Skip to content

Advertisement

  • Research article
  • Open Access
  • Open Peer Review

Epidemiology of HIV, syphilis, and hepatitis B and C among manual cane cutters in low-income regions of Brazil

  • 1,
  • 1,
  • 1,
  • 2,
  • 1,
  • 2,
  • 1,
  • 2,
  • 3,
  • 3,
  • 1,
  • 4,
  • 1 and
  • 1Email authorView ORCID ID profile
BMC Infectious Diseases201818:546

https://doi.org/10.1186/s12879-018-3439-4

  • Received: 28 May 2018
  • Accepted: 9 October 2018
  • Published:
Open Peer Review reports

Abstract

Background

In recent decades the epidemic of asymptomatic sexually transmitted infections has extended deep into Brazil, including small towns and rural areas. The purpose of this study was to investigate the epidemiology of HIV, syphilis, and hepatitis B (HBV) and hepatitis C viruses (HCV), and to evaluate immunization coverage against hepatitis B in a group of rural workers in Brazil.

Methods

In 2016, a cross-sectional study was conducted with 937 manual sugarcane cutters of the Midwest and Northeast Regions of Brazil. All individuals were interviewed and screened for HIV, syphilis, HBV and HCV. Correlating factors with lifetime HBV infection were investigated using logistic regression. Positive Predictive Values, Negative Predictive Values, sensitivity and specificity were also calculated relative to vaccination against Hepatitis B, comparing anti-HBs titers to vaccination reports.

Results

Most reported previous hospitalization (55%), occupational injuries (54%), sharing of personal items (45.8%), alcohol consumption (77.2%), multiple sexual partners in previous 12 months (39.8%), and no condom use during sexual intercourse in last 12 months (46.5%). Only 0.2% reported using injection drugs. Anti-HIV-1 was detected in three individuals (0.3%). Serological markers of lifetime syphilis (treponemal test) were detected in 2.5% (95% CI: 1.6–3.6) of participants, and active syphilis (treponemal test and VDRL) present in 1.2%. No samples were positive for anti-HCV. The prevalence of lifetime HBV infection (current or past infection) was 15.9%, and 0.7% (95% CI 0.4 to 1.5) were HBsAg-positive. Previous hospitalization (OR 1.53, CI 1.05–2.24, p < 0.01) and multiple sexual partners in the last 12 months (OR 1.80, CI 1.25–2.60, p < 0.01) were predictors for lifetime HBV infection. Although 46.7% (95% CI 43.4–49.9) of individuals reported having been vaccinated against hepatitis B, only 20.6% (95% CI 18.1–23.3) showed serological evidence of previous hepatitis B vaccination (positive for anti-HBs alone).

Conclusions

The high prevalence of syphilis and HBV compared to the general population and the high frequency of risk behaviors show the potential for sexual and parenteral dissemination of these agents in this rural population. In addition, the low frequency of hepatitis B vaccinated individuals suggests a need for improved vaccination services.

Keywords

  • Sexually transmitted diseases
  • Rural population
  • Poverty areas
  • Viral hepatitis vaccines

Background

Despite advancements in prevention and diagnosis, asymptomatic sexually transmitted infections are a major challenge for global infection control [1, 2]. Worldwide, 36.7 million people are living with HIV [3], while approximately 5.6 million new cases of syphilis occur each year [4]. Hepatitis B and C, in turn, are also a major public health challenge, and 325 million people are chronic carriers of these viruses [2]. Although globally the hepatitis B vaccine has decreased the burden of hepatitis B virus infection significantly, most adult individuals remain susceptible to HBV [2].

The distribution of asymptomatic sexually transmitted infections varies worldwide, and studies have shown that social, economic and behavioral conditions influence their epidemiology [4, 5]. Therefore, in general, higher prevalences of HIV, syphilis, and hepatitis B and C have been found in low- and middle-income countries compared to developed countries [4, 6].

In Brazil, the epidemic of HIV infection started in the industrialized regions of the southeast and south, and vulnerable urban groups have the highest burden of this infection [79]. However, in the last decade the HIV epidemic has reached inner cities and rural regions, far from the epicenter of the epidemic, where access to health services is limited and often low quality [10]. Further, HIV infection is often accompanied by other asymptomatic sexually transmitted infections such as syphilis and viral hepatitis, which, like HIV, have great potential for dissemination in impoverished vulnerable populations [1]. There are few studies in Brazil on the epidemiology of these infections in less populated regions of the country [8, 10].

Brazil is the largest producer of sugar cane in the world, and sugar cane-based industries are a significant economic activity. Brazil’s sugar-alcohol industry employs around 500,000 workers linked exclusively to sugarcane [11] and almost 90% of production takes place in the Central and Southern regions of the country, followed by the Northeast region [12]. Although the mechanization of sugarcane cutting has been expanded in the last decade, this trend occurred predominantly in the Southern Region. In the Midwestern and Northeastern region, manual cane cutting remains the principal mode of cane harvesting. This activity is physically and mentally taxing, and despite advances in working conditions, these individuals still experience exploitation and dangerous working conditions as well as social marginalization [13].

Due the nature of sugar cane cutting, these workers are usually males, young adults, and sexually active [14]. The seasonality of sugarcane cultivation and the possibility of better income encourages the temporary inter-regional migration of workers, who live their lives isolated from their families and partners for months. Most of them live in large communal houses on sugarcane farms, where the sharing of personal care items is frequent. Further, on their days off they visit the cities or villages nearby sugarcane plantations to buy personal items and have fun, which can include binge drinking and unsafe sexual encounters [15].

This corollary of factors may put manual sugar cane cutters at high risk of asymptomatic sexually transmitted infections, and they could be potential disseminators of these infections in remote regions. However, data about the epidemiology of these vulnerable rural workers is virtually non-existent in Brazil. This study estimated HIV, viral hepatitis B and C, and syphilis prevalence, and analyzed risk factors for lifetime HBV infection, and evaluated immunization against hepatitis B in sugarcane cutters in Central and Northeastern Brazil.

Methods

This is a cross-sectional, multicenter study in Goiás (Midwest Region) and Paraíba (Northeast Region), Brazil. Goiás has an estimated population of 6,778,772, monthly nominal household income per capita of $348 and a Human Development Index (HDI) of 0.735. Paraíba has an estimated population of 4,025,558 inhabitants, monthly nominal household income per capita of $240 and HDI of 0.658. The agricultural industry that has been developed in both states has great significance to the national economic situation [16].

In Goiás there are 38 alcohol and sugar producing units distributed across different regions of the state, and in 14 of them manual cane harvesting is still used. Among them, four were in harvest activity during the period of the study, and they were included in the investigation. In Paraíba there are nine alcohol and sugar production plants, only one sugar producing unit was eligible, being that It used manual cutting and was active [17]. This is the largest sugar producing unit in the State.

The minimum required sample, considering a statistical power of 80% (β = 20%), significance level of 95%, (< 0,05), precision of 0.5%, design effect of 1.5 and a global prevalence for anti-HIV for the general population at 0.39% [18] was 895 manual sugar cane cutters.

Inclusion criteria were: be a manual sugar cane cutter (by self-report) and be aged 18 years or older. Five alcohol and sugar producing units agreed to participate in the study, representing the manual sugar cane cutters from these regions (Fig. 1).
Fig. 1
Fig. 1

Geographical location of the sampling sites in the states of Goiás (GO) and Paraíba (PB), Central-West and Northeast regions, respectively

Data collection was carried out from February to September 2016. All participants signed a free and informed consent form, approved by the research ethics committee of the Federal University of Goiás and Paraíba, according to resolution CNS No. 466/12, under protocols 042796/2015 and 1,507,737/2016, respectively. Participants were interviewed by trained research assistants using a structured script containing questions about sociodemographic characteristics, work characteristics, risk behaviors for sexually transmitted infections (STIs), also referred to as sexually transmitted diseases (STDs) and viral hepatitis, as well as vaccination status. “Reported Shared Accommodation” was defined as individuals who shared their living space with roommates or flatmates, or in shared employer-provided housing.

Rapid screening tests for HIV (Bioeasy HIV, Republic of Korea) and syphilis (Alere Syphilis, Republic of Korea) were performed on all participants, as well as confirmatory rapid tests for HIV (Abon™ HIV 1/2/O, China). For complementary serological tests for syphilis, hepatitis B, and C, 10 ml of blood were collected.

For syphilis, positive samples per the treponemal test (Rapid Test) were retested by a non-treponemal test - venereal disease research laboratory (VDRL) (Wiener Lab, Argentina). For study purposes, active syphilis was defined as the participant being positive for both tests [19, 20]. For hepatitis B and C, all samples were tested for HBsAg, anti-HBs, total anti-HBc, and anti-HCV by enzymatic immunoassay using Biokit S.A., Spain. Persons with positive tests were referred for diagnostic confirmation and/or treatment.

Interview data and serological test results were digitized and analyzed using the STATA statistical software version 13.0 (StataCorp, College Station, TX). Prevalences were calculated with 95% confidence intervals. Univariate and multivariate analyses were performed to identify factors associated with lifetime HBV infection. The term “lifetime HBV infection” refers to the presence of the HBsAg and/or anti-HBc markers, indicating current or past HBV infection. Therefore, for the purposes of analysis, cases that showed isolated positivity for anti-HBs were excluded. Initially, risk factors for seropositivity to lifetime HBV infection were estimated. Those factors that presented a statistically significant association (p < 0.20) were subjected to multivariate Logistic regression analysis and controlled by “work region”. The Chi-squared, Chi-squared test for trend, Fisher’s exact test, and student’s t tests were used to evaluate differences between proportions. The significance level used in the tests was 5%. Positive Predictive Values (PPV) and Negative Predictive Values (NPV) were also calculated for sensitivity and specificity related to self-reported vaccination against Hepatitis B (complete series), considering the serological profile of immunization as the gold standard (i.e. HBsAb positive only).

Results

A total of 937 manual sugar cane cutters were recruited and agreed to participate in the study (Table 1). All were male and 68.9% were under 40 years of age. Regarding education, almost half (47.4%) reported having 4 or fewer years of education. Most participants were married (77.5%). In terms of region, 85.7% were from the Northeast of the country; however, 67.9% worked in plants located in the Central region of Brazil. The average monthly salary was $554.10.
Table 1

Sociodemographic characteristics of manual sugar cane cutters in the Northeast and Central regions of Brazil, 2016 (n = 937)

Variables

Participants

%

n = 937

Sex

 Male

937

100.0

Agea mean (standard deviation)

35.4 (9.2)

 

  = < 29

266

28.4

 30–39

380

40.5

 = > 40

291

31.1

Educationa mean (standard deviation)

5.2 (3.6)

 

  < = 4

444

47.4

  > 4

493

52.6

Civil Status

 Married

726

77.5

 Single

211

22.5

Region of Origin

 Northeast

803

85.7

 Midwest

129

13.8

 North

4

0.4

 Southeast

1

0.1

Work region

  

 Paraíba

301

32.1

 Goiás

636

67.9

Incomeb mean (standard deviation)

554.1 (165.7)

 

  ≤ 461

326

34.8

 462–615

412

44

  > 616

199

21.2

aYears; bUS$/per month

Table 2 shows risk factors for sexual and bloodborne pathogens reported by the sugar cane cutters in this study (Table 2). Most reported previous hospitalization (55%), occupational injuries (54%), sharing of personal items – such as razor blades, nail pliers, toothbrushes (45.8%), alcohol consumption (77.2%), age of first sexual intercourse before 16 years old (49.4%), multiple sexual partners (last 12 months) (39.8%), and no condom use during sexual intercourse (last 12 months) (46.5%).
Table 2

Risk factors for sexual and bloodborne pathogens in manual sugar cane cutters in the Northeast and Central regions of Brazil, 2016 (n = 937)

Variables

N

%

Knowledge of signs or symptoms of STI in women (no)

639

68.2

Knowledge of signs or symptoms of STI in men (no)

600

64

Tattoos or piercings on body (yes)

106

11.3

Previous transfusion (yes)

38

4.1

Previous hospitalization (yes)

515

55

Previous occupational injuries (yes)

505

54

Reported shared accommodation (yes)

277

29.6

Sharing sharp personal care items (yes)

429

45.8

History of incarceration (yes)

90

9.6

History of drug use (yes)

126

13.4

History of marijuana use (yes)

110

11.7

History of cocaine/crack use (yes)

43

4.6

History of injection drug use (yes)

2

0.2

Drinking alcohol (yes)

723

77.2

Age of first sexual intercourse = <  15 years (15.7; 2.7)a

463

49.4

History of STI (yes)

101

10.8

History of homosexual relations (yes)

52

5.5

History of sexual abuse (yes)

13

1.4

Sexual partner number = > 2 in the last 12 months (2.8; 4.6)a

373

39.8

No condom use at least once in the past 12 months

436

46.5

Report of genital ulcer/sore in the last 12 months (yes)

34

3.6

Report of genital discharge in the last 12 months (yes)

29

3.1

aMean; standard deviation

Anti-HIV-1 was detected in three individuals (0.3%; 95% CI: 0.1–1.0). Serological markers of lifetime syphilis (Treponemal test) were detected in 2.5% (95% CI: 1.6–3.6) of sugar cane cutters, and of active syphilis (Treponemal test and VDRL) in 1.2% (95% CI: 0.6–2.1). The prevalence of lifetime HBV infection was 15.9% (95% CI: 13.7–18.4), where 0.7% (95% CI: 0.4–1.5) were HBsAg-positive, 9.8% (95% CI: 8.1–11.9) were for both anti-HBs and anti-HBc markers, and 5.3% (95% CI: 4.1–7.0) were positive for anti-HBc alone. No samples tested positive for anti-HCV (Table 3).
Table 3

Prevalences of HBV, HCV, HIV, and Syphilis serological markers in manual sugar cane cutters in the Northeast and Central regions of Brazil, 2016 (n = 937)

Serological markers

Positive

(CI 95%)a

n

%

Isolated HBsAg

1

0.1

0.0–0.6

HBsAg + anti-HBc

6

0.6

0.3–1.4

Anti-HBs + anti-HBc

92

9.8

8.1–11.9

Anti-HBc alone

50

5.3

4.1–7.0

Lifetime HBV infection

149

15.9

13.7–18.4

Anti-HBs alone

193

20.6

18.1–23.3

Anti-HCV

0

 

Lifetime Syphilis (TT)b

23

2.5

1.6–3.6

Active Syphilis (TTb and VDRLc)

11

1.2

0.6–2.1

Anti-HIV

3

0.3

0.1–1.0

aCI: Confidence Interval bTT: treponemal test cVDRL Venereal disease research laboratory

Among those sugar cane cutters positive for HBsAg and/or anti-HBc (n = 149), 4% (6/149) of the subjects were also positive by the Treponemal tests, 2% (3/149) for VDRL and one for anti-HIV-1 (0.7%).

In univariate analyses for lifetime HBV infection, six variables showed p value < 0.20 and were included in the multivariate model: civil status, history of incarceration, history of marijuana use, history of cocaine/crack, previous hospitalization, age at first sexual intercourse, history of STI, number of sexual partners and no condom use at least once in the past 12 months. The final model showed previous hospitalization (OR 1.53, CI 1.05–2.24, p = 0.027) and multiple sexual partners in the last 12 months (OR 1.8, CI 1.25–2.60, p < 0.01) were predictors for lifetime HBV infection among the sugar cane cutters investigated (Table 4).
Table 4

Univariate and multivariate analyses of risk factors associated with HBV of sugar cane cutters, Northeast and Central regions of Brazil, 2016

Variable

Univariate analysisa

Multivariate analysisa

HBV

Pvalue

ORb(95% CI)

HBV

Positive

Negative

Pvalue

ORb (95% CI)

(n = 149)

(595)

Age (years) (36.7; 8.9)c

 18–29

31 (19.4%)

129 (80.6%)

 

1

  

 30–39

65 (20.4%)

254 (79.6%)

0.796

1.06 (0.66–1.71)

  

  > =40

53 (20%)

212 (80%)

0.875

1.04 (0.63–1.70)

  

Education (years) (4.7; 3.5)c

  < =4

74 (19.2%)

311 (80.8%)

 

1

  

  > 4

75 (20.9%)

284 (79.1%)

0.569

1.10 (0.77–1.59)

  

Civil Status

 Married

110 (18.5%)

484 (81.5%)

 

1

 

1

 Single

39 (26%)

111 (74%)

0.042

1.54 (1.02–2.35)

0.300

1.27 (0.81–1.98)

Reported shared accommodation

 No

112 (21%)

422 (79%)

 

1

  

 Yes

37 (17.6%)

173 (82.4%)

0.304

0.80 (0.53–1.22)

  

Work region

 Northeast

44 (17.7%)

204 (82.3%)

 

1

  

 Midwest

105 (21.2%)

391 (78.8%)

0.271

1.24 (0.84–1.84)

  

History of incarceration

 No

129 (19.3%)

541 (80.7%)

 

1

 

1

 Yes

20 (27%)

54 (73%)

0.115

1.55 (0.89–2.69)

0.122

1.55 (0.89–2.70)

History of marijuana use

 No

136 (20.9%)

516 (79.1%)

 

1

 

1

 Yes

13 (14.1%)

79 (85.9%)

0.134

0.62 (0.34–1.15)

0.084

0.58 (0.31–1.08)

History of cocaine/crack use

 No

147 (20.7%

564 (79.3%)

 

1

 

1

 Yes

2 (6.1%)

31 (93.9%)

0.058

0.25 (0..6–1.05)

0.067

0.26 (0.06–1.10)

Tattoos or piercings on body

 No

131 (19.8%)

530 (80.2%)

 

1

  

 Yes

18 (21.7%)

65 (78.3%)

0.689

1.12 (0.64–1.95)

  

Drinking alcohol

 No

29 (16.8%)

144 (83.2%)

 

1

  

 Yes

120 (21%)

451 (79%)

0.222

1.32 (0.84–2.06)

  

Previous transfusion

 No

144 (20.1%)

574 (79.9%)

 

1

  

 Yes

5 (19.2%)

21 (80.8%)

0.918

0.95 (0.35–2.56)

  

Previous hospitalization

 No

54 (16.2%)

280 (83.8%)

 

1

 

1

 Yes

95 (23.2%)

315 (76.8%)

0.018

1.56 (1.07–2.26)

0.027

1.53 (1.05–2.24)

Previous work accident

 No

64 (18.5%)

281 (81.5%)

 

1

  

 Yes

85 (21.3%)

314 (78.7%)

0.350

1.18 (0.83–1.71)

  

Sharing sharp personal care items

 No

78 (18.8%)

337 (81.2%)

 

1

  

 Yes

71 (21.6%)

258 (78.4%)

0.346

1.18 (0.83–1.70)

  

Age at first sexual intercourse (years) (15.7; 2.7)c

 7–15

86 (22.9%)

289 (77.1%)

 

1

 

1

  > =16

63 (17.1%)

306 (82.9%)

0.046

0.69 (0.48–0.99)

0.116

0.74 (0.51–1.07)

History of STI

 No

126 (18.9%)

539 (81.1%)

 

1

 

1

 Yes

23 (29.1%)

56 (70.9%)

0.035

1.75 (1.04–2.96)

0.088

1.59 (0.93–2.72)

History of homosexual relations

 No

139 (19.8%)

564 (80.2%)

 

1

  

 Yes

10 (24.4%)

31 (75.6%)

0.474

1.30 (0.62–2.73)

  

History of sexual abuse

 No

146 (19.9%)

589 (80.1%)

 

1

  

 Yes

3 (33.3%)

6 (66.7%)

0.325

2.02 (0.49–8.16)

  

Number of sexual partners in the last 12 months (2.6; 3.4)c

  < =1

74 (16.2%)

383 (83.8%)

 

1

 

1

  > =2

75 (26.1%)

212 (73.9%)

0.001

1.83 (1.27–2.63)

0.002

1.8 (1.25–2.60)

No condom use at least once in the past 12 months

 No

84 (22.2%)

295 (77.8%)

 

1

 

1

 Yes

65 (17.8%)

300 (82.2%)

0.138

0.76 (0.53–1.09)

0.866

1.04 (0.67–1.61)

Report of genital ulcer/sore in the last 12 months

 No

140 (19.6%)

573 (80.4%)

 

1

  

 Yes

9 (29%)

22 (71%)

0.205

1.67 (0.75–3.72)

  

Report of genital discharge in the last 12 months

 No

144 (20.1%)

574 (79.9%)

 

1

  

 Yes

5 (19.2%)

21 (80.8%)

0.918

0.95 (0.35–2.56)

  

aLogistic Regression, adjusted by work region; bOdds Ratio; cMean; standard deviation

Although 46.7% (95% CI: 43.4–49.9) of individuals reported having been vaccinated against hepatitis B, only 20.6% (95% CI: 18.1–23.3) showed serological profile of previous hepatitis B vaccination (positive for anti-HBs alone) and the mean age was 30.7 years (SD: 8.5). Therefore, self-reported previous HBV vaccination reports showed a positive predictive value and specificity to identify individuals immunized against hepatitis B of only 27.6% and 57.4%, respectively. The negative predictive value and sensitivity of the vaccination report were 85.6% and 62.7%, respectively.

Discussion

In Brazil, the epidemic of HIV/AIDS is moving from urban centers and reaching small cities and villages [10], and this investigation supports this dynamic. Most rural workers were poor seasonal migrants with low education, from small cities of the poorest regions of Brazil (North and Northeast). In fact, the anti-HIV-1 prevalence found among these sugar cane cutters was similar to that found in the general population in Brazil and worldwide. In 2016, the World Health Organization reported a prevalence of 0.8% [0.7–0.9%] in adults [21], and in Brazil, a rate of 0.39% among people aged 15 to 49 years is estimated [18].

The potential of HIV dissemination in the study population may be measured by the prevalence of other sexually transmitted infections. Unlike HIV, the lifetime syphilis prevalence found among study participants was higher than that estimated in the general population worldwide and in Brazil [18, 22]. A meta-analysis including data of 154 countries showed a global pooled mean prevalence of 1.11% (95% CI: 0.99–1.22). Further, when only studies carried out in American regions were considered, the prevalence decreased to 0.13 (95% CI: 0.09–0.19) [20]. In Brazil, a survey carried out among 35,460 Brazilian male conscripts found a lifetime syphilis prevalence of 0.55% (95% CI: 0.45–0.61) [23].

Concerning hepatitis B, though the prevalence of lifetime HBV infection suggests a low HBV endemicity among the sugarcane cutters investigated, it should be emphasized this prevalence was slightly higher than that estimated in the urban population (20 to 69 year) from the Midwest (12.4%; 95% CI: 11.1–14.3) and Northeast (12.1%; 95% CI: 10.5–13.9) regions of Brazil [24]. On the other hand, this prevalence was similar to that reported recently in populations at risk for STIs, such as sex workers (17.1%; 95% CI: 11.6–23.4) [25] and men who have sex with men (MSM) (15.4%; 95% CI: 8.7–25.8) in Goiás [26]. In addition, seven individuals were HBsAg positive, being therefore potential disseminators of HBV. Further, six individuals had been infected by HBV and T. pallidum, and three of them had active syphilis. One sugar cane cutter had been infected by HBV and HIV.

The asymptomatic characteristics of these infections favor their quiet dissemination. In the absence of knowledge of these diseases, diagnosis and treatment, they scatter efficiently in vulnerable populations that present risk behaviors, like manual sugarcane cutters [27, 28]. In this study, these conditions favorable to STI dissemination were present. The average education level reported was only 4 years of study and few had knowledge about STIs and access to public health services. Indeed, of the total, 40% had not sought health services in the last 12 months, and 30% had only sought health services one time (data not shown).

The analyses of potential risk factors for HBV identified two predictors: multiple partners and previous hospitalization. HBV sexual transmission is well established [2], and supports the potential of sugar cane cutters as disseminators of other STIs, including HIV. In fact, the use of condoms during sexual intercourse is not a regular practice and the consumption of alcohol is high in this population. These behaviors have encouraged the spread of STIs [1, 29].

In this investigation, the high frequency of previous hospitalization (n = 520) was a surprise, and we could speculate that this occurred due to workplace hazards including those that present multiple health-risk situations [30]. In this study, 509/943 individuals reported an occupational injury, and 156/943 suffered one in the last 12 months. These rural workers are exposed to long daily shifts and numerous injuries, including stress, dehydration, bites of venomous animals, accidents, burns by sunburn or by fire, poisoning by pesticide residues, etc. [3032]. Sometimes these situations require health care and hospitalizations, which in low-income regions may be a cause of HBV infection [33]. This is often a consequence of a lack of resources to perform proper hygiene as well as staff trained in proper patient safety procedures. Brazil is a continental country with large economic and cultural diversity [34]. Therefore, the findings of previous hospitalization as a predictor of lifetime HBV infection among sugar cane cutters, suggest HBV dissemination in healthcare facilities where infection control measures may be a luxury where qualified human resources, equipment, and supplies are scarce, favoring parenteral transmission. In fact, previous studies conducted in Brazil have also shown an association between invasive medical procedures and HBV infection [3537].

Hepatitis B vaccine is the main preventive measure against HBV infection [2]. In Brazil, currently, the HBV vaccine is available free of charge for the entire population [22]. Despite this policy, vaccine coverage is still low among adults, mainly men [38]. In this investigation, only 20.6% of sugarcane cutters had isolated anti-HBs protective titers, indicating previous immunization. Low education, low-income and lack of public health services very probably contributed to these findings. In fact, some authors have shown that individuals with a greater understanding of the disease and with a higher economic level tend to be vaccinated against hepatitis B compared to those who are unaware of hepatitis B vaccine [39].

The best information about an individual’s previous vaccination is their vaccination card [40]. If it is not available, many health professionals trust in the verbal report of previous vaccination [41]. However, this study supports that a hepatitis B vaccination self-report is not an accurate indicator of previous vaccination status. In fact, our findings showed that a self-report of HBV vaccination had a sensitivity and specificity of 62.7% and 57.4% to identify individuals immunized against HBV, respectively. In a study conducted in the United States with 818 individuals of an integrated health care system, better results were found (sensitivity and specificity of 73% and 67%, respectively), but the social differences between these two populations are noteworthy, including education and income [42]. Therefore, a report of previous hepatitis B vaccination should not be considered an indicator of hepatitis B immunization, mainly in impoverished populations. For these populations, in the absence of the vaccination card, “Don’t Ask, Vaccinate”! [43].

There were no cases of hepatitis C among the individuals investigated. HCV is predominantly transmitted by blood. Therefore, transfusion of unscreened blood and sharing of syringes and needles among drug addicts has been the major cause of HCV transmission [2]. However, these were uncommon among the individuals studied and should explain in part our findings.

This investigation has some limitations. Initially, due to financial restrictions the data collection was carried out in February and March in Paraíba, Northeast Region, which is the period at the end of the sugar cane harvest season. Therefore, only one mill was included in the study. However, this represents the biggest mill in the region. Further, the study was conducted in only two states, and may not represent all Brazilian manual sugar cane cutters, although these two states represent the most significant alcohol producing areas in Brazil. All interviews were performed face-to-face, therefore some personal and private questions may have biased responses, and therefore underestimate the prevalence of such sensitive variables as condom use, sex with men who have sex with men (MSM), illicit drug use, etc. Otherwise, some strategies were used to minimize potential biases: previously trained male interviewers, and private places for interviews.

Conclusion

This research presents the situation of poor, rural workers from non-industrialized areas of Brazil, a population often disregarded from a public health standpoint. The situation of these young men includes wide circulation of HIV and high prevalences of syphilis and HBV compared to the national population. In addition, the variables associated with HBV infection, multiple partners and previous hospitalization, showed the risk of dissemination of sexually and parenterally transmitted infections in this rural population. Finally, the low frequency of individuals vaccinated against hepatitis B suggests a need for improved vaccination services. It is therefore recommended that sugar and ethanol plants act to strengthen specific prevention and health promotion programs for rural sugarcane workers in Brazil.

Abbreviation

CI: 

Confidence Interval

HBV: 

Hepatitis B virus

HCV: 

Hepatitis C virus

HDI: 

Human development index

HIV: 

Human immunodeficiency virus

MSM: 

Men who have sex with men

NPV: 

Negative predictive values

PPV: 

Positive predictive values

STD: 

Sexually transmitted disease

STI: 

Sexually transmitted infection

TT: 

Treponemal test

VDRL: 

Venereal disease research laboratory

Declarations

Acknowledgements

We would like to thank the members of the Center for Studies in Epidemiology and Care in Infectious Diseases, with emphasis on Viral Hepatitis/ Núcleo de Estudos em Epidemiologia e Cuidados em Agravos Infecciosos, com ênfase em Hepatites Virais (NECAIH) for their participation during the planning, execution, and evaluation of this study. Brian Ream edited this manuscript in English.

Funding

This study was made possible by the financial support of the National Counsel of Scientific and Technological Development in Brazil/Conselho Nacional de Desenvolvimento Científico e Tecnológico do Brasil, funding call: CNPq Universal/2014, and by the University Extension Program/Programa de Extensão Universitária (ProExt 2016/2017).

Availability of data and materials

The datasets supporting the conclusions of this article are included within the article and its tables. Additional data may be available from the corresponding author upon reasonable request.

Authors’ contributions

DFNCR study concept and design, data collection, literature search. LRCR study concept and design, data collection, literature search. CAS study concept and design, data collection, literature search. BRO data collection, literature search. TLSM data collection, literature search. RMBM study concept and design, data collection, literature search. MAM study concept and design, data collection, literature search. MASC study concept and design, data collection, literature search. JPS study concept and design, data collection, literature search. ACOS study concept and design, data collection, literature search. MMS study concept and design, data collection, literature search. KAAC study concept and design, literature search, data collection, statistical analyses, data interpretation and supervision, drafting of the manuscript. RLC critical revision of the manuscript for important intellectual content. SAT study concept and design, data collection, critical revision of the manuscript for important intellectual content and supervision. All authors read and approved the final manuscript.

Ethics approval and consent to participate

This study was approved by the Research Ethics Committees of Brazil in Goiás and Paraíba, according to resolution CNS No. 466/12, under protocols 042796/2015 and 1,507,737/2016, respectively. All individuals who agreed to participate in the study provided written informed consent, through a signature or thumbprint.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
Faculty of Nursing, Federal University of Goias/Universidade Federal de Goiás, Goiânia, GO, Brazil
(2)
Institute of Tropical Pathology and Public Health, Federal University of Goias/Universidade Federal de Goiás, Goiânia, GO, Brazil
(3)
Faculty of Nursing, Federal University of Paraiba/Universidade Federal da Paraíba, João Pessoa, PB, Brazil
(4)
Department of Epidemiology, College of Public Health and Health Professions and College of Medicine, University of Florida, Gainesville, FL, USA

References

  1. Unemo M, Bradshaw CS, Hocking JS, de Vries HJC, Francis SC, Mabey D, Marrazzo JM, Sonder GJB, Schwebke JR, Hoornenborg E, Peeling RW, Philip SS, Low N, Fairley CK. Sexually transmitted infections: challenges ahead. Lancet Infect Dis. 2017;17(8)::e235–e279. https://doi.org/10.1016/S1473-3099(17)30310-9..View ArticleGoogle Scholar
  2. World Health Organization [WHO]. Global Hepatitis Report. (2017). http://apps.who.int/iris/bitstream/10665/255016/1/9789241565455-eng.pdf?ua=1. Accessed 19 Jan 2018.
  3. World Health Organization [WHO]. HIV/AIDS Fact sheet Updated July 2017. (2017). http://www.who.int/mediacentre/factsheets/fs360/en/. Accessed 19 Jan 2018.
  4. Peeling RW, Mabey D, Kamb ML, Chen XS, Radolf JD, Benzaken AS. Syphilis. Nat Rev Dis Primers. 2017;3:17073. https://doi.org/10.1038/nrdp.2017.73.View ArticleGoogle Scholar
  5. Frew PM, Parker K, Vo L, Haley D, O'Leary A, Diallo DD, Golin CE, Kuo I, Soto-Torres L, Wang J, Adimora AA, Randall LA, Del Rio C, Hodder S, HIV Prevention Trials Network 064 (HTPN) Study Team. Socioecological factors influencing women's HIV risk in the United States: qualitative findings from the women's HIV SeroIncidence study (HPTN 064). BMC Public Health. 2016;16(1):803. https://doi.org/10.1186/s12889-016-3364-7.View ArticlePubMedPubMed CentralGoogle Scholar
  6. Degenhardt L, Peacock A, Colledge S, Leung J, Grebely J, Vickerman P, Stone J, Cunningham EB, Trickey A, Dumchev K, Lynskey M, Griffiths P, Mattick RP, Hickman M, Larney S. Global prevalence of injecting drug use and sociodemographic characteristics and prevalence of HIV, HBV, and HCV in people who inject drugs: a multistage systematic review. Lancet Glob Health. 2017;5(12):e1192–e1207. https://doi.org/10.1016/S2214-109X(17)30375-3.View ArticleGoogle Scholar
  7. Saffier IP, Kawa H, Harling G. A scoping review of prevalence, incidence and risk factors for HIV infection amongst young people in Brazil. BMC Infect Dis. 2017;17(1):675. https://doi.org/10.1186/s12879-017-2795-9. View ArticlePubMedPubMed CentralGoogle Scholar
  8. Souto FJ. Distribution of hepatitis B infection in Brazil: the epidemiological situation at the beginning of the 21 st century. Rev Soc Bras Med Trop. 2016;49(1):11–23. https://doi.org/10.1590/0037-8682-0176-2015. View ArticlePubMedGoogle Scholar
  9. Puga MA, Bandeira LM, Pompilio MA, Croda J, Rezende GR, Dorisbor LF, Tanaka TS, Cesar GA, Teles SA, Simionatto S, Novais AR, Nepomuceno B, Castro LS, Lago BV, Motta-Castro AR. Prevalence and incidence of HCV infection among prisoners in Central Brazil. PLoS One. 2017;12(1). https://doi.org/10.1371/journal.pone.0169195.View ArticleGoogle Scholar
  10. Komninakis SV, Mota ML, Hunter JR, Diaz RS. Late presentation HIV/AIDS is still a challenge in Brazil and worldwide. AIDS Res Hum Retrovir. 2017. https://doi.org/10.1089/AID.2015.0379. View ArticleGoogle Scholar
  11. União da Indústria de Cana-de-Açúcar [ÚNICA]. Avanço Da Mecanização Incentiva Adoção De Tecnologias De Última Geração Em Sp. (2013). http://www.unica.com.br/noticia/2981091792031019628/avancodamecanizacaoincentivaadocaodetecnologiasdeultimageracaoemsp. Accessed 19 Jan 2018.
  12. Companhia Nacional de Abastecimento [CONAB]. Acompanhamento Da Safra Brasileira De Cana-De-Açúcar, Primeiro Levantamento, Abril 2017. Monitoramento agrícola – Cana-de-açúcar. 2017;4(1):1–57 http://www.conab.gov.br/OlalaCMS/uploads/arquivos/17_04_20_14_04_31_boletim_cana_portugues_-_1o_lev_-_17-18.pdf. Accessed 19 Jan 2018.Google Scholar
  13. Morte CC. Por Exaustão No Trabalho. Universidade Federal da Bahia, Salvador. Caderno CRH. 2017;30(79):105–20 http://www.redalyc.org/articulo.oa?id=347651659007. Accessed 19 Jan 2018.View ArticleGoogle Scholar
  14. Costa PFF, Silva MS, Santos SL. O desenvolvimento (in)sustentável do agronegócio canavieiro. Ciênc saúde coletiva. 2014;19(10):3971–80. https://doi.org/10.1590/1413-812320141910.09472014.View ArticleGoogle Scholar
  15. Rosendo JS, Matos PF. Social impacts with the end of the manual sugarcane harvest: a case study in Brazil. Sociol Int J. 2017;1(4). https://doi.org/10.15406/sij.2017.01.00020.
  16. Instituto Brasileiro de Geografia e Estatística[IBGE]. Conheça Cidades E Estados Do Brasil. (2017). https://cidades.ibge.gov.br/brasil. Accessed 19 Jan 2018.
  17. Novacana. As usinas de Açúcar e Etanol do Brasil. (2017). https://www.novacana.com/usinas_brasil/. Accessed 19 Jan 2018.
  18. Ministério da Saúde. Secretaria de Vigilância em Saúde. Boletim Epidemiológico HIV. Brasília. 2015;4(1).Google Scholar
  19. Henao-Martínez AF, Johnson SC. Diagnostic tests for syphilis: new tests and new algorithms. Neurol Clin Pract. 2014;4(2):114–22. https://doi.org/10.1212/01.CPJ.0000435752.17621.48.View ArticlePubMedPubMed CentralGoogle Scholar
  20. Smolak A, Rowley J, Nagelkerke N, Kassebaum NJ, Chico RM, Korenromp EL, Abu-Raddad LJ. Trends and predictors of syphilis prevalence in the general population: global pooled analyses of 1103 prevalence measures including 136 million syphilis tests. Clin Infect Dis. 2017. https://doi.org/10.1093/cid/cix975.View ArticleGoogle Scholar
  21. World Health Organization [WHO]. Data on the size of the HIV/AIDS epidemic. (2017). http://apps.who.int/gho/data/view.main.22500WHOREG?lang=en Acessed 19 Jan 2018.Google Scholar
  22. Brasil. Ministério da Saúde. Secretaria de Vigilância em Saúde. Departamento de DST, Aids e Hepatites Virais. Protocolo Clínico e Diretrizes Terapêuticas para Atenção Integral às Pessoas com Infecções Sexualmente Transmissíveis / Ministério da Saúde, Secretaria de Vigilância em Saúde, Departamento de DST, Aids e Hepatites Virais. – Brasília: Ministério da Saúde. 2015. p. 120. ISBN 978-85-334-2352-7.Google Scholar
  23. Ribeiro D, Rezende EF, Pinto VM, Pereira GF, Miranda AE. Prevalence of and risk factors for syphilis in Brazilian armed forces conscripts. Sex Transm Infect. 2012;88(1):32–4. https://doi.org/10.1136/sextrans-2011-050066. View ArticlePubMedGoogle Scholar
  24. Pereira LM, Martelli CM, Merchán-Hamann E, Montarroyos UR, Braga MC, de Lima ML, Cardoso MR, Turchi MD, Costa MA, de Alencar LC, Moreira RC, Figueiredo GM, Ximenes RA. Hepatitis study group. Population-based multicentric survey of hepatitis B infection and risk factor differences among three regions in Brazil. Am J Trop Med Hyg. 2009;81(2):240–7.View ArticleGoogle Scholar
  25. Matos MA, França DDDS, Carneiro MADS, Martins RMB, Kerr LRFS, Caetano KAA, Pinheiro RS, Araújo LA, Mota RMS, Matos MAD, Motta CARC, Teles SA. Viral hepatitis in female sex workers using the respondent-driven sampling. Rev Saude Publica. 2017;51:65. https://doi.org/10.1590/S1518-8787.2017051006540. View ArticlePubMedPubMed CentralGoogle Scholar
  26. Oliveira MP, MA1 M, Silva AM, Lopes CL, Teles SA, Matos MA, Spitz N, Araujo NM, Mota RM, Kerr LR, Martins RM. Prevalence, risk behaviors, and Virological characteristics of hepatitis B virus infection in a Group of men who Have sex with men in Brazil: results from a respondent-driven sampling survey. PLoS One. 2016;11(8). https://doi.org/10.1371/journal.pone.0160916.View ArticleGoogle Scholar
  27. Mendoza C. Hot news: HIV epidemics - current burden and future prospects. AIDS Rev. 2017;19(4).Google Scholar
  28. O'Hara GA, McNaughton AL, Maponga T, Jooste P, Ocama P, Chilengi R, Mokaya J, Liyayi MI, Wachira T, Gikungi DM, Burbridge L, O'Donnell D, Akiror CS, Sloan D, Torimiro J, Yindom LM, Walton R, Andersson M, Marsh K, Newton R, Matthews PC. Hepatitis B virus infection as a neglected tropical disease. PLoS Negl Trop Dis. 2017;11(10). https://doi.org/10.1371/journal.pntd.0005842.View ArticleGoogle Scholar
  29. Gamarel KE, Nichols S, Kahler CW, Westfall AO, Lally MA, Wilson CM. Adolescent medicine trials network for HIV/AIDS intervention. A cross-sectional study examining associations between substance use frequency, problematic use and STIs among youth living with HIV. Sex Transm Infect. 2017. https://doi.org/10.1136/sextrans-2017-053334. View ArticleGoogle Scholar
  30. Rocha FLS, Marziale MHP, Hong S. Work and health conditions of sugar cane workers in Brazil. Rev Esc Enferm USP. 2010;44(4):974–9.View ArticleGoogle Scholar
  31. Priuli RMA, Moraes MS, Chiaravalloti RM. The impact of stress on the health of sugar cane cutters. Rev Saude Publica. 2014;48(2):225–31.View ArticleGoogle Scholar
  32. Wesseling C, Aragón A, González M, Weiss I, Glaser J, Bobadilla NA, Roncal-Jiménez C, Correa-Rotter R, Johnson RJ, Barregard L. Kidney function in sugarcane cutters in Nicaragua - a longitudinal study of workers at risk of Mesoamerican nephropathy. Environ Res. 2016;147:125–32.View ArticleGoogle Scholar
  33. Umare A, Seyoum B, Gobena T, Haile Mariyam T. Hepatitis B virus infections and associated factors among pregnant women attending antenatal Care Clinic at Deder Hospital, eastern Ethiopia. PLoS One. 2016;11(11). https://doi.org/10.1371/journal.pone.0166936.View ArticleGoogle Scholar
  34. Szwarcwald CL, Junior PRBS, Marques AP, Almeida WS, Montilla DER. Inequalities in healthy life expectancy by Brazilian geographic regions: findings from the National Health Survey 2013. Int J Equity Health. 2016;15(141). https://doi.org/10.1186/s12939-016-0432-7.
  35. Arboleda M, Castilho MC, Fonseca JCF, Albuquerque BC, Saboia RC, Yoshida CFT. Epidemiological aspects of hepatitis B and D virus in the northern region of Amazonas, Brazil. Trans R Soc Trop Med Hyg. 1995;89:481–3.View ArticleGoogle Scholar
  36. Teles SA, Martins RMB, Silva SA, DMF G, DDP C, Vanderborght BOM, Yoshida CFT. Hepatitis B virus infection profile in central Brazilian hemodialysis population. Rev Inst Med Trop Sao Paulo. 1998;40(5):281–6.View ArticleGoogle Scholar
  37. Ximenes RA, Figueiredo GM, Cardoso MR, et al. Population-based multicentric survey of hepatitis B infection and risk factors in the north, south, and southeast regions of Brazil, 10-20 years after the beginning of vaccination. Am J Trop Med Hyg. 2015;93(6):1341–8.View ArticleGoogle Scholar
  38. Nelson NP, Easterbrook PJ, McMahon BJ. Epidemiology of hepatitis B virus infection and impact of vaccination on disease. Clin Liver Dis. 2016;20(4):607–28. https://doi.org/10.1016/j.cld.2016.06.006.View ArticlePubMedPubMed CentralGoogle Scholar
  39. Zhu D, Guo N, Wang J, Nicholas S, Wang Z, Zhang G, Shi L, Wangen KR. Socioeconomic inequality in hepatitis B vaccination of rural adults in China. Hum Vaccin Immunother. 2017;26. https://doi.org/10.1080/21645515.2017.1396401. View ArticleGoogle Scholar
  40. Murray CJ, Shengelia B, Gupta N, Moussavi S, Tandon A, Thieren M. Validity of reported vaccination coverage in 45 countries. Lancet. 2003;362(9389):1022–7. https://doi.org/10.1016/S0140-6736(03)14411-X.View ArticlePubMedGoogle Scholar
  41. Schweitze A, Akmatov MK, Krause G. Hepatitis B vaccination timing: results from demographic health surveys in 47 countries. Bull World Health Organ. 2017;95(3):199–209. https://doi.org/10.2471/BLT.16.178822.View ArticleGoogle Scholar
  42. Rolnick SJ, Parker ED, Nordin JD, Hedblom BD, Wei F, Kerby T, Jackson JM, Crain AL, Euler G. Self-report compared to electronic medical record across eight adult vaccines: do results vary by demographic factors? Vaccine. 2013;37:3928–35. https://doi.org/10.1016/j.vaccine.2013.06.041.View ArticleGoogle Scholar
  43. Kuo I, Mudrick DW, Strathdee SA, Thomas DL, Sherman SG. Poor validity of self-reported hepatitis B virus infection and vaccination status among young drug users. Clin Infect Dis. 2004;38(4):587–90. https://doi.org/10.1086/381440.View ArticlePubMedGoogle Scholar

Copyright

© The Author(s). 2018

Advertisement