Abstract
Introduction
Being allergic to penicillin can lead to the overuse of broad-spectrum antibiotics, contributing to the growing problem of multidrug resistance. Knowing the exact allergy history is essential as some circumstances may allow reinitiating penicillin. This study focused on assessing the prevalence and characteristics of self-reported penicillin allergy in the Saudi Arabian population.
Methods
We conducted a nationwide cross-sectional study via an electronic self-administered questionnaire directed toward the Saudi Arabian general adult population. Variables about respondent demographics as well as type and characteristics of the allergy were collected.
Results
One hundred ninety-three out of 2022 participants who completed the survey (9.5%) reported allergy to penicillin, with the most reported reaction being anaphylaxis in 89 participants (46.1%), non-anaphylaxis reported by 69 participants (35.8%). Twenty-two participants (11.4%) were identified as not having a true allergy due to reporting a tolerability issue or a non-penicillin-type agent. About 38% reported that the allergy occurred more than ten years ago.
Conclusion
This is the first study to report the prevalence and characteristics of self-reported penicillin allergy in Saudi Arabia. The data from this study provides valuable information to consider starting in-hospital penicillin de-labeling programs and providing evidence for healthcare providers to consider re-challenging certain qualified patients.
Keywords: Penicillin allergy, Allergy prevalence, True allergy, Anaphylaxis
1. Introduction
Penicillin belongs to a large group of antibiotics called beta-lactams which are widely used to treat various types of bacterial infections (Bhattacharya, 2010). Hypersensitivity reactions to beta-lactams, specifically penicillin, remain the most common drug allergy nowadays. About 10% of patients report having a penicillin allergy; nevertheless, up to 90% do not have a true IgE-mediated allergic reaction (Sogn et al., 1992, Gadde et al., 1993). Symptoms of a penicillin allergic reaction vary with the most commonly reported to be swelling/angioedema, rash, hives, and anaphylaxis (Albin and Agarwal, 2014). Female gender, elderly, and increased use of antibiotics are the primary factors predisposing a patient to high rates of antibiotic allergy (Macy and Poon, 2009).
Several studies have reported a lack of proper penicillin allergy documentation, including the presence of misdiagnosed or mislabeled information (Shah et al., 2016). Poor beta-lactam allergy documentation without determining the specific allergen or the characteristics of the allergic reaction may lead to beta-lactam avoidance which may adversely impact the effectiveness of patient care (Shah et al., 2016). Accurate documentation is also necessary to differentiate allergy from intolerance or adverse effects (Kufel et al.,2019). Among primary issues with carrying a label of penicillin allergy is that patients and clinicians are often unaware that penicillin allergies may fade over time (Kufel et al.,2019).
The issues mentioned above may lead to the use of a broader spectrum, less effective antibiotic with a narrower safety profile compared to penicillin like fluoroquinolones, vancomycin, and macrolides (Blumenthal et al., 2018). This can contribute to the growing problem of antimicrobial resistance in Saudi Arabia (Zowawi, 2016, Shibl et al., 2014, Al-Obeid et al., 2015).
To date, few research has been dedicated towards examining the characteristics of penicillin allergies amongst different patient populations (Albin and Agarwal, 2014). To our knowledge, there are no published studies documenting those details in a Saudi Arabian population. Therefore, this study aimed to determine the prevalence and characteristics of self-reported penicillin allergy in the Saudi Arabian population.
2. Material and methods
2.1. Study design
A nationwide cross-sectional electronic self-administered questionnaire was randomly distributed in January 2022 via social media platforms targeting the Saudi Arabian general population who were 18 years or older residing in Saudi Arabia.
The questionnaire was built based on reviewing the literature to understand the aspects that need to be covered. The questionnaire was later reviewed by three experts and tested on a small sample of 10 participants prior to it being distributed. After pilot testing, we took the participants' feedback, and minor wording changes were made to simplify the questions for the recipients.
2.2. Sample size
The estimated Saudi Arabian population is 34 million. Using a single population proportion formula, considering a 95% confidence interval and 5% precision, the sample size required equals 384. By rounding to the nearest 100, a minimum of 400 responses was targeted.
2.3. Data analysis
Data management, visualizing data, and statistical analysis were carried out using SAS statistical software (version 9.4, SAS Institute, Cary, NC). Descriptive analyses based on the frequency and percentage distributions were conducted for all variables, including the baseline demographics of all respondents to the questionnaire and all the answers of participants who indicated having a penicillin allergy. A Chi-square test was performed to evaluate group differences for demographic variables between participants who reported having penicillin allergy versus no penicillin allergy. We further test these differences in inferential crude and adjusted logistic regression models. Statistical significance thresholds were set at significance level α = 0.05; all tests were 2-tailed.
2.4. Survey and outcomes
The study's primary outcome was the prevalence of self-reported penicillin allergy in the Saudi Arabian population. The secondary outcome was the characteristics of the allergy. These outcomes were targeted by including questions about prior exposure to a penicillin and the type of reaction that was experienced. To distinguish true allergy from side effects, we asked further questions stratifying different types of reaction manifestations, including how the allergy was dealt with and whether the participant was on any other medications were included. Other questions included whether the participant had undergone penicillin allergy skin testing or desensitization. Finally, questions regarding cephalosporin allergies, nasal allergies, and asthma were included in the questionnaire, along with demographic questions.
Responses about the type of allergic reaction were categorized into three different groups: anaphylaxis, non-anaphylaxis, and not true allergy. Those who reported anaphylaxis or an allergic reaction accompanied with shortness of breath, tachycardia, or unconsciousness were added to the anaphylaxis group. If the reaction was rash or itching, then it would be added to the non-anaphylaxis group. Lastly, reports about intolerability such as nausea, vomiting, diarrhea, tachycardia, blurry vision, headache, fever, gastritis, oral thrush and pain, vaginitis, or wounds that are not accompanied by an allergic reaction or reporting a non-penicillin drug were classified as a not true allergy.
3. Results
3.1. Demographics
Two thousand and fifty-eight participants responded to the survey. A total of 2022 consented and completed the survey (98.25 %). Female participation accounted for 76.3% of the responses. Most responses were from the age groups of 18–24 years (34.2%) and 25–34 years (29.6%), and only 2.5% of the participants were 65 years or older. The central region accounted for most of the responses with a percentage of 68.6%, and about 57% were bachelor’s degree holders. Table 1 represents the baseline demographics of the participants.
Table 1.
Baseline demographics.
| Characteristics |
Entire Participants |
Penicillin Allergic |
Non-Penicillin Allergic |
P-value | |||
|---|---|---|---|---|---|---|---|
| No. | % | No. | % | No. | % | ||
| Total | 2,022 | 100 | 193 | 9.5 | 1,829 | 90.5 | |
| Age | |||||||
| 18–24 | 691 | 34.2 | 44 | 22.7 | 624 | 34.1 | 0.13 |
| 25–34 | 599 | 29.6 | 66 | 34.5 | 556 | 30.4 | |
| 35–44 | 296 | 14.6 | 35 | 18.0 | 261 | 14.3 | |
| 45–54 | 200 | 9.9 | 16 | 8.3 | 175 | 9.6 | |
| 55–64 | 185 | 9.2 | 25 | 12.9 | 169 | 9.3 | |
| 65 and older | 51 | 2.5 | 7 | 3.6 | 44 | 2.4 | |
| Gender | |||||||
| Female | 1,542 | 76.3 | 160 | 83.0 | 1,382 | 75.5 | 0.02* |
| Male | 480 | 23.7 | 33 | 17.0 | 447 | 24.5 | |
| Region | |||||||
| Central region | 1,387 | 68.6 | 121 | 62.4 | 1,266 | 69.3 | 0.18 |
| Eastern region | 163 | 8.1 | 22 | 11.3 | 141 | 7.7 | |
| Northern region | 55 | 2.7 | 6 | 3.1 | 81 | 4.4 | |
| Southern region | 94 | 4.7 | 13 | 6.7 | 49 | 2.7 | |
| Western region | 323 | 16.0 | 31 | 16.5 | 292 | 15.9 | |
| Education | |||||||
| Middle school or lower | 49 | 2.4 | 7 | 3.6 | 42 | 2.3 | 0.76 |
| High school | 379 | 18.7 | 34 | 17.5 | 345 | 18.9 | |
| Diploma | 181 | 9.0 | 15 | 7.7 | 166 | 9.1 | |
| Bachelor’s degree | 1,151 | 56.9 | 111 | 57.7 | 1,040 | 56.8 | |
| Postgraduate education | 262 | 13.0 | 26 | 13.4 | 236 | 12.9 | |
Means statistically significant.
3.2. Prevalence of penicillin allergy
One hundred ninety-three participants reported penicillin allergy, which suggests a proximate 9.5% penicillin allergy prevalence in Saudi Arabia. Using a logistic regression model, we tested the demographics of the respondents on the likelihood of reporting yes versus no to having a penicillin allergy. The logistic regression models revealed that females are 78% more likely than males to report having a penicillin allergy (Adjusted Odds Ratio [Adj-OR] 1.78; 95% Confidence Interval [CI], 1.18–2.68; P-vale, 0.01). On the other hand, respondents aged 18 to 24 are 64% less likely to report having a penicillin allergy than those aged 65 and older (OR, 0.36; 95% CI, 0.15–0.88; P-value, 0.03). (Table 2)
Table 2.
Logistic regression analysis for assessing reporting penicillin allergy among the Saudi Arabian Population.
|
Crude |
Adjusted |
|||
|---|---|---|---|---|
| OR (95% CI) | P-value | OR (95% CI) | P-value | |
| Age | ||||
| 18–24 | 0.50 (0.21–1.17) | 0.11 | 0.36 (0.15–0.88) | 0.03* |
| 25–34 | 0.68 (0.29–1.56) | 0.36 | 0.51 (0.21–1.23) | 0.14 |
| 35–44 | 0.84 (0.35–2.02) | 0.71 | 0.72 (0.30–1.78) | 0.48 |
| 45–54 | 0.60 (0.23–1.54) | 0.28 | 0.48 (0.18–1.27) | 0.14 |
| 55–64 | 0.90 (0.36–2.21) | 0.82 | 0.76 (0.30–1.90) | 0.56 |
| 65 and older | Ref. | Ref. | ||
| Gender | ||||
| Female | 1.58 (1.07–2.33) | 0.02* | 1.78 (1.18–2.68) | 0.01* |
| Male | Ref. | Ref. | ||
| Region | ||||
| Central region | 0.87 (0.58–1.31) | 0.51 | 0.85 (0.56–1.28) | 0.43 |
| Eastern region | 1.42 (0.79–2.53) | 0.24 | 1.41 (0.79–2.53) | 0.25 |
| Northern region | 1.11 (0.44–2.80) | 0.82 | 1.28 (0.51–3.25) | 0.61 |
| Southern region | 1.46 (0.73–2.91) | 0.28 | 1.62 (0.81–3.25) | 0.18 |
| Western region | Ref. | Ref. | ||
| Education | ||||
| Middle school or lower | 1.51 (0.62–3.71) | 0.37 | 1.15 (0.45–2.94) | 0.77 |
| High school | 0.90 (0.52–1.53) | 0.68 | 0.95 (0.53–1.69) | 0.85 |
| Diploma | 0.82 (0.42–1.60) | 0.56 | 0.85 (0.43–1.68) | 0.64 |
| Bachelor’s degree | 0.98 (0.62–1.53) | 0.92 | 1.00 (0.63–1.60) | 0.98 |
| postgraduate education | Ref. | Ref. | ||
Abbreviations: OR, odds ratio; CI, confidence interval.
Means statistically significant.
3.3. Characteristics of penicillin allergy
About two-thirds of participants reported a penicillin allergy that was identified by themselves. The remaining was informed by the physician or by their parents. Participants were asked how many years it had been since they experienced the allergic reaction, and 37.6% reported that they experienced it more than ten years ago. Only 69 participants (35.6%) had the allergy confirmed with a skin test. Among penicillin allergic participants, 19.6% reported an allergy to cephalosporins, approximately 47% reported a history of nasal allergy, and 15% had a history of asthma (Table 3).
Table 3.
Characteristics of penicillin allergy.
| Question | Frequency | % |
|---|---|---|
| How did you know about your penicillin allergy? | ||
| Noticed by the participant | 135 | 69.6 |
| Informed by a physician | 29 | 15.0 |
| Informed by parents | 28 | 14.4 |
| Do not remember | 1 | 0.5 |
| When did you experienced the allergic reaction to penicillin? | ||
| Less than 5 years | 63 | 32.5 |
| 5–10 years | 36 | 18.6 |
| More than 10 years | 73 | 37.6 |
| I don’t know | 21 | 11.3 |
| Time between exposure and allergic reaction | ||
| Less than 1 h | 71 | 36.6 |
| 1–24 h | 80 | 41.2 |
| Days to weeks | 18 | 9.3 |
| I don’t know | 24 | 12.9 |
| Were you taking new medications at the time of exposure to penicillin? | ||
| Yes | 20 | 10.4 |
| No | 135 | 69.9 |
| I don’t know | 38 | 19.7 |
| Was epinephrine or an antihistamine administered at the time of the allergy? | ||
| Yes | 62 | 32.0 |
| No | 81 | 42.3 |
| I don’t know | 50 | 25.8 |
| Have you done a penicillin skin allergy test? | ||
| Yes, and the allergy was confirmed with a skin test | 69 | 35.6 |
| Yes, and the allergy was denied with a skin test | 12 | 6.2 |
| No | 112 | 58.3 |
| Have you previously undergone penicillin desensitization? | ||
| Yes | 16 | 8.3 |
| No | 177 | 91.7 |
| Are you allergic to cephalosporins? | ||
| Yes | 38 | 19.6 |
| No | 156 | 80.4 |
| Do you have a nasal allergy? | ||
| Yes | 92 | 47.4 |
| No | 102 | 52.6 |
| Do you have asthma? | ||
| Yes | 29 | 15.0 |
| No | 165 | 85.1 |
When analyzing the data regarding the causative penicillin antibiotic, we found the top two reported causative antibiotics were penicillin 29.2% and amoxicillin/clavulanic acid 21.9%, followed by 17.88% of participants who reported that they do not know the name of the penicillin antibiotic (Fig. 1).
Fig. 1.
Frequency of reported allergic reaction to penicillin antibiotics. Note: Participants were able to choose more than one penicillin antibiotic.
After assessing the reported allergic reactions and reported antibiotics, twenty-two participants were identified to likely not have a true allergy. Of those, eleven had a tolerability issue rather than a true allergy, two reported a causative agent that is not a penicillin-type antibiotic, and three reported tolerability issue and a causative agent that is not a penicillin-type antibiotic. The drugs that responders misidentified as a penicillin-type antibiotics were vancomycin, cefuroxime, metronidazole, sulfa, and ibuprofen. However, four of those 22 participants reported that a skin test confirmed their allergy. A list of reported reactions to penicillin that are not true allergies is described in Table 4.
Table 4.
Type and frequency of reported not true allergy.
| Not true allergy | Frequency |
|---|---|
| Nausea and vomiting | 7 |
| Diarrhea | 7 |
| Headache | 3 |
| Fever | 3 |
| Tachycardia | 5 |
| Blurry vision | 1 |
| Gastritis | 1 |
| Oral pain and thrush | 1 |
| Vaginitis | 1 |
| Wounds | 1 |
The majority of responses (89 participants) had an anaphylactic reaction (46.1%), followed by non-anaphylactic reactions reported by 69 participants (35.8%) (Fig. 2). Of those who reported anaphylaxis, only 39 (43.82%) reported receiving epinephrine or an antihistamine injection. Moreover, among the 89 participants who reported an anaphylaxis reaction, 7 participants reported a negative penicillin skin test. Anaphylaxis was more frequently reported with penicillin 47 times and amoxicillin/clavulanate 30 times. Those aged between 25 and 34 were the most to report an anaphylactic reaction, followed by the 18 – 24 age group. In addition, the most frequently reported reaction in the non-anaphylaxis group was rash, which was reported by 53 participants, followed by itching, reported by 39 participants. The least reported reaction was swelling by 6 participants and was mainly reported as facial swelling (lips or eyes) (Fig. 3). Moreover, 5 of the 69 who reported a non-anaphylaxis reaction reported a negative penicillin skin test.
Fig. 2.
Classifications of reported reactions.
Fig. 3.
Types of reported non-anaphylactic allergic reaction. Note: Participants were able to choose more than one type of reaction.
4. Discussion
This cross-sectional study aimed to estimate the national prevalence of penicillin allergy in Saudi Arabia and to determine its characteristics. In the present study, we found that the prevalence of self-reported penicillin allergy among our population was 9.5%, and about half reported anaphylactic type reactions. In addition, we found that females are more likely to experience penicillin allergy than males in our population.
To the best of our knowledge, this is the first study to examine the prevalence and characteristics of penicillin allergy amongst the Saudi Arabian population. The prevalence of penicillin allergy in our study is within the range reported in previous studies with other populations in different settings (4.5%-12%) (Albin and Agarwal, 2014, Gomes et al., 2004, Kerr, 1994, Zhou et al., 2016). Higher rates of penicillin allergy have been reported in females and older ages, consistent with our findings (Albin and Agarwal, 2014, Macy and Poon, 2009, Zhou et al., 2016). In terms of comorbidities, nearly half of penicillin-allergic participants in this study had a history of nasal allergy (47.4%). Furthermore, our results showed a higher percentage of cephalosporin allergy (19.6%) among participants who reported penicillin allergy. In a retrospective study of patients with documented penicillin allergy, the percentage of patients who reported asthma or allergic rhinitis were 30.6% and 27.5%, respectively (Albin et al., 2014). In addition, they found that only a few patients (1.6%) had documented concomitant cephalosporin allergy (Albin et al., 2014).
Another important finding from this study is the percentage of participants who reported anaphylactic reaction to penicillin 89 (46.11%). This number is higher than what was previously reported as skin reaction was the most common manifestation in other studies (Kerr, 1994, Gomes et al., 2004, Albin and Agarwal, 2014). For example, in Albin et al. study, only 6.8% of patients had a history of documented anaphylaxis. This variation between our study and others might be attributed to the differences in the type of population, study design, and setting. However, when we looked closely at the participants who reported anaphylaxis, only 39 (20.2%) of them got epinephrine or antihistamine injection at the time of reaction. In addition, those who explicitly reported anaphylaxis were 33 (17%) participants and the remaining 56 participant where classified based on symptoms which reflects how they are usually assessed in real practice. This raises an important question regarding the accuracy of the reported number of anaphylaxis and participants’ understanding of the different types of allergic reactions.
Taking the full history, including the age at which the allergic reaction had manifested, is particularly important. In the present study, about one-third of participants reported that they experienced a penicillin-allergic reaction more than ten years ago. It has been proven that a considerable number of patients could potentially tolerate the use of penicillin safely after such time. About 80% of patients lose their penicillin sensitivity and may tolerate penicillin after ten years (Blanca et al., 1999). Efforts have been made to assess penicillin allergy status by taking a more detailed history from patients to differentiate tolerability issues from allergic reactions. In addition, performing penicillin allergy skin testing is considered the most helpful in detecting IgE-mediated reactions (Justo et al., 2019).
Our results showed that about 11.4% of participants were likely not to have a true penicillin allergy based on the reported reaction or the causative agents. Furthermore, of those who reported penicillin allergy, 12 participants reported receiving negative skin test results, yet they still identified themselves as penicillin allergic. Misdiagnoses of true penicillin allergy are common and associated with negative consequences due to avoidance of beta-lactam antibiotics. Blumenthal et al. study found that using second-line options of antibiotics like clindamycin, vancomycin, or gentamicin for surgical prophylaxis in patients with penicillin allergy was associated with increased odds of surgical site infection (Blumenthal et al., 2018). In another study, patients with methicillin-susceptible Staphylococcus aureus bacteremia who reported penicillin allergy and received vancomycin had the poorest outcomes in terms of rates of cure, recurrence, and adverse drug reactions in comparison with other groups who were treated with cefazolin (Blumenthal et al., 2015). Such studies serve as golden examples amplifying the importance of de-labeling allergies whenever possible. It has also been proven that patients with labeled penicillin allergy have a 5.5% longer hospital length of stay than non-allergic patients and a 28.4% higher antibiotic expenses rate (Powell et al., 2020). Therefore, de-labeling penicillin allergy will reduce expenses by using penicillin as a first choice, but more importantly, by minimizing hospitalization days (Powell et al., 2020).
Although this study is the first in our population, it is essential to interpret the results considering the limitations. The self-reporting of penicillin allergy may lead to an overestimation of its prevalence. This could be caused by the inability to differentiate intolerability versus allergy or confusing names of the causative agent. In addition, most of the participants were female, young, and from the central Saudi Arabian region, which could potentially put the results at risk for selection bias. Another factor that could increase the risk of selection bias is the online questionnaire distribution, which might draw more attention from those who experienced allergies than those who did not. However, we believe this study provides insight into our population's prevalence and characteristics of self-reported penicillin allergy. Further studies are needed to assess penicillin allergies via reviewing medical records to obtain accurate data about the causative agents and the experienced allergic reactions.
5. Conclusion
Knowing the prevalence and characteristics of self-reported penicillin allergy in Saudi Arabia can set the ground for starting an in-hospital penicillin de-labeling program to optimize the use of antibiotics, as well as encourage healthcare providers to re-challenge specific patients after obtaining an accurate history of the allergy.
Funding
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Ethical considerations
The Institutional Review Board of King Abdullah International Medical Research Center approved this study (protocol number NRC21R/478/11). We obtained informed consent from all participants at the beginning of the questionnaire. In the informed consent, participants were informed about the purpose of the study. Participants were also informed that their responses would be kept anonymous.
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Footnotes
Peer review under responsibility of King Saud University.
Supplementary data to this article can be found online at https://doi.org/10.1016/j.jsps.2022.12.006.
Appendix A. Supplementary material
The following are the Supplementary data to this article:
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