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Scaling up Pediatric HIV Testing by Incorporating Provider-Initiated HIV Testing Into all Child Health Services in Hurungwe District, Zimbabwe

Musarandega, Reuben, MSc*; Mutede, Blessing, MD, MPH*; Mahomva, Agnes, MD, MPH*; Nyamayaro, Wenceslas, MD, MPH; Mushavi, Angela, MD, MMED; Lindan, Christina, MD, MSc; Machekano, Rhoderick, PhD, MPH§

JAIDS Journal of Acquired Immune Deficiency Syndromes: January 1, 2018 - Volume 77 - Issue 1 - p 78–85
doi: 10.1097/QAI.0000000000001564
Implementation Science

Background: Practical ways are needed to scale-up pediatric HIV testing in sub-Saharan Africa, where testing is usually limited to HIV-exposed children in maternal and child health clinics.

Methods: We implemented an enhanced pediatric HIV testing program in 33 health facilities in Zimbabwe by integrating HIV testing into all pediatric health services. We collected individual data on children tested by having health care workers complete a program-specific child health booklet. We compared numbers of children tested before and during the program using routinely collected aggregate program data reported by health facilities.

Results: A total of 12,556 children aged 0–5 years were recorded in child health booklets; 9431 (75.1%) had information on HIV testing, of whom 7326 (77.7%) were tested; 7167 had test results of whom 122 (1.7%) were HIV-infected. Among children seen in outpatient clinics, 82.1% were tested compared with 66.5% tested among children seen in maternal/child health clinics. Of the 122 HIV-infected children identified, 77 (63.1%) could be missed under existing pediatric testing guidelines. The number of HIV-infected children identified during the 6-month program increased by 55% compared with the prior 6-month period (RR = 1.55, 95% CI: 1.22 to 1.96). Factors independently associated with HIV infection included being malnourished (adjusted odds ratio [AOR] = 7.7, 95% CI: 2.1 to 28.6), being exposed to TB (AOR = 8.1, 95% CI: 2.0 to 32.2), and having an HIV-infected mother (AOR = 41.6, 95% CI: 15.9 to 108.8).

Conclusions: Integrating HIV testing into all pediatric health services is feasible and can assist in identifying HIV-infected children who could be missed in current testing guidelines.

*Elizabeth Glaser Pediatric AIDS Foundation, Harare, Zimbabwe;

Ministry of Health and Child Care, Harare, Zimbabwe;

Global Health Sciences, University of California, San Francisco, CA; and

§Elizabeth Glaser Pediatric AIDS Foundation, Washington, DC.

Correspondence to: Reuben Musarandega, MSc, 107 King George, Avondale, Harare 263, Zimbabwe (e-mail:

Funding for this study was provided by the Children's Investment Fund Foundation and U.S. NIMH, R25MH064712, which supported the writing of this manuscript.

The authors have no conflicts of interest to declare.

The findings and conclusions in this manuscript are those of the authors and do not necessarily represent the views of CIFF which funded the program, EGPAF and the Zimbabwe MOHCC which implemented the program and UCSF which supported the development of this manuscript.

Received January 19, 2017

Accepted September 20, 2017

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In sub-Saharan Africa, more than 50% of HIV-infected children are diagnosed well after 2 months of age, leading to high rates of AIDS-related mortality.1–7 Strategies for pediatric HIV testing usually target children known to have an HIV-infected mother and those with signs and symptoms of HIV disease. In addition, testing is usually performed in a limited number of clinic settings. This approach is not adequate to identify the majority of HIV-infected children.8–17 Practical ways of scaling-up pediatric HIV testing are needed, particularly to identify the children who miss diagnosis in infancy and those who are infected through breastfeeding.

Zimbabwe has a generalized HIV epidemic, with 14.7% of 15–49 year olds estimated, through modeling, to be infected in 2015. Surveillance of antenatal clinics in 2012 found that 16% of pregnant women were HIV-infected.18,19 A 2014 representative population-based survey estimated the mother-to-child transmission (MTCT) rate of HIV at 18 months of age to be 6.7%, above the UNAIDS target of 5% or less.20

The 2015 Zimbabwe national HIV testing guidelines based on the World Health Organization (WHO) recommend children with a known HIV-infected mother or HIV disease symptoms to be prioritized for HIV testing.21 All HIV-exposed children between 6 weeks and 8 months of age are to be tested using an HIV DNA PCR, whereas those 9 months of age and above are to be tested with serial rapid antibody tests with confirmation of a positive result by a DNA PCR test. The guidelines also recommend that children be tested in a wide range of settings when presenting to any health care clinic.

Despite these guidelines, pediatric HIV testing in Zimbabwe continues to face many challenges. Children are mostly tested during postnatal maternal and infant visits. Children known to be HIV-exposed who are breastfeeding, generally up to 2 years of age, and those who present with symptoms of HIV disease are more likely to be tested.20–24 Unfortunately, however, not all nurses caring for children have been trained to collect a dried blood spot or perform a rapid HIV test. In addition, only 3 laboratories in the country perform DNA PCR testing. Specimens need to be transferred from more than 1500 clinics and hospitals, many of which are located in remote areas without reliable transportation. The central laboratories suffer frequent equipment breakdowns and reagent stock-outs. Some parents are unwilling to provide consent for their children to be tested because they are concerned about stigma, or fear that a child's positive test result will reflect their own HIV status.20,22,24

To improve identification of HIV-infected children in Zimbabwe, the Elizabeth Glaser Paediatric AIDS Foundation (EGPAF) implemented a program designed to integrate HIV testing within all pediatric health services. This paper describes how the program was implemented and evaluates whether the program increased testing and identification of previously undiagnosed HIV-infected children below 5 years of age. The program was part of a wider initiative to link and retain HIV-infected children on treatment.

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EGPAF implemented the expanded pediatric HIV testing program in all 33 health facilities (1 district hospital, 3 rural hospitals, and 29 rural health centers) in Hurungwe district, one of 63 districts in Zimbabwe, and is located in the northern part of the country. In 2015, the district's population was 339,172 of which 16% were children below the age of 5 years.25 This district was selected because it had an estimated mother-to-child transmission rate of 12.1%, which was higher than the national average of 6.7%.20

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Description of the Enhanced Pediatric HIV Testing Program

Table 1 presents the activities that were implemented as part of the program. EGPAF staff first held meetings with the Ministry of Health and Child Care (MOHCC) HIV program managers at the national and provincial levels to explain and gain support for the program. Together with MOHCC district staff, government ministries for local government, education and social services and other HIV testing partners, EGPAF conducted targeted community meetings to raise public awareness about the need for HIV testing of children. EGPAF and MOHCC facility staff held meetings with village health workers (VHWs) at each health facility encouraging them to refer young children to health facilities for HIV testing. A baseline assessment evaluating the adequacy of staff, training needs and the availability of HIV testing commodities, among other factors, was conducted at all study facilities. EGPAF used the baseline assessment findings to plan trainings and to engage the district health management team in addressing critical staffing needs. Nurses from all health facilities were trained during workshops on how to perform pediatric HIV testing, and how to record data in a program-specific child health booklet and routine MOHCC registers and forms.



The EGPAF program required nurses to offer HIV testing to all children below 5 years of age who had never been tested and children below 2 years of age who had more than 3 months old HIV-negative test results presenting to any inpatient or outpatient clinic.

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HIV Testing

The existing HIV status of a child was based on patient records. If records were not available and the child's status could not be verified, the child was retested. For children below 9 months of age, nurses collected finger-prick-dried blood spot specimens and sent them to the National Microbiology Reference Laboratory in Harare for PCR testing (COBAS Ampliprep/COBAS Taqman 96; HIV-1 QUAL Test System; COBAS, Roche Diagnostics, Branchburg, NJ). Children aged 9–24 months underwent serial rapid HIV antibody testing of finger-prick blood specimens using Alere Determine HIV-1/2 (Alere Medical Co. Ltd., Matsudo Shi Chiba, Japan) and Uni-Gold Recombigen (Trinity Biotech, Co Wilcow Bray, Ireland) HIV test kits. Positive and discordant antibody test results were confirmed by DNA PCR testing. Children > 24 months to 5 years of age underwent serial rapid HIV antibody testing only.

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Support and Supervision of Program Activities

During program implementation, teams comprised of EGPAF and MOHCC district staff conducted monthly support and supervision visits to each health facility to reinforce the expanded HIV testing program. During these visits, the teams reviewed the pediatric HIV testing registers to assess the extent of service provision and to encourage improved documentation. They discussed challenges faced by the staff and collaboratively identified solutions. In addition, program staff conducted workshops with pediatric nurses from all health facilities during which achievements and challenges were discussed, and experiences were shared.

The program was implemented by EGPAF's technical staff in collaboration with MOHCC district and facility-level staff. The EGPAF strategic information, research and technical teams, and MOHCC district staff conducted the baseline assessment before program implementation. The EGPAF strategic information and research teams conducted the program evaluation independently of program implementation. The strategic information team collected all program evaluation data. The baseline assessment, community meetings, and nurse training workshops were implemented between January and March 2015; the enhanced pediatric testing program was implemented between April and September 2015.

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Data Collection and Measurements

To be able to determine how many children were being tested and their characteristics, a child health booklet was developed and issued to the mother or caregiver of each child seeking health services at each health facility during the program. Nurses were to complete and file carbon-copies of the booklet at the health facility; mothers or caregivers would keep the booklet and bring it to each clinic visit. The booklet was used to record information on demographics, clinical characteristics, and HIV testing. The variables collected included child's age, sex, type of health facility (district hospital, rural hospital, rural health centre), clinic visited within the health facility (outpatient, inpatient, maternal and child health and other clinic including TB, nutrition, rehabilitation, and mothers' HIV treatment clinic), reason for clinic visit (sick child or routine health check), presenting symptoms (fever, cough, diarrhea, ear problem, disability, malnutrition, exposure to TB), and mother's HIV status. Malnutrition was defined as having edema, a mid-upper arm circumference (MUAC) <12.5 mm, wasting, or stunting. Children were considered to have been exposed to TB if they once lived with a person with active TB or had symptoms of TB (had a cough of more than 2 weeks duration, fever, and weight loss). Mother's HIV status was determined by reviewing antenatal care cards; when these were not available, HIV status was determined by asking the mother or caregiver.

In addition to data collected on the program-specific booklet, routine aggregate data reported by health facilities to the district MOHCC office were collected during program implementation on numbers of children tested for HIV and number of HIV-infected children identified. The routine aggregate health facility data were collected during the baseline assessment for the 6 months before implementation (October 2014–March 2015) and routinely during program implementation (April–September 2015). These data would be used to compare numbers of children tested before and during program implementation; no information on demographics or clinical characteristics are recorded in these routine reports.

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Data Analysis

Data from booklets were entered into a Microsoft Access database. A random sample of 10% of child health booklet forms was double-entered to determine accuracy of the data entry, which was satisfactory with less than 3% discordance on all variables. Using booklet data, we estimated the distribution of socio-demographic and clinical characteristics of children seen at the clinics and determined the proportion in each category who were tested for HIV and found to be HIV-infected. Among the subset of children who were known to have been exposed to an HIV-infected mother, we summarized the distribution of demographic and clinical characteristics, and the numbers and proportions in each category who underwent HIV testing and who were HIV-infected. We performed univariate and multivariate logistic regression analysis to identify factors associated with HIV infection. In the first multivariate logistic regression model, we included all characteristics of the children except type of health facility, which we did not expect to be associated with HIV infection in Zimbabwe where the HIV epidemic is generalized and HIV and pediatric health services are decentralized to clinics. In a second multivariate logistic regression model, we assessed possible markers of infection in the absence of mother's HIV status. We estimated the additional number of HIV-infected children who were identified through the expanded testing program who would otherwise not have been tested if current national guidelines were followed.

Using aggregate data from health facility reports, we summarized the total number of children tested and found to be HIV-infected for the 6 months before program implementation and during the implementation period, stratified by age. Routine district-based data only include information on age category and on no other demographic or clinical characteristics. Based on the mean number of children tested and found to be HIV-infected per month, we calculated rate ratios (RR) with 95% confidence intervals (CI) stratified by age to compare levels of testing before and during implementation. Data from child health booklets could not be used for comparing time periods because the booklet was used only during program implementation. We used STATA version 13.0 to analyze child health booklet data and R to analyze aggregate health facility data.26

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Ethical Considerations

The MOHCC and Medical Research Council of Zimbabwe reviewed and approved the study. Caregiver consent to test the children was waived because HIV testing was being done in routine health service provision by health facilities.

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Information on 12,556 children seen at the 33 health facilities over 3 months of data collection was recorded in child health booklets, of whom 9431 (75.1%) had HIV information on whether they were tested or not (Fig. 1). Of the children with HIV testing information, 7326 (77.7%) actually underwent HIV testing, and 7167/7326 (76.0%) of these had information on the results of the test; 122/7167 (1.7%) were identified as being HIV-infected. The demographic and clinical characteristics of all the children seen who had data recorded on booklets (N = 9431) are summarized in Table 2. More than 60% of the children were less than 2 years old. About two-thirds (67.2%) of the children were seen at rural health centers and a third (32.8%) at district or rural hospitals. Most children (71.4%) were seen at outpatient clinics, and 26.5% were seen in maternal and child health (MCH) clinics. More than 90 percent (92.3%) of the children presented with an illness; 56.5% with a cough and 41.2% with a fever. Children who had no HIV testing information (3125/12,556; 24.9%) were similar to those who had information on testing (data not shown) with respect to all characteristics.





The proportion of children who were tested did not differ substantially by demographic or clinical characteristics although children older than 9 months were more likely to be tested than the younger children (>80% versus <72%). A greater proportion of children (82.1%) in pediatric outpatient clinics were tested compared with those seen in MCH clinics (66.5%). HIV prevalence was highest among children with a disability (6.6%), who were malnourished (6.9%), who had an HIV-infected mother (9.5%) and those who were exposed to TB (28.6%). Among the 122 HIV-infected children, 77 (63.1%) children had unknown/negative mother's HIV status (40) or had known positive mother's HIV status but older than 2 years (37) and no symptoms of HIV infection.

Table 3 presents the characteristics of children known to have HIV-infected mothers (HIV-exposed children) and who had information on HIV testing (N = 833). Overall, 761 (92.4%) of known HIV-exposed children were tested and received their results and 9.5% were HIV sero-positive. In this group, HIV prevalence was higher among children aged 2 to 5 years (17.6%), those with malnutrition (30.8%), and those who were exposed to TB (30.8%).



Factors independently associated with HIV infection among all children included malnutrition [adjusted odds ratio (AOR) = 7.7, 95% CI: 2.1 to 28.6], being exposed to TB (AOR = 8.1, 95% CI: 2.0 to 32.2) and having an HIV-infected mother (AOR = 41.6, 95% CI: 5.9 to 108.8) (Table 4). In a model excluding mother's HIV status, disability (AOR = 5.3, 95% CI: 1.4 to 20.1), malnutrition (AOR = 5.1, 95% CI: 1.9 to 13.5), and exposure to TB (AOR = 33.2, 95% CI: 13.0 to 84.9) were independently associated with HIV infection.



Results from the comparison of aggregate health facility data on children tested before and during program implementation are presented in Table 5. The number of children tested increased by 94% between the baseline and program implementation period (rate ratio [RR] = 1.94, 95% CI: 1.86 to 2.03), and the number of HIV-infected children identified increased by 55% (RR = 1.55, 95% CI: 1.22 to 1.96).



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Our results demonstrate that expanding pediatric HIV testing into a wide variety of health facility settings is achievable. More than 77% of children who had their HIV test information recorded in the child health booklet received an HIV test. Similar results were found in a study of provider-initiated testing in Harare, Zimbabwe, in which 76% of children 6–15 years of age underwent HIV testing.24 If we assume that the children in our study who did not have any information on whether they were tested or not, had not undergone testing, then the proportion tested would reduce to 58%. Even so, comparison of aggregate district-level data demonstrated that the number of children who were tested nearly doubled in the 6-month program implementation period compared with the 6-month period before implementation.

In sub-Saharan Africa, pediatric HIV testing is focused on early infant diagnosis of HIV-exposed children, with testing mostly performed during maternal and infant postnatal health visits.8,12–16 This is despite the fact that many more children are seen in outpatient clinics where HIV testing is not performed routinely, partly because of very high patient volumes which can overwhelm the ability of health care workers to provide any additional services, including pediatric HIV testing.21 Despite this barrier, we found that nurses were able to test 82% of the children who presented to outpatient clinics, nearly 20% more than the proportion tested in maternal/child health clinics. However, the success of this program was dependent on EGPAF supporting the training of more nurses on how to perform HIV testing, covering the short-fall of test kits and gloves when stock-outs occurred, and providing regular support visits to motivate nurses to test the children.

Integrating HIV testing into a range of pediatric health services resulted in more than a 50% increase in the number of HIV-infected children identified in the 6-month implementation period compared with the 6-month period before program implementation. In addition, it enabled us to identify HIV-infected children who otherwise would have been missed. The Zimbabwean national guidelines recommend testing of HIV-exposed infants at 6 weeks and at the end of breastfeeding at 18–24 months. The identification of nearly two-thirds of the HIV-infected children outside the existing testing algorithm emphasizes the importance of not restricting HIV testing in children. A significant number of children can be missed by current testing practices, which focus more on confirmed HIV-exposed infants (first test before 2 months of age and final test at end of breastfeeding) and children with HIV disease symptoms. This can result in late initiation of ART and increased mortality of the HIV-infected infants. Studies from sub-Saharan Africa have shown that HIV-infected mothers may be less likely to return for follow-up infant testing once the child's initial PCR test is negative;27,28 yet an estimated 10% of vertical infections occur during breastfeeding.20,29

We identified factors, other than having a known HIV-infected mother, that were associated with HIV infection in these young children. These included being malnourished and being exposed to TB. In Zimbabwe, 80% of TB patients are HIV-infected; hence, exposure to TB is likely to indicate exposure to HIV.30 Disability is also likely to be associated with HIV infection in children because it had statistically significant odds ratios in the univariate model and the multivariate model that excluded mother's HIV status. Neurocognitive impairment, developmental delays, and motor abnormalities such as spasticity have been observed among pediatric HIV patients and may account for the high HIV prevalence among children with disability and likely association between disability and HIV infection in our study.31,32 Being malnourished likely reflects severe HIV disease and has been associated with disease progression and mortality in children.33 This finding suggests that if mother's HIV status is unknown, disability, malnutrition, and TB exposure are probable HIV infection markers in children.

Incorporating HIV testing into child survival programs that target diseases such as malnutrition, disability, and TB is a recommended pediatric HIV case-finding strategy, referred to as the “double-dividend” approach.8,10–17 This strategy attempts to reduce child mortality holistically by identifying and treating HIV infection together with its comorbid conditions in children.8,34,35 Although the largest proportion of children presenting to child health clinics in our study had symptoms of cough, diarrhea and/or fever, the proportion of those children who were found to be HIV-infected was comparatively low—from one to 2 percent. This is because these symptoms reflect the most common pediatric illnesses and HIV disease. We did not collect detailed enough information about persistence and severity of these symptoms to better identify those children in whom these symptoms were more likely to be associated with HIV infection. As a result, we have not attempted to develop algorithms for identifying children most likely to be HIV-infected based on these data. However, others have attempted to develop screening tools, and the Zimbabwe MOHCC is currently developing an algorithm to identify most-at-risk children to target with widespread HIV testing approaches.36,37

This study had several limitations. The number of children tested and found to be HIV-infected who were reported to the district from health facility registers differed from the number recorded on child health booklets. During support visits, healthcare workers (HCWs) reported that they were more likely to enter data on the booklets than on the registers, in part because the booklets were also used as a health assessment checklist and partly because the children's caregivers liked the booklets. Even so, about a quarter of all the children missed HIV testing information and a fifth were recorded as not tested. We did not capture information on reasons why these children missed HIV testing data and various reasons are possible that could include poor documentation by HCWs. Reasons why some children were not tested could include refusal by caregivers and prior knowledge of a child's HIV status. Finally, we did not collect detailed information on symptom duration or severity and disease staging which could be used to develop algorithms for identifying children that are most likely to be HIV-infected. Despite these limitations, we were able to expand HIV testing across a range of pediatric health services and identify HIV-infected children that could be missed if existing testing practices were maintained. Lessons learned from this experience could be used for scaling up pediatric HIV testing in Zimbabwe.

In conclusion, the findings from this study support the integration of pediatric HIV testing within a greater range of child health services to identify HIV-infected children who might be missed under current pediatric testing strategies. Further studies are recommended to evaluate cost-effective options of this strategy including the development of algorithms for identifying older children (more than 2 years of age) without HIV disease symptoms, who may be HIV-infected, and are to be targeted with HIV testing to make the strategy more cost-effective. Expansion of pediatric testing, however, will require better commodity forecasting to ensure availability of test kits and other supplies, training of more HCWs on how to test children and supportive supervision to motivate HCWs to test and accurately record data. Wider use of the child health booklet in Zimbabwe is recommended as an integrated child health assessment checklist, longitudinal child health record, and integrated data collection tool.

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The authors acknowledge the Zimbabwe Ministry of Health and Child Care and partners who collaborated with EGPAF in the implementation of the program; the health care workers who provided HIV testing services to the children and recorded the data in the registers and child health booklets; the University of California, San Francisco's International Traineeships in AIDS Prevention Studies (ITAPS).

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HIV testing and counseling; pediatric HIV; PMTCT; children; Zimbabwe; Africa

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