simultaneously, is currently under investigation (K. Israel-Ballard, DrPh, personal communication March 15, 2011). However, it will be necessary to document if peak milk temperatures with “batch heating” are similar to those attained when heating a single jar (the method used during virologic safety studies) before recommending this method.
In all contaminated specimens that we tested, bacterial growth that occurred during 6 hours of storage was minimal, albeit statistically significant, and did not result in bacterial counts considered potentially unsafe (105 CFU/mL)17; heating eliminated all pathogens. We surmise that the 1 sample that was positive for bacteria after heating was contaminated after heating, as the preheated sample was bacteriologically negative. Nevertheless, if milk is to be stored, we recommend that milk be heated before storage, when possible, to further minimize the “theoretical” risk of staphylococcal food poisoning. It is also important to note that current recommendations are that expressed human milk may be stored for 6–8 hours at ambient temperatures up to 25°C,19 with conflicting evidence regarding storage safety at higher temperatures.20–22 We have previously demonstrated that FH breastmilk does not significantly impact the antimicrobial properties of the milk23 but note the need for more work to determine the “shelf-life” of expressed breastmilk, heated or unheated, at ambient temperatures above 25°C.
The proportion of mothers who chose to express and heat treat their milk was somewhat less than the 66% of 30 eligible mothers who did so in a similar study in rural Zimbabwe.24 The high rate of uptake in the Zimbabwean study may have been due, in part, to a social marketing campaign that promoted expression and heat-treatment of breastmilk for any mother (even those who are HIV-negative). Our study was performed in the absence of such generalized messages. Although that approach likely decreases stigma, such messages may have unintended consequences, eg, creating a barrier for HIV-negative women who might otherwise leave fresh expressed breastmilk for their infant when separated. Another salient difference between our study and that of Mbuya et al24 is that in our study, education and support about FH was provided by lay counselors with a much less intensive home visit schedule (mean of 15.8 visits over 7 m) than did the nurse counselors in Zimbabwe (21 visits over 8 weeks). Use of lay counselors could be a more cost-effective and sustainable practice given the dearth of health care workers in countries hardest hit by HIV/AIDS25 and where limited resources make breastfeeding imperative.26
There are several limitations to this study. This population was self-selected as we enrolled willing participants in a research study on infant feeding, and therefore does not necessarily represent the population of all HIV-infected mothers in the area. Women with the most supportive home environments may have enrolled, potentially resulting in a greater proportion of mothers opting to try FH. Alternatively, the burden of study participation may have deterred mothers who would otherwise have chosen to provide Flash-heated breastmilk to their uninfected infants. Further, some of the questionnaires were administered by the counselors who were supporting EBF and FH, possibly resulting in reporting bias.
In summary, our findings add significantly to understanding the feasibility of heat-treatment of breastmilk and reinforce those from Zimbabwe that suggest FH is feasible for many HIV-infected women. Although extended ARV prophylaxis for either the breastfeeding mother or her breastfed child is currently considered to be the optimal strategy for prevention of mother-to-child transmission (PMTCT),8 the low coverage of ARV prophylaxis in sub-Saharan Africa27 suggests the need for complementary PMTCT strategies. As with all medical interventions in resource-limited settings, ARV agents are sometimes temporarily unavailable due to “stock-outs”; it will be important for mothers to be aware of the WHO-recommended option to express and heat treat their breastmilk during this time of increased transmission risk. In addition to the 4 scenarios for which use of heat-treated breastmilk is currently recommended by WHO,8 Flash-heated breastmilk could also be provided after ARV cessation at 12 months to further prolong provision of safe breastmilk to these vulnerable infants. Indeed, breastmilk continues to have dual nutritional and immunoprotective importance beyond the first year, the latter evidenced by the 1.6-fold increase in mortality from infectious causes amongst nonbreastfed infants in resource-poor settings compared with their breastfed counterparts in the second year of life.28
Based on the feasibility data to date, a clinical trial of the effects of flash-heated breastmilk on infant health outcomes is warranted. Only with such information will it be possible to provide both PMTCT programs and the families they serve with evidence-based recommendations. Finally, as countries seek to implement the 2010 WHO guidance, rigorous monitoring and evaluation around their inclusion of heat-treatment within PMTCT programs is necessary to appropriately guide scale-up of such strategies.
The authors gratefully acknowledge funding from the National Institutes of Health (NIH R01HD057602) and the Thrasher Research Fund. The authors warmly thank Makilika study staff and the mothers and babies who participated in the study.
1. UNAIDS. AIDS Epidemic Update. Geneva, Switzerland: WHO; 2009.
2. Horvath T, Madi BC, Iuppa IM, et al.. Interventions for preventing late postnatal mother-to-child transmission of HIV. Cochrane Database Syst Rev. 2009; CD006734.
3. Kourtis AP, Lee FK, Abrams EJ, et al.. Mother-to-child transmission of HIV-1: timing and implications for prevention. Lancet Infect Dis. 2006;6:726–732.
4. Kuhn L, Sinkala M, Semrau K, et al.. Elevations in mortality associated with weaning persist into the second year of life among uninfected children born to HIV-infected mothers. Clin Infect Dis. 2010;50:437–444.
5. Arpadi S, Fawzy A, Aldrovandi GM, et al.. Growth faltering due to breastfeeding cessation in uninfected children born to HIV-infected mothers in Zambia. Am J Clin Nutr. 2009;90:344–353.
6. Kafulafula G, Hoover DR, Taha TE, et al.. Frequency of gastroenteritis and gastroenteritis-associated mortality with early weaning in HIV-1-uninfected children born to HIV-infected women in Malawi. J Acquir Immune Defic Syndr. 2010;53:6–13.
7. Onyango-Makumbi C, Bagenda D, Mwatha A, et al.. Early weaning of HIV-exposed uninfected infants and risk of serious gastroenteritis: findings from two perinatal HIV prevention trials in Kampala, Uganda. J Acquir Immune Defic Syndr. 2010;53:20–27.
10. Israel-Ballard K, Coutsoudis A, Chantry CJ, et al.. Bacterial safety of flash-heated and unheated expressed breastmilk during storage. J Trop Pediatr. 2006;52:399–405.
11. Israel-Ballard K, Donovan R, Chantry C, et al.. Flash-heat inactivation of HIV-1 in human milk: a potential method to reduce postnatal transmission in developing countries. J Acquir Immune Defic Syndr. 2007;45:318–323.
12. Chantry CJ, Israel-Ballard K, Moldoveanu Z, et al.. Effect of flash-heat treatment on immunoglobulins in breast milk. J Acquir Immune Defic Syndr. 2009;51:264–267.
13. Israel-Ballard KA, Abrams BF, Coutsoudis A, et al.. Vitamin content of breast milk from HIV-1-infected mothers before and after flash-heat treatment. J Acquir Immune Defic Syndr. 2008;48:444–449.
14. Food and Agricultural Organization of the United Nations. Human Energy Requirements: Report of a Joint FAO/WHO/UNU Expert Consultation. October 17–24, 2001;Rome, Italy. 2004. Available at: ftp://ftp.fao.org/docrep/fao/007/y5686e/y5686e00.pdf
. Accessed June 13, 2011.
15. Raisler J, Alexander C, O'Campo P. Breast-feeding and infant illness: a dose-response relationship? Am J Public Health. 1999;89:25–30.
16. Bilenko N, Ghosh R, Levy A, et al.. Partial breastfeeding protects Bedouin infants from infection and morbidity: prospective cohort study. Asia Pac J Clin Nutr. 2008;17:243–249.
17. Lawrence RA, Lawrence LR. Breastfeeding: A Guide for the Medical Profession. 7th ed. Philadelphia, PA: Elsevier Mosby; 2010.
18. Academy of Breastfeeding Medicine Protocol Committee. ABM Clinical Protocol #9: Use of Galactogogues in Initiating or Augmenting the Rate of Maternal Milk Secretion (First Revision January 2011). Breastfeed Med. 2011;6:41–49.
19. Academy of Breastfeeding Protocl Committee, Eglash, A. ABM clinical protocol #8: human milk storage information for home use for full-term infants (original protocol March 2004; revision #1 March 2010). Breastfeed Med. 2010;5:127–130.
20. Hamosh M, Ellis LA, Pollock DR, et al.. Breastfeeding and the working mother: effect of time and temperature of short-term storage on proteolysis, lipolysis, and bacterial growth in milk. Pediatrics. 1996;97:492–498.
21. Ajusi JD, Onyango FE, Mutanda LN, et al.. Bacteriology of unheated expressed breast milk stored at room temperature. East Afr Med J. 1989;66:381–387.
22. Igumbor EO, Mukura RD, Makandiramba B, et al.. Storage of breast milk: effect of temperature and storage duration on microbial growth. Cent Afr J Med. 2000;46:247–251.
23. Chantry CJ, Wiedeman J, Buehring G, et al.. Effect of flash-heat treatment on antimicrobial activity of breastmilk. Breastfeed Med. 2011;6:111–116.
24. Mbuya MN, Humphrey JH, Majo F, et al.. Heat treatment of expressed breast milk is a feasible option for feeding HIV-exposed, uninfected children after 6 months of age in rural Zimbabwe. J Nutr. 2010;140:1481–1488.
25. Nakakeeto ONL, Umaranayake L. The global strategy to eliminate HIV infection in infants and young children: a seven-country assessment of costs and feasibility. AIDS. 2009;23:987–995.
26. Young SL, Mbuya MN, Chantry CJ, et al.. Current knowledge and future research on infant feeding in the context of HIV: basic, clinical, behavioral, and programmatic perspectives. Adv Nutr. 2011;2:225–243.
28. WHO Collaborative Study Team on the Role of Breastfeeding on the Prevention of Infant Mortality. Effect of breastfeeding on infant and child mortality due to infectious diseases in less developed countries: a pooled analysis. Lancet. 2000;355:451–455.
Keywords:© 2012 Lippincott Williams & Wilkins, Inc.
HIV; infant feeding; breastmilk; pasteurization; feasibility; heat-treatment; Flash-heat; maternal-to-child transmission