To the Editor: International air travel can lead to the rapid global dissemination of infectious agents. Unlike products and byproducts of animal origin imported between countries under agreements that legally establish sanitary standards, products introduced into a country illegally or irregularly do not follow specific standards and can come from any source, thereby posing a risk to the health status of a country. Animal products transported clandestinely in baggage can contain infectious agents harmful to animal and human health (1–4). We investigated Brucella spp., Mycobacterium bovis, and Mycobacterium avium subsp. paratuberculosis (MAP) in dairy products seized from baggage of passengers on flights at the 2 main international airports (Guarulhos Airport, São Paulo, and Galeão Airport, Rio de Janeiro, in Brazil.
During 2010–2011, 12 missions were instigated by the International Agriculture Surveillance (VIGIAGRO/MAPA) in airports to detect and seize unauthorized dairy products carried by passengers; 195 products were collected from multiple flights from different destinations. Baggage was scanned by using an x-ray machine and, on detection of a product, was opened by the owner in the presence of a federal agriculture inspector. To avoid contamination, the products were not opened and were sent to the designated Ministry of Agriculture, Livestock and Food Supply Laboratory in their original packaging. All seized products were packed according to the International Air Transport Association standards (5) and transported by commercial aviation with official monitoring to the laboratory.
After completing real-time quantitative PCR (Promega, Madison, WI, USA) using TaqMan technology (Life Technologies, Darmstadt, Germany), we extracted DNA directly from the sample (6,7). The technique for the detection of MAP and eryD Brucella (except strain 19 Brucella abortus) and also using the region RD4 to detect M. bovis were proposed by Irange et al. (8). To detect M. bovis, we used the primers M. bovis-88-F (5′-CGC.CTT.CCT.AAC.CAG.AAT.TG-3′), M. bovis-88-R (5′-GGA.GAG.CGC.CGT.TGT.AGG-3′) and to detect Brucella, we used Bru-Eri-Taq-92-F (5′-GCC.ACA.CTT.TCT.GCA.ATC.TG-3′) and Bru-Eri-Taq-92-F (5′-GCG.GTG.GAT.AAT.GAA.ATC.TGC-3′).
We analyzed 35 containers of dulce de leche, a caramelized milk paste confection, from Argentina (n = 30), Angola (n = 1), and Uruguay (n = 4). We tested all specimens for Brucella spp. and MAP, and 32 for M. bovis. We detected MAP in 1 specimen from Argentina and 1 from Uruguay, Brucella spp. in 3 specimens from Argentina and 1 from Uruguay, and M. bovis in 1 specimen from Argentina.
Three containers of liquid milk from the United States were collected and analyzed for the presence of MAP; 2 were analyzed for M. bovis and Brucella. Brucella was detected in 1 specimen. Five containers of powdered milk were seized: 2 from Chile, 2 from Angola, and 1 from Portugal. Brucella was detected in 1 container from Chile; Brucella and M. bovis were found in 1 container from Angola. Four containers of yogurt were seized, 1 each from the United States, China, Angola, and South Africa. MAP was detected in those from Angola and South Africa, and the yogurt from South Africa also showed Brucella.
We analyzed samples from 147 cheeses that were confiscated from baggage owned by travelers from 21 countries, mainly from Italy (24.5%), Portugal (22.4%), and France (14.3%). M. bovis was identified in 18 (17.5%) cheeses collected from Italy, Portugal, Spain, the United States, the Netherlands, Lebanon, Morocco, and Norway. MAP was amplified in specimens from 13 cheeses from Spain, United States, Iraq, Israel, Norway, Peru, France, and Portugal, the last 2 countries showed the highest occurrence. Brucella was detected in 62 of the cheeses analyzed, which originated in Bolivia, Chile, Iraq, Lebanon, and Morocco (n = 1 in each country), Netherlands, Israel, and Norway (n = 2 in each country), Turkey and Spain (n = 3 in each country), United States, France and England (n = 4 in each country), Portugal (n=10), and Italy (n = 23).
Both M. bovis and Brucella were detected in 13 (8.8%) cheeses (1 each from Spain, Netherlands, Morocco, and Norway; 4 from Portugal, and 5 from Italy); Brucella and MAP were detected in 4 (2.7%) cheeses (Spain, France, Portugal, and Iraq). Co-amplification of the 3 genes (Brucella + MAP + M. bovis) occurred in 3 (2%) cheeses (United States, Norway, and Portugal). Among the cheeses analyzed, 84 (57.1%) contained isolates that amplified >1 of the genes for the 3 bacteria examined.
Of the 166 dairy products analyzed, Brucella was detected in 70 (42.1%). Cheeses were the most seized products (n = 121) and had the highest number of Brucella-positive results (62/121[51.2%]). Brucella was detected in dairy products that originated in Argentina, Spain, France, Iraq, Israel, Italy, Lebanon, Portugal, and Turkey; it was detected in 4 (21%) of the 19 cheeses from France and in 3 of the 4 (75%) cheeses that originated in Spain. M. bovis was detected in dulce de leche from Argentina, powdered milk from Chile, and in cheeses from Spain, Netherlands, Italy, Lebanon, Morocco, Norway, and Portugal.
Bacteria can be introduced into a country through contaminated animal products that are brought across borders illegally. The risk may be even greater when these products are carried in passengers’ baggage on international flights because of the growing number of international travelers and the wide range of origins of these passengers. Greater attention should be given to agricultural surveillance at airports to mitigate the risk for introduction of these products.
de Melo CB, de Sá MEP, Souza AR, de Oliveira AM, Mota PMPC, Campani, PR, et al. Bacteria in dairy products in baggage of incoming travelers, Brazil [letter]. Emerg Infect Dis. 2014 Nov [date cited]. http://dx.doi.org/10.3201/eid2011.13142
Author affiliations: University of Brasília, Brasília, Brazil (C.B. de Melo, A.R. Souza, C. McManus, L. Seixas Author affliliations:); Ministry of Agriculture, Livestock and Food Supply (MAPA), Brasília, Brazil (M.E.P. de Sa); MAPA, Galeão Airport, Rio de Janeiro, Brazil (P.R Campani); MAPA, Guarulhos Airport, São Paulo, Brazil (J.O. Luna); MAPA, Confins International Airport, Belo Horizonte/Confins, Brazil (S. Cabral Pinto); MAPA, Brasilia International Airport (BSB), Brasília, Brazil (F.F. Schwingel); MAPA, Pedro Leopoldo, Brazil (A.M. de Oliveira, P.M.P.C. Mota).
Schneider H. Good governance of national Veterinary Services. Rev. Sci. Tech. 2011;30:325–38 [cited 2011 Apr]. PubMed
Hartnett E, Adkin A, Seaman M, Cooper J, Watson E, Coburn H, A quantitative assessment of the risks from illegally imported meat contaminated with foot and mouth disease virus to Great Britain. Risk Anal. 2007;27:187–202 . DOIPubMed
Brückner GK. Ensuring safe international trade: how are the roles and responsibilities evolving and what will the situation be in ten years’ time? Rev. Sci. Tech. 2011;30:317–24 [cited 2011 Apr].
de Melo CB, de Sa MEP, Alves FF, McManus C, Aragão LF, Belo BB, Profile of international air passengers intercepted with illegal animal products in baggage at Guarulhos and Galeão airports in Brazil. SpringerPlus 2014: 3:69.
International Air Transport Association. 3.6.2 Division 6.2—Infectious substances. 2011 January 1 [cited 2011 Aug 10]. http://www.iata.org/whatwedo/cargo/dgr/Documents/DGR52_InfectiousSubstances(DGR362).pdf
Millar BC, Jiru X, Moore JE, Earle JAP. A simple and sensitive method to extract bacterial, yeast and fungal DNA from blood culture material. J Microbiol Methods. 2000;42:139–47. DOIPubMed
Dias NL. Staphylococcus aureus identification, evaluation of the enterotoxigenic potential and methicillin resistance by the PCR technique in dulce de leche samples in the Sete-Lagoas microregion, in the State of Minas Gerais, Brazil (dissertation) [in Portuguese]. Belo Horizonte, Minas Gerais, Brazil: Federal University of Minas Gerais, 2010.
Irenge LM, Walravens K, Govaerts M, Godfroid J, Rosseels V, Huygen K, Development and validation of a triplex real-time PCR for rapid detection and specific identification of M. avium sub sp. paratuberculosis in faecal samples. Vet Microbiol. 2009;136:166–72. DOIPubMed
Emerging Infectious Diseases, Volume 20, Number 11—November 2014
Luna JO, Pinto SC, Schwingel FF, McManus C, Seixas L