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Antimicrobial Reports

Parents’ Perspective of Antibiotic Usage in Children: A Nationwide Survey in Italy

Pierantoni, Luca MD*; Lo Vecchio, Andrea MD; Lenzi, Jacopo MD; Corsi, Vincenza MD§; Campana, Lara MD; Luca Trobia, Gian MD; Amendolea, Antonella MD**; Di Felice, Benedetta MD††; Alighieri, Giovanni MD‡‡; Fabrizio, Giovanna Carmela MD§§; Bisceglia, Massimo MD¶¶; Peia, Francesco MD∥∥; Chiale, Federica MD***; Bartolomei, Beatrice MD†††; Siciliano, Chiara MD‡‡‡; Di Battista, Caterina MD§§§; Passone, Eva MD¶¶¶; di Giovanni, Chiara MD∥∥∥; Piergentili, Edward MD****; Donà, Daniele MD††††; Buonsenso, Danilo MD‡‡‡‡,§§§§,¶¶¶¶; on behalf of the Surveys in Pediatric Infectious Diseases study group∥∥∥∥

Author Information
The Pediatric Infectious Disease Journal: October 2021 - Volume 40 - Issue 10 - p 906-911
doi: 10.1097/INF.0000000000003221

Abstract

Antibiotics represent the most widely prescribed drugs in children worldwide, both in hospital and community settings.1 Italian pediatric antimicrobial prescription rates are among the highest in Europe, especially in preschool children with respiratory tract infections.2,3 It has been reported a 20%–50% rate of unnecessary or inappropriate prescriptions4–6 with broad-spectrum antibiotics prescribed for viral infections7,8 or antibiotic courses significantly longer than needed.9 In the Italian pediatric primary care setting, antibiotics represent almost 50% of overall prescriptions, with coamoxiclav representing 38.4% of total reimbursed medicines, followed by cephalosporins (22.4%) and macrolides (18.8%).10

Several inappropriate prescribing determinants have been identified, including diagnostic uncertainty, lack of knowledge, and parents’ expectation regarding antibiotic prescription.11–14 Indeed, an overestimation of benefits, as well as an underestimation of harms, have been reported for several medical treatments. This attitude, together with parental pressure for a prescription, may impact antibiotic overuse.15

Moro et al identified the 2 main determinants of antibiotics request by Italian parents that may impact antibiotic overuse. First, the misinformation that most common pediatric illnesses do not benefit from antibiotics due to their viral etiology. Second, the lack of support to caregivers managing sick children drives a prescription request to shorten symptoms duration.16 Besides, as reported in the literature, the high socioeconomic status of parents17 or being a doctor or pharmacist18 was associated with a lower antibiotic prescribing since they could have greater flexibility in taking days off from work to bring their child back to the pediatrician if symptoms did not resolve or could be better informed about the appropriateness of antibiotic treatment.

On the other hand, it has been demonstrated that parents usually seek for diagnosis and not necessarily ask for antibiotics19,20 and, in most cases, the prescriptions were influenced by clinicians’ interpretation of symptoms rather than parental behavior, indicating how communication between clinicians and patients/caregivers has still room for improvement.21

Given the wide use of broad-spectrum antibiotics in the Italian pediatric population, understanding antibiotic prescribing drivers remains a crucial priority for health research nationally. The aim of this study is to evaluate assess parents’ knowledge about antibiotic therapy and resistance, their perception about the attitude of the caregiver in antibiotic prescription and their propensity for antibiotics administration through a targeted survey addressed precisely to parents’ perspective.

METHODS

This prospective observational study was conducted in 20 (100%) Italian Regions between February 1 and April 30, 2020, by using a standardized questionnaire developed by the coordinating center in Rome, revised and preliminary tested in 3 pediatric collaborating centers (Bologna, Padova, Napoli) before the online dissemination through the SurveyMonkey platform. The study was approved by the Institute Review Board of the A. Gemelli University Hospital of Rome.

The above-mentioned questionnaire was addressed to parents and caregivers who were invited through several channels:

  • Hospital: the parents of hospitalized patients or those who accessed the Pediatric Emergency Department of the participating centers were involved by verbal invitation or publicity posters.
  • Outpatient: the link was sent to Primary Care Pediatricians, inviting them to submit the questionnaire to their patients’ parents.
  • Social: the common social communication channels (Facebook, Whatsapp, etc.) have been used to disseminate the questionnaire since the beginning of the COVID-19 pandemic led to a drastic change in the organization of in/outpatient services.

The Questionnaire

The questionnaire consists of 50 items grouped into 4 sections:

  • (1) Demographic characteristics: Questions collecting information about participants and characteristics of their family nucleus.
  • (2) Knowledge about antibiotic therapy. The section included questions to assess the overall parents’ knowledge about antibiotic indications and some brief clinical scenarios to investigate their attitudes toward the correct use of antibiotics.
  • (3) Prescribing attitude of the caregiver and administration of antibiotics. This part includes questions about antibiotic therapy for the child, his/her pediatrician’s prescriptive behavior, and the parent’s possible pressure on pediatrician about an antimicrobial prescription. From this section on, the main reasons for overprescriptions emerged and were quantified.
  • (4) Knowledge about antibiotic resistance. The parents’ knowledge and perspective on antibiotic resistance were sought, evaluating their real perception of the problem.

The first question was used to collect parent consent to participate. Personally, identifiable information was not collected.

Statistical Analysis

Summary statistics were presented as frequencies and percentages. The association of sociodemographic characteristics with knowledge of antibiotics, antibiotic use and antibiotic resistance knowledge was investigated with multivariable logistic regression analysis. Outcome measures with highly skewed distributions (Shannon’s diversity index <0.1) were discarded from this analysis.22,23 As shown in Table, Supplemental Digital Content 1, http://links.lww.com/INF/E430, the outcomes with >2 categories were collapsed to 2 before doing the logistic models, following the principle that each reference category had to pertain to the dimension of appropriateness and knowledgeability.

All data were analyzed using Stata version 15 (StataCorp 2017; Stata Statistical Software: Release 15. College Station, TX; StataCorp LP). The significance level was set at 5% alfa error, and pairwise deletion of missing data was used.

RESULTS

Study Population

Six thousand six hundred twenty-five parents completed the questionnaire. The distribution of respondents across Italy and sociodemographic characteristics of parents who participated in the survey is shown in Figure 1. Data showed a prevalence of Italian parents over 30 years of age, mostly married or cohabitant, caring for 1 or 2 children. Education attainment and residence area were homogeneously distributed, whereas families’ economic income was over 50,000 euros in only 12.2% of participants. Although the Italian Health System ensures primary care of all children through primary care pediatricians, 25.4% of participants also referred to a private pediatrician for their child.

FIGURE 1.
FIGURE 1.:
Geographic distribution and demographic characteristics of the survey respondents.

Knowledge of Antibiotic Therapy

Details about the overall knowledge about antibiotics in our study population are reported in Table 1. Only 77.6% of parents were aware that only bacteria are the target of antibiotics. Nevertheless, 99.4% of parents were aware that antibiotics are useful only in certain circumstances and 92.9% of parents knew that the antibiotic has no direct effect on fever. Considering specific indications, many parents (83.99%) knew that antibiotic therapy might be delayed for a few days, waiting for diseases’ spontaneous resolution. Almost all parents (97.38%) were aware that the most common colds could heal without antibiotics, while 44.6% of parents thought that antibiotic therapy is mandatory in the case of pharyngitis.

TABLE 1. - Parents’ Knowledge About Antibiotics (N = 6625)
Questions and Answers N %
Antibiotics kill (6 missing)
 Only bacteria 5137 77.6
 Bacteria and viruses 714 10.8
 Only viruses 404 6.1
 All microorganisms 364 5.5
The use of antibiotics (4 missing)
 Is limited to specific circumstances 6579 99.4
 Is always indicated in case of fever 42 0.6
In case of fever, antibiotics (5 missing)
 Have no direct effect on fever 6148 92.9
 Break fever 332 5.0
 Reduce fever 140 2.1
In case of otitis, antibiotics (8 missing)
 Are not always necessary, and a watchful waiting approach is recommended 5547 83.8
 Are always necessary 721 10.9
 Should be taken as soon as possible 349 5.3
In case of exudative pharyngitis, antibiotics (7 missing)
 Are limited to specific circumstances 3664 55.4
 Are always necessary 2954 44.6
In case of flu, antibiotics (7 missing)
 Are limited to specific circumstances 6578 99.4
 Are always necessary 40 0.6
Common colds can clear up without antibiotic (9 missing)
 True 6443 97.4
 False 173 2.6

Prescribing Attitude of the Caregiver and Administration of Antibiotics

Answers about antibiotic use are described in Table, Supplemental Digital Content 2, http://links.lww.com/INF/E431. The most relevant results were represented by the perceived prescription of antibiotics during pharyngitis [Q23], the high amoxicillin-clavulanate prescription (the single most prescribed antibiotic [Q27]), and the number of antibiotic prescriptions during the last 12 months [Q29]. On the opposite, almost all parents were aware of correct practice during urinary tract infections (if their child has had one), about correct antibiotic administration and efficacy.

A little but relevant percentages of parents administered antibiotics by self-prescription (10.4%) or by remote consultation of the pediatrician, either by phone call (19.9%) or by phone message (9.6%). Reasons for and administration route of antibiotic self-prescription are listed in Q34–36. Almost 13% of families had an antibiotic supply at home.

If the antibiotic therapy was administered on parents’ initiative seeking medical advice only later, 76.1% declared that the physicians explicitly expressed their disagreement with their decision, but in almost all cases continued the ongoing therapy up to a total of 5 or 7 days.

Almost all parents (92.2%) believed they have never influenced the pediatrician in prescribing the antibiotic. However, if the parent thought antibiotic therapy was necessary but the pediatrician did not prescribe it, 49% said they accepted the doctor’s decision without discussion, 44.69% accepted it but asked for clarification to better understand it, while 5.7% considered it necessary to receive a second opinion. Almost all respondents (97.4%) never thought pediatricians because they rarely prescribed antibiotics, but 13.4% of parents thought of changing child pediatrician for perceived overprescription.

Knowledge on Antibiotic Resistance

Table 2 reports details about parents’ knowledge of antibiotic resistance. The notion that excessive use of antibiotics can make them lose their effectiveness in killing bacteria was known to only 57.4% of parents, despite almost all parents (93%) being aware that antibiotics could select resistant bacteria. Antibiotic resistance was recognized as a global burden by 84% of parents and 84.7% of them knew they could actively fight antibiotic resistance. However, only 66.1% received information on antibiotic resistance from their family pediatrician.

TABLE 2. - Parents’ and Caregivers’ Knowledge About Antibiotic Resistance (N = 6625)
Questions and Answers N %
An excessive use of antibiotics (7 missing)
 Makes antibiotics lose their effectiveness 3799 57.4
 Weakens the immune system 2704 40.9
 Is not a problem 115 1.7
What do you think about antibiotic resistance?* (15 missing)
 It is a global problem 5554 84.0
 I have never heard of it 659 10.0
 It is not a big deal—we have plenty of antibiotics in our armory 325 4.9
 It is not a big deal—new antibiotics can be developed 160 2.4
 It does not exist 93 1.4
There is nothing I can do to hinder antibiotic resistance (36 missing)
 False 5582 84.7
 True 1007 15.3
Has your family pediatrician ever told you about antibiotic resistance? (11 missing)
 Yes 4370 66.1
 No 2244 33.9
An excessive use of antibiotics can select resistant bacteria (23 missing)
 Yes 6137 93.0
 No 465 7.0
You can reduce antibiotic resistance by: (28 missing)
 Getting recommended vaccines 1789 27.1
 Assuming antibiotics as soon as fever develops 103 1.6
 Sharing antibiotics with the family 42 0.6
 None of the above 4663 70.7
The mode of transmission of resistant bacteria is: (7 missing)
 Through contact from person-to-person 2075 31.3
 Through food, water or contact with animals 720 10.9
 By touching a surface that has the bacterium on it 357 5.4
 All of the above 3251 49.1
 I do not know 215 3.2
*Multiselect question (the sum of percentages exceeds 100%).

Multivariate Logistic Regression

The impact of sociodemographic characteristics on knowledge of antibiotics (see Table, Supplemental Digital Content 3, http://links.lww.com/INF/E432) emerges in different issues.

Knowledge of antibiotics’ efficacy for only bacterial infections was higher in families with both parents over 30 years of age married or cohabitant, 2 children, and families with higher net income or at least 1 graduated parent.

Regarding antibiotics’ efficacy in reducing fever, a significantly lower number of incorrect answers were found in families with a parent over 30 years and with at least 1 graduated parent. Participants with children over 10 years of age answered this question with a significantly higher incorrect answer.

Considering the appropriateness of antibiotic prescriptions, families with at least 1 graduated parent or children more than 6 years of age knew better that antibiotics are not always necessary, and watchful waiting is recommended.

Table, Supplemental Digital Content 4, http://links.lww.com/INF/E433 reports multivariate logistic regression analysis of the association between sociodemographic characteristics and antibiotic use.

Despite a wrong knowledge about time for antibiotic efficacy was reported by a small percentage of participants, statistically higher odds were found among families with lower income and a child under 2 years.

Relevant heterogeneous behavior emerged on questions about reported antibiotic prescription by pediatricians. Higher odds of at least 1 antibiotic administration were documented in families with 2 children or 3–5 years of age or Southern Italy. Conversely, lower odds were reported in families with at least 1 graduated parent.

Worst data emerge about the remote antibiotic prescription. Higher odds of prescription without pediatrician evaluation were documented in families with more than 1one child, with both graduated parents, higher incomes, or children older than 3 years. Remote prescriptions (either by a phone call or text), self-prescription, or parents’ influence on pediatrician prescriptions showed similar patterns, with higher odds in families with a child over 3 years of age, one or more siblings graduated parents with income higher than 50,000 € per year.

Table, Supplemental Digital Content 5, http://links.lww.com/INF/E434 reports multivariable logistic regression analysis results investigating the association of sociodemographic characteristics with antibiotic resistance knowledge.

About loss of effectiveness when excessively used, higher odds of misinformation were found among participants not born in Italy. On the opposite, lower odds of misinformation were found among families with at least graduated parents or net income over 25,000 € per year.

Participants’ misconception that they could do nothing to hinder antibiotic resistance was significantly higher in participants with children over 10 years of age. Still, lower odds were found among families with at least 1 graduated parent or net income over 25.000 € per year.

The lack of information on antibiotics resistance by the pediatrician was reported with lower odds in families with 2 or more children over 2 years of age and families with higher income. Higher odds of disinformation were found in participants not born in Italy.

The wrong belief that antibiotic abuse may not select resistant bacteria is significantly lower when a parent has a secondary school level of instruction. Higher odds for this wrong concept were found in participants born outside Italy.

Considering personal contribution to lower antibiotic resistance, none of the possible choices were appropriate, and lower odds of correct responses were found in families with both parents over 30 years or if at least one of them was graduated.

Finally, knowledge about ways of transmission of antibiotic resistance was reported with lower odds by participants born outside Italy, families with net income over 25,000 € per year, or at least 1 graduated parent or resident in Insular Italy.

DISCUSSION

This study described the parents’ perspective on a wide range of crucial antibiotic use practices in children. To our knowledge, this study involved the largest number of parents reporting their understanding of antibiotic use and their experience and obtained a complete and representative national coverage.

Investigating the parent’s general knowledge about antibiotics (area 2 of the questionnaire), we found that about 88% of parents are aware that antibiotics are useful only against bacterial infections, in line with previous findings reported by Bert et al24 Although most respondents admitted the absence of direct effects of antibiotics on fever, the latter remains a common driver of antibiotic prescription in childhood. Previous evidence reported that about 1/5 of caregivers believe that antibiotics work against pain and inflammation, and a percentage of them administered antibiotics every time their child had a fever.24 In our cohort, less than 1% of respondents believe the antibiotic is always useful in case of fever.

Respondents’ probability of giving correct answers was relatively high (over 80%) regarding specific pathologies (such as otitis and colds). On the contrary, less than half of parents (44%) believe the antibiotic is always necessary for exudative pharyngitis. However, these data must be correlated with clinical practice: 30% of clinicians prescribe antibiotics without first performing rapid swab for Group A Streptococcus, in contrast to what is indicated by national guidelines.

The third area of the questionnaire investigates the experience of parents and the prescriptive attitudes of their pediatricians. Compared with previous reports, we documented a higher proportion of parents who were aware of the importance of respecting antibiotic doses and timing prescribed by the pediatrician (99.4% vs. 85% reported by Bert et al24).

However, we reported an inappropriately high prescription of amoxicillin/clavulanate, in line with previous prescription data25 and the most recent report by the Italian Pharmacy Agency about drug monitoring use in Italy.10

As a positive finding, we reported a significantly reduced self-prescription compared with previous evidence collected in Italy.24 In comparison to 2014, the proportion of parents who gave antibiotics without prescription varied from 25% to 6.5%, with a greater chance of self-prescription by caregivers with a high level of education, high-income families, or more than 1 child. This suggests that more significant experience and self-confidence allowed the parent to choose the therapy independently, without medical advice. Similarly, we found a correlation between the high-level education, parents’ experience (age and number of children), and the increase in correct answers about the use of antibiotics, independently from family income, profession and setting.

Our survey showed that parents’ theoretical knowledge of antibiotics increased compared with the past. This could partly be attributed to antibiotic awareness campaigns. However, importance must be given to the parents interviewed’ overall high level of education in our study.

The third area of the questionnaire also investigated the parent’s influence on the pediatrician’s prescribing choices: 93% of parents believe they have never influenced the caregiver. This result is very encouraging: in fact, numerous previous studies had highlighted how important this element was in the choices made by prescribers.26,27 Among the determinants that influence antibiotic prescribing in Italy, communicative factors are preeminent, laying the foundations for a relationship of trust between doctor and patient-parent. In support of this hypothesis, it could be noted that more than half of the parents were not satisfied with the decision when in disagreement with the pediatrician’s choice. It is comforting to know that more parents have thought about changing pediatricians because of their antibiotics overprescription (14% of the interviewees), compared with those who thought about it because they see “too few” prescribed than expected (3%). This suggests that the parental perception of antibiotic therapy is centered on the risks of overprescription.

In the fourth area of the questionnaire, the knowledge relating to antibiotic resistance was investigated. The results that emerged show the current need to communicate more information on this issue. The latter finding must be considered since children are the main users of antibiotics, and pediatric prescription changes may have a relevant impact at the global level.

The high percentage of parents who believed they could do nothing to overcome this problem, and the low percentage of parents who said they have heard about antibiotic resistance through their pediatrician, imposes the need to improve the caregiver’s communication, making parents aware about antibiotic resistance, how this is fueled, and what people can do to reduce it.

As pediatricians, we must communicate better during visits, and as a scientific society, we must learn to use the web as a route to vehicle information. This study may therefore represent the first step for a joined (pediatricians and caregivers) implementation strategy to reduce inappropriate antimicrobial prescriptions. According to Eurostat data, the internet was the leading source of health information for 51% of the people who responded to the survey carried out in 28 European Union countries.28

Finally, as already emerged from the 2014 survey, parents with a low socioeconomic level and foreign parents were less prepared to use antibiotics and antibiotic resistance. This is an unacceptable inequality that the whole community of healthcare professionals must fight. As pediatricians, we are the guarantors of children’s health, and, as such, we must take charge of them and their families to ensure fair, safe, and convincing prescribing practices.

Our study has some limitations to address. The administration of the questionnaire “face to face,” as had happened at the beginning of the data collection, would have been the best solution.29 However, since the start of the lockdown for the COVID-19 pandemic, most respondents were reached via social media. Therefore, it was not possible to check any alternative sources of information during the compilation. Also, 56% of the respondents in our survey had a high level of education, while in Italy, those with a tertiary qualification are only 19% of the population.30 This means that administering the questionnaire or the topic has made an upstream selection for the general population.

In conclusion, our study suggests that parents’ knowledge and attitudes toward antibiotic use and prescription are improving compared with previous studies, while there is still a gap regarding antibiotic resistance, particularly on practices that can reduce its burden. Our study’s negative finding is that families from low-income settings or those born abroad have significantly more misconceptions about important antibiotic practices. This is an important field of intervention and investigation during the following years.

ACKNOWLEDGMENTS

SPID group: Marcello Lanari, Prof,1 Eleonora Bellini, MD,1 Vita Antonella Di Stefano, MD,5 Tiziana Virginia Sciacca, MD,5 Roberta Massaro,20 Ilaria Lazzareschi,20 Cristina De Rose,20 Piero Valentini,20 Guido Castelli Gattinara and Andrzej Krzysztofiak (OPBG, Rome), Silvia Garazzino (Regina Margherita Children’s Hospital, Turin), Sonia Bianchini (ASST Santi Paolo e Calo, Milan), Elisabetta Venturini and Carlotta Montagnani (Meyer Children’s University Hospital, Florence), Giangiacomo Nicolini (San Martino Hospital, Belluno).

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Keywords:

parents; antibiotics; knowledge; antibiotic resistance

Supplemental Digital Content

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