http://orcid.org/0000-0001-6076-1803
ABSTRACT
Introduction : Rabies continues to be one of the most important viral diseases and remains a significant threat to public health across the globe. The World Health Organization (WHO) has determined that most rabies cases occur in children. Dog bites on humans are a major public-health problem. Poland has not achieved rabies free status yet. Post-exposure prophylaxis (PEP) in humans can effectively prevent death after exposure to a potentially infected animal.
The aim : The main objective of this study was to estimate the frequency of PEP among children exposed to animals, who had attended consultations at the Department of Infectious Diseases for Children in the Jan Boży Hospital in Lublin.
Patients and methods : We retrospectively analyzed the medical records from the period of 2010–2016 of all pediatric patients (0–17 years of age) who had been exposed to animals and attended consultations at the Department of Infectious Diseases for Children in the Jan Boży Hospital in Lublin.
Results : During the studied period, 519 children who had been exposed to animals attended consultations, and a prophylactic procedure consisting of active immunization was applied to 32.8%. The male children accounted for 55.3%. The mean age was 9.2 years. The biggest group of children (406) had been exposed to dogs, 62 children to cats, and 15 to rats. Most children had upper-limbs injuries. During the studied period, i.e. 2010–2016, there were 1713 confirmed cases of rabid animals in Poland, and 60 cases were recorded in the Lublin Province. We did not observe any cases of rabies in our exposed and vaccinated patients.
Conclusions : The number of rabid animals in the Lublin Province had decreased to low levels, but the expected decrease in the number of PEP's administered did not occur. Since all children were vaccinated in accordance with the recommendations, the possible reason for vaccination's being administered in the quantities greater than the number of rabid animals recorded in the Lublin Province are bites by animals unavailable for veterinary observations and also the lack of more frequent reports regarding the current epizootic situation of rabies. The use of rabies immunoglobulin (RIG) in children in the Lublin Province is at a very low level, i.e. at 0.58%. The yearly numbers of exposed pediatric patients were at similar levels, which indicates that education programs should be introduce to reduce the number of animal bites in children.
Introduction
Rabies is an acute progressive fatal encephalitis caused by a negative stranded RNA virus species of the Lyssavirus genus, family Rhabdoviridae of the Mononegavirales order. The current classification of lyssaviruses defines 14 genetically divergent species.Citation1
Rabies is still one of the most common viral zoonoses and remains a significant threat to public health across the globe. This infection is transmitted from animals through saliva via a bite wound, a scratch wound, or by the licking of a mucous membrane. Although human-to-human transmission has not been proven, cases of rabies transmission through corneal, liver, kidney, lung and vascular grafts transplantation from infected donors have been described.Citation2,Citation3 Rabies is still present on the European continent. In the last decade, more than 90% of the rabies cases occurring in Europe were reported in wildlife. Wild vector species represent a high risk to human populations. The raccoon dog (Nyctereutes procyonoides) has become a major factor in the epidemiology of rabies in Eastern and Northern Europe, and is now the second most important wildlife species infected with rabies after the red fox. Also, domestic animals may carry and transmit the disease. Rabies in dogs is the main cause of rabies-induced morbidity and mortality in humans, putting over 3.3 billion people at risk of being exposed to the disease. Most industrialized countries have eliminated rabies from domestic dog populations.Citation4 The terrestrial rabies posed a serious problem in Poland in the 20th Century, but within the past decades the epidemiological situation has started to change. The introduction of safe and immunogenic cell-culture-based vaccine, and mass oral immunization of foxes that began in 1993 in Poland were the key factors in the successful strategy for the elimination of rabies. The vaccination of domestic animals (dogs and cats) also plays an important role in preventing this disease. According to Polish recommendations, annual vaccination of dogs is obligatory and the costs of vaccination are borne by the owner of the animal.Citation5
Rabies is essentially a fatal viral disease with a total of nineteen documented human survivors. All except 3 who recovered to lead independent lives, had gross neurological impairment.Citation6 Currently, there are about 60 000 human rabies deaths worldwide yearly.Citation7 The highest numbers of human deaths due to rabies are observed in India and Philippines.Citation8 The last case of human rabies in Poland was reported in 2002.Citation9
Human rabies prevention relies largely on vaccination. In Poland, recommendations for rabies post exposure prophylaxis followed the national and WHO guidelines, which recommend that people should receive PEP when bitten by an animal suspected of being infected by rabies. PEP in humans includes cleansing and disinfecting the wound or point of contact, and administering anti-rabies immunization. Rabies vaccine should be given to contacts involving category II and category III exposures (single or multiple trans-dermal bites, scratches or contamination of mucus membranes with saliva, and suspected contact with bats). Infiltration by purified rabies immunoglobulin (RIG) in and around the wound is recommended for severe categories of exposure. The vaccination schedule includes five doses of rabies vaccine given on days 0, 3, 7, 14 and 30 (the Essen regimen). The WHO recommends the observation of a suspected animal source for 10 days. Clinicians make an individual risk assessment for each patient exposed to the animal, and decide whether to administer the rabies vaccine with or without immunoglobulin according to the general recommendations, epidemiological data and the category of the bite. The veterinary situation is taken into account in this assessment, i.e. the species of the biting animal and the possibility of carrying out examination of the animal, whenever it can be identified. Furthermore, there seems to be large variations in the use of PEP and especially RIG between European countries, with some countries overreacting and others under-prescribing.Citation10,Citation11
The diagnosis of rabies in animals in Poland is based on techniques recommended by the WHO, and the unified fluorescent antibody test (FAT) procedure is applied in veterinary regional laboratories authorized to perform rabies diagnosis.Citation11
The aim
The main objective of this study was to estimate the frequency of PEP among children who had been exposed to animals and attended consultations at the Department of Infectious Diseases for Children in the Jan Boży Hospital in Lublin. We also tried to evaluate whether the decrease in the number of animal-rabies cases resulted in a decrease in the number of PEP's administered. We further analyzed age, gender, wound care, localization and the demographic data of the exposed patients. The aim was also to assess the animal species suspected as a source of rabies exposure by analyzing the epizootic situation of rabies in animals in Poland and in the Lublin Province.
Patients and methods
We retrospectively analyzed medical records from the years 2010–2016 of all pediatric patients (0–17 years of age) who had been exposed to animals, and had attended consultations in the Department of Infectious Diseases for Children in the Jan Boży Hospital in Lublin.
A standard case-report form was completed for each exposed patient and was performed based on the included data analysis. For the study, the medical records of all the patients exposed to animals and who attended consultations at the Dispensary for Rabies Prophylaxis were reviewed and nobody was excluded from the study. Descriptive statistics were used and the data were not analyzed electronically.
Ethical approval was obtained from the Ethics Committee of the Medical University of Lublin, Poland.
Results
During the studied seven-year period (2010–2016), 519 children who had been exposed to animals attended consultations in the Department of Infectious Diseases for Children at the Jan Boży Hospital in Lublin (Eastern Poland). The male children accounted for 55.3% (287 cases) and the female children for 44.7% (232 cases). The mean age was 9.2 years (ranging from 5 months to 17 years). The majority of the exposures occurred in urban areas (58.4%). In the study group there were 303 residents of cities and 216 residents of villages. The range of time variation between exposure and consultation ranged from 2 days to 6 hours (an average of 18 hours).
The biggest group of children (406) had been exposed to dogs. In this group there were 224 male children and 182 female children. Sixty two children (11.9%) had been exposed to cats, 15 to rats, 6 to bats, 6 to field mice, and 6 to unidentified wildlife. Four children had been exposed to squirrels, and 4 to moles. Two children had been exposed to rabbits, 2 to ferrets, and 2 to red foxes. One person had been exposed to a horse, 1 to a doe, 1 to a hedgehog, and 1 to a guinea pig. The total number of children exposed to particular animal species in the period from 2010 to 2016 is presented in .
Table 1. Total number of children exposed to particular animal species from 2010–2016.
In the study group, 51.8% of all the exposed had had category I, 35% had category II, and 13.2% had category III contact. All children with category III contact had been bitten by dogs. In all the exposed patients, washing of the wound was done. All patients presenting with categories II or III exposures attended consultations at the Department of Surgery and Wound Care, and the surgical recommendations were followed. Most of the children had had upper- limb injuries (44.3%), followed by lower-limb wounds (40.3%). Among the children with injuries to the head and neck, 98% had had dog-bite injuries. In this group the mean age was 5.9 years. The body site of injuries in the children exposed to animal bites is presented in .
The total number of consulted and vaccinated children in studied years are presented in .
Table 2. Total number of consulted and vaccinated children from 2010 to 2016.
Out of the 519 children attending consultations, 170 (32.8%) were vaccinated, and 167 children had 5 doses of rabies vaccine. In 3 patients (2 exposed to bats, 1 exposed to a dog) the vaccination was interrupted due to negative result of a direct fluorescent antibody test from animal brain tissue. Among the vaccinated children, 116 had been exposed to dogs, 29 to cats, 11 to rats, 6 to bats, 5 to field mice, and 3 to moles. The total number of vaccinated children after exposure to particular animal species is presented in .
Table 3. Total number of vaccinated children after exposition to particular animal species from 2010–2016.
Table 4. Body site of injury in children exposed to animal bites.
Two children had been exposed abroad. One children had had a dog bite in Turkey in 2013 (a 13 year-old-girl had had an upper-limb injury, and she received her first dose of rabies vaccine abroad). In 2014, a 9-year-old girl had had an upper-limb injury inflicted by a cat in Tunisia, and she had received 2 doses of rabies vaccine abroad. In only one case (0.58% of all those vaccinated) an 11-year-old-boy bitten by unidentified dogs in 2011 (RIG) was given with his vaccination. Rabies immunoglobulin was given intramuscularly, and was not injected in or around the wounds. This patient presented with multiple category-III contact, with deep wounds located in the patient's face and neck.
For each exposed child, an individual risk assessment was made, based on the general recommendations, epidemiological data, the category of the bite, and the animal which was the potential source of infection. In the group of vaccinated patients, animals were not available for veterinary observation or testing, and in 6 cases the children had been exposed to unidentified wildlife.
Out of the 519 exposed children, 67.2% did not have PEP applied. In these cases, no risk factors were detected. The children from this group had had category-I exposures (51.8%) with no direct contact with animals, or the contact was through intact skin with no bites or scratches. PEP was also not applied to children exposed to animals with no symptoms of the disease under veterinary observation (15.4%). In the study group, there were no persons re-exposed to animal bites.
We did not observed any case of rabies in our exposed and vaccinated patients. It is obligatory in Poland to report exposures to animals which require PEP administration, and human rabies cases, to the Sanitary Inspection Services, which are responsible for future procedures. In Poland, both RIG and rabies vaccine are provided free of charge to patients. During the studied period since 2010–2016 there were 1713 cases of confirmed rabid animals in Poland, and 60 cases were noted in the Lublin Province. Rabies was confirmed in bats, foxes, racoon dogs, martens, badgers and deer. Among domestic animals there were rabies infected dogs, cats, cattle, equine, goat sheep, and pigs. The total numbers of rabid animals in Poland and in Lublin province in 2010–2016 are presented in .
Table 5. Total number of rabid animals in Lublin Province and in Poland in 2010–2016.
Discussion
Animal bites are a significant cause of morbidity and mortality worldwide. A half of the global human population lives in a canine-rabies-endemic areas, being considered at risk of contracting rabies. Globally, millions of people are bitten by dogs, but most of the fatal cases occur in children. According to a WHO-APCRI survey, the animal mainly responsible for human-rabies deaths was the dog (96.2%). Dog bites account for 0.3% to 1.5% of all pediatric presentations for medical attention, and they most frequently occur in young children. The location of injuries due to dog bites is largely dependent on age. In younger children, the most-frequently affected areas are the head, face, and neck. In older children, bites to the extremities are the most common.Citation12,Citation13 Data presented by Arjan B van As et al indicate that dog bites to the head, face and neck were responsible for 0.5% of all trauma-unit presentations in children. The mean age of the children was 5.1 years. Male children accounted for 68% of the patients, and the peak incidence of bits to the face occurred in children aged 2 to 4 years.Citation14 The annual incidence of dog bites seen in emergency departments in France has been estimated at around 0.03–0.05 per 1000 individuals aged < 15 years. Data presented by Gautret P. et al indicate that individuals aged 0–29 years were over-represented among injured individuals (53.5%) compared to the whole population (38.7%).Citation15
The exact number of dog bites occurring annually in Poland is unidentified. In our study, the majority of children (78.2%) had been exposed to dog bites. The results from our study indicated that the number of dog bites was higher in male children, and the most common site of bite was the lower limb. We also observed head and neck injuries in the younger children (the mean age was 5.9 years).
Cat bites account for 5% to 10% of animal bite wounds, and occur most often in adult women, usually on the extremities. 8 In our study 11.9% of all the children who attended consultations had been exposed to cats. In this group there were 32 male children and 30 female children (the mean age in this group was 8.7 years).
Since domestic animals can serve as a link to the rabies virus between wildlife and humans, the vaccination of dogs and cats continues to be an extremely effective public-health measure in preventing rabies in humans. The data from the literature indicate that in rural areas of the Lublin Province only 64.8% of dogs and 19.8% of cats are vaccinated properly. 5 Data regarding the vaccination of domestic animals from the urban areas of our Province are not available. In our study, out of 406 dogs which had been bitten the children, 304 were available for veterinary observation. In this group 280 (92.1%) had been properly vaccinated against rabies. Our data indicate a high percentage of dogs vaccinated against rabies in urban areas in the Lublin Province.
The number of reported cases of rabies in domestic animals in Poland decreased substantially, and from 2010–2016 in the Lublin Province rabies was confirmed in 18 cats, and in 16 dogs.Citation16
Exposure to wildlife among children is rare (2.9%), and most of these had been exposed to rats. Similar data were reported by Kilic B, et al who reported rat bites in 3% of exposed individuals.Citation17 There were 18 rabies-infected rats found in Poland since 1985, and the last case was in 2001.Citation9 Rabies remained rare in rodents, but the transmission of rabies virus via exposure to a rabid rodent might be possible. Small rodents are rarely infected with rabies, but they can transmit rabies to humans.Citation18 In our study most of the rodents were not available for veterinary observation and testing.
Exposure to foxes was the reason for vaccination in 2 children (1.2% of all those vaccinated). Epidemiological data showed a significant decrease in the number of rabies cases in foxes in Poland, from 3084 in 1992 to 10 in 2015. In 2010 an increase in rabies incidence was observed in Poland, with 117 fox-rabies cases recorded. Phylogenetic analysis of isolates from the outbreak showed their high similarity with the strains circulating in Ukraine and Romania, which might suggest the possible source of origin of the rabies virus in the outbreak.Citation19
Bats have been shown to be an important reservoir of rabies virus. Bat rabies has been laboratory-confirmed in different parts of the world. In Europe, bat rabies in humans is very rare, but in some other parts of the world it is more frequently observed. Exposure to bats, or their secretions, should be considered a potential rabies risk, regardless of the world region in which the exposure occurs.Citation7 In our study PEP was applied to all children exposed to bats. In 2 patients vaccination was stopped due to negative results of a direct fluorescent antibody test from animal brain tissue. In Poland, in the period from 2010 to 2016 there were 62 bats with confirmed rabies.Citation7,Citation16
As a result of the ongoing implementation of ORV, the number of rabies cases reported annually in Europe steadily declined from 17 202 in 1978 to 7581 in 2010. During this period, nine countries successfully eliminated fox rabies from their territory, but regularly reported imported cases of rabies, mainly in pets. The illegal importation of infected animals poses a threat of rabies introduction into rabies-free areas.Citation20
Poland has not achieved rabies-free status yet. It should be pointed out that the rabies situation in the Lublin Province is caused, inter alia, by a cross-border problem. The increasing rabies incidence in the neighboring regions of Ukraine resulted in the re-infection of the Polish side along the common borders. This situation forced the veterinary authority to safeguard its territory by maintaining a vaccination belt in those border areas. Also, animal movement from other parts of Poland to our Province can result in the spread of rabies virus.Citation19
The annual number of animal rabies cases in the Lublin Province has decreased to low levels, and a concomitant decrease in the number of PEP's administered was anticipated but it has actually failed to occur. A similar conclusion has been presented by Middleton D et al. According to the authors, two possible reasons why the rate of PEP administration has not decreased include the strict adherence to recommended guidelines and the administration of PEP when it is not recommended. According to the authors, a reduction in the number of post-exposure prophylaxis administered consistent with the decrease in the animal-rabies cases would provide some financial savings for the Government.Citation21,Citation22 Data from our study indicate that in exposed children PEP was administered in accordance with WHO guidelines.
Immunization followed category-II and category-III exposures to animals in which rabies could neither be ruled out nor confirmed. The possible reason why the number of vaccination's being greater than the number of rabid animals recorded in the Lublin Province are bites by animals unavailable for veterinary observations and also the lack of more frequent reports regarding the current epizootic situation of rabies. Each year about 29 million people receive the PEP regimen worldwide, which prevents an estimated 327 000 annual deaths from rabies.Citation23 In Poland PEP is administered to approximately 7000 people annually, and only 0.8% of these patients also receive RIG. The data from the literature indicate that in some countries in central and Eastern Europe RIG is under-prescribed.Citation11 In our study RIG was applied to only one patient (0.58%).
To prevent rabies cases in humans, certain strategies to improve rabies prophylaxis should be introduced. This involves public education strategies to prevent exposure to animals (e.g. not to touch unattended animals). Another strategy involves a wildlife rabies control program which includes reducing the incidence of rabies vectors such as foxes. The vaccination of domestic animals to provide a barrier when the animal acts as a bridge vector between wildlife and humans also plays an important role. To increase the total number of vaccinated dogs, especially in rural areas, the costs of vaccination could be covered by the government or by the local authorities. The next strategy involves providing post-exposure prophylaxis to humans. Education and resources for public health staff and healthcare providers who assess animal exposure to improve the interpretation of guidelines for PEP are important strategies in prophylaxis.Citation21,Citation22
Since 1989, the European Union (EU) has become the driving force for supporting rabies eradication programs and has been co-financing ORV programs in Member States. Following the accession of Poland to the EU in 2004, the total number of reported rabies cases in Poland has significantly decreased and there is a reasonable hope that the list of rabies-free countries in Europe will increase in the near future. However the risk of recurrence of rabies from bordering infected areas still exists so reliable data from all European countries are needed for more accurate surveillance and coordination in the fight against rabies.
This explains, among others, the significance of data presented in this manuscript.
Our study is a retrospective review of medical records, which is not an ideal way to provide comprehensive information on PEP. As this is one of the limitations of our current study, new research about PEP in children in Poland should be performed.
Conclusions
The exact number of children exposed to animals, and the frequency of PEP administered to the children in the Lublin Province, have in fact remained unknown, and such data have not been published so far. Actually, we have been the first to report data on PEP in children exposed to animals in the Lublin Province. Our data indicate a marked decrease in animal-rabies cases but the Lublin Province has not achieved rabies-free status yet, so children are still at risk of exposure to rabid animals.
The results from our study indicate that the most injuries to children resulted from dog bites.
By 2016 the number of rabid animals in the Lublin Province had decreased to low levels, yet the expected decrease in the number of PEP's administered did not occur. Since all children were vaccinated in accordance with the recommendations, the possible reason for vaccination's being administered in the quantities greater than the number of rabid animals recorded in the Lublin Province are bites by animals unavailable for veterinary observations and also the lack of more frequent reports regarding the current epizootic situation of rabies.
The use of RIG in pediatric patients was very low, and was administered to only one patient (0.58%).
We observed that the yearly numbers of exposed patients were at similar levels, which indicates that education programs should be introduced to reduce the number of exposures in children.
Disclosure of potential conflicts of interest
No potential conflicts of interest were disclosed.
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