Not Recommended,But Done: Breastfeeding with HIV in Germany

Abstract

Breastfeeding (BF) in mothers living with HIV (MLWH) is still discussed controversially in resource-rich settings. In Germany, where formula feeding is recommended for MLWH single BF cases have been reported, but no systematic data collection and analysis are available so far. This study, titled HELENE, aims to fill this data gap. A questionnaire covering the course of BF was distributed by a graduate student visiting each study site. Information was collected from patient files and by personal communication with the health care provider. Primary study objectives were the duration of BF and the maternal antiretroviral treatment (ART). Fifteen treatment centers across Germany contributed a total of 42 BF cases, observed from May 2009 to July 2020. There was an increasing number of BF cases over time. The median duration of BF was 20 weeks varying from single BF of colostrum to 104 weeks. All BF women except one elite controller received ART: 39% non-nucleoside reverse transcriptase inhibitor-, 37% INSTI-, 29% protease inhibitor-based regimens; one woman was on maraviroc. Thirty-nine percent of the ART regimens included drugs that were not recommended by the German–Austrian pregnancy guidelines. Our findings highlight the diversity of BF cases in Germany in terms of duration, maternal ART, and monitoring. Since the number of BF cases is increasing, guidelines are obliged to implement more detailed recommendations on BF, the monitoring of BF mothers, and the follow-up of the infants. There is an urgent need for prospective national and European data collections to further improve HIV prevention of mother-to-child transmission (PMTCT) in the setting of BF.

Introduction

Breastfeeding (BF) by mothers living with HIV (MLWH) is strongly recommended in settings where alternatives to BF are not affordable, acceptable, sustainable, or safe.¹ In these resource-limited settings WHO advises women living with HIV (WLWH) to exclusively breastfeed for 6 months. If they receive antiretroviral treatment (ART) BF should be continued up to 12 or 24 months, respectively. For WLWH with access to lifelong ART there are no restrictions regarding the duration of BF. In high-income countries, however, HIV guidelines endorse against BF, since HIV can be transmitted through breast milk and it is assumed that formula feeding is available to all mothers.^2
–4 Despite the current recommendations for bottle feeding there are WLWH who decide to breastfeed their infants. The PROMISE study (Promoting Maternal Infant Survival Everywhere) was the first randomized trial that directly compared maternal ART versus infant antiretroviral prophylaxis regarding HIV prevention of mother-to-child transmission (PMTCT) during BF. It was conducted from June 2011 to October 2014 in sub-Saharan Africa and India. Two thousand four hundred thirty-one mother-child pairs were included in the final analysis.⁵ The risk of HIV transmission during BF with ART was 0.3% after 6 months and 0.6% after 12 months of BF. Both maternal ART as well as infant prophylaxis were effective and safe in the PROMISE study.

However, it is still not entirely clear whether Undetectable = Untransmittable (U = U) does also apply to BF.⁶ In Germany the first case of BF by a mother living with HIV was presented in 2013.^7,8 Among German HIV specialists only a few more cases of BF were discussed since then, but there has never been any systematic nationwide data collection so far.

At the end of 2018 an estimated number of 87,900 people were living with HIV in Germany. Among them 17,300 were women (19.7%).⁹ Annually 400–500 WLWH give birth in Germany.¹⁰ The German HIV pregnancy registry, under the umbrella of the German AIDS Society (DAIG), started to collect data of pregnancy courses as well as maternal and infant outcome in 2012.¹¹ However, detailed data on BF is not being reported to the registry yet, since BF is not recommended by the German–Austrian pregnancy guidelines to date. The study HELENE (HIV and breastfeeding—retrospective analysis of cases in Germany) aims to fill this data gap.

Methods

HELENE is a retrospective multi-center study collecting data on BF mothers with HIV in Germany. The data collection was performed from November 2018 to July 2020. In October 2017 a prestudy survey was conducted to estimate the number of German HIV specialists who had previously been taking care of BF women. The survey was supported by the German AIDS society (DAIG), the German Association of Physicians Specialized in HIV Care (DAGNÄ), the Deutsche Aidshilfe (DAH) as well as several HIV community networks.

The study protocol for HELENE was submitted for ethic approval on August 30, 2018. HELENE received the ethic approval on November 15, 2018 (308/18). [Ethic committee of the University Hospital Frankfurt; 308/18]

Primary study objectives were the duration of BF; maternal ART and viral load (VL) results perinatally and during the BF period. Undetectable VL was defined as HIV-1-RNA-PCR <50 copies/mL.

Secondary study objectives were demographic data, information on the course of pregnancy, the BF period, maternal ART, and postexposure prophylaxis of the neonates.

Included were WLWH in Germany, >18 years of age, who breastfed their infants since their HIV diagnosis and openly communicated BF to their health care providers.

A questionnaire was designed for the data collection. It was distributed by a graduate student, visiting all HELENE study sites. Information on BF was collected from patient files as well as by personal communication with the HIV specialist. Owing to the General Data Protection Regulation (GDPR) all data were anonymized.

Statistical analysis

Data were managed and analyzed with EXCEL 365 (Microsoft Corp., Redmond, WA). A descriptive analysis was carried out.

Data capturing of relevant information, for example, maternal age, year of BF, time of HIV diagnosis, Centers for Disease Control and Prevention (CDC)-stage, pregnancy week and mode of delivery, duration of BF, maternal ART, VL during pregnancy and BF, CD4 cell counts, previous births, comorbidities, country of birth, education, profession, neonatal postexposure prophylaxis (Neo-PEP), and adverse events in the breastfed infants was conducted by the primary investigator.

Results

The prestudy survey identified 20 centers where women with HIV who breastfed their infants had already been cared for. Fifteen centers participated in the study.

HELENE included a total of 42 BF cases with the first case reported in 2009. The median age of the BF mothers was 33 years [range, 18–45 years, interquartile range (IQR) 8]. The majority, 27 (64%), of women, was born abroad, predominantly (82%) in sub-Saharan African countries. The median time since HIV diagnosis was 5 years (range, <1–37 years, IQR 7), including one woman being vertically infected. The clinical CDC stage was stage A in 38 women (93%) and stage B in 3 women (7%). There was no CDC stage C.

Median duration of the BF period was 20 weeks ranging from single BF of colostrum up to 104 weeks of BF (IQR 19). At the time of delivery all women with available data had an undetectable VL defined as VL <50 copies/mL; VL results of two women were not available at that time point. Both women had a suppressed VL in the prior test. VL results of 37 women were available during the BF period. Two women experienced a viral rebound; one in BF week 12 with a VL of 76 copies/mL and the other one in BF week 4 with a VL of 867 copies/mL, respectively. The woman with 76 copies/mL had started ART with tenofovir disoproxil fumarate/emtricitabine (TVD/FTC) and raltegravir in pregnancy week 13 with a VL >100,000 copies/mL. The VL was fully suppressed for the first time during the third trimester of pregnancy. The woman with the VL of 867 copies/mL had started tenofovir disoproxil/emtricitabine and dolutegravir in pregnancy week 38 with a baseline VL of 8500 copies/mL. The VL was <50 copies/mL at the time of delivery. Both women stopped BF immediately after their viral rebound. The first woman most likely experienced a viral blip resulting in 76 copies/mL, but we were not able to verify that assumption because the woman stopped ART after weaning. The second woman with the viral rebound of 867 copies/mL had an undetectable VL again in the next analysis. In this case we assume that adherence issues are most likely to have caused the viral rebound.

Maternal VL during the BF period was not tested in a standardized way. Most centers (42%) performed a HIV-1-RNA-PCR every 4 weeks, 23% every 4–8 weeks, 19% every 12 weeks, and 15% in other time intervals. The maternal HIV-VL was tested in blood. Two centers additionally performed HIV-1-RNA-PCR in breastmilk in a total of five women. All VL results in the breastmilk samples were <50 copies/mL.

Mean CD4 cell count at preconception was 742/μL (262–1220), in the first trimester 718/μL (329–1385), in the second trimester 633/μL (100–1300), third trimester 700/μL (156–1400), at delivery 699/μL (172–1400) and 845/μL (213–1544) during the BF period.

One BF woman was an HIV elite controller and did not receive ART during pregnancy or BF. All other 41 women were on ART; 30 (73%) already preconceptional and 11 (27%) starting ART during pregnancy. The following antiretroviral drugs were used during the BF period: 40 (98%) women received a nucleoside reverse transcriptase inhibitor (NRTI), 12 (29%) women were on a ritonavir-boosted protease inhibitor (PI/r), 16 (39%) on non-nucleoside reverse transcriptase inhibitor (NNRTI)-based regimens and 15 (37%) women received an integrase inhibitor (INSTI). The BF mother on the NRTI-free regime was on dual ART, INSTI plus boosted PI. One maternal ART was modified during the BF period: In the patient receiving tenofovir, emtricitabine, and nevirapine, tenofovir was switched to tenofovir alafenamide. Tables 1 and 2

Table 1.

Maternal Antiretroviral Treatment During Pregnancy

ART during pregnancy
NRTI	40
TDF, FTC	37	92.5%
TAF, FTC^a	1	2.5%
ABC/3TC	1	2.5%
3TC	1	2.5%
PI	14
ATV/r	4	28.6%
LPV/r	4	28.6%
DRV/r	6	42.9%
INSTI	16
RAL	11	68.8%
DTG^a	6	37.5%
EVG/c^a	3	18.8%
NNRTI	16
RPV^a	9	56.3%
NVP	7	43.8%
Entry inhibitor	1
MRC^a	1	100.0%
No ART (elite controller)	1	100.0%

Drugs not recommended for the use in pregnancy by the corresponding German–Austrian guidelines at the time of prescription.

3TC, lamivudine; ABC, abacavir; ART, antiretroviral treatment; ATV/r, atazanavir/ritonavir; DRV/r, darunavir/ritonavir; DTG, dolutegravir; EVG/c, elvitegravir/cobicistat; FTC, emtricitabine; LPV/r, lopinavir/ritonavir; MRC, maraviroc; NNRTI, non-nucleoside reverse transcriptase inhibitor; NVP, nevirapine; RAL, raltegravir; RPV, rilpivirine; PI, protease inhibitor; TAF, tenofovir alafenamide; TDF, tenofovir disoproxil.

Table 2.

Maternal Antiretroviral Treatment During Breastfeeding

ART during BF
NRTI	40
TDF, FTC	37	92.5%
TAF, FTC	1	2.5%
ABC/3TC	1	2.5%
3TC	1	2.5%
PI	12
ATV/r	2	16.7%
LPV/r	4	33.3%
DRV/r	6	50.0%
INSTI	15
RAL	10	66.7%
DTG	3	20.0%
EVG/c	2	13.3%
NNRTI	16
RPV	9	56.3%
NVP	7	43.8%
Entry inhibitor	1
MRC	1	100.0%
No ART (elite controller)	1	100.0%

BF, breastfeeding.

Comorbidities of the BF women were one case of chronic hepatitis B, one chronic hepatitis C, one woman with sickle cell anemia, one with multiple sclerosis and one woman with depression. The woman suffering from depression as well as one additional woman were using illicit drugs during their pregnancy and BF period.

Twenty-seven (64%) women were multipara. Data on previous BF experience were available for 23 women and 12 (52%) of them had already breastfed a previous child. Most women addressed their desire to breastfeed already during pregnancy; data are available for 37 women; 34 (92%) women addressed the issue of BF actively during pregnancy and 3 (8%) women after delivery. For 9/42 (21%) BF women no data on mixed feeding were available. Among 33 women with available data 19 (58%) practiced exclusive BF, whereas 14 (42%) offered additional food to their infants.

For 40 women data on the mode of delivery was available. Twenty-eight (70%) of these women had a vaginal delivery, 7 (18%) needed an emergency caesarean delivery (CD) and 5 women (13%) underwent a planned CD. The median pregnancy week at delivery was week 40 (36–42, IQR 1).

All BF women were in care of an HIV specialist. For their first presentation during pregnancy data were available for 41 women. Twenty-one (51%) of them had already been in care before they got pregnant. Ten (24%) presented during the first trimester, 7 (17%) during the second trimester and 3 (7%) in the third trimester.

HELENE also addressed the educational level of the BF women. Data on education were available for 23 women. Twelve (52%) of these women graduated from high school or university, 8 (35%) women graduated from secondary school and 3 (13%) women did not graduate from school. Data on occupation were available for 34 women. Twenty-two (65%) of them had been working when they got pregnant. Table 3

Table 3.

Characteristics of the Breastfeeding Mothers

Characteristics of the BF mothers
Maternal age (in years) n = 42
Mean	31.95
Median	33
Min	18
Max	45
IQR	8
Mode of delivery n = 40
Vaginal	28	70.0%
Cesarean delivery	5	12.5%
Emergency cesarean delivery	7	17.5%
Duration of BF (in weeks) n = 42
Mean	22.5
Median	20
Min	0.14
Max	104
IQR	19
Country of origin n = 42
Germany	15	35.7%
Other countries	27	64.3%
Other countries of origin n = 27
Sub-Saharan Africa	22	81.5%
Latin America	1	3.7%
Eastern Europe/Central Asia	3	11.1%
Others	1	3.7%
Time since HIV diagnosis (in years) n = 41
Mean	6.4
Median	5
Min	<1
Max	37
IQR	7
CDC n = 41
A	38	92.7%
B	3	7.3%
C	0	0%
Multipara n = 42
Yes	27	64.3%
No	15	35.7%
BF experienced n = 23
Yes	12	52.2%
No	11	47.8%
Mixed feeding n = 33
Yes	14	42.4%
No	19	57.6%
Expressed wish to breastfeed n = 37
Before pregnancy	0	0%
During pregnancy	34	91.9%
Postpartum	3	8.1%
Occupied before pregnancy n = 34
Yes	22	64.7%
No	12	35.3%
Educational level n = 23
High school or university	12	52.2%
Secondary school	8	34.8%
No graduation	3	13.0%
Pregnancy week of delivery (in weeks) n = 40
Mean	40
Median	40
Min	36
Max	42
IQR	1
First contact with HIV specialist n = 41
before pregnancy	21	51.2%
First trimester	10	24.4%
Second trimester	7	17.1%
Third trimester	3	7.3%

CDC, Centers for Disease Control and Prevention; IQR, interquartile range.

Data on Neo-PEP were available for 29/42 (69%) infants. The median time on Neo-PEP was 2 weeks, varying from 2 to 16 weeks (IQR 0). No adverse events were reported in the breastfed infants.

We observed an increasing number of BF WLWH in Germany over time, with one case in 2009 and 13 cases in 2018. Owing to the COVID-19 pandemic and associated restrictions it was not feasible to continue the data collection as planned and because of this special situation not all BF cases from 2019 to 2020 could be added to the data set. In addition, women still BF at the moment might have been missed due to the retrospective character of HELENE Fig. 1.

FIG. 1.

BF cases per year. Owing to the SARS-CoV2-pandemic the data collection needed to be stopped; therefore, there are missing cases for 2019 and 2020 based on the retrospective character of HELENE. BF, breastfeeding.

Discussion

HELENE is the first study on BF and HIV in Germany. The results demonstrate a small but increasing number of WLWH who breastfeed their infants despite contrary recommendations.⁴ For the past 12 years we were able to retrospectively analyze 42 BF cases with an increasing number over time. The women were most likely to be multipara (64%), BF experienced (52%), well educated (52%), and born abroad (64%). The majority of them gave birth by vaginal delivery (70%). The increasing numbers reflect a growing need for normality in the context of HIV and pregnancy. Most women (92%) expressed the decision to breastfeed early in pregnancy. Results from the PACIFY study support the described trend toward BF. A survey in pregnant WLWH in 12 UK clinics was performed from June 2017 to June 2018 including 94 women; 38% of the women stated that they would like to breastfeed their infants.¹²

Nevertheless, HELENE might even be underestimating the number of BF cases in Germany due to the retrospective character of the study and because we were only able to include mothers who openly communicated BF to their health care providers. Since all HIV specialists strongly recommended formula feeding women with HIV might have been reluctant to disclose BF. In addition, our study was only conducted in centers specialized in HIV care. So we might have missed BF women who were looked after in other settings.

Data on BF and HIV are still missing for resource-rich countries. So far case reports have been published by a Canadian study group (n = 3) and Belgium authors (n = 2).^13,14 The National Surveillance of HIV in Pregnancy and Childhood (NSHPC) in the United Kingdom performed a database analysis of 7187 live birth deliveries, including 155 BF cases; observational period 2012–2019.¹⁵ The median duration of BF in the United Kingdom was 7 weeks with a range from 1 day to 2 years. In comparison with these data women included in HELENE breastfed for a longer time period (median 20 weeks) also presenting a wide range of duration from single BF of colostrum to 2.2 years of BF. The mean duration of BF in the general population in Germany is 8 months (KIGGS study) and exclusive BF is recommended by the National German Breastfeeding Committee for at least 4–6 months.^16
–18

The percentage of women born abroad was high in both studies; NSHPC: 83%; HELENE: 64%. The majority of BF women in Germany was multipara and already experienced in BF. Comparable data on BF experience were not presented by NSHPC. Since WHO guidelines recommend BF in resource limited countries women for example, from sub-Saharan Africa might have put into practice what they were advised to do in their country of origin. Mixed feeding before 6 months of age was reported in 11.1% of BF cases in the United Kingdom, whereas HELENE analyzed 42.4% mixed feeding but did not further differentiate according to age.

NSHPC data show that 93.0% of BF MLWH in the United Kingdom had been diagnosed before they got pregnant. In HELENE 73.2% of the BF women knew their HIV status before conception. In addition, HELENE contributes data on first presentation during pregnancy. Fifty-one percent of the BF women already were in care of an HIV specialist when they got pregnant, 24% presented during the first trimester, 17% during the second, and 7% during the last 12 weeks of pregnancy. Except one elite controller all BF women received ART. ART regimens of the BF women were NNRTI based in 39%, INSTI based in 37%, and contained a ritonavir boosted PI in 29%. One woman was on maraviroc. Sixteen out of 41 (39%) BF women were treated with drugs that were not recommended by the German–Austrian HIV pregnancy guidelines.⁴ HELENE did not include data of non-BF women but was able to compare their findings to recent data from the German HIV pregnancy registry. Indeed, the portion of 39% of not recommended drugs is higher than what is usually seen in pregnant women with HIV. In women who conceived under ART 27% were treated with drugs not recommend by the national guidelines; women who started ART during pregnancy the percentage was 11%.¹⁹

HIV-1-RNA-PCR was <50 copies/mL in all women at the start of BF. Two women experienced a viral rebound during the BF period with 76 and 867 copies/mL, respectively. Both women stopped BF immediately. Maternal VL during the BF period was not tested in a standardized way. Most centers (42%) tested every 4 weeks, 23% every 4–8 weeks, 19% every 12 weeks, and 15% in other time intervals. During the observational period of HELENE the German–Austrian guidelines did not give detailed recommendations concerning VL testing in BF mothers. The British HIV Association (BHIVA) guidelines, the Swiss guidelines, and the European guidelines recommend monthly VL testing.^3,20,21

HIV mother-to-child transmission through BF was not a study objective of HELENE. The follow-up and outcome of the breastfed infants could not be included in the study protocol due to the GDPR in Germany. Nevertheless, the missing data on MTCT is a limitation of our study. However, for the observational period the national survey of the Robert Koch Institute (RKI) did not register any new HIV infections that were likely to be caused by BF.²² The few vertical transmissions cases that occurred from 2009 to date were carefully processed by the RKI. Nevertheless, cases might have been missed because of the lack of clear recommendations for the follow-up of HIV-exposed breastfed children.

Conclusions

The results from HELENE highlight the need to address the issue of BF as early as possible in pregnant WLWH. Even though the number of BF cases is still small, it is increasing over time. The diversity of the BF cases especially in terms of duration, maternal ART, and BF monitoring reflects the need for a standardized procedure. Recommendations for the management of BF should urgently be implemented in national HIV pregnancy guidelines, including patient information for a shared decision making. The Swiss und UK guidelines already offer this approach.^20,21 Prospective data acquisition needs to be implemented on a national and on an European level to further improve the interdisciplinary management of BF WLWH and the follow-up of their infants.

Footnotes

Authors' Contributions

All authors meet the four criteria for authorship of the International Committee of Medical Journal Editors recommendations. L.H. and A.H. contributed to the study conception and design, and drafted the article. L.H., F.A., C.F.-S., D.G., P.J., C.J.-O., P.K., R.K., A.R., A.R., E.R., S.R., J.-A.R., G.S., C.S., A.U., A.V.B., K.V.W., and A.H. participated in the acquisition of data. All authors were involved in the critical review of the article for important intellectual content and gave final approval of the version to be published.

Author Disclosure Statement

F.A. reported personal fees from Abbvie, Gilead Sciences, MYR Pharma and ViiV. A.H. received speaker fees from Gilead Sciences, Janssen-Cilag and MSD, and also participated in MSD advisory boards. Support of congress participation was provided by Gilead Sciences and Janssen-Cilag. P.K. reports personal fees from Abbvie, Gilead Sciences, Sanofi, and ViiV. C.S. reported personal fees from Abbvie, Gilead Sciences, Hexal, Janssen-Cilag, MSD, Pfizer, TAD, and ViiV. G.S. received funding from Gilead Sciences and speaker fees from Gilead Sciences, ViiV Health care, Bristol Meyer Squibb, MSD and Hormosan for participation in advisory boards, data safety monitoring boards, and for preparation of educational materials and lecturing fees.

Funding Information

No funding was received for this article.

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