Human rabies: evaluation of post-exposure prophylaxis prevalence in Ceará, Brazil, 2007-2015

Kellyn Kessiene de Sousa Cavalcante Carlos Henrique Alencar About the authors

Abstract

Objective:

to analyze the prevalence of inadequate human anti-rabies post-exposure prophylaxis in patients attacked by animals in the state of Ceará, Brazil, 2007-2015.

Methods:

this was a study of the prevalence of inadequate prophylaxis procedures, using data on reported cases of accidents involving animals potentially capable of transmitting rabies registered on the Notifiable Diseases Information System (SINAN) from January 2007 to December 2015.

Results:

of the 231,694 reported cases, 95.8% were found to have inadequate procedures, especially in young people aged under 19 (37.6%), with no difference between the sexes (p=0.04); higher prevalence rate of inadequate procedures occurred with regard to exposure to bites (PR=1.03 - 95%CI 1.02;1.03), multiple injuries (PR=1.07 - 95%CI 1.06;1.07), accidents involving dead/missing animals (RP=1.05 - 95%CI 1.05;1.06), and vaccine treatments (RP=1.03 - 95%CI 1.02;1.03).

Conclusion:

high prevalence of inadequate procedures indicates the need for a better epidemiological evaluation of cases and compliance with the Human Rabies Prophylaxis Technical Standards, in order to ensure adequate anti-rabies prophylaxis procedures.

Keywords:
Prevalence; Post-Exposure Prophylaxis; Rabies; Health Services; Epidemiological Monitoring

Introduction

Human rabies is a highly prevalent anthropozoonosis transmitted to humans by inoculation of the rabies virus present in saliva or secretions of an infected animal, mainly by biting.11. Veloso RD, Aerts DRGC, Fetzer LO, Anjos CB, Sangiovanni JC. Perfil epidemiológico do atendimento antirrábico humano em Porto Alegre, RS, Brasil. Ciênc Saúde Coletiva. 2011 dez;16(12):4875-84. doi: 10.1590/S1413-81232011001300036.
https://doi.org/10.1590/S1413-8123201100...
This disease continues to be a public health problem due to its serious clinical consequences, high fatality and costs of post-exposure treatment and medical care.22. Malanczyn AA, Selow MLC, Toniolo RMM. Análise das notificações de acidentes antirrábicos no município de curitiba, nos últimos 3 anos. Rev Dom Acadêmico. 2017;1(1).

Between 2009 and 2011, there were 592,000 anti-rabies attendances per year in Brazil.33. Wada MY, Rocha SM, Maia-Elkhoury ANS. Situação da raiva no Brasil, 2000 a 2009. Epidemiol Serv Saúde. 2011 dez;20(4):509-18. doi: 10.5123/S1679-49742011000400010.
https://doi.org/10.5123/S1679-4974201100...
This frequency increased in the period from 2011 to 2016, with 3,628,549 human anti-rabies attendances reported in the country, especially in the Southeast and Northeast regions, where a greater number of cases were recorded: 1,433,773 and 998,008 notifications, respectively.44. Ministério da Saúde (BR). Análise da situação epidemiológica da Raiva no Brasil, no período de 2011 a 2016* [Internet]. 2016 [citado 2018 set 13]. Disponível em: Disponível em: http://portalarquivos2.saude.gov.br/images/pdf/2016/maio/27/Informe-epidemiol--gico-raiva.pdf
http://portalarquivos2.saude.gov.br/imag...

Whenever exposure to the virus is suspected, human rabies prophylaxis is the main control measure. In these cases, a Notifiable Disease Information System (SINAN) human anti-rabies attendance notification form must be filled in.55. Francelino BLBS, Cavalcante KKS, Alencar CHM. Completude das notificações de atendimentos antirrábicos humanos pós-exposição no estado do Ceará, 2007 a 2015. Enc Univers UFC. 2016;1(1):5050. The post-exposure prophylaxis regimen is composed of procedures that range from simply washing the wounded area with soap and water, to complete treatment with serum and vaccine.66. Frias DFR, Nunes JOR, Carvalho AAB. Proposta de nova metodologia de apoio para indicação racional de profilaxia antirrábica humana pós-exposição. Arq Ciênc Saúde UNIPAR. 2016 jan-abr;20(1):9-18. doi: 10.25110/arqsaude.v20i1.2016.4955.
https://doi.org/10.25110/arqsaude.v20i1....
Vaccine dosage is the same regardless of the patient’s age, sex or weight.77. Brito WI, Pazdziora AZ. Análise das condutas profiláticas da raiva humana realizadas em Primavera do Leste/MT, 2011: avaliação sobre o uso dos insumos. Rev Epidemiol Control Infect. 2013 jul-set;3(3):87-92. The decision to initiate post-exposure prophylaxis should be made following complete and thorough anamnesis of the case in accordance with the Human Rabies Prophylaxis Technical Standards.88. Ministério da Saúde (BR). Secretaria de Vigilância em Saúde. Departamento de Vigilância Epidemiológica. Normas técnicas de profilaxia da raiva humana [Internet]. Brasília: Ministério da Saúde; 2014[citado 2018 ser 13]. 60 p. Disponível em: Disponível em: http://portalarquivos.saude.gov.br/images/pdf/2015/outubro/19/Normas-tecnicas-profilaxia-raiva.pdf
http://portalarquivos.saude.gov.br/image...

Analysis of accidents caused by animals potentially capable of transmitting rabies enables the evaluation and improvement of health care and epidemiological surveillance services, thus informing secure and correct indication of prophylactic treatment and targeting of individual and collective prevention and control actions.22. Malanczyn AA, Selow MLC, Toniolo RMM. Análise das notificações de acidentes antirrábicos no município de curitiba, nos últimos 3 anos. Rev Dom Acadêmico. 2017;1(1).

Given the importance and the need to provide input to support human rabies epidemiological information and actions for its surveillance and control, we sought to analyze the prevalence of inadequate human anti-rabies prophylaxis among patients attacked by animals in Ceará, Brazil, between 2007 and 2015.

Methods

This was a prevalence study based on secondary data, using information taken from notification forms for accidents caused by animals potentially capable of transmitting rabies registered on the SINAN system by the Ceará State Health Department epidemiological surveillance sector from January 1st 2007 to December 31st 2015.

The state of Ceará is located in the Northeast region of Brazil. It has a population of almost 9 million inhabitants and an area of approximately 149,000 km², divided into 184 municipalities. Ceará’s Public Health system is comprised of municipal and state hospitals, totaling 164 inpatient hospital units and 2,198 outpatient units, in addition to 652 primary health care units.99. Ministério da Saúde (BR). Departamento de informática do SUS, 2016 [Internet]. 2017 [citado 2017 mar 13]. Disponível em: Disponível em: http:// datasus.saude.gov.br/informacoes-de-saude/ferramentas/tabwin
http:// datasus.saude.gov.br/informacoes...

According to the Brazilian Institute of Geography and Statistics (IBGE), in 2014 there were 944,000 households (35.2%) with dogs in Ceará, and 725,000 (28%) with cats. Of these households, 76.3% had had these animals vaccinated against rabies that same year.99. Ministério da Saúde (BR). Departamento de informática do SUS, 2016 [Internet]. 2017 [citado 2017 mar 13]. Disponível em: Disponível em: http:// datasus.saude.gov.br/informacoes-de-saude/ferramentas/tabwin
http:// datasus.saude.gov.br/informacoes...

The study analyzed the following variables:

  1. a) sociodemographic characteristics

  2. - age group (in years: <1, 1-19, 20-39, 40-59, 60 and over);

  3. - sex (male, female);

  4. - ethnicity/skin color (brown, white, black, Asian, indigenous);

  5. - level of schooling (illiterate, junior school, middle school, high school, higher education); and

  6. - area of residence (urban, rural, peri-urban areas);

  7. b) injury

  8. - type of exposure (indirect contact, scratching, licking, biting, other);

  9. - injury location (hands/feet, lower limbs, upper limbs, head/neck, torso, mucous membrane), injury presentation (single, multiple, without injury); and

  10. - lesion depth (superficial, deep, lacerations);

  11. c) characteristics of the animal involved

  12. - species (dog, cat, bat, other); and

  13. - animal condition (healthy, suspect, rabid, dead/missing); and

  14. d) type of treatment (observation, observation and vaccine, vaccine, serum and vaccine, other).

To define whether case procedure was adequate or inadequate for the type of exposure suffered by the patient, the 'mild case procedure' and 'serious case procedure' variables were created, based on the Human Rabies Prophylaxis Technical Standards.88. Ministério da Saúde (BR). Secretaria de Vigilância em Saúde. Departamento de Vigilância Epidemiológica. Normas técnicas de profilaxia da raiva humana [Internet]. Brasília: Ministério da Saúde; 2014[citado 2018 ser 13]. 60 p. Disponível em: Disponível em: http://portalarquivos.saude.gov.br/images/pdf/2015/outubro/19/Normas-tecnicas-profilaxia-raiva.pdf
http://portalarquivos.saude.gov.br/image...

Mild cases were defined by the presence of superficial injuries covering a small area, usually only on the torso and limbs. Serious cases were considered to be: injuries to the head, face, neck, hand, digital pulp and/or sole of the foot; deep, multiple or extensive injuries to any region of the body; licking of mucous membranes; and deep wound caused by an animal claw.77. Brito WI, Pazdziora AZ. Análise das condutas profiláticas da raiva humana realizadas em Primavera do Leste/MT, 2011: avaliação sobre o uso dos insumos. Rev Epidemiol Control Infect. 2013 jul-set;3(3):87-92.,1010. Fernandes MIM. Acidentes rábicos em município do norte do Paraná: uma análise do perfil, conduta e sistema de notificação [dissertação]. Botucatu (SP): Universidade Estadual Paulista Julio de Mesquita Filho, Faculdade de Medicina de Botucatu; 2013. As such, with the aim of evaluating the prophylactic case procedure adopted for each attendance, the 'adequate prophylactic procedure' variable was created, considered to be the outcome of this study, resulting from the characteristics of cases described as 'mild case procedure' or 'serious case procedure'. This classification included variables related to the type of injury, location and depth of lesion, type of exposure, species and condition of the animal involved, as well as whether or not vaccination treatment was initiated. Patient care that did not follow the Ministry of Health protocol or had records with blank or incomplete data was considered to be inadequate, whether because of lack of or excess treatment.

The prevalence coefficients for accidents caused by animals potentially capable of transmitting rabies were standardized using the direct method. The standard population used as the denominator was the population of Ceará state in 2010 as per the IBGE demographic census. Data on the resident population estimated for each year was obtained from the Brazilian Unified Health System IT Department (DATASUS) website.99. Ministério da Saúde (BR). Departamento de informática do SUS, 2016 [Internet]. 2017 [citado 2017 mar 13]. Disponível em: Disponível em: http:// datasus.saude.gov.br/informacoes-de-saude/ferramentas/tabwin
http:// datasus.saude.gov.br/informacoes...

The data were exported and analyzed using Stata version 11.2 (Stata Corp LP, College Station, TX, USA). In order to test associations of interest, prevalence ratios (PR) were calculated with a 95% confidence interval (95%CI) and Pearson’s chi-squared test or Fisher's exact test were carried out using a 5% significance level. The spatial distribution of the incidence coefficients was plotted using ArcGis version 9.2.

The study project was submitted to Plataforma Brasil and was approved by the Federal University of Ceará Research Ethics Committee on 6 April 2017 - Certification of Submission for Ethical Appraisal (CAAE) No. 64830316.0.0000.5054 - being in accordance with the principles of National Health Council (CNS) Resolution No. 466, dated 12 December 2012 (autonomy, non-maleficence, beneficence, justice and equity). The study was based on secondary data taken from the SINAN system with no identification of individuals surveyed.

Results

From 2007 to 2015, there were 231,694 registered cases of accidents caused by animals potentially capable of transmitting rabies in Ceará state. Of this total, 222,036 (95.8%) showed inadequate procedures regarding anti-rabies prophylactic treatment as recommended by the Ministry of Health. In addition, incompleteness was found on the forms used for the notification of accidents caused by animals potentially capable of transmitting rabies, with a total of 142,562 fields with no information or information unknown. A higher proportion of this missing information was found for the variables 'schooling' (32.9%) and 'lesion depth' (11.5%).

The period between 2010 and 2011 showed a greater increase in standardized coefficients of prevalence of inadequate procedure, from 24.64 (2010) to 36.54 (2011) per 10,000 inhabitants. The highest value of this coefficient was observed in 2015: 41.58 attendances per 10,000 inhab. (Figure 1).

Figure 1
- Standardized prevalence coefficients for inadequate human rabies procedure attendances (per 10,000 inhabitants), per annum, Ceará, 2007-2015

The number of inadequate procedures was more frequent in the 1 to 19 years age range (n=82,545; 37.6%). There was no difference between the sexes, with PR=0.99 (95% CI 0.99; 1.00). With regard to ethnicity/skin color, only the Asian category had a slightly higher prevalence ratio of 1.02 (95%CI 1.01;1.02). People with complete primary school education had slightly higher prevalence than those with other levels of schooling and this was statistically significant (PR=1.01 - 95% CI1.01;1.02). Those living in urban areas had the largest amount of inadequate prophylaxis (n=143,691; 70.3%) and had prevalence 7% higher (95%CI 1.05;1.08) than those living in the peri-urban area of municipalities in Ceará (Table 1).

Table 1
- Bivariate analysis of human rabies attendances according to sociodemographic characteristics and suitability of procedure adopted, Ceará, 2007-2015

The wound characteristic with the highest prevalence of inadequate procedures was exposure to bites (PR=1.03 95% CI1.02;1.03). Wounds located in hands/feet - 86,169 notifications (38.4%) - were more frequent and 1.06 times more prevalent regarding inadequate procedures (95%CI 1.06;1.07) (Table 2).

Table 2
- Bivariate analysis of human rabies according to characteristics of the wound and suitability of the procedure adopted, Ceará, 2007-2015

Multiple injuries showed higher prevalence of inadequate procedure (PR=1.07 95% CI 1.06;1.07) when compared to single injuries. Another characteristic having more prevalent inadequate prophylactic procedure was deep wounds (PR=1.09 95% CI1.08;1.09). It should be noted that some patients have more than one type of exposure and lesion location (Table 2).

Dogs were the main animals involved (n=162,243; 70.0%) and accidents caused by them were associated with a greater proportion of inadequate procedure (69.6%; 154.505/221.943); however, inadequate procedure was 1.05 times more prevalent among people attacked by other types of animals (PR=1.05 CI95% 1.04;1.05) when compared to those attacked by dogs. Other types of animals involved included primates, domestic herbivores, foxes, skunks, capybaras, pigs, cattle, horses, rabbits, lizards, donkeys, agoutis, boars and sheep.

The most frequent animal condition was that of healthy animals in relation to inadequate procedures found (71.3%). There was higher prevalence (PR=1.05 CI95% 1.05;1.06) of care provided to victims of animals classified as dead/missing when compared to cases involving healthy animals.

The treatment prescribed for the highest proportion of attendances (48.1%) was observation together with vaccination, although it had a lower inadequate procedure prevalence ratio (PR=0.95 - IC95% 0.94;0.95) when compared with to patients being advised just to keep the animal under observation for ten days. Treatment having the highest prevalence of inadequate procedures (PR=1.03 95%CI1.02;1.03) was vaccine prescription. Treatment was interrupted in 8,151 (6.1%) cases and these had a high prevalence of inadequate procedures (PR=1.05 95% CI1.04;1.05) (Table 3).

Table 3
- Bivariate analysis of human rabies according to species of attacking animal, type of treatment and suitability of procedure adopted, Ceará, 2007-2015

Serum was not prescribed in 85.2% of cases and inadequate procedures were 5% more prevalent (95% CI1.05;1.06) in these cases when compared to cases in which serum was prescribed as treatment.

The municipalities of Guaramiranga, Jijoca de Jericoacoara and Jaguaruana, located in the mid north, northwest and northeast regions of Ceará state, had the highest prevalence of attendances with inadequate procedures per 10,000 inhab.: 222.26, 131.45 and 115.05 respectively. A little more than half of the municipalities (54.3%) had low prevalence rates, with values between 0.10 and 29.88 for inadequate procedures per 10,000 inhab. The lowest values were recorded in the municipality of Poranga (2.83 per 10,000 inhab.) in the western region of the state, and Altaneira (2.91 per 10,000 inhab.) and Umari (6.05 per 10,000 inhab.) in the southern region of the state (Figure 2).

Figure 2
- Standardized prevalence coefficients for inadequate human rabies procedure attendances (per 10,000 inhabitants), per municipality, Ceará, 2007-2015

Discussion

Our study found that between 2007 and 2015 in the state of in Ceará, more than 90% of attendances for accidents caused by animals potentially capable of transmitting rabies involved inadequate procedures when compared to anti-rabies prophylactic treatment recommended by the Ministry of Health. Among cases involving inadequate procedures, indicators point to biting as the most frequent exposure type, as well as prevalence of multiple deep injuries to the hands/feet, with prescription of vaccines being the type of post-exposure treatment adopted.

It is probable that inadequate procedures increased during the period studied due to the high turnover of physicians or nurses and absence of education actions. The findings of our study suggest the possibility of health professionals being insecure when prescribing treatment. In most cases, these professionals usually indicate more doses than necessary for the type of patient exposure, failing to take into consideration the epidemiological aspects of each case of accidents caused by animals potentially capable of transmitting rabies.1111. Carvalho WO, Soares DFPP, Franceschi VCS. Características do atendimento prestado pelo serviço de profilaxia da raiva humana na rede municipal de saúde de Maringá-Paraná, no ano de 1997. Inf Epidemiol SUS. 2002 mar;11(1):25-35. doi: 10.5123/S0104-16732002000100004.
https://doi.org/10.5123/S0104-1673200200...

These results are similar to those found in the United States, specifically in the municipality of Carolina, where indicated anti-rabies treatment was found to be inadequate in 98% of attendances between 1995 and 2003. Among cases receiving treatment, 40% did not need it, and among those not treated, 6.3% should have received treatment.1212. Moriwaki AM, Masukawa MLT, Uchimura NS, Santana RG, Uchimura TT. Evaluation of primary care prophylaxis post-exposure to the rabies virus. Acta Paul Enferm. 2013;26(5):428-35. doi: 10.1590/S0103-21002013000500005.
https://doi.org/10.1590/S0103-2100201300...
Inadequate and insufficient procedures can be propitious to the development of human rabies when the vaccine or serum regimen is not sufficient for proper treatment.1818. Minitério da Saúde (BR). Sistema de informação do programa nacional de imunizações, 2015 [Internet]. 2016 [citado 2018 fev 13]. Disponível em: Disponível em: http://pni.datasua.gov.br
http://pni.datasua.gov.br...

In contrast, some studies conducted in Brazil have suggested that the proportion of inadequate anti-rabies procedures varies between 3.8% and 24.7%. These studies found that 96.2%, 93.9% and 92.0% of the attendances had adequate procedures in the cities of Porto Alegre (2006), Curitiba (2010) and Maringá (1997), respectively, showing a low percentage of inadequate procedures.11. Veloso RD, Aerts DRGC, Fetzer LO, Anjos CB, Sangiovanni JC. Perfil epidemiológico do atendimento antirrábico humano em Porto Alegre, RS, Brasil. Ciênc Saúde Coletiva. 2011 dez;16(12):4875-84. doi: 10.1590/S1413-81232011001300036.
https://doi.org/10.1590/S1413-8123201100...
,1010. Fernandes MIM. Acidentes rábicos em município do norte do Paraná: uma análise do perfil, conduta e sistema de notificação [dissertação]. Botucatu (SP): Universidade Estadual Paulista Julio de Mesquita Filho, Faculdade de Medicina de Botucatu; 2013.,1111. Carvalho WO, Soares DFPP, Franceschi VCS. Características do atendimento prestado pelo serviço de profilaxia da raiva humana na rede municipal de saúde de Maringá-Paraná, no ano de 1997. Inf Epidemiol SUS. 2002 mar;11(1):25-35. doi: 10.5123/S0104-16732002000100004.
https://doi.org/10.5123/S0104-1673200200...
In Southern Brazil, no human rabies cases have been reported since 1987, and Paraná was the first Brazilian state to control rabies.1111. Carvalho WO, Soares DFPP, Franceschi VCS. Características do atendimento prestado pelo serviço de profilaxia da raiva humana na rede municipal de saúde de Maringá-Paraná, no ano de 1997. Inf Epidemiol SUS. 2002 mar;11(1):25-35. doi: 10.5123/S0104-16732002000100004.
https://doi.org/10.5123/S0104-1673200200...

Prescription of anti-rabies treatment in excess of what is necessary may possibly be due to fear of patients becoming ill. However, adequate procedures ensure proper prevention of the disease. Considering the high risk of exposure to rabies, the approaches adopted in the state of Ceará related to cases of serious injury should use correct prophylaxis prescribed and monitored according to Ministry of Health standards.88. Ministério da Saúde (BR). Secretaria de Vigilância em Saúde. Departamento de Vigilância Epidemiológica. Normas técnicas de profilaxia da raiva humana [Internet]. Brasília: Ministério da Saúde; 2014[citado 2018 ser 13]. 60 p. Disponível em: Disponível em: http://portalarquivos.saude.gov.br/images/pdf/2015/outubro/19/Normas-tecnicas-profilaxia-raiva.pdf
http://portalarquivos.saude.gov.br/image...

We emphasize the importance of completeness and consistency when filling out notification forms for accidents caused by animals potentially capable of transmitting rabies as this helps to indicate the most adequate prophylactic procedure for each case.55. Francelino BLBS, Cavalcante KKS, Alencar CHM. Completude das notificações de atendimentos antirrábicos humanos pós-exposição no estado do Ceará, 2007 a 2015. Enc Univers UFC. 2016;1(1):5050.

In Campo Grande, capital of Mato Grosso do Sul state, in 2002, 49.4% of the 723 people attended to did not complete full anti-rabies treatment because the local health service did not undertake active tracing.1313. Rigo L, Honer MR. Análise da profilaxia da raiva humana em Campo Grande, Mato Grosso do Sul, Brasil, em 2002 human rabies prophylaxis in Campo Grande, Mato Grosso do Sul State, Brazil, 2002. Cad Saúde Pública. 2005 nov-dez;21(6):1939-45. doi: 10.1590/S0102-311X2005000600044.
https://doi.org/10.1590/S0102-311X200500...
It is important to highlight that active tracing of people who fail to attend medical appointments is one of the actions recommended for surveillance of human rabies, in order to ensure treatment with better results and quality.1414. Bertozzi M, Rinaldi VE, Cara GD, Appignani A. A glance at rabies pre-exposure and post-exposure prophylaxis for dog bites. Afr J Paediatr Surg. 2016 Apr-Jun;13(2):107-8. doi: 10.4103/0189-6725.182569.
https://doi.org/10.4103/0189-6725.182569...
Failure to initiate treatment or failure to follow treatment correctly can result in patients being victims of rabies.1515. Souza DN, Carnieli Júnior P, Macedo CI, Oliveira RN, Batista HBCR, Rodrigues AC, et al. Phylogenetic analysis of rabies virus isolated from canids in North and Northeast Brazil. Arch Virol. 2017 Jan;162(1):71-7. doi: 10.1007/s00705-016-3079-1.
https://doi.org/10.1007/s00705-016-3079-...

Health professionals should be constantly trained and supervised as to the treatment procedures for accidents with animals potentially capable of transmitting rabies and protection of patients through the rational use of immunobiologicals, always performing a thorough epidemiological investigation of each case, as well as filling out all fields of the SINAN system notification from.55. Francelino BLBS, Cavalcante KKS, Alencar CHM. Completude das notificações de atendimentos antirrábicos humanos pós-exposição no estado do Ceará, 2007 a 2015. Enc Univers UFC. 2016;1(1):5050.,66. Frias DFR, Nunes JOR, Carvalho AAB. Proposta de nova metodologia de apoio para indicação racional de profilaxia antirrábica humana pós-exposição. Arq Ciênc Saúde UNIPAR. 2016 jan-abr;20(1):9-18. doi: 10.25110/arqsaude.v20i1.2016.4955.
https://doi.org/10.25110/arqsaude.v20i1....
,1414. Bertozzi M, Rinaldi VE, Cara GD, Appignani A. A glance at rabies pre-exposure and post-exposure prophylaxis for dog bites. Afr J Paediatr Surg. 2016 Apr-Jun;13(2):107-8. doi: 10.4103/0189-6725.182569.
https://doi.org/10.4103/0189-6725.182569...

There was a predominance of inadequate anti-rabies procedures among people with a low level of schooling, namely those in the illiterate and complete junior school categories66. Frias DFR, Nunes JOR, Carvalho AAB. Proposta de nova metodologia de apoio para indicação racional de profilaxia antirrábica humana pós-exposição. Arq Ciênc Saúde UNIPAR. 2016 jan-abr;20(1):9-18. doi: 10.25110/arqsaude.v20i1.2016.4955.
https://doi.org/10.25110/arqsaude.v20i1....
,1616. Filgueira AC, Cardoso MD, Ferreira LOC. Profilaxia antirrábica humana: uma análise exploratória dos atendimentos ocorridos em Salgueiro-PE, no ano de 2007. Epidemiol Serv Saúde. 2011 abr-jun;20(2):233-44. doi: 10.5123/S1679-49742011000200012.
https://doi.org/10.5123/S1679-4974201100...
As well as facilitating the spread of the virus in a given area, social factors also reveal that the lower the level of local development, the greater the indiscriminate mixing between humans and animals and the lower the levels of hygiene.

In Ceará, the urban area stood out as the place of residence. This fact was also found in the states of Santa Catarina and Paraná between 2002 and 2007.1010. Fernandes MIM. Acidentes rábicos em município do norte do Paraná: uma análise do perfil, conduta e sistema de notificação [dissertação]. Botucatu (SP): Universidade Estadual Paulista Julio de Mesquita Filho, Faculdade de Medicina de Botucatu; 2013. An increase in the animal population in public places can be considered to be a threat to public health, given the possibility of attack and zoonosis transmission.99. Ministério da Saúde (BR). Departamento de informática do SUS, 2016 [Internet]. 2017 [citado 2017 mar 13]. Disponível em: Disponível em: http:// datasus.saude.gov.br/informacoes-de-saude/ferramentas/tabwin
http:// datasus.saude.gov.br/informacoes...

The control of urban rabies in cats and dogs in Ceará is done mainly by means of anti-rabies vaccination campaigns coordinated by the State Health Department in accordance with Ministry of Health recommendations. In the campaign held in 2016, Ceará achieved coverage of 89.5% of dogs vaccinated.1818. Minitério da Saúde (BR). Sistema de informação do programa nacional de imunizações, 2015 [Internet]. 2016 [citado 2018 fev 13]. Disponível em: Disponível em: http://pni.datasua.gov.br
http://pni.datasua.gov.br...
The recommended Brazilian Ministry of Health goal is that 80% of dogs should be immunized annually.1111. Carvalho WO, Soares DFPP, Franceschi VCS. Características do atendimento prestado pelo serviço de profilaxia da raiva humana na rede municipal de saúde de Maringá-Paraná, no ano de 1997. Inf Epidemiol SUS. 2002 mar;11(1):25-35. doi: 10.5123/S0104-16732002000100004.
https://doi.org/10.5123/S0104-1673200200...
,1919. Martins VB, Oliveira FG, Dias AVAB, Moreira WC. Avaliação do diagnóstico laboratorial do programa de controle da raiva urbana no Rio de Janeiro, Brasil entre 2002-2011. Vig Sanit Debate. 2015 ago;3(3):56-63. doi: 10.3395/2317-269x.00245.
https://doi.org/10.3395/2317-269x.00245...
However, Ceará is still considered a state with a risk of rabies transmission to humans, because there is no homogeneity in canine vaccination among municipalities, nor are cases recorded: the last rabies case, which resulted in death, was recorded in October 2016 in the municipality of Iracema in the mid eastern region of the state (latitude -5.80, longitude -38.30).2020. Ministério da Saúde (BR). Secretaria de Vigilância em Saúde. Nota informativa conjunta nº 001, de 2016 - DEVIT/SVS/MS e COPROM/SESA/CE. Informações sobre casos de raiva em Iracema - CE [Internet]. 2016 [citado 2018 set 13]. Disponível em: Disponível em: http://www.saude.ce.gov.br/index.php/notas-tecnicas?download=2751%3Anota
http://www.saude.ce.gov.br/index.php/not...

Vaccination of susceptible animals, control of the canine population and post-exposure prophylaxis are important strategies for reducing the risk of occurrence of rabies.2121. Arya JM, Dewitt K, Scott-Garrard M, Chiang YW, Prausnitz MR. Rabies vaccination in dogs using a dissolving microneedle patch. J Control Release. 2016 Oct;239:19-26. doi: 10.1016/j.jconrel.2016.08.012.
https://doi.org/10.1016/j.jconrel.2016.0...

The municipalities of Santana do Acaraú and Acarape, in mid north region of Ceará, had high incidence coefficients for attendances with inadequate procedures. This finding goes hand in hand with the lower rates of coverage of the 2016 animal anti-rabies vaccination campaign.1818. Minitério da Saúde (BR). Sistema de informação do programa nacional de imunizações, 2015 [Internet]. 2016 [citado 2018 fev 13]. Disponível em: Disponível em: http://pni.datasua.gov.br
http://pni.datasua.gov.br...
On the other hand, the municipalities of Pentecoste and Guaramiranga, although they had high incidence of inadequate prophylactic procedures, achieved vaccine coverage rates of 93.2% and 100.9%, 18 respectively, this being above the target recommended by the Ministry of Health. In these municipalities, control of the canine population is recommended in places where a high number of accidents involving animals potentially capable of transmitting rabies is recorded.2222. Ilyas N, Rahim K, Latif Z. Incidence of dog bite in rural area (Chountra), District Rawalpindi, Province Punjab, Pakistan. J Med Allied Sci. 2017 Jul;7(2):99-102. doi: 10.5455/jmas.263073.
https://doi.org/10.5455/jmas.263073...

Although dogs were the main animals to attack humans, higher prevalence of inadequate procedures occurred in relation to other animal species, possibly because some of the animals mentioned are not potential rabies transmitters, such as rabbits and hamsters, and do not require prophylactic treatment.88. Ministério da Saúde (BR). Secretaria de Vigilância em Saúde. Departamento de Vigilância Epidemiológica. Normas técnicas de profilaxia da raiva humana [Internet]. Brasília: Ministério da Saúde; 2014[citado 2018 ser 13]. 60 p. Disponível em: Disponível em: http://portalarquivos.saude.gov.br/images/pdf/2015/outubro/19/Normas-tecnicas-profilaxia-raiva.pdf
http://portalarquivos.saude.gov.br/image...
,2323. Abdrakhmanov SK, Beisembayev KK, Кorennoy FI, Yessembekova GN, Кushubaev DB, Кadyrov AS. Revealing spatio-temporal patterns of rabies spread among various categories of animals in the Republic of Kazakhstan, 2010-2013. Geospatial Health. 2016 May;11(2):455. doi: 10.4081/gh.2016.455.
https://doi.org/10.4081/gh.2016.455...
In Brazil, from 2000 to 2009, three cases of human rabies transmitted by herbivores were confirmed. In all three cases, transmission occurred by direct manipulation of saliva and not because of attacks by these animals.33. Wada MY, Rocha SM, Maia-Elkhoury ANS. Situação da raiva no Brasil, 2000 a 2009. Epidemiol Serv Saúde. 2011 dez;20(4):509-18. doi: 10.5123/S1679-49742011000400010.
https://doi.org/10.5123/S1679-4974201100...

Inadequate procedures were most prevalent in relation to accidents involving animals in the dead/missing category. This is another finding of concern, because when accidents are caused by an animal in this condition they are considered to be serious and require complete post-exposure treatment with cell culture vaccines and/or administration of anti-rabies serum up until the third dose of the vaccine, according to the Human Rabies Prophylaxis Technical Standards published by the Brazilian Ministry of Health.88. Ministério da Saúde (BR). Secretaria de Vigilância em Saúde. Departamento de Vigilância Epidemiológica. Normas técnicas de profilaxia da raiva humana [Internet]. Brasília: Ministério da Saúde; 2014[citado 2018 ser 13]. 60 p. Disponível em: Disponível em: http://portalarquivos.saude.gov.br/images/pdf/2015/outubro/19/Normas-tecnicas-profilaxia-raiva.pdf
http://portalarquivos.saude.gov.br/image...

Higher prevalence of inadequate procedures in the case of animals in the dead/missing category suggests that when health professionals indicate the prophylactic procedure to be used, they do not take into account the condition of the animal involved, as found in a study conducted in Southeast Brazil, where post-exposure prophylaxis was initiated based only on the characteristics of the wounds.2424. Frias DFR, Nunes JOR, Carvalho AAB. Caracterização de agravos causados por cães e gatos a seres humanos no município de Jaboticabal, São Paulo, durante o período de 2000 a 2009. Arch Vet Sci. 2012:17(3):63-70. doi: 10.5380/avs.v17i3.24824.
https://doi.org/10.5380/avs.v17i3.24824...

In our study, the most common type of exposure was biting. According to research conducted in 2006 in the municipality of Porto Alegre, Rio Grande do Sul,11. Veloso RD, Aerts DRGC, Fetzer LO, Anjos CB, Sangiovanni JC. Perfil epidemiológico do atendimento antirrábico humano em Porto Alegre, RS, Brasil. Ciênc Saúde Coletiva. 2011 dez;16(12):4875-84. doi: 10.1590/S1413-81232011001300036.
https://doi.org/10.1590/S1413-8123201100...
and in 2011 in the municipality of Primavera do Leste, Mato Grosso,1313. Rigo L, Honer MR. Análise da profilaxia da raiva humana em Campo Grande, Mato Grosso do Sul, Brasil, em 2002 human rabies prophylaxis in Campo Grande, Mato Grosso do Sul State, Brazil, 2002. Cad Saúde Pública. 2005 nov-dez;21(6):1939-45. doi: 10.1590/S0102-311X2005000600044.
https://doi.org/10.1590/S0102-311X200500...
people recognize that this type of exposure represents a great risk of contamination by the rabies virus, due to there being several points for virus entry - which is not the case with scratches, licking or indirect contact.

Multiple injuries to the hands/feet77. Brito WI, Pazdziora AZ. Análise das condutas profiláticas da raiva humana realizadas em Primavera do Leste/MT, 2011: avaliação sobre o uso dos insumos. Rev Epidemiol Control Infect. 2013 jul-set;3(3):87-92.,2525. Silva GM, Brandespim DF, Rocha MDG, Leite RMB, Oliveira JMB. Notificações de atendimento antirrábico humano na população do município de Garanhuns, Estado de Pernambuco, Brasil, no período de 2007 a 2010. Epidemiol Serv Saúde. 2013 jan-mar;22(1):95-102. doi: 10.5123/S1679-49742013000100010.
https://doi.org/10.5123/S1679-4974201300...
,2626. Cavalcante KK, Florêncio CM, Alencar CH. Profilaxia antirrábica humana pós-exposição: características dos atendimentos no estado do Ceará, 2007-2015. J Health Biol Sci. 2017;5(4):337-45. doi: 10.12662/2317-3076jhbs.v5i4.1348.p337-345.2017.
https://doi.org/10.12662/2317-3076jhbs.v...
had the highest proportion of inadequate procedures. In these cases, wound location and lesion depth in nerve endings facilitate the virulence of the etiologic agent, potentiate the risk involved and impose the need for complete treatment with anti-rabies serum and vaccine.88. Ministério da Saúde (BR). Secretaria de Vigilância em Saúde. Departamento de Vigilância Epidemiológica. Normas técnicas de profilaxia da raiva humana [Internet]. Brasília: Ministério da Saúde; 2014[citado 2018 ser 13]. 60 p. Disponível em: Disponível em: http://portalarquivos.saude.gov.br/images/pdf/2015/outubro/19/Normas-tecnicas-profilaxia-raiva.pdf
http://portalarquivos.saude.gov.br/image...
Furthermore, we found that lacerations and deep wounds were considered protective factors against inadequate procedures, given that as they are usually caused by animals considered to be suspect, such cases are characterized as serious accidents.1010. Fernandes MIM. Acidentes rábicos em município do norte do Paraná: uma análise do perfil, conduta e sistema de notificação [dissertação]. Botucatu (SP): Universidade Estadual Paulista Julio de Mesquita Filho, Faculdade de Medicina de Botucatu; 2013. These characteristics of protection - place of injury and lesion depth -, which were also detected in a study conducted in the state of Paraná, decreased by 82% and 64%, respectively, the risk of inadequate procedure.1010. Fernandes MIM. Acidentes rábicos em município do norte do Paraná: uma análise do perfil, conduta e sistema de notificação [dissertação]. Botucatu (SP): Universidade Estadual Paulista Julio de Mesquita Filho, Faculdade de Medicina de Botucatu; 2013.

There was a higher percentage of vaccine prescription for post-exposure anti-rabies treatment,1717. Silva AMR. Características do atendimento anti-rábico humano no Estado de Santa Catarina, área considerada sob controle para a raiva no ciclo urbano-2002 a 2007 [Trabalho de Conclusão de Curso]. Florianópolis (SC): Departamento de Saúde Pública do Centro de Ciências da Saúde, Universidade Federal de Santa Catarina, 2007. although it is a procedure indicated only in the case of dogs and cats that can be kept under observation, due to the rabies incubation period, or in cases of mild accidents88. Ministério da Saúde (BR). Secretaria de Vigilância em Saúde. Departamento de Vigilância Epidemiológica. Normas técnicas de profilaxia da raiva humana [Internet]. Brasília: Ministério da Saúde; 2014[citado 2018 ser 13]. 60 p. Disponível em: Disponível em: http://portalarquivos.saude.gov.br/images/pdf/2015/outubro/19/Normas-tecnicas-profilaxia-raiva.pdf
http://portalarquivos.saude.gov.br/image...
,2323. Abdrakhmanov SK, Beisembayev KK, Кorennoy FI, Yessembekova GN, Кushubaev DB, Кadyrov AS. Revealing spatio-temporal patterns of rabies spread among various categories of animals in the Republic of Kazakhstan, 2010-2013. Geospatial Health. 2016 May;11(2):455. doi: 10.4081/gh.2016.455.
https://doi.org/10.4081/gh.2016.455...
It is therefore not recommended for accidents classified as serious in our study.

Higher prevalence of inadequate procedures was related to indication of treatment with anti-rabies serum. Serum should only be used in the following cases: a serious accident in which the animal (dog or cat) has disappeared, died or become rabid; an accident involving an animal clinically suspected of having rabies at the moment of the attack; or a serious accident caused by a wild animal or by production.77. Brito WI, Pazdziora AZ. Análise das condutas profiláticas da raiva humana realizadas em Primavera do Leste/MT, 2011: avaliação sobre o uso dos insumos. Rev Epidemiol Control Infect. 2013 jul-set;3(3):87-92. However, lack of integration between health professionals who prescribe anti-rabies regimens and veterinarians, with regard to verification of the attacking animals, does not provide the security needed to contraindicate the administration of immunobiologicals.

Probably due to insecurity, health professionals who prescribe treatment administer anti-rabies prophylaxis without following the Ministry of Health protocol.66. Frias DFR, Nunes JOR, Carvalho AAB. Proposta de nova metodologia de apoio para indicação racional de profilaxia antirrábica humana pós-exposição. Arq Ciênc Saúde UNIPAR. 2016 jan-abr;20(1):9-18. doi: 10.25110/arqsaude.v20i1.2016.4955.
https://doi.org/10.25110/arqsaude.v20i1....
,2121. Arya JM, Dewitt K, Scott-Garrard M, Chiang YW, Prausnitz MR. Rabies vaccination in dogs using a dissolving microneedle patch. J Control Release. 2016 Oct;239:19-26. doi: 10.1016/j.jconrel.2016.08.012.
https://doi.org/10.1016/j.jconrel.2016.0...
Indication of the type of treatment to be used should be in accordance with the characteristics of the accident, always taking into account the type of exposure, the injury and the condition of the attacking animal,88. Ministério da Saúde (BR). Secretaria de Vigilância em Saúde. Departamento de Vigilância Epidemiológica. Normas técnicas de profilaxia da raiva humana [Internet]. Brasília: Ministério da Saúde; 2014[citado 2018 ser 13]. 60 p. Disponível em: Disponível em: http://portalarquivos.saude.gov.br/images/pdf/2015/outubro/19/Normas-tecnicas-profilaxia-raiva.pdf
http://portalarquivos.saude.gov.br/image...
,2626. Cavalcante KK, Florêncio CM, Alencar CH. Profilaxia antirrábica humana pós-exposição: características dos atendimentos no estado do Ceará, 2007-2015. J Health Biol Sci. 2017;5(4):337-45. doi: 10.12662/2317-3076jhbs.v5i4.1348.p337-345.2017.
https://doi.org/10.12662/2317-3076jhbs.v...
so that unnecessary treatments are not prescribed as, in addition to causing health risks, this can result in the inefficient use of public funds and even lead to acute shortages of immunobiologicals.22. Malanczyn AA, Selow MLC, Toniolo RMM. Análise das notificações de acidentes antirrábicos no município de curitiba, nos últimos 3 anos. Rev Dom Acadêmico. 2017;1(1).,1717. Silva AMR. Características do atendimento anti-rábico humano no Estado de Santa Catarina, área considerada sob controle para a raiva no ciclo urbano-2002 a 2007 [Trabalho de Conclusão de Curso]. Florianópolis (SC): Departamento de Saúde Pública do Centro de Ciências da Saúde, Universidade Federal de Santa Catarina, 2007.

This study can contribute to the human rabies control program in Ceará, given that it describes the characteristics of inadequate prophylactic procedures used, emphasizing that there is a need to improve care for people attacked by animals as well as the need to implement specific health education actions targeting health workers and the population in general.

This research has limitations related to the use of secondary data, mainly because of notification forms having fields with missing or incomplete information or not filled out adequately. However, these difficulties do not imply loss of information.

High indication of human anti-rabies treatments prescribing inadequate procedures suggests a need for better evaluation of the epidemiological profile of each case, careful observation of the attacking animal, as well as continuous adherence to the Human Rabies Prophylaxis Technical Standards, in order to improve the quality of records of accidents caused by animals potentially capable of transmitting rabies and favoring the decision of whether or not to initiate anti-rabies prophylaxis in an adequate and safe manner, without risk to the patient.

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  • ERRATUM
    In the article “Human rabies: evaluation of post-exposure prophylaxis prevalence in Ceará, Brazil, 2007-2015”, DOI: 10.5123/S1679-49742018000400009, published on Epidemiology and Health Services, 27(4):1-12:
    Original text:
    not because of attacks by these animals.2424. Frias DFR, Nunes JOR, Carvalho AAB. Caracterização de agravos causados por cães e gatos a seres humanos no município de Jaboticabal, São Paulo, durante o período de 2000 a 2009. Arch Vet Sci. 2012:17(3):63-70. doi: 10.5380/avs.v17i3.24824.
    https://doi.org/10.5380/avs.v17i3.24824...
    only on the characteristics of the wounds.2525. Silva GM, Brandespim DF, Rocha MDG, Leite RMB, Oliveira JMB. Notificações de atendimento antirrábico humano na população do município de Garanhuns, Estado de Pernambuco, Brasil, no período de 2007 a 2010. Epidemiol Serv Saúde. 2013 jan-mar;22(1):95-102. doi: 10.5123/S1679-49742013000100010.
    https://doi.org/10.5123/S1679-4974201300...
    Multiple injuries to the hands/feet77. Brito WI, Pazdziora AZ. Análise das condutas profiláticas da raiva humana realizadas em Primavera do Leste/MT, 2011: avaliação sobre o uso dos insumos. Rev Epidemiol Control Infect. 2013 jul-set;3(3):87-92.,2626. Cavalcante KK, Florêncio CM, Alencar CH. Profilaxia antirrábica humana pós-exposição: características dos atendimentos no estado do Ceará, 2007-2015. J Health Biol Sci. 2017;5(4):337-45. doi: 10.12662/2317-3076jhbs.v5i4.1348.p337-345.2017.
    https://doi.org/10.12662/2317-3076jhbs.v...
    ,27
    the injury and the condition of the attacking animal,88. Ministério da Saúde (BR). Secretaria de Vigilância em Saúde. Departamento de Vigilância Epidemiológica. Normas técnicas de profilaxia da raiva humana [Internet]. Brasília: Ministério da Saúde; 2014[citado 2018 ser 13]. 60 p. Disponível em: Disponível em: http://portalarquivos.saude.gov.br/images/pdf/2015/outubro/19/Normas-tecnicas-profilaxia-raiva.pdf
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    ,27
    24. Wada MY, Rocha SM, Maia-Elkhoury ANS. Situação da Raiva no Brasil, 2000 a 2009. Epidemiol Serv Saúde. 2011 out-dez;20(4):509-18. doi: 10.5123/S1679- 49742011000400010.
    25. Frias DFR, Nunes JOR, Carvalho AAB. Caracterização de agravos causados por cães e gatos a seres humanos no município de Jaboticabal, São Paulo, durante o período de 2000 a 2009. Arch Vet Sci. 2012:17(3):63-70. doi: 10.5380/avs.v17i3.24824.
    26. Silva GM, Brandespim DF, Rocha MDG, Leite RMB, Oliveira JMB. Notificações de atendimento antirrábico humano na população do município de Garanhuns, Estado de Pernambuco, Brasil, no período de 2007 a 2010. Epidemiol Serv Saúde. 2013 jan-mar;22(1):95-102. doi: 10.5123/S1679-49742013000100010.
    27. Cavalcante KK, Florêncio CM, Alencar CH. Profilaxia antirrábica humana pós-exposição: característicasdos atendimentos no estado do Ceará, 2007-2015. J Health Biol Sci. 2017;5(4):337-45. doi: 10.12662/2317-3076jhbs.v5i4.1348.p337-345.2017.
    Corrected text:
    not because of attacks by these animals.33. Wada MY, Rocha SM, Maia-Elkhoury ANS. Situação da raiva no Brasil, 2000 a 2009. Epidemiol Serv Saúde. 2011 dez;20(4):509-18. doi: 10.5123/S1679-49742011000400010.
    https://doi.org/10.5123/S1679-4974201100...
    only on the characteristics of the wounds.2424. Frias DFR, Nunes JOR, Carvalho AAB. Caracterização de agravos causados por cães e gatos a seres humanos no município de Jaboticabal, São Paulo, durante o período de 2000 a 2009. Arch Vet Sci. 2012:17(3):63-70. doi: 10.5380/avs.v17i3.24824.
    https://doi.org/10.5380/avs.v17i3.24824...
    Multiple injuries to the hands/feet77. Brito WI, Pazdziora AZ. Análise das condutas profiláticas da raiva humana realizadas em Primavera do Leste/MT, 2011: avaliação sobre o uso dos insumos. Rev Epidemiol Control Infect. 2013 jul-set;3(3):87-92.,2525. Silva GM, Brandespim DF, Rocha MDG, Leite RMB, Oliveira JMB. Notificações de atendimento antirrábico humano na população do município de Garanhuns, Estado de Pernambuco, Brasil, no período de 2007 a 2010. Epidemiol Serv Saúde. 2013 jan-mar;22(1):95-102. doi: 10.5123/S1679-49742013000100010.
    https://doi.org/10.5123/S1679-4974201300...
    ,2626. Cavalcante KK, Florêncio CM, Alencar CH. Profilaxia antirrábica humana pós-exposição: características dos atendimentos no estado do Ceará, 2007-2015. J Health Biol Sci. 2017;5(4):337-45. doi: 10.12662/2317-3076jhbs.v5i4.1348.p337-345.2017.
    https://doi.org/10.12662/2317-3076jhbs.v...
    the injury and the condition of the attacking animal,88. Ministério da Saúde (BR). Secretaria de Vigilância em Saúde. Departamento de Vigilância Epidemiológica. Normas técnicas de profilaxia da raiva humana [Internet]. Brasília: Ministério da Saúde; 2014[citado 2018 ser 13]. 60 p. Disponível em: Disponível em: http://portalarquivos.saude.gov.br/images/pdf/2015/outubro/19/Normas-tecnicas-profilaxia-raiva.pdf
    http://portalarquivos.saude.gov.br/image...
    ,2626. Cavalcante KK, Florêncio CM, Alencar CH. Profilaxia antirrábica humana pós-exposição: características dos atendimentos no estado do Ceará, 2007-2015. J Health Biol Sci. 2017;5(4):337-45. doi: 10.12662/2317-3076jhbs.v5i4.1348.p337-345.2017.
    https://doi.org/10.12662/2317-3076jhbs.v...
    24. Frias DFR, Nunes JOR, Carvalho AAB. Caracterização de agravos causados por cães e gatos a seres humanos no município de Jaboticabal, São Paulo, durante o período de 2000 a 2009. Arch Vet Sci. 2012:17(3):63-70. doi: 10.5380/avs.v17i3.24824.
    25. Silva GM, Brandespim DF, Rocha MDG, Leite RMB, Oliveira JMB. Notificações de atendimento antirrábico humano na população do município de Garanhuns, Estado de Pernambuco, Brasil, no período de 2007 a 2010. Epidemiol Serv Saúde. 2013 jan-mar;22(1):95-102. doi: 10.5123/S1679-49742013000100010.
    26. Cavalcante KK, Florêncio CM, Alencar CH. Profilaxia antirrábica humana pós-exposição: características dos atendimentos no estado do Ceará, 2007-2015. J Health Biol Sci. 2017;5(4):337-45. doi: 10.12662/2317-3076jhbs.v5i4.1348.p337-345.2017.

History

  • Received
    23 Jan 2018
  • Accepted
    06 Aug 2018
  • Online publication
    29 Nov 2018
Secretaria de Vigilância em Saúde - Ministério da Saúde do Brasil Brasília - Distrito Federal - Brazil
E-mail: leilapgarcia@gmail.com