Parental Perceptions of Giardiasis: A Study in an Outpatient Paediatric Hospital Setting in Havana, Cuba

Background. Giardia lamblia is an important cause of diarrhoeal disease throughout the world. Giardiasis— a mild and self-limiting disease that this protozoan causes— is perceived as a harmful disease. Aim. To explore the general level of awareness about giardiasis, clinical features, mode of transmission, prevention, and consequences and describe the sources and channels of information caregivers would prefer using to be informed about this disease. Methods. A cross-sectional survey was conducted among caregivers attending to the outpatient paediatric hospital setting in Havana. Results. A total of 202 caregivers were interviewed. Nearly 73% considered giardiasis as a modern problem, and 39% considered that it could be a fatal disease. Although 76.7% were aware that small intestine is the organ affected, other localizations were cited. Abdominal pain and diarrhoea were recognized as the commonest symptoms. Around one-third could identify that giardiasis may spread through drinking unboiled water and unwashed vegetables other incorrect ways were mentioned; respondents with more than 12 years of formal education were more likely to have better knowledge. Discussion. Strategies to control giardiasis need to be through an integrated approach aiming at boosting caregivers' knowledge and encouraging healthcare workers to act as a readily available source for health information.


Introduction
Giardia lamblia, probably the most frequent pathogenic intestinal protozoan infection in man, is an important cause of diarrhoeal disease in children and adults throughout the world. Although giardiasis-the disease this protozoan causes-is usually perceived as mild and self-limiting, symptoms generally subside within 2-3 weeks in otherwise healthy individuals. is infectious disease may have both immediate and long-term consequences including chronic diarrhoea with or without dehydration and intestinal malabsorption, recurrent abdominal pain, and weight loss [1]. Additionally, it has been currently related to chronic fatigue [2], postinfectious irritable bowel syndrome [3,4], and particularly, in early childhood, poor cognitive function and failure to thrive [5]; all of these have attracted an increasing attention to this protozoan infection in the recent years.
Despite its worldwide distribution, Giardia is more common in developing countries. Data from surveys, excluding documented outbreaks, indicate that in industrialized countries the prevalence rate is between 2% and 5%. In contrast, it ranges from 20% to 30% in developing countries [1]. Data on the prevalence of giardiasis in Cuba is limited; in a national survey the overall prevalence of Giardia infection was estimated to be 6.02% [6]. However, higher prevalences have been found among young children attending day-care centres and primary schools [7][8][9][10]. Clinical giardiasis also gives the impression to be a common reason for hospitalization in paediatric hospitals in the capital of Cuba [11,12]; where, according to a study of risk factors for Giardia infection among hospitalized children, it seems that, at least at the individual level, giardiasis-prevention activities in Havana should be focused on health education to improve personal hygiene and food-related practices [12].
Health education (HE) continues to be one of the most important strategies in the �ght against intestinal parasites [13]. Appropriate management of giardiasis, including patient education to promote adherence to preventive measures that may protect against infection and reinfection, not only might reduce the frequency of outpatient clinic visits and hospitalizations for giardiasis, but also could reduce the costs associated with this disease.
In childhood giardiasis, mothers and other caregivers, are therefore, of foremost importance in recognizing the disease and seeking treatment for their wards. Very little is known about the perceptions of parents and carers when dealing with giardiasis in the paediatric setting. eir ideas and behaviours concerning giardiasis might enhance or interfere with the effectiveness of giardiasis prevention and control. Understanding their perceptions concerning this disease is an important step towards the disease control. A qualitative study in Cuba by  reported de�ciencies in the children caregivers' knowledge and practices concerning giardiasis [14].
It is important to assess the current knowledge about giardiasis before devising an intervention strategy for education campaigns among general population. e purpose of this study was to (1) explore the perceptions of a group of caregivers about medical aspects of giardiasis (clinical features, modes of transmission, prevention, and consequences), its prevention and treatment; (2) assess the sources and channels of information caregivers would prefer using to be informed about giardiasis. All of this might highlight areas where the support of health care professionals can be improved.

Study Design and
Setting. is was a descriptive crosssectional study conducted between January and March 2010, at Academic Paediatric Hospital Centro Habana (APHCH), Havana, Cuba. is 226-bed study hospital is a governmentfunded and public facility which provides secondary and tertiary medical care and active ambulatory and emergency services, within all clinical and surgical specialities, for children from all over Cuba but mainly to the paediatric population from the municipalities of Centro Habana, Cerro, Habana Vieja, and Plaza municipalities.

Inclusion and Exclusion
Criteria. e study included respondents aged >18 years who were willing to participate in the study and gave individual verbal consent. Only health professionals and students in the medical professions were excluded to avoid selection bias.

Questionnaire.
A structured questionnaire was designed on the basis of a qualitative research conducted in the same hospital by the authors [14]. e questionnaire was peer-reviewed and discussed with health care professionals working within paediatric wards and also was pilot-tested on random patients' relatives at the hospital over a 1-week period to evaluate the language used, to verify the relevance of the questions, and for clarity and consistency. Results were retested aer completion to verify the answers. e questionnaire was then modi�ed accordingly. It focused on basic demographic data (age and gender), education, and questions about their knowledge regarding giardiasis, mode of transmission, organ affected, its suggestive signs and symptoms, prevention, most reliable method of diagnosis, and whether giardiasis was a curable disease. Additionally, caregivers were also assessed about from which sources and channels they would like to receive information on giardiasis. It took around 10 minutes to complete an interview. Answers were categorized into either correct (if matching the medically correct answer) or incorrect.

Questionnaire Administration.
All consecutive parents/carers who ful�lled the eligibility criteria for inclusion and who agreed to participate were recruited if they were either new attenders or reattending. Respondents were adult members of patients' families (parents/carers) who visited the outpatient clinic of APHCH for gastrointestinal problems. Aer the interviewers, who were three of the research team authors (Y. Salazar, M. Alfonso, and I. V. Dawkins), explained the purpose of the study and obtained individual verbal consent from the respondents, they administered the questionnaire to parents/carers, while waiting for the consultation of their child. e interviews were conducted in private to maintain con�dentiality and to reduce the in�uence of relations of peers.

Ethical
Approval. e study was approved by the APHPC's Ethics for Research Committee. Verbal informed consent was obtained from the study participants before the research instruments were administered. Con�dentiality of all information obtained from participants was maintained by not allowing information to be accessible to nonmembers of the research team.
2.6. Data Analysis. Database was prepared using Epi Info Version 6.0, and accordingly data entry was done. Frequency ISRN Preventive Medicine 3 distributions were obtained. In the exploration of possible associations between respondent characteristics and awareness about transmission and prevention, analysis was done taking into account education of respondents, which was categorized into two categories (less than 12 years of formal education or ≥12 years of formal education) and age of respondents (less than 40 year of age and ≥40 years of age). Crude odds ratio (OR), their 95% con�dence intervals (CIs) and values were calculated with set at 0.05.

General Knowledge about Giardiasis Characteristics.
Of the 202 caregivers, more than half (72.7%) considered that giardiasis is a modern problem, and, although almost half (47.5%) stated that this disease could not lead to death, 39.1% did, and 13.4% did not know. Small intestine was correctly identi�ed as the site of giardiasis by 125 (61.9%) of the caregivers. However, more than one organ was mentioned as a possible target of Giardia infection including gallbladder (66 (32.7%)) and liver (54 (26.7%)). For 127 (62.9%) of respondents those who harbour Giardia infection not necessarily feel or know about it. irty-two (15.8%) of the respondents did not have knowledge about the signs and symptoms of giardiasis. ose having knowledge mentioned abdominal pain (77.6%), diarrhoea (70.6%), and loss of weight 59.4% as the symptoms of giardiasis. However, other clinical manifestations including hives, itching, spots in the skin, and tiredness were mentioned for more than 30% (Table  1).

Diagnostic
Tests. e majority of caregivers, 171 (84.6%), considered the microscopy of duodenal aspirate as the most effective diagnostic tool for giardiasis. e microscopy of faecal smears was only cited by 18 (8.9%) respondents (Table  1).

Transmission.
One hundred and sixty-nine caregivers (83.6%) in this study knew that Giardia could be transmitted through drinking unboiled water and unwashed vegetables and fruits intake. e other modes of transmission mentioned by interviewees were walking barefoot and using utensils previously used by patients with giardiasis (Table 2). ose with an education of 12 years of formal education or more were four times more likely to be aware of prevention than those with less than 12 years of education (OR = 4.5, 95% CI = 1.9-10.8). Interaction between knowledge of transmission and age was tested and found to have no signi�cance (Table 3).

Treatment and Prevention.
Nearly all caregivers (95.5%) were aware that giardiasis was a curable disease (Table 4). Almost all the respondents 175 (86.3%) considered giardiasis to be preventable, most of them (169 (83.6%)) believe that prevention could be achieved by drinking boiled water, washing hands, and washing vegetables and fruits; 86.3%, 89.6%, and 91.5%, respectively. Other actions including avoiding walking barefoot and avoiding utensils used by patients with giardiasis were also mentioned by a group of them (Table  5). ose with an education of 12 years of formal education or more were nearly three times more likely to be aware of prevention than those with less than 12 years of education (OR = 2.8, 95% CI = 1.3-5.9). No signi�cant association was observed between knowledge of prevention and age (Table 5).
3.6. Sources and Channels. One hundred and ��y-nine of the caregivers stated that they did not receive information on giardiasis during the last year from any source or channel. Caregivers were asked which methods they would prefer to know or to improve their knowledge about giardiasis. Among the suggested sources and channels, television was mentioned by 130 (64.3%), nurses and medical doctors 107 (52.9%), printed materials-lea�ets, posters, and pamphlets-94 (46.5%), and radio 35 (17.3%).

Discussion
e goals of treating symptomatic giardiasis properly are to minimize the duration of illness, ensure cure, stop transmission of infection, and could also be to prevent the emergence of drug resistance. Caregivers' input, as in other areas of medicine involving children, seems to be critical to clinical management in paediatric giardiasis. e importance of providing caregivers with appropriate information is to enable them to participate effectively in giardiasis recognition, and preventative measures should be recognized.
Even when there were some important gaps in various issues, it was encouraging to observe that in most issues caregivers' perceptions on giardiasis closely paralleled that of the biomedical understanding. is coincidence should be used as an entry point for a broader HE activity, which is then expanded to also accommodate other disease aspects, that is, its mode of transmission, signs and symptoms, and appropriate prevention methods, to provide accurate and complete knowledge on giardiasis.
Internationally, this disease is gaining increasing attention, �rst as a reemerging infectious disease in industrialized countries and, second, as a part of the "Neglected Disease Initiative" by the World Health Organization [15]. Its diagnosis has been established progressively with improving sanitation and with fading of the role of fatal epidemic infections as the overwhelming everyday problem. ese, together with the fact that in Cuba high prevalences have been reported among young children attending day-care centres and primary schools [7,8], might be justifying the perception held by most respondents that this disease is a modern problem. Additionally, Giardia has also been frequently isolated from faeces of Cuban children with diarrhoea, and it seems to be a common cause of children hospitalization [11,12,16]. ese could have led some caregivers to conclude that this disease could cause death. Giardia organisms primarily affect the proximal small intestine; however, during the last decades, there have been various reports concerning other localizations of Giardia trophozoites including gallbladder [17], urinary tract [18], gastric mucosa [19][20][21], colonic and ileal mucosa [22,23], and pancreas [24]. e majority of caregivers were able to recognize that Giardia infection is frequently asymptomatic, and diarrhoea and abdominal pain are the clinical manifestations of symptomatic giardiasis. is is probably due to the educational message in the mass media stating that two of the primary clinical features of symptomatic intestinal parasitic diseases are diarrhoea and abdominal pain. is could be of importance, taking into account that an early treatment-in some aspects-could depend upon prompt recognition of symptoms and signs of giardiasis in the household, mainly by caregivers. Other clinical manifestation very frequently mentioned by the caregivers was urticaria. It was surprising because, although this sign has been reported associated with giardiasis in the scienti�c literature [25][26][27][28], it is not so common. Considering the frequent asymptomatic nature of this infection and the high prevalence of this protozoan worldwide, urticaria most of the times indicates that it is necessary to look for an alternative diagnosis. Nevertheless, it should be stated that, coincidently, in a survey of knowledge, perceptions and practices about giardiasis in 63 gastroenterologist of Havana, it was evidenced that 55.6% of these specialists in Havana stated that this parasitic infection was a frequent cause of cutaneous manifestations [29].
e intermittent excretion of Giardia cysts might be affecting the perceptions of the microscopic study of faecal specimens which for most of the caregivers considered useless. At the same time, there was also an overreliance on the microscopic examination of duodenal aspiration. is could be a re�ection of a common practice in the clinical setting. Two studies on knowledge and practices on giardiasis among gastroenterologist and dermatologists in Havana showed that 52.4% of gastroenterologists [29] and 64% of dermatologist [30] considered that duodenal aspiration was the best way to diagnose this parasitic disease. Certainly, duodenal aspirate is a valuable diagnostic aid for avoiding delays in diagnosis and prolongation of patient morbidity. However, this situation could be counterproductive because other parasitologic diagnoses-potentially causing disease-including intestinal helminths and protozoa could be lost.
e caregivers demonstrate a general knowledge of giardiasis transmission and prevention. However, there were some important gaps concerning these two issues which indicate that people today tend to combine all of the general preventive measures against intestinal parasitic infections, maybe, as a re�ection of a result of previous activities directed at intestinal parasites control. Additionally, there exists a link between hygiene and infection, which is a common theme in the lay literature, and caregivers could be able to make connections and draw inferences from previous similar experiences. G. lamblia remains the leading waterborne diarrhoea-causing disease [31,32], either when people drink accidentally or swallow water from contaminated or untreated sources (no heat inactivation, �ltration, or chemical disinfection). Outbreaks of giardiasis linked to drinking water and food handlers have been documented. e correct treatment of water and food and hand hygiene (i.e., hand washing with soap and water or the use of a waterless, alcoholbased hand rub) are considered the most important measures in preventing infections transmitted via the faecal-oral route. It has been recently shown in a systematic review the impact of interventions to improve hand washing with soap in the community could reduce diarrhoea risk by 47% [33]. In the USA, an outbreak of giardiasis, involving multiple modes of transmission, eventually stopped, possibly in�uenced by a vigorous hand washing campaign [34].
In the present study, the higher educational level of the caregivers had a positive in�uence on the knowledge of transmission and prevention of giardiasis. e parents' educational level is one of the factors of health inequalities among children [35]. Education is important for health because of the opportunities it creates to obtain better material living conditions; well-educated people are less likely to be unemployed, and more likely to have full-time jobs, ful�lling work, and high income. A good example could be a study carried out in Peru where participants with greater wealth indexes were associated with protection against Giardia and persistent Giardia infections (>14 days) [36]. In a study carried out in Portugal, children with mothers without any education were more likely to be infected with Giardia than those with educated mothers. Similarly, children living with fathers with no education had a 12.26 times higher risk of being infected with Giardia than those with educated fathers [37]. is highlights the need for giardiasis HE programmes and material targeted at groups with special needs. Even in a country like Cuba, where the educational level is very high, groups still exist where low education and thus higher risk of diseases, such as giardiasis, may interact to create an unfavourable situation.
To target populations for prevention messages, it is important to know which sources and channels of information are most frequently reported as being used to keep informed about a speci�c topic. Consistent with a previous study [11], it was found that television was the preferred channel of information, followed closely behind by their medical doctors, and printed materials.
HE materials such as posters and brochures may be an effective way to disseminate health information, providing such information in the local language that could be displayed at prominent places, such as health facilities and community centres. At present, access to culturally appropriate and easy-to-understand educational materials on giardiasis is lacking. Based on this study, it may be recommended that HE materials oriented towards increasing the knowledge in different issues of giardiasis should be developed. An interesting experience comes from a study carried out in schools in south Tehran. e case group and their mothers were separately covered by the HE programmes that included washing hands with soap, cutting nails, washing vegetables, and making the families knowledgeable about giardiasis and its effects on their children. All the programmes were performed by HE methods, that is, poster, video �lm, faceto-face meetings, and pamphlets. e control group had not undergone any health education programme. ree months later, a triple stool examination was done in both groups to check reinfection. Aer the implementation of the programmes, the mean of the mother's awareness about controlling of giardiasis increased from 6.54% to 27.16% ( 0.00001), without any variation in the control group in this item. e mean of children's information about giardiasis and its methods of control in the case and control groups before implementation of the HE programmes was 4.76% and 4.86%, respectively, but aer the implementation of the programs, it increased to 16.3% in the case group but remained at 4.86% in the control group ( 0.00001). Aer antigiardial treatment, both groups were cured of the Giardia infection. Aer implementation of HE programs, the rate was 23.3% in the case group but 86.7% in the control group, indicating a signi�cant difference between the two groups [38].
e interpersonal communication, which is the most effective method of communicating health information [39], that takes place in the doctor's offices and the waiting room may offer the opportunity for physicians and other health care professionals to display their potential to play a signi�cant role in promoting individual patient action and contributing to the development of social norms concerning health behaviour. Health care workers (medical doctors and nurses) occupy a position of high credibility and trust which make their pronouncement well received; they have a wellrecognized role encouraging prevention. However, as key communicators, they need the necessary skills to carry out activities that allow discussions, feedback, and explanation to the target audience. In the Cuban context, some studies carried out among gastroenterologist, and dermatologists have evidenced the necessity of improving the giardiasis management and prevention information they provide to their patients [29,30]. is might be a fruitful area for future health intervention campaigns.

Limitations of the Study
Study participants were restricted to caregivers who were recruited from only one health facility, and, therefore, their views may be biased by contact with the same paediatric gastroenterology team and their standard educational practices. Participants were recruited among parents/carers attending to the hospital (a majority resided in Havana), and thus we likely failed to capture the views of people in other provinces. As parents were recruited from those taking their children to the outpatient clinic for gastroenterology and within population are likely to be a large group of children who have giardiasis, it is reasonable to assume that parents of these children are more likely to know what giardiasis is than parents from the general population. Additionally, it should be noted that people attending health facilities at a hospital are expected to have a relatively greater awareness about common health issues. ere is not a previous study in this area, and hence this questionnaire survey was the �rst to explore some of the issues in detail. �ace-to-face administration of the questionnaire might have led to some degree of bias in the interviewees' responses.

Conclusions
e study has revealed reasonable knowledge of the symptoms of giardiasis; however, there is a need for educational intervention directed towards correcting misconceptions. ere was a need for an effective education programme focusing on giardiasis transmission and prevention which should be emphasised in order to avoid reinfections. e central necessity of caregivers' involvement in developing educational strategies that re�ect their understandings and interpretations of this disease should not be overlooked.