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ORIGINAL RESEARCH

Evaluation of antiretroviral-related errors and interventions by the clinical pharmacist in hospitalized HIV-infected patients

E Carcelero,1 M Tuset,1 M Martin,1 E De Lazzari,2 C Codina,1 J Miró3 and JM Gatell3

1Department of Pharmacy, Hospital Clinic, Barcelona, Spain, 2Biostatistic Unit, Hospital Clinic, Barcelona, Spain and 3Department of Infectious Diseases, Hospital Clinic, Barcelona, Spain

Objectives The aim of the study was to identify antiretroviral-related errors in the prescribing of medication to HIV-infected inpatients and to ascertain the degree of acceptance of the pharmacist’s interventions.

Methods An observational, prospective, 1-year study was conducted in a 750-bed tertiary-care teaching hospital by a pharmacist trained in HIV pharmacotherapy. Interactions with antiretrovirals were checked for contraindicated combinations. Inpatient antiretroviral prescriptions were compared with outpatient dispensing records for reconciliation. Renal and hepatic function was monitored to determine the need for dose adjustments.

Results The prescriptions for 247 admissions (189 patients) were reviewed. Sixty antiretroviral-related problems were identified in 41 patients (21.7%). The most common problem was contraindicated combinations (n 5 20; 33.3%), followed by incorrect dose (n 5 10; 16.7%), dose omission (n 5 9; 15%), lack of dosage reduction in patients with renal or hepatic impairment (n 5 6; 10% and n 5 1; 1.7%, respectively), omission of an antiretroviral (n 5 6; 10%), addition of an alternative antiretroviral (n 5 5; 8.3%) and incorrect schedule according to outpatient treatment (n 5 3; 5%). Fifteen out of 20 errors were made during admission. A multivariate analysis showed that factors associated with an increased risk of antiretroviral-related problems included renal impairment [odds ratio (OR) 3.95; 95% confidence interval (CI) 1.39–11.23], treatment with atazanavir (OR 3.53; 95% CI 1.61–7.76) and admission to a unit other than an infectious diseases unit (OR 2.50; 95% CI 1.28– 4.88). Use of a nonnucleoside reverse transcriptase inhibitor was a protective factor (OR 0.33; 95% CI 0.13–0.81). Ninety-two per cent of the pharmacist’s interventions were accepted.

Conclusion Antiretroviral-related errors affected more than one-in-five patients. The most common causes of error were contraindicated or not recommended drug–drug combinations and dose-related errors. A clinical pharmacist trained in HIV pharmacotherapy could help to detect errors and reduce the duration of their effect.

Keywords: antiretroviral agents, drug interactions, hospital, medication errors, pharmacy service

Accepted 4 January 2011

Background

Previous studies suggest that patients receiving long-term medication are at risk of accidental prescription errors on admission to hospital [1,2]. HIV-infected patients receiving

highly active antiretroviral therapy (HAART) are at substantial risk of antiretroviral medication errors during hospitalization, because of the complexity of HAART regimens and the possibility of drug–drug interactions (which can place patients at risk of toxicity or drug resistance) [3]. These errors may not have been resolved when patients are discharged. When part of the antire- troviral regimen is missed or antiretroviral levels are low as

Correspondence: Esther Carcelero, Department of Pharmacy, Hospital Clinic, Villarroel, 170 escalera 8, Sótano 08036, Barcelona, Spain. Tel: 1 34 932275479; fax: 1 34 932275457; e-mail: [email protected], [email protected]

DOI: 10.1111/j.1468-1293.2011.00915.x HIV Medicine (2011), 12, 494–499 r 2011 British HIV Association

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a result of interactions or dosage errors, the virus can replicate and resistance to treatment can appear. In contrast, toxicity can occur when an interaction leads to increased antiretroviral concentrations or the patient receives a higher dose than the correct one. Resistance or toxicity is more likely to occur when the error is extended in time or when the error has not been resolved before the patient’s discharge.

Some authors have confirmed that HAART-related errors are common in hospitalized patients and that admission of an HIV-infected patient by a physician not specialized in infectious diseases could be a risk factor for drug-related problems [4].

The aims of this study were to identify and describe HAART-related errors in medication prescribed to HIV- infected patients admitted to a tertiary teaching hospital and to determine the degree of acceptance of the pharmacist’s interventions.

Methods

We conducted an observational, prospective, 1-year study (between 1 January and 31 December 2007). Twice a week (on Tuesday and Thursday), a pharmacy resident trained in HIV pharmacotherapy and supported by a staff infectious diseases pharmacist identified patients aged at least 18 years who had been admitted to the Hospital Clinic (a 750- bed tertiary teaching hospital in Barcelona, Spain) and prescribed HAART.

A list was made of all inpatients who were prescribed antiretroviral drugs. Admissions made on Fridays, at weekends and on Mondays were recorded on Tuesday afternoon. Admissions made on Tuesdays, Wednesdays and Thursdays were recorded on Thursday afternoon.

The following data were recorded for all patients: age, gender, risk factors for HIV infection, admitting service, serum creatinine level and liver function (serum albumin, total bilirubin, transaminases, and international normal- ized ratio). For those patients with an altered creatinine value (41.2 mg/dL), the glomerular filtration rate was calculated using the Cockcroft–Gault equation [5]. For those patients with any abnormal liver function test result, the admission report was checked to determine whether they had cirrhosis, in which case the Child–Pugh score [6,7] was also recorded. Concomitant medication was reviewed twice weekly to check for drug–drug interactions.

HAART errors were classified as follows: contraindicated or not recommended drug–drug combinations, incorrect or incomplete antiretroviral regimen, omitted dose, incorrect dose (not matching the outpatient prescription), lack of dose reduction for renal or hepatic impairment and incorrect schedule [8].

In Spain, HIV-infected patients pick up their antiretro- viral medication in the outpatient pharmacy unit of the hospital that they attend for care. Therefore, it was easy for us to determine the patient’s HAART regimen. In our hospital, pharmacists dispensing medication to HIV- infected patients have access to an internal database containing the medical records of all HIV-infected outpatients followed at our hospital HIV clinic. Both this database and pharmacy dispensing records were checked to identify discrepancies. The inpatient regimen was consid- ered correct if it matched the outpatient regimen. For those patients not followed at the hospital HIV clinic, admission data were also checked to rule out transcription errors.

Drug–drug interactions were checked for contraindicated or not recommended combinations using national and international HIV websites [9–11]. If an error or interaction was detected, the pharmacist phoned the attending physician or nurse or added a footnote with a recommen- dation to the computerized prescription, so that the attending physician could see it the following day. The acceptance of the pharmacist’s recommendations was also reviewed during the following days. If the error was not corrected within 48 h of the recommendation, the prescrip- tion was classed as not accepted.

Data were entered into an ACCESS 2.0 database (Microsoft Corp., Redmond, WA, USA).

Statistical analysis

For the descriptive analysis, qualitative variables were expressed as percentages and frequencies; quantitative variables were expressed as the mean (standard deviation [SD]). Fisher’s exact test was used to analyse contingency tables. Odds ratios (ORs) for risk factors associated with HAART-related problems were analysed using a general- ized estimating equation model. This multivariate model takes into account the correlation between different admissions belonging to the same patient.

The statistical analysis was performed using STATA (StataCorp. 2007, Stata Statistical Software, Release 10; Stata Corporation, College Station, TX, USA).

Results

Over a 1-year period, we reviewed the prescriptions for 247 admissions of 189 HIV-infected patients who received antiretroviral therapy. Forty-one patients were admitted more than once during the study period. Table 1 summarizes the demographic characteristics of these patients. The distribution of admissions by service was as follows: infectious diseases unit, 135 (54.7%); other medical units, 58 (23.5%); surgery services, 38 (15.4%);

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intensive care units, nine (3.6%); and units with surgical and nonsurgical patients, seven (2.8%).

A total of 60 antiretroviral drug-related problems were identified in 41 patients (21.7% of the admitted patients had at least one antiretroviral problem).

The types of HAART-related errors found are shown in Table 2. The most common was drug–drug interaction (33.3%), not only between antiretroviral agents, but also between antiretrovirals and other drugs. Atazanavir was the drug most commonly involved in interactions. The second most common problem was incorrect dose (16.7%), and the third most common was dose omission (15%), followed by lack of dosage reduction in patients with renal

or hepatic impairment (11.7%), omission of one or more antiretroviral medications (10%), addition of an alternative antiretroviral drug (8.3%) and incorrect schedule according to outpatient treatment (5%). Table 3 provides the antiretroviral prescribing errors detected in this study.

Almost all the antiretroviral-related errors occurred at admission (15; 75%). The error occurred in the HIV clinic in only five cases and was not resolved on admission (four cases of lack of dosage reduction in patients with renal impairment; one case of a contraindicated interaction).

Of 112 admissions to services other than infectious diseases in which antiretroviral agents had been prescribed, 39 had at least one antiretroviral drug-related error (34.8%), compared with 21 out of 135 admissions in the infectious diseases unit (15.6%).

In the multivariate analysis, the factors associated with an increased risk of HAART-related problems (Table 4) were renal impairment [OR 3.95; 95% confidence interval (CI) 1.39–11.23], treatment with atazanavir (OR 3.53; 95% CI 1.61–7.76) and admission to a unit other than an infectious diseases unit (OR 2.50; 95% CI 1.28–4.88). Prescription of a nonnucleoside reverse transcriptase inhibitor was a protective factor (OR 0.33; 95% CI 0.13– 0.81). No statistical relationship was found between HAART-related problems and the following factors: age, sex, risk group, liver impairment, nucleoside reverse transcriptase inhibitor-based HAART, a protease inhibitor other than atazanavir, and being treated with an anti- retroviral with different presentations.

The most common intervention by the pharmacist was a footnote on the prescription (45 of 60; 75%), followed by a telephone call to the attending physician (22 of 60; 36.7%) or nurse (6 of 60; 10%).

The pharmacist made an intervention in all of the 60 errors detected. This was well accepted in most cases (55 of 60; 91.7%), and the error was resolved. Five interventions were not accepted (8.3%): lack of dosage reduction in patients with renal impairment (three cases), lack of efavirenz dosage reduction in a patient with hepatic impairment (one case), and a contraindicated combination (atazanavir and omeprazole; one case).

Discussion

There is evidence that antiretroviral errors are common during hospital admission. Mok et al. [4] prospectively reviewed the medical records of 83 HIV-infected patients who received antiretroviral therapy for 20 months and identified a total of 176 drug-related problems in 71 patients (86% of the patients had at least one problem associated with their antiretroviral regimen). Over 4 months, Pastakia et al. [12] prospectively evaluated

Table 1 Demographic characteristics of hospitalized patients receiving antiretroviral therapy (n 5 189)

Variable

HAART-related errors

P-valueYes No

Male [n (%)] 34 (25.2) 101 (74.8) 0.174* Female [n (%)] 7 (12.9) 47 (87.0) Age (years) 47 � 11w 45 � 10w 0.230z Risk group [n (%)]§

Injecting drug use 16 (21.9) 57 (78.1) 0.462*

Heterosexual 11 (24.4) 34 (75.6) Homosexual 9 (18) 41 (82) Other 3 (42.9) 4 (57.1)

HAART, highly active antiretroviral therapy. *Fisher’s exact test. wMean (standard deviation). zt-test. §n 5 175.

Table 2 Types of highly active antiretroviral therapy (HAART)-related error

Type of error

Number of patients* (n 5 41)

% of all errors (n 5 60)

Contraindicated or not recommended drug–drug combinations

20 33.3

Incorrect dose (not matching outpatient prescription)

10 16.7

Higher dose 5 Lower dose 5

Dose omission (antiretroviral marketed in different doses; dose at prescription was omitted)

9 15

Lack of dose reduction in patients with renal or hepatic impairment

7 11.7

Renal impairment 6 Hepatic impairment 1

Omission of one or more antiretroviral drugs 6 10 Prescription of alternative antiretroviral drugs 5 8.3 Incorrect schedule according to outpatient treatment and/or current guidelines

3 5

*A patient could have more than one type of HAART-related error.

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antiretroviral prescribing errors in 68 hospitalized HIV- infected patients and found that there was at least one error in 72% of cases; in 56% of cases, the error had the potential to cause moderate to severe discomfort or clinical impairment. In a retrospective study, Purdy et al. [13] identified 108 clinically significant prescribing errors involving antiretrovirals during a 34-month study period in hospitalized HIV-infected patients. Overall, errors occurred in 5.8% of inpatients prescribed antiretroviral medication. Rastegar et al. [14] retrospectively identified 61 antiretroviral errors in 54 admissions (percentage of total admissions, 25.8%) over a 1-year period. In a 6-month study, Heelon et al. [3] found 73 HAART errors in 41 patients (21% of hospitalized patients with HIV infection), most of which were the result of incomplete regimens. In our study, 21.7% of HIV-infected patients admitted and prescribed antiretroviral therapy had at least one prescrip- tion-related problem. These results are similar to those of Rastegar et al. and Heelon et al. The most commonly observed problems are inappropriate dosage and drug– drug interactions. Mok et al. [4] found that, among 251 prescriptions for antiretroviral agents, the dosage was

Table 3 Antiretroviral prescribing errors detected in this study

Type of error Description

Contraindicated combination (n 5 20)

Patients were prescribed omeprazole while receiving atazanavir (n 5 18) A patient treated with efavirenz began voriconazole (no dose adjustment data from pharmacokinetic studies were available at the time) (n 5 1) A patient treated with lopinavir/ritonavir was prescribed rifampicin (n 5 1)

Incorrect dose of an antiretroviral agent (n 5 10)

A patient was prescribed nevirapine 200 mg qd when his current regimen was 400 mg qd (n 5 1) A patient was prescribed ritonavir 200 mg instead of 100 mg (n 5 1) Patients were prescribed ritonavir 100 mg bid instead of 100 mg qd (n 5 2) A patient was prescribed saquinavir 200 mg tid. His current regimen was 1500 mg qd (n 5 1) A patient with renal impairment was prescribed abacavir 150 mg/day (one-quarter of a tablet bid). He was receiving one tablet of abacavir 300 mg bid (600 mg/ day), as the dosage of abacavir does not need to be adjusted in renal impairment (n 5 1) A patient with renal impairment was prescribed lamivudine 50 mg qd. His current regimen was 25 mg (n 5 1) A patient was prescribed 1 capsule of atazanavir qd. His current dose was 2 capsules qd (n 5 1) A patient was prescribed atazanavir 200 mg bid. His current dose was 300 mg/day (n 5 1) A patient was prescribed efavirenz 200 mg qd instead of 600 mg qd (n 5 1)

Lack of dose reduction in patients with renal or hepatic impairment (n 5 7)

A patient with hepatic cirrhosis Child C was prescribed efavirenz 600 mg qd. Efavirenz is contraindicated in Child C patients (risk of toxicity). Plasma concentrations were not determined (n 5 1) A patient was prescribed didanosine 400 mg qd. His current dose was 125 mg qd (he was undergoing dialysis) (n 5 1) A patient was prescribed lamivudine 300 mg qd. His current dose was 25 mg qd (he was undergoing dialysis) (n 5 1) A patient was prescribed lamivudine 300 mg qd. He had renal impairment and the correct dose adjusted to renal function was 150 mg (n 5 1) A patient was prescribed stavudine 30 mg bid. The correct dose adjusted to renal function was 20 mg bid (n 5 1) A patient was prescribed abacavir 600 mg 1 lamivudine 300 mg. His serum creatinine was 2.6 mg/dL (n 5 1) A patient was prescribed lamivudine 50 mg qd. His current dose was 25 mg qd (he was undergoing dialysis) (n 5 1)

Antiretroviral dose omitted (n 5 9)

Patients were prescribed atazanavir 2 capsules qd. The dose was not specified (n 5 2) Patients receiving didanosine as outpatient treatment were prescribed didanosine 1 capsule qd and the dose was not indicated (n 5 2) Patients were prescribed lamivudine 1 tablet qd (the dose was not specified) (n 5 3) Patients were prescribed stavudine 1 capsule bid (the dose was not specified) (n 5 2)

One or more antiretrovirals omitted (n 5 6)

A patient was prescribed ritonavir 100 mg bid but not tipranavir, which was the current protease inhibitor (boosted by ritonavir) (n 5 1)

Table 3 (Contd.)

Type of error Description

A patient was prescribed ritonavir 100 mg bid but not fosamprenavir, which was the current protease inhibitor (boosted by ritonavir) (n 5 1) A patient whose current regimen was stavudine, didanosine, darunavir and ritonavir was not prescribed stavudine (n 5 1) A patient whose current regimen was tenofovir, nevirapine, atazanavir and ritonavir was not prescribed atazanavir (n 5 1) Patients were prescribed only part of their current regimens. Emtricitabine 200 g 1 tenofovir 300 mg was missing (n 5 2)

Prescription of an antiretroviral that was not part of the patient’s current regimen (n 5 5)

Patients were prescribed ritonavir 100 mg instead of lamivudine (n 5 2) A patient was prescribed his current antiretroviral regimen and efavirenz, which did not belong to his chronic treatment schedule (n 5 1) A patient was prescribed amprenavir instead of tipranavir (n 5 1) A patient was prescribed zidovudine bid instead of zidovudine 1 lamivudine (n 5 1)

Incorrect schedule (n 5 3)

A patient treated with atazanavir was prescribed one capsule at breakfast and the other at dinner instead of both capsules at the same time (n 5 1) A patient was prescribed 2 tablets of abacavir 1 lamivudine 1 zidovudine at breakfast instead of 1 tablet bid (n 5 1) A patient treated with atazanavir and ritonavir was prescribed atazanavir at breakfast and ritonavir at dinner instead of both drugs at the same time (n 5 1)

bid, twice daily; qd, once daily; tid, three times a day.

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inappropriate in 57 cases (37 excessive and 20 insufficient), accounting for 32.4% of all detected problems. The lack of an adjustment for renal insufficiency was also considered an excessive dosage; this happened on 19 occasions. Forty- six drug–drug interactions were identified (26.1% of all detected problems); 36 of the 83 patients included in the review (43.4%) had an incomplete antiretroviral regimen (20.4% of all problems detected). Dosage error was also the most common type of error detected by Rastegar et al. [14] (34 admissions; 16.3%); 18 of these errors were inap- propriate dosage adjustment in patients with renal insufficiency. The next most common error was contra- indicated combinations (12 admissions; 5.2%), followed by receiving two or fewer antiretroviral agents (eight cases; 3.8%). In seven admissions (3.3%) there was an unex- plained delay in continuing HAART. Gray et al. [15] analysed the causes of HIV medication errors in MED- MARX, a voluntary database reporting inpatient medica- tion errors. They found that the most common causes of error were inappropriate dosing (38%), followed by incorrect medication (32%). In our study, interactions caused by contraindicated or not recommended drug–drug combinations (33.3%) were slightly higher than in the study by Mok et al. [4]. We found that, in total, dose-related problems (incorrect dose, dose omission, and lack of dose adjustment in patients with renal or hepatic impairment) accounted for 43.3% of all errors. This result is comparable to those of Mok et al. [4] and Gray et al. [15]

Risk factors associated with a HAART-related error in our study were similar to those found by Mok et al. [4]: renal impairment, an atazanavir-containing regimen, and admission by a service other than the infectious diseases service. We also found that receiving a nonnucleo- side reverse transcriptase inhibitor was a protective factor.

There is abundant evidence that antiretroviral drug- related errors on admission are frequent and may be of clinical relevance. Clinical pharmacists with training in HIV pharmacotherapy can play an important role in correcting such errors. They should closely monitor prescriptions to identify problems and resolve them as soon as possible in order to prevent toxicity or drug resistance. Our results show that the pharmacist’s recom- mendations were frequently accepted.

This study has several limitations. First, hospitalized patients prescribed an antiretroviral were only followed twice a week. Admissions made on Fridays, at weekends, and on Mondays were recorded on Tuesday afternoon, so some patients could have been missed if they were admitted and discharged between our monitoring dates. Secondly, the method used did not allow us to detect errors of complete HAART omission during hospitalization. Delays in continu- ing the outpatient regimen were not detected either. Thirdly, we did not assess dispensing or administration errors, or the clinical outcomes of our interventions (prevention of drug toxicity or drug resistance). These limitations mean that it is difficult to make generalizations based on our results. Finally, the current recommendations for atazanavir in combination with proton pump inhibitors differ from those available when the study was performed: atazanavir can be used with proton pump inhibitors at present, although only at low doses in treatment-naı̈ve patients. Most of the patients admitted during the study period were treatment- experienced.

Conclusion

Errors in, or problems with, the HAART regimen were common among HIV-infected hospitalized patients pre- scribed antiretroviral agents (approximately one-in-five patients). The most common issues were contraindicated or not recommended drug–drug combinations and dose- related errors. Factors associated with an increased risk of such problems were renal impairment, receiving atazana- vir, and admission to a unit other than an infectious diseases unit. Receiving nonnucleoside reverse transcrip- tase inhibitors was a protective factor.

Clinical pharmacists trained in HIV pharmacotherapy could help to detect errors and reduce the duration of their effects, thus improving the quality of prescription in hospitalized HIV-infected patients.

Acknowledgements

We are grateful to Kenneth Lawrence (Tufts Medical Center, Boston, MA) for useful suggestions and to Thomas O’Boyle for editorial assistance.

Table 4 Adjusted odds ratios for risk factors associated with a highly active antiretroviral therapy (HAART)-related error (245 episodes)

Variable Adjusted odds ratio 95% CI P-value

Renal impairment No 1 0.010 Yes 3.950 (1.390–11.228)

NNRTI No 1 0.015 Yes 0.329 (0.134–0.805)

Atazanavir No 1 0.002 Yes 3.532 (1.608–7.756)

Service Infectious diseases 1 0.007 Other 2.504 (1.285–4.881)

CI, confidence interval; NNRTI, nonnucleoside reverse transcriptase inhibitor.

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