Skip to main content
Top
Published in: BMC Infectious Diseases 1/2017

Open Access 01-12-2017 | Research article

Prevalence and molecular characteristics of Staphylococcus aureus, including methicillin resistant strains, isolated from bulk can milk and raw milk products in pastoral communities of South-West Uganda

Authors: Benon B. Asiimwe, Rossella Baldan, Alberto Trovato, Daniela M. Cirillo

Published in: BMC Infectious Diseases | Issue 1/2017

Login to get access

Abstract

Background

Staphylococcus aureus strains are now regarded as zoonotic agents. In pastoral settings where human-animal interaction is intimate, multi-drug resistant microorganisms have become an emerging zoonotic issue of public health concern. The study of S. aureus prevalence, antimicrobial resistance and clonal lineages in humans, animals and food in African settings has great relevance, taking into consideration the high diversity of ethnicities, cultures and food habits that determine the lifestyle of the people. Little is known about milk carriage of methicillin resistant S. aureus strains (MRSA) and their virulence factors in Uganda. Here, we present the prevalence of MRSA in bulk can milk and raw milk products in pastoral communities of south-west Uganda. We also present PFGE profiles, spa-types, as well as frequency of enterotoxins genes.

Methods

S. aureus was identified by the coagulase test, susceptibility testing by the Kirby-Bauer disc diffusion and E-test methods and MRSA by detection of the mecA gene and SCCmec types. The presence of Panton – Valentine Leucocidin (PVL) genes and staphylococcal enterotoxins was determined by PCR, while genotyping was by PFGE and spa typing.

Results

S. aureus were isolated from 30/148 (20.3%) milk and 11/91(12%) sour milk samples. mecA gene carriage, hence MRSA, was detected in 23/41 (56.1%) of the isolates, with 21 of the 23 (91.3%) being SCCmec type V; while up to 30/41 (73.2%) of the isolates were resistant to tetracycline. Only five isolates carried the PVL virulence gene, while PFGE typing revealed ten clusters (ranging from two seven isolates each) that comprised 83% of the sample, and only eight isolates with unique pulsotypes. The largest PFGE profile (E) consisted of seven isolates while t7753, t1398, and t2112 were the most common spa-types. Thirty seven of the 41 strains (90.2%) showed at least one of the eight enterotoxin genes tested, with sem 29 (70.7%), sei 25 (61%) and seg 21 (51.2%) being the most frequently observed genes.

Conclusion

This is the first study to demonstrate MRSA and enterotoxin genes in raw milk and its products in Uganda. The fact that over 90% of the isolates carried at least one gene encoding enterotoxins shows a high risk of spread of foodborne diseases through milk in this setting.
Literature
1.
go back to reference van Loo IH, Diederen BM, Savelkoul PH, Woudenberg JH, Roosendaal R, et al. Methicillin-resistant Staphylococcus aureus in meat products, the Netherlands. Emerg Infect Dis. 2007;13:1753–5.CrossRefPubMedPubMedCentral van Loo IH, Diederen BM, Savelkoul PH, Woudenberg JH, Roosendaal R, et al. Methicillin-resistant Staphylococcus aureus in meat products, the Netherlands. Emerg Infect Dis. 2007;13:1753–5.CrossRefPubMedPubMedCentral
2.
go back to reference Juhasz-Kaszanyitzky E, Janosi S, Somogyi P, Dan A, van der Graaf-van Bloois L, et al. MRSA transmission between cows and humans. Emerg Infect Dis. 2007;13:630–2.CrossRefPubMedPubMedCentral Juhasz-Kaszanyitzky E, Janosi S, Somogyi P, Dan A, van der Graaf-van Bloois L, et al. MRSA transmission between cows and humans. Emerg Infect Dis. 2007;13:630–2.CrossRefPubMedPubMedCentral
3.
go back to reference Garcia-Alvarez L, Holden MT, Lindsay H, Webb CR, Brown DF, et al. Meticillin-resistant Staphylococcus aureus with a novel mecA homologue in human and bovine populations in the UK and Denmark: a descriptive study. Lancet Infect Dis. 2011;11:595–603.CrossRefPubMedPubMedCentral Garcia-Alvarez L, Holden MT, Lindsay H, Webb CR, Brown DF, et al. Meticillin-resistant Staphylococcus aureus with a novel mecA homologue in human and bovine populations in the UK and Denmark: a descriptive study. Lancet Infect Dis. 2011;11:595–603.CrossRefPubMedPubMedCentral
4.
go back to reference Normanno G, Corrente M, La Salandra G, Dambrosio A, Quaglia NC, et al. Methicillin-resistant Staphylococcus aureus (MRSA) in foods of animal origin product in Italy. Int J Food Microbiol. 2007;117:219–22.CrossRefPubMed Normanno G, Corrente M, La Salandra G, Dambrosio A, Quaglia NC, et al. Methicillin-resistant Staphylococcus aureus (MRSA) in foods of animal origin product in Italy. Int J Food Microbiol. 2007;117:219–22.CrossRefPubMed
5.
go back to reference Lee JH. Methicillin (Oxacillin)-resistant Staphylococcus aureus strains isolated from major food animals and their potential transmission to humans. Appl Environ Microbiol. 2003;69:6489–94.CrossRefPubMedPubMedCentral Lee JH. Methicillin (Oxacillin)-resistant Staphylococcus aureus strains isolated from major food animals and their potential transmission to humans. Appl Environ Microbiol. 2003;69:6489–94.CrossRefPubMedPubMedCentral
6.
go back to reference Kasozi KI, Tingiira JB, Vudriko P. High prevalence of subclinical mastitis and multidrug resistant Staphylococcus aureus are a threat to dairy cattle production in Kiboga District (Uganda). Open J Vet Med. 2014;4:35–43.CrossRef Kasozi KI, Tingiira JB, Vudriko P. High prevalence of subclinical mastitis and multidrug resistant Staphylococcus aureus are a threat to dairy cattle production in Kiboga District (Uganda). Open J Vet Med. 2014;4:35–43.CrossRef
7.
go back to reference Kateete DP, Kabugo U, Baluku H, Nyakarahuka L, Kyobe S, et al. Prevalence and antimicrobial susceptibility patterns of bacteria from milkmen and cows with clinical mastitis in and around Kampala, Uganda. PLoS One. 2013;8:e63413.CrossRefPubMedPubMedCentral Kateete DP, Kabugo U, Baluku H, Nyakarahuka L, Kyobe S, et al. Prevalence and antimicrobial susceptibility patterns of bacteria from milkmen and cows with clinical mastitis in and around Kampala, Uganda. PLoS One. 2013;8:e63413.CrossRefPubMedPubMedCentral
8.
go back to reference Kamau NPM, Dolci S, Jans C, Wangoh J, Lacroix C, et al. Phenotypic and genotypic antibiotic resistance patterns of Staphylococcus aureus from raw and spontaneously fermented camel milk. Eur J Nutr Food Safety. 2013;3:87–98.CrossRef Kamau NPM, Dolci S, Jans C, Wangoh J, Lacroix C, et al. Phenotypic and genotypic antibiotic resistance patterns of Staphylococcus aureus from raw and spontaneously fermented camel milk. Eur J Nutr Food Safety. 2013;3:87–98.CrossRef
9.
go back to reference De Buyser ML, Dufour B, Maire M, Lafarge V. Implication of milk and milk products in food-borne diseases in France and in different industrialised countries. Int J Food Microbiol. 2001;67:1–17.CrossRefPubMed De Buyser ML, Dufour B, Maire M, Lafarge V. Implication of milk and milk products in food-borne diseases in France and in different industrialised countries. Int J Food Microbiol. 2001;67:1–17.CrossRefPubMed
10.
go back to reference Kateete DP, Namazzi S, Okee M, Okeng A, Baluku H, et al. High prevalence of methicillin resistant Staphylococcus aureus in the surgical units of Mulago hospital in Kampala, Uganda. BMC Res Notes. 2011;4:326.CrossRefPubMedPubMedCentral Kateete DP, Namazzi S, Okee M, Okeng A, Baluku H, et al. High prevalence of methicillin resistant Staphylococcus aureus in the surgical units of Mulago hospital in Kampala, Uganda. BMC Res Notes. 2011;4:326.CrossRefPubMedPubMedCentral
11.
go back to reference Seni J, Bwanga F, Najjuka CF, Makobore P, Okee M, et al. Molecular characterization of Staphylococcus aureus from patients with surgical site infections at Mulago Hospital in Kampala, Uganda. PLoS One. 2013;8:e66153.CrossRefPubMedPubMedCentral Seni J, Bwanga F, Najjuka CF, Makobore P, Okee M, et al. Molecular characterization of Staphylococcus aureus from patients with surgical site infections at Mulago Hospital in Kampala, Uganda. PLoS One. 2013;8:e66153.CrossRefPubMedPubMedCentral
12.
go back to reference Grace D, Omore A, Randolph T, Kang'ethe E, Nasinyama GW, et al. Risk assessment for Escherichia coli O157:H7 in marketed unpasteurized milk in selected east African countries. J Food Prot. 2008;71:257–63.CrossRefPubMed Grace D, Omore A, Randolph T, Kang'ethe E, Nasinyama GW, et al. Risk assessment for Escherichia coli O157:H7 in marketed unpasteurized milk in selected east African countries. J Food Prot. 2008;71:257–63.CrossRefPubMed
13.
go back to reference Genigeorgis CA. Present state of knowledge on staphylococcal intoxication. Int J Food Microbiol. 1989;9:327–60.CrossRefPubMed Genigeorgis CA. Present state of knowledge on staphylococcal intoxication. Int J Food Microbiol. 1989;9:327–60.CrossRefPubMed
15.
go back to reference Kerouanton A, Hennekinne JA, Letertre C, Petit L, Chesneau O, et al. Characterization of Staphylococcus aureus strains associated with food poisoning outbreaks in France. Int J Food Microbiol. 2007;115:369–75.CrossRefPubMed Kerouanton A, Hennekinne JA, Letertre C, Petit L, Chesneau O, et al. Characterization of Staphylococcus aureus strains associated with food poisoning outbreaks in France. Int J Food Microbiol. 2007;115:369–75.CrossRefPubMed
16.
17.
go back to reference Cheesbrough M District laboratory practice in tropical countries, part 2. 2nd edition.: 62-70, 132-143, 157-234. 2005.CrossRef Cheesbrough M District laboratory practice in tropical countries, part 2. 2nd edition.: 62-70, 132-143, 157-234. 2005.CrossRef
18.
go back to reference Zhang K, McClure JA, Elsayed S, Louie T, Conly JM. Novel multiplex PCR assay for characterization and concomitant subtyping of staphylococcal cassette chromosome mec types I to V in methicillin-resistant Staphylococcus aureus. J Clin Microbiol. 2005;43:5026–33.CrossRefPubMedPubMedCentral Zhang K, McClure JA, Elsayed S, Louie T, Conly JM. Novel multiplex PCR assay for characterization and concomitant subtyping of staphylococcal cassette chromosome mec types I to V in methicillin-resistant Staphylococcus aureus. J Clin Microbiol. 2005;43:5026–33.CrossRefPubMedPubMedCentral
19.
go back to reference Paterson GK, Larsen AR, Robb A, Edwards GE, Pennycott TW, et al. The newly described mecA homologue, mecALGA251, is present in methicillin-resistant Staphylococcus aureus isolates from a diverse range of host species. J Antimicrob Chemother. 2012;67:2809–13.CrossRefPubMedPubMedCentral Paterson GK, Larsen AR, Robb A, Edwards GE, Pennycott TW, et al. The newly described mecA homologue, mecALGA251, is present in methicillin-resistant Staphylococcus aureus isolates from a diverse range of host species. J Antimicrob Chemother. 2012;67:2809–13.CrossRefPubMedPubMedCentral
20.
go back to reference Lina G, Piemont Y, Godail-Gamot F, Bes M, Peter MO, et al. Involvement of Panton-Valentine leukocidin-producing Staphylococcus aureus in primary skin infections and pneumonia. Clin Infect Dis. 1999;29:1128–32.CrossRefPubMed Lina G, Piemont Y, Godail-Gamot F, Bes M, Peter MO, et al. Involvement of Panton-Valentine leukocidin-producing Staphylococcus aureus in primary skin infections and pneumonia. Clin Infect Dis. 1999;29:1128–32.CrossRefPubMed
21.
go back to reference Baldan R, Tassan Din C, Semeraro G, Costa C, Cichero P, et al. Severe community-onset infections in healthy individuals caused by community-acquired MRSA in an Italian teaching hospital, 2006-2008. J Hosp Infect. 2009;72:271–3.CrossRefPubMed Baldan R, Tassan Din C, Semeraro G, Costa C, Cichero P, et al. Severe community-onset infections in healthy individuals caused by community-acquired MRSA in an Italian teaching hospital, 2006-2008. J Hosp Infect. 2009;72:271–3.CrossRefPubMed
22.
go back to reference Tenover FC, Arbeit RD, Goering RV, Mickelsen PA, Murray BE, et al. Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J Clin Microbiol. 1995;33:2233–9.PubMedPubMedCentral Tenover FC, Arbeit RD, Goering RV, Mickelsen PA, Murray BE, et al. Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J Clin Microbiol. 1995;33:2233–9.PubMedPubMedCentral
23.
go back to reference Mellmann A, Friedrich AW, Rosenkotter N, Rothganger J, Karch H, et al. Automated DNA sequence-based early warning system for the detection of methicillin-resistant Staphylococcus aureus outbreaks. PLoS Med. 2006;3:e33.CrossRefPubMedPubMedCentral Mellmann A, Friedrich AW, Rosenkotter N, Rothganger J, Karch H, et al. Automated DNA sequence-based early warning system for the detection of methicillin-resistant Staphylococcus aureus outbreaks. PLoS Med. 2006;3:e33.CrossRefPubMedPubMedCentral
24.
go back to reference Jarraud S, Mougel C, Thioulouse J, Lina G, Meugnier H, et al. Relationships between Staphylococcus aureus genetic background, virulence factors, agr groups (alleles), and human disease. Infect Immun. 2002;70:631–41.CrossRefPubMedPubMedCentral Jarraud S, Mougel C, Thioulouse J, Lina G, Meugnier H, et al. Relationships between Staphylococcus aureus genetic background, virulence factors, agr groups (alleles), and human disease. Infect Immun. 2002;70:631–41.CrossRefPubMedPubMedCentral
25.
go back to reference Diep BA, Carleton HA, Chang RF, Sensabaugh GF, Perdreau-Remington F. Roles of 34 virulence genes in the evolution of hospital- and community-associated strains of methicillin-resistant Staphylococcus aureus. J Infect Dis. 2006;193:1495–503.CrossRefPubMed Diep BA, Carleton HA, Chang RF, Sensabaugh GF, Perdreau-Remington F. Roles of 34 virulence genes in the evolution of hospital- and community-associated strains of methicillin-resistant Staphylococcus aureus. J Infect Dis. 2006;193:1495–503.CrossRefPubMed
26.
go back to reference Kuroda M, Ohta T, Uchiyama I, Baba T, Yuzawa H, et al. Whole genome sequencing of meticillin-resistant Staphylococcus aureus. Lancet. 2001;357:1225–40.CrossRefPubMed Kuroda M, Ohta T, Uchiyama I, Baba T, Yuzawa H, et al. Whole genome sequencing of meticillin-resistant Staphylococcus aureus. Lancet. 2001;357:1225–40.CrossRefPubMed
27.
go back to reference Gill SR, Fouts DE, Archer GL, Mongodin EF, Deboy RT, et al. Insights on evolution of virulence and resistance from the complete genome analysis of an early methicillin-resistant Staphylococcus aureus strain and a biofilm-producing methicillin-resistant Staphylococcus epidermidis strain. J Bacteriol. 2005;187:2426–38.CrossRefPubMedPubMedCentral Gill SR, Fouts DE, Archer GL, Mongodin EF, Deboy RT, et al. Insights on evolution of virulence and resistance from the complete genome analysis of an early methicillin-resistant Staphylococcus aureus strain and a biofilm-producing methicillin-resistant Staphylococcus epidermidis strain. J Bacteriol. 2005;187:2426–38.CrossRefPubMedPubMedCentral
28.
go back to reference Sakwinska O, Giddey M, Moreillon M, Morisset D, Waldvogel A, et al. Staphylococcus aureus Host range and human-bovine host shift. Appl Environ Microbiol. 2011;77:5908–15.CrossRefPubMedPubMedCentral Sakwinska O, Giddey M, Moreillon M, Morisset D, Waldvogel A, et al. Staphylococcus aureus Host range and human-bovine host shift. Appl Environ Microbiol. 2011;77:5908–15.CrossRefPubMedPubMedCentral
29.
go back to reference Jorgensen HJ, Mork T, Caugant DA, Kearns A, Rorvik LM. Genetic variation among Staphylococcus aureus strains from Norwegian bulk milk. Appl Environ Microbiol. 2005;71:8352–61.CrossRefPubMedPubMedCentral Jorgensen HJ, Mork T, Caugant DA, Kearns A, Rorvik LM. Genetic variation among Staphylococcus aureus strains from Norwegian bulk milk. Appl Environ Microbiol. 2005;71:8352–61.CrossRefPubMedPubMedCentral
30.
go back to reference Chaalal W, Aggad H, Saidi N, Kihal M. Prevalence and antimicrobial resistance of Methicillin-resistant Staphylococcus aureus isolated from raw meat and bovine milk in Algeria. Adv Environ Biol. 2014;8:1–5. Chaalal W, Aggad H, Saidi N, Kihal M. Prevalence and antimicrobial resistance of Methicillin-resistant Staphylococcus aureus isolated from raw meat and bovine milk in Algeria. Adv Environ Biol. 2014;8:1–5.
31.
go back to reference Corrente M, Normanno G, Martella V, Bellacicco AL, Quaglia NC, et al. Comparison of methods for the detection of methicillin resistance in Staphylococcus aureus isolates from food products. Lett Appl Microbiol. 2007;45:535–9.CrossRefPubMed Corrente M, Normanno G, Martella V, Bellacicco AL, Quaglia NC, et al. Comparison of methods for the detection of methicillin resistance in Staphylococcus aureus isolates from food products. Lett Appl Microbiol. 2007;45:535–9.CrossRefPubMed
32.
go back to reference Witte W, Pasemann B, Cuny C. Detection of low-level oxacillin resistance in mecA-positive Staphylococcus aureus. Clin Microbiol Infect. 2007;13:408–12.CrossRefPubMed Witte W, Pasemann B, Cuny C. Detection of low-level oxacillin resistance in mecA-positive Staphylococcus aureus. Clin Microbiol Infect. 2007;13:408–12.CrossRefPubMed
33.
go back to reference Bhattacharya D, Carleton H, Tsai CJ, Baron EJ, Perdreau-Remington F. Differences in clinical and molecular characteristics of skin and soft tissue methicillin-resistant Staphylococcus aureus isolates between two hospitals in northern California. J Clin Microbiol. 2007;45:1798–803.CrossRefPubMedPubMedCentral Bhattacharya D, Carleton H, Tsai CJ, Baron EJ, Perdreau-Remington F. Differences in clinical and molecular characteristics of skin and soft tissue methicillin-resistant Staphylococcus aureus isolates between two hospitals in northern California. J Clin Microbiol. 2007;45:1798–803.CrossRefPubMedPubMedCentral
34.
go back to reference Ganga R, Riederer K, Sharma M, Fakih MG, Johnson LB, et al. Role of SCCmec type in outcome of Staphylococcus aureus bacteremia in a single medical center. J Clin Microbiol. 2009;47:590–5.CrossRefPubMedPubMedCentral Ganga R, Riederer K, Sharma M, Fakih MG, Johnson LB, et al. Role of SCCmec type in outcome of Staphylococcus aureus bacteremia in a single medical center. J Clin Microbiol. 2009;47:590–5.CrossRefPubMedPubMedCentral
35.
go back to reference Zecconi A, Cesaris L, Liandris E, Dapra V, Piccinini R. Role of several Staphylococcus aureus virulence factors on the inflammatory response in bovine mammary gland. Microb Pathog. 2006;40:177–83.CrossRefPubMed Zecconi A, Cesaris L, Liandris E, Dapra V, Piccinini R. Role of several Staphylococcus aureus virulence factors on the inflammatory response in bovine mammary gland. Microb Pathog. 2006;40:177–83.CrossRefPubMed
36.
go back to reference Aires-de-Sousa M, Parente CE, Vieira-da-Motta O, Bonna IC, Silva DA, et al. Characterization of Staphylococcus aureus isolates from buffalo, bovine, ovine, and caprine milk samples collected in Rio de Janeiro state, Brazil. Appl Environ Microbiol. 2007;73:3845–9.CrossRefPubMedPubMedCentral Aires-de-Sousa M, Parente CE, Vieira-da-Motta O, Bonna IC, Silva DA, et al. Characterization of Staphylococcus aureus isolates from buffalo, bovine, ovine, and caprine milk samples collected in Rio de Janeiro state, Brazil. Appl Environ Microbiol. 2007;73:3845–9.CrossRefPubMedPubMedCentral
37.
go back to reference Hetem DJ, Bootsma MC, Troelstra A, Bonten MJ. Transmissibility of livestock-associated methicillin-resistant Staphylococcus aureus. Emerg Infect Dis. 2013;19:1797–802.CrossRefPubMedPubMedCentral Hetem DJ, Bootsma MC, Troelstra A, Bonten MJ. Transmissibility of livestock-associated methicillin-resistant Staphylococcus aureus. Emerg Infect Dis. 2013;19:1797–802.CrossRefPubMedPubMedCentral
38.
go back to reference Normanno G, Firinu A, Virgilio S, Mula G, Dambrosio A, et al. Coagulase-positive Staphylococci and Staphylococcus aureus in food products marketed in Italy. Int J Food Microbiol. 2005;98:73–9.CrossRefPubMed Normanno G, Firinu A, Virgilio S, Mula G, Dambrosio A, et al. Coagulase-positive Staphylococci and Staphylococcus aureus in food products marketed in Italy. Int J Food Microbiol. 2005;98:73–9.CrossRefPubMed
39.
go back to reference Mathieu AM, Isigidi BK, Devriese LA, Godard C, Vanhoof R. Characterization of Staphylococcus aureus and salmonella spp. strains isolated from bovine meat in Zaire. Int J Food Microbiol. 1991;14:119–25.CrossRefPubMed Mathieu AM, Isigidi BK, Devriese LA, Godard C, Vanhoof R. Characterization of Staphylococcus aureus and salmonella spp. strains isolated from bovine meat in Zaire. Int J Food Microbiol. 1991;14:119–25.CrossRefPubMed
40.
go back to reference Rall VL, Vieira FP, Rall R, Vieitis RL, Fernandes A Jr, et al. PCR detection of staphylococcal enterotoxin genes in Staphylococcus aureus strains isolated from raw and pasteurized milk. Vet Microbiol. 2008;132:408–13.CrossRef Rall VL, Vieira FP, Rall R, Vieitis RL, Fernandes A Jr, et al. PCR detection of staphylococcal enterotoxin genes in Staphylococcus aureus strains isolated from raw and pasteurized milk. Vet Microbiol. 2008;132:408–13.CrossRef
41.
go back to reference Rosec JP, Gigaud O. Staphylococcal enterotoxin genes of classical and new types detected by PCR in France. Int J Food Microbiol. 2002;77:61–70.CrossRefPubMed Rosec JP, Gigaud O. Staphylococcal enterotoxin genes of classical and new types detected by PCR in France. Int J Food Microbiol. 2002;77:61–70.CrossRefPubMed
42.
go back to reference Jarraud S, Peyrat MA, Lim A, Tristan A, Bes M, et al. Egc, a highly prevalent operon of enterotoxin gene, forms a putative nursery of superantigens in Staphylococcus aureus. J Immunol. 2001;166:669–77.CrossRefPubMed Jarraud S, Peyrat MA, Lim A, Tristan A, Bes M, et al. Egc, a highly prevalent operon of enterotoxin gene, forms a putative nursery of superantigens in Staphylococcus aureus. J Immunol. 2001;166:669–77.CrossRefPubMed
Metadata
Title
Prevalence and molecular characteristics of Staphylococcus aureus, including methicillin resistant strains, isolated from bulk can milk and raw milk products in pastoral communities of South-West Uganda
Authors
Benon B. Asiimwe
Rossella Baldan
Alberto Trovato
Daniela M. Cirillo
Publication date
01-12-2017
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2017
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-017-2524-4

Other articles of this Issue 1/2017

BMC Infectious Diseases 1/2017 Go to the issue