Text Message Reminder–Recall to Increase HPV Immunization in Young HIV-1-Infected Patients

Abstract

HIV infected patients have higher rates of HPV infection, worse disease progression, increase severity of disease, and are at higher risk for intraepithelial neoplasia and cancer than their HIV negative counterparts. We conducted a yearlong pilot project to evaluate the impact of text message HPV immunization reminder-recall in young HIV-1 positive patients in a large urban academic HIV clinic. We found that text message reminder-recall improved HPV immunization uptake in a young, primarily black and un- or under-insured HIV-1 infected patients. As communication by texting is characteristic of teens and young adults in the general population, text message reminder-recalls should be considered a viable option to improve vaccination rates among young HIV patients.

Introduction

Human papilloma virus (HPV) is the causative agent for genital warts, recurrent respiratory papillomatosis, oropharyngeal cancer, and cervical and anal dysplasia as well as cancer. ¹ The HPV is the most common sexually transmitted infection in the United States and worldwide; it is estimated that 79 million Americans are currently infected with HPV. ^2,3 The HPV rates are higher in HIV-infected patients, with a 66% estimated prevalence in HIV-positive women and 90% in HIV-positive men who have sex with men (MSM). ^4,5 With increased immunosuppression, HIV-infected patients coinfected with HPV have worse HPV progression, with more severe genital warts, more anal and cervical dysplasia, and are at higher risk for intraepithelial neoplasia and cancer. ^{4,6 -9} In 1993, cervical carcinoma was added to the Centers for Disease Control surveillance definition for AIDS because of its frequency among HIV-infected women. Even with antiretroviral therapy (ART), HIV-infected patients have 2-fold higher risk of anal cancer than HIV-uninfected patients. ¹⁰ HIV-positive MSM are 60 times more likely to develop anal cancer than an HIV-negative individual. In addition, HIV-infected patients are often infected with multiple HPV subtypes. ¹¹

Immunization reminder–recall systems have been utilized to identify patients who are due or past due for recommended immunizations and have been shown to both improve vaccination coverage and be cost-effective in the outpatient setting. ^12,13 A recent survey found that 98% of Americans aged 18 to 29 and 78% of teens aged 12 to 17 have a cell phone. ¹⁴ Overall, 75% of all teens text, and 63% say they exchange text messages every day with people in their lives, which surpasses their frequency of communication by cell phone or landline phones, face-to-face contact outside school, social networking, instant messaging, and e-mailing. ¹⁵ Text message and e-mail reminder–recall systems have been used successfully in younger populations to increase interventions and prevention of sexually transmitted diseases.

We conducted a pilot study to evaluate the feasibility and efficacy of text and e-mail reminder–recalls in an urban HIV-infected adolescent and young adult population eligible to receive HPV vaccination.

Methods

This prospective cohort study was conducted between July 2013 and June 2014 in an academic HIV outpatient clinic in Cincinnati, Ohio, USA. All HIV-1-infected patients aged 16 to 26 years were included in the final analysis, except for 15 individuals who died or moved away. Patients must have made at least 1 clinic visit in the previous academic year (July 1, 2012-July 1, 2013), to be considered part of the study. Monthly HPV immunization status was evaluated. Of the 11 clinic physicians, 1 physician utilized monthly text or e-mail message reminders exclusively; the intervention group and patients in the other physician panels received no text or e-mail reminder and served as the control group. As this was a pilot project, out-of-convenience patients were not randomized.

Cell phone numbers and e-mail addresses were obtained from the patient’s electronic medical record. All patients in the intervention group had a cell phone and could receive text messages; cell phone numbers were verified at each clinical encounter. Patients in the intervention group who had not yet completed the 3-dose HPV vaccine series were sent monthly text messages until they received all 3 doses. Text messages did not include any personal health identifying information but simply reminded the patients they were due for an immunization and to schedule a nurse appointment. Although the e-mail addresses were collected, no e-mail was exchanged as it was planned for use only if the patient did not return to clinic or if they preferred e-mail communication. No patients preferred e-mail communication. Every 3 months each pair of physician and primary nurse received an updated list of those eligible for HPV vaccination. They also received a deidentified list that indicated their vaccine completion rate in comparison to the other physicians, as providers have been shown to change their clinical practice based on the feedback that they are different from their peers. ¹⁶

The primary outcome of this study was receipt of ≥1 and all 3 HPV vaccinations at 6 and 12 months. We collected immunization data, age, and gender from the electronic medical record. The χ² test was used to evaluate the differences between the intervention and control groups with regard to receipt of ≥1 and all 3 HPV vaccinations. Multivariable logistic regression was used to assess the impact of age, gender, and race/ethnicity. This study received institutional review board approval from the University of Utah.

Results

A total of 255 patients aged 16 to 26 years were seen in our clinic from July 1, 2013, to June 30, 2014, with 28 in the intervention group and 212 controls; 15 patients were excluded from the final analysis as they either moved or died during the study period. Patients in the intervention group were more likely to be black and uninsured compared to the control group (Table 1).

Table 1.

Characteristics of Intervention and Control Groups.

	Intervention, mean (SD) or No. (%)	Control, Mean ± SD or No. (%)	P Value
Age, years	22.8 ± 2.6	23.5 ± 1.9	<.05
Sex			.61
Female	7 (25)	41 (19)
Male	21 (75)	171 (81)
Race			.06
Black	23 (82)	128 (60)
White	5 (18)	69 (33)
Other	0	15 (7)
Insurance			.427
Uninsured	17 (61)	103 (49)
Medicaid	7 (25)	60 (28)
Private	4 (14)	49 (23)

Abbreviation: SD, standard deviation.

More patients who were sent a monthly text or e-mail message received ≥1 HPV immunization than controls, at both time points—60.9% versus 19.4% (41.5% difference, P < .05) at 6 months and 89.3% versus 32.1% (57.2% difference, P < .05) at 12 months (see Figure 1). Similarly, more patients completed the 3-dose HPV series in the intervention group than control, at both time points—13% versus 4.3% at 6 months (8.7% difference, P =. 107) and 32.1% versus 9.4% at 12 months (22.7% difference, P < .05)

Figure 1.

Percentages of patients receiving HPV vaccination at time 0, 6, and 12 months.

Multivariate analysis that controlled for age, sex, race/ethnicity, and insurance status found only intervention status to be significantly associated with receipt of at least 1 HPV vaccine at 6 months—AOR (adjusted odds ratio) 5.1 (95% confidence interval [CI]: 2.0-13.0) and 12 months—AOR 12.6 (95% CI: 3.6-42.9).

Discussion

The HPV vaccination has proven benefits in the HIV-uninfected population and because HPV coinfection is common among young persons with HIV, it is especially important to confer these benefits to this population. Although HIV-infected patients are often already infected with HPV at the time they acquire HIV, they may not be infected with the oncogenic types targeted by the HPV vaccine. In 2 large studies of HIV-infected women, HPV type 16 was found in 30%, HPV type 18 varied from 12% to 19% among the 3 countries studied, and infection with all 4-vaccine strains was <3%. ^17,18 In HIV-infected men, infection rates of 50% and 23% were found for types 16 and 18, respectively. ¹⁹ The quadrivalent HPV vaccination was immunogenic in a study of HIV-infected women although those with HIV RNA >10 000 copies/mL and/or CD4 counts <200 cells/mm³ had lower rates of seroconversion. ²⁰

This pilot quality improvement effort demonstrated the efficacy of text message reminders in HIV-infected teens and young adults. Patients who received text messages were significantly more likely to receive ≥1 or all 3 HPV vaccinations. All of these young patients were able to receive text messages and had an e-mail address prior to the intervention. A common barrier in contacting patients via texting in a low-income and sometimes transient population has been the inability to contact patients due to frequently changing cell phone numbers and other contact information, so e-mail was used as a backup means of communication.

A limitation to this study is the small patient population as this was a pilot study. We did not assess the acceptability among our patients nor what time of day is most acceptable to receive text messages from our clinic. Larger-scale implementation of text message reminder–recall for immunizations will need to include input from the patients with regard to acceptability, time messages delivered, and the cost to each patient especially those with limited data plans. Another limitation is that although many of the providers exchanged text and e-mail messages with their patients in this clinical setting, out of convenience only 1 provider was selected to use text messaging reminders exclusively.

Text messaging could be a highly useful tool to keep HIV-infected adolescents and young adults engaged in care, reminding them not only of immunizations that are due but also of clinic appointments and other key health-related information. Few large randomized controlled studies from Kenya, India, and Guatemala have demonstrated text messaging improved ART adherence and viral load suppression, and our study is the first to describe text messaging in the context of immunization in this population. ^{21 -24} Text messaging could allow for quicker interventions and improve patient outcomes. Electronic medical records have become the standard in the United States and some are capable of linking with text message platforms or have their own mobile app, allowing provider to have another tool to efficiently communicate with an adolescent and young adult population and to improve outcomes in this vulnerable group.