Development of a questionnaire and screening model for lipedema

Alexandre Campos Moraes Amato Fernando Campos Moraes Amato Daniel Augusto Benitti Lorena Guimarães Lima Amato About the authors

Resumo

Contexto

O lipedema é muito subdiagnosticado e faltam ferramentas auxiliares diagnósticas de baixo custo. Baseado em um questionário de avaliação sintomática, criamos e validamos um questionário de rastreamento do lipedema.

Objetivos

Os objetivos do trabalho foram a identificação de perguntas clínicas relevantes, a elaboração de questionário de rastreamento e a criação de modelo de predição do lipedema.

Métodos

Um questionário simplificado foi criado e aplicado em um grupo de pacientes com e sem lipedema, sendo avaliada a probabilidade de acerto no diagnóstico.

Resultados

Os 109 pacientes que responderam ao questionário eram do sexo feminino e as questões foram compreendidas. O modelo preditivo com perguntas individuais mostrou excelente probabilidade de acerto, de 91,2%, e o modelo preditivo com somatória de pontos também teve boa probabilidade de acerto, de 86,15%.

Conclusões

O questionário de rastreamento do lipedema é um instrumento prático, de fácil e rápida aplicação, que pode ser utilizado em nossa população para a identificação de possíveis pacientes com lipedema, aumentando o nível de suspeição no momento da anamnese e exame físico.

Palavras-chave:
questionários; lipedema; obesidade; linfedema

Abstract

Background

Lipedema is greatly underdiagnosed and there is a lack of low-cost tools to facilitate diagnostic. We created a lipedema screening questionnaire based on a questionnaire for assessing symptoms.

Objectives

The study objectives were to identify relevant clinical questions, develop a screening questionnaire, and construct a model for predicting lipedema.

Method

A simplified questionnaire was constructed and administered to a sample of patients with and without lipedema and then the probability of correct diagnosis was analyzed.

Results

All 109 patients who answered the questionnaire were female and all of them understood the questions. A predictive model using individual question scores achieved an excellent probability of correct diagnosis, at 91.2%, and a predictive model based on total score also achieved a good probability of correct diagnosis, at 86.15%.

Conclusions

The lipedema screening questionnaire is a practical instrument that is quick and easy to administer and can be used with our population for identification of possible lipedema patients, raising the level of suspicion when taking a patient’s history and conducting a physical examination.

Keywords:
questionnaires; lipedema; obesity; lymphedema

INTRODUCTION

Lipedema has been described in Brazil by Moraes, who refers to it as lipofilia membralis.11 Moraes IN. Cânones da beleza. Rev Cult e Saude. 2003;1:25-30. It is characterized by abnormal bilateral build-up of fat in the gluteus, legs, and upper limbs that may be accompanied by orthostatic edema in postpubertal women.22 Amato ACM. Is Lipedema a Unique Entity? EC Clin Med Cases Reports. 2020;2:1-7. Anecdotal cases in men have also been described.33 Chen S-G, Hsu S-D, Chen T-M, Wang HJ. Painful fat syndrome in a male patient. Br J Plast Surg. 2004;57(3):282-6. http://dx.doi.org/10.1016/j.bjps.2003.12.020. PMid:15006533.
http://dx.doi.org/10.1016/j.bjps.2003.12...
While the pathophysiology of lipedema is still little understood, it has a high prevalence in the population, explained by its genetic aspect and its hormonal influence on cyclical inflammatory symptoms.22 Amato ACM. Is Lipedema a Unique Entity? EC Clin Med Cases Reports. 2020;2:1-7. It has been described as a low-level inflammatory process involving the lymphatic and adipose system,22 Amato ACM. Is Lipedema a Unique Entity? EC Clin Med Cases Reports. 2020;2:1-7. which is supported by a recent study by Wanshu Ma et al.44 Ma W, Rockson SG, Oliver G. Platelet factor 4 is a biomarker for lymphatic-promoted disorders. JCI Insight. 2020;5(13):e135109. http://dx.doi.org/10.1172/jci.insight.135109. PMid:32525843.
http://dx.doi.org/10.1172/jci.insight.13...
These characteristics provoke typical symptoms, which are very often interpreted incorrectly, in addition to the build-up of fat. As a result, although lipedema is actually a distinct condition, it is often confused with more frequently diagnosed diseases, such as obesity and lymphedema.55 Fife CE, Maus EA, Carter MJ. Lipedema: a frequently misdiagnosed and misunderstood fatty deposition syndrome. Adv Skin Wound Care. 2010;23(2):81-4. http://dx.doi.org/10.1097/01.ASW.0000363503.92360.91. PMid:20087075.
http://dx.doi.org/10.1097/01.ASW.0000363...
,66 Beninson J, Edelglass JW. Lipedema - the non-lymphatic masquerader. Angiology. 1984;35(8):506-10. http://dx.doi.org/10.1177/000331978403500806. PMid:6476475.
http://dx.doi.org/10.1177/00033197840350...
Lipedema is a disease with high prevalence, but low recognition and diagnosis, which is frequently underdiagnosed or confused with gynecoid obesity, lymphedema, or even venous insufficiency.22 Amato ACM. Is Lipedema a Unique Entity? EC Clin Med Cases Reports. 2020;2:1-7. Conservative estimates of the prevalence of lipedema in the general population range from 0.06 to 11%.55 Fife CE, Maus EA, Carter MJ. Lipedema: a frequently misdiagnosed and misunderstood fatty deposition syndrome. Adv Skin Wound Care. 2010;23(2):81-4. http://dx.doi.org/10.1097/01.ASW.0000363503.92360.91. PMid:20087075.
http://dx.doi.org/10.1097/01.ASW.0000363...
,77 Campos A, Amato M, Vofchuk D, et al. Lipedema associado a obesidade, linfedema e insuficiência venosa: relato de um caso. Diagnóstico e Trat. 2020;25:4-8.

Diagnosis of lipedema is essentially clinical, defined by symmetrically disproportionate build-up of fat in the lower limbs combined with complaints of orthostatic edema,55 Fife CE, Maus EA, Carter MJ. Lipedema: a frequently misdiagnosed and misunderstood fatty deposition syndrome. Adv Skin Wound Care. 2010;23(2):81-4. http://dx.doi.org/10.1097/01.ASW.0000363503.92360.91. PMid:20087075.
http://dx.doi.org/10.1097/01.ASW.0000363...
with pain often present. The feet are not affected by the increase in size, except in advanced stages of lipolymphedema, in which edema of the feet is secondary to lymphatic insufficiency that is not present in earlier stages.88 Reich-Schupke S, Altmeyer P, Stücker M. Thick legs - not always lipedema. J Dtsch Dermatol Ges. 2013;11(3):225-33. PMid:23231593.,99 Forner-Cordero I, Szolnoky G, Forner-Cordero A, Kemény L. Lipedema: an overview of its clinical manifestations, diagnosis and treatment of the disproportional fatty deposition syndrome - systematic review. Clin Obes. 2012;2(3-4):86-95. http://dx.doi.org/10.1111/j.1758-8111.2012.00045.x. PMid:25586162.
http://dx.doi.org/10.1111/j.1758-8111.20...
Edema that does not involve the feet is an important sign for distinguishing lipedema from common obesity and lymphedema. Since there are no specific laboratory test markers of lipedema, with the exception of the promise shown recently by platelet factor 4,44 Ma W, Rockson SG, Oliver G. Platelet factor 4 is a biomarker for lymphatic-promoted disorders. JCI Insight. 2020;5(13):e135109. http://dx.doi.org/10.1172/jci.insight.135109. PMid:32525843.
http://dx.doi.org/10.1172/jci.insight.13...
clinical diagnosis requires a high level of suspicion on the part of the treating physician. A questionnaire specifically for lipedema was developed in Germany1010 Rapprich S, Dingler A, Podda M. Liposuktion ist eine wirksame Therapie beim Lipödem - Ergebnisse einer Untersuchung mit 25 Patientinnen. J Ger Soc Dermatology 2011; 9: 33-41. and translated for Brazil by Amato et al.1111 Amato ACM, Amato FCM, Benitti DA, et al. Tradução adaptação cultural e validação do questionário de avaliação sintomática do lipedema (QuASiL). J Vasc Bras. 2020 [citado 2020 set 30];19:e20200049. http://www.scielo.br/scielo.php?script=sci_arttext&pid=S1677-54492020000100318&lng=en&nrm=iso
http://www.scielo.br/scielo.php?script=s...
It is based on a quality of life questionnaire for patients with lymphatic diseases1111 Amato ACM, Amato FCM, Benitti DA, et al. Tradução adaptação cultural e validação do questionário de avaliação sintomática do lipedema (QuASiL). J Vasc Bras. 2020 [citado 2020 set 30];19:e20200049. http://www.scielo.br/scielo.php?script=sci_arttext&pid=S1677-54492020000100318&lng=en&nrm=iso
http://www.scielo.br/scielo.php?script=s...
,1212 Augustin M, Bross F, Földi E, Vanscheidt W, Zschocke I. Development, validation and clinical use of the FLQA-l, a disease-specific quality of life questionnaire for patients with lymphedema. Vasa. 2005;34(1):31-5. http://dx.doi.org/10.1024/0301-1526.34.1.31. PMid:15786935.
http://dx.doi.org/10.1024/0301-1526.34.1...
and was adapted to include 15 self-report criteria rated on an analog scale from 0 to 10. It is considered a lipedema symptoms scale and has not been validated as diagnostic or screening tool.

In view of the poor availability of objective instruments for screening for lipedema in Brazil and worldwide and considering that data on quality of life are important for selection and for interpretation of clinical progress, this study was conducted with the objective of identifying relevant questions and creating a mathematical prediction model, with the intention of raising the pre-assessment level of suspicion.

METHODS

The process of identification and simplification of relevant questions suitable for self-report administration began by assessing the Portuguese translation of the symptoms questionnaire in its adapted form (Table 1). This questionnaire was converted into an on-line digital version using secure software appropriate for development and analysis of questionnaires (SurveyMonkey, California, United States) and was administered to 109 volunteers, with or without a prior lipedema diagnosis made during a medical consultation, but self-reported on the questionnaire. The study was approved by Ethical Committee (number 3.268.401).

Table 1
Final version of the lipedema screening questionnaire (translated from the Portuguese original that was administered).

Diagnosis of lipedema

Diagnosis of lipedema is still eminently clinical. An experienced assessor used the following criteria to classify members of the group with the disease: suggestive clinical history in postpubertal women; symmetrical bilateral deposits of fat below the hips, but not involving the feet (negative Stemmer sign); non-depressible edema (negative Godet sign), resistant to raising the limbs; areas affected painful and sensitive to palpation; and increased capillary fragility, with spontaneous ecchymosis.22 Amato ACM. Is Lipedema a Unique Entity? EC Clin Med Cases Reports. 2020;2:1-7.,33 Chen S-G, Hsu S-D, Chen T-M, Wang HJ. Painful fat syndrome in a male patient. Br J Plast Surg. 2004;57(3):282-6. http://dx.doi.org/10.1016/j.bjps.2003.12.020. PMid:15006533.
http://dx.doi.org/10.1016/j.bjps.2003.12...
,55 Fife CE, Maus EA, Carter MJ. Lipedema: a frequently misdiagnosed and misunderstood fatty deposition syndrome. Adv Skin Wound Care. 2010;23(2):81-4. http://dx.doi.org/10.1097/01.ASW.0000363503.92360.91. PMid:20087075.
http://dx.doi.org/10.1097/01.ASW.0000363...
,66 Beninson J, Edelglass JW. Lipedema - the non-lymphatic masquerader. Angiology. 1984;35(8):506-10. http://dx.doi.org/10.1177/000331978403500806. PMid:6476475.
http://dx.doi.org/10.1177/00033197840350...
,88 Reich-Schupke S, Altmeyer P, Stücker M. Thick legs - not always lipedema. J Dtsch Dermatol Ges. 2013;11(3):225-33. PMid:23231593.,99 Forner-Cordero I, Szolnoky G, Forner-Cordero A, Kemény L. Lipedema: an overview of its clinical manifestations, diagnosis and treatment of the disproportional fatty deposition syndrome - systematic review. Clin Obes. 2012;2(3-4):86-95. http://dx.doi.org/10.1111/j.1758-8111.2012.00045.x. PMid:25586162.
http://dx.doi.org/10.1111/j.1758-8111.20...

Administration of questionnaires

During the on-line validation of the questionnaire, volunteers from a specific group of women with and without lipedema agreed to answer the questionnaire in electronic format, without external help, and free to fill in all data as they saw fit. The sampling technique was non-probabilistic by convenience, and subjects were invited to take part after assessment at a Lymphedema and Angiodysplasia Clinic. Women over the age of 18 years seen for any type of complaint were recruited. Men were excluded, as were women who did not sign the consent form, had serious arterial or venous conditions, or could not speak or understand Portuguese.

The primary objective of this study was to develop a simple questionnaire that would be quick to answer, for screening for lipedema. A secondary objective was to construct a mathematical model for predicting lipedema based on the questionnaire.

Statistical analysis

Statistical analysis was conducted after the consistency of the data had been checked manually. Descriptive statistics and frequencies were calculated. Correlations between questionnaire variables were assessed using Spearman correlations and the Shapiro-Wilk test. Correlations with total scores were assessed using Pearson’s correlation coefficients. Statistical analysis was performed using Student’s t test. We adopted a p < 0.05 level of statistical significance for the correlations. The software used for data analysis was Excel (Microsoft, Novo Mexico, United States) and Wizard 1.9.40 (Evan Miller, Massachusetts, United States).

This study complies with the National Health Council (Conselho Nacional de Saúde) standards set out in resolution 196/96 regulating research involving human beings. It also adheres to the Helsinki Declaration and was approved by the Plataforma Brasil Research Ethics Committee, under protocol CAAE: 09590919.6.0000.0081.

RESULTS

One hundred and nine women with a known prior diagnosis completed the questionnaire. All interviewees understood the questions. None of the questions were considered non-applicable. The proportion between patients with and without lipedema was uniform (z score, p = 0.389) (Table 2).

Table 2
Characteristics of the sample.

The preliminary analysis found that the majority of questions were significant, although the items “During or soon after pregnancy/breastfeeding, did you put on weight or notice changes to your thighs/legs, hips, buttocks, and/or arms?” (z score, p = 0.148) and “During the menopause, did you put on weight or notice changes to your thighs/legs, hips, buttocks, and/or arms?” (with no positive responses) did not attain the minimum number necessary for statistical analysis. They were therefore removed before creation of the predictive model using individual questions. Without these items, the receiver operating characteristic curve (ROC Curve) has an area of 0.912, which enabled construction of the mathematical predictive model (Figure 1B).

Figure 1
A) Receiver operating characteristic curve (ROC Curve) for analysis of total questionnaire score. B) ROC Curve for predictive model using individual question scores.

The total number of points summed (total score) was positively correlated with lipedema diagnosis (Pearson’s correlation p < 0.001 and chi-square p < 0.001), with odds ratio (OR) of 1.434 and standard error of 0.094 (constant of 0.046 and standard error of 0.028). The area under the ROC curve for total score is 0.8615 (Figure 1A). The mean time taken to complete the questionnaire was 3 minutes and 38 seconds, with a 100% rate of fully completed questionnaires.

Prediction model

The formula for calculating the probability of lipedema using total score uses a total score coefficient of 0.361 and a constant of -3.075, as follows:

e ( c o e f t o t a l s c o r + c o n s tan t ) + 1 1

This formula can be used to plot the model for predicting lipedema diagnosis (Figure 2).

Figure 2
Model for prediction of lipedema diagnosis based on the total score.

The formula for calculating the probability of lipedema using the scores for each individual question employs a different coefficient for each question included (Table 3) as follows:

Table 3
Multivariate analysis of the influence of individual questions on lipedema diagnosis.
e ( c o e f p 1 + c o e f p 2 + c o e f p 3 + c o e f p 4 + c o e f p 7 + c o e f p 8 + c o e f p 9 + c o n s tan t ) + 1 1

This formula can be used to plot an individualized model for predicting lipedema.

DISCUSSION

Lipedema is greatly underdiagnosed because there are no definitive and simple laboratory tests, imaging exams, or genetic tests1313 Dayan E, Kim JN, Smith ML, et al. Lipedema - The disease they call FAT: An overview for clinicians. Boston, MA: Lipedema Simplified Publications, The Friedman Center for Lymphedema Research and Treatment at The Center. and because it is easily confused with other diseases such as lymphedema, gynecoid obesity, and lipohypertrophy.1414 Child AH, Gordon KD, Sharpe P, et al. Lipedema: an inherited condition. Am J Med Genet A. 2010;152A(4):970-6. http://dx.doi.org/10.1002/ajmg.a.33313. PMid:20358611.
http://dx.doi.org/10.1002/ajmg.a.33313...
Failure to correctly diagnose lipedema patients delays treatment of their disease, enabling it to progress.1313 Dayan E, Kim JN, Smith ML, et al. Lipedema - The disease they call FAT: An overview for clinicians. Boston, MA: Lipedema Simplified Publications, The Friedman Center for Lymphedema Research and Treatment at The Center. Lipedema symptoms and complaints may be considered subjective, particularly during the earlier phases, and are confused with other diseases that are more frequently seen in vascular clinics, such as chronic venous insufficiency, obesity, and lymphedema, revealing a need for standardization to increase the objectivity of diagnosis of this disease. It is therefore important to develop and validate instruments that can be used to assess the clinical impact of lipedema and facilitate definitive diagnosis.

Although the questions “During or soon after pregnancy/breastfeeding, did you put on weight or notice changes to your thighs/legs, hips, buttocks, and/or arms?” and “During the menopause, did you put on weight or notice changes to your thighs/legs, hips, buttocks, and/or arms?” did not attain statistical significance, we believe that the low number of individuals who had experienced these specific situations may have impacted on the scores for these questions, but not on the overall results of the questionnaire, which achieved good performance both for the individual model based on the scores for each question (area under the ROC curve = 0.912) and for the model based on total score (area under the ROC curve = 0.8615). These models can be interpreted as offering a high probability of correct diagnosis for distinguishing between patients with and without lipedema, at 91.2% and 86.15%, respectively.1515 Mandrekar JN. Receiver operating characteristic curve in diagnostic test assessment. J Thorac Oncol. 2010;5(9):1315-6. http://dx.doi.org/10.1097/JTO.0b013e3181ec173d. PMid:20736804.
http://dx.doi.org/10.1097/JTO.0b013e3181...
Notwithstanding, these questions are clinically relevant and may have a positive impact on the proposed tool, increasing its sensitivity and specificity. Therefore, we should continue to extend these analyses using larger samples. The statistical method used is useful for assessing sensitivity, but not necessarily specificity. In view of this, the questionnaire can be considered useful for preliminary assessment, but not for definitive diagnosis.

While the present study found evidence that the questionnaire has excellent predictive properties for lipedema diagnosis, correlating self-reported symptoms with lipedema diagnosis, we should remember the cyclical nature of lipedema symptoms22 Amato ACM. Is Lipedema a Unique Entity? EC Clin Med Cases Reports. 2020;2:1-7. which could discretely alter the results at different times, although the questions were designed to minimize this effect.

This tool was developed for screening for symptoms and to increase treating physicians’ diagnostic suspicion but should not be relied upon for definitive diagnosis. Proceeding with prospective assessments after this study should yield greater clinical applicability for the tool.

CONCLUSIONS

The lipedema screening questionnaire is a practical instrument that is quick and easy to administer and can be used in our population for preliminary identification of patients who possibly have lipedema. This increases the level of suspicion when taking patient history and conducting a physical examination. Additional studies are still needed to assess the instrument as a support for definitive lipedema diagnosis and its correlations with other clinical features.

  • How to cite: Amato ACM, Amato FCM, Benitti DA, Amato LGL. Development of a questionnaire and screening model for lipedema. J Vasc Bras. 2020;19: e20200114. https://doi.org/10.1590/1677-5449.200114
  • Financial support:

    None.
  • The study was carried out at Disciplina de Cirurgia Vascular, Universidade de Santo Amaro (UNISA), São Paulo, SP, Brazil.

References

  • 1
    Moraes IN. Cânones da beleza. Rev Cult e Saude. 2003;1:25-30.
  • 2
    Amato ACM. Is Lipedema a Unique Entity? EC Clin Med Cases Reports. 2020;2:1-7.
  • 3
    Chen S-G, Hsu S-D, Chen T-M, Wang HJ. Painful fat syndrome in a male patient. Br J Plast Surg. 2004;57(3):282-6. http://dx.doi.org/10.1016/j.bjps.2003.12.020 PMid:15006533.
    » http://dx.doi.org/10.1016/j.bjps.2003.12.020
  • 4
    Ma W, Rockson SG, Oliver G. Platelet factor 4 is a biomarker for lymphatic-promoted disorders. JCI Insight. 2020;5(13):e135109. http://dx.doi.org/10.1172/jci.insight.135109 PMid:32525843.
    » http://dx.doi.org/10.1172/jci.insight.135109
  • 5
    Fife CE, Maus EA, Carter MJ. Lipedema: a frequently misdiagnosed and misunderstood fatty deposition syndrome. Adv Skin Wound Care. 2010;23(2):81-4. http://dx.doi.org/10.1097/01.ASW.0000363503.92360.91 PMid:20087075.
    » http://dx.doi.org/10.1097/01.ASW.0000363503.92360.91
  • 6
    Beninson J, Edelglass JW. Lipedema - the non-lymphatic masquerader. Angiology. 1984;35(8):506-10. http://dx.doi.org/10.1177/000331978403500806 PMid:6476475.
    » http://dx.doi.org/10.1177/000331978403500806
  • 7
    Campos A, Amato M, Vofchuk D, et al. Lipedema associado a obesidade, linfedema e insuficiência venosa: relato de um caso. Diagnóstico e Trat. 2020;25:4-8.
  • 8
    Reich-Schupke S, Altmeyer P, Stücker M. Thick legs - not always lipedema. J Dtsch Dermatol Ges. 2013;11(3):225-33. PMid:23231593.
  • 9
    Forner-Cordero I, Szolnoky G, Forner-Cordero A, Kemény L. Lipedema: an overview of its clinical manifestations, diagnosis and treatment of the disproportional fatty deposition syndrome - systematic review. Clin Obes. 2012;2(3-4):86-95. http://dx.doi.org/10.1111/j.1758-8111.2012.00045.x PMid:25586162.
    » http://dx.doi.org/10.1111/j.1758-8111.2012.00045.x
  • 10
    Rapprich S, Dingler A, Podda M. Liposuktion ist eine wirksame Therapie beim Lipödem - Ergebnisse einer Untersuchung mit 25 Patientinnen. J Ger Soc Dermatology 2011; 9: 33-41.
  • 11
    Amato ACM, Amato FCM, Benitti DA, et al. Tradução adaptação cultural e validação do questionário de avaliação sintomática do lipedema (QuASiL). J Vasc Bras. 2020 [citado 2020 set 30];19:e20200049. http://www.scielo.br/scielo.php?script=sci_arttext&pid=S1677-54492020000100318&lng=en&nrm=iso
    » http://www.scielo.br/scielo.php?script=sci_arttext&pid=S1677-54492020000100318&lng=en&nrm=iso
  • 12
    Augustin M, Bross F, Földi E, Vanscheidt W, Zschocke I. Development, validation and clinical use of the FLQA-l, a disease-specific quality of life questionnaire for patients with lymphedema. Vasa. 2005;34(1):31-5. http://dx.doi.org/10.1024/0301-1526.34.1.31 PMid:15786935.
    » http://dx.doi.org/10.1024/0301-1526.34.1.31
  • 13
    Dayan E, Kim JN, Smith ML, et al. Lipedema - The disease they call FAT: An overview for clinicians. Boston, MA: Lipedema Simplified Publications, The Friedman Center for Lymphedema Research and Treatment at The Center.
  • 14
    Child AH, Gordon KD, Sharpe P, et al. Lipedema: an inherited condition. Am J Med Genet A. 2010;152A(4):970-6. http://dx.doi.org/10.1002/ajmg.a.33313 PMid:20358611.
    » http://dx.doi.org/10.1002/ajmg.a.33313
  • 15
    Mandrekar JN. Receiver operating characteristic curve in diagnostic test assessment. J Thorac Oncol. 2010;5(9):1315-6. http://dx.doi.org/10.1097/JTO.0b013e3181ec173d PMid:20736804.
    » http://dx.doi.org/10.1097/JTO.0b013e3181ec173d

Publication Dates

  • Publication in this collection
    11 Dec 2020
  • Date of issue
    2020

History

  • Received
    27 June 2020
  • Accepted
    06 Aug 2020
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