Reheating food and rice
Previous advice to avoid reheating cooked food was reviewed in the context of known risk and potential benefit to the patient. There was no evidence that correctly reheated food, increases food poisoning risk in immunocompromised individuals. Therefore guidance on cooling, storing and reheating cooked food safely has been added to the recommendations. The exception to this advice is reheating cooked rice. The spores of Bacillus cereus and Bacillus subtilis found in rice, survive the cooking process. These develop into bacteria that multiply very quickly at ambient temperatures and may not be adequately killed during reheating. Therefore rice should be served hot and eaten immediately after it is first cooked.
There was no evidence to support any change to the existing recommendations regarding water. Campylobacter has been found and can flourish in bottled and mineral water (4-6) and Legionella, Pseudomonas aeruginosa and Pseudomonas fluorescens have been isolated from commercially available bottled still water (5;7;8). Non-carbonated bottled water may also contain large amounts of gram negative bacteria such as Stenotrophomonas maltophillia (9). Therefore recommendations continue to support avoiding non-carbonated bottled water, mineral water and water from fresh wells during neutropenia < 0.5.
Clarification regarding water from water coolers and dispensers has been added to the current consensus. Contamination and poor maintenance of dispensers can again be a risk factor in the immunocompromised for cryptosporidiosis (9;10), Pseudomonas aerunginosa (11;12) and Pseudomonos fluorescens (9;13).
Ice is now stipulated as safe if made from the appropriate water sources. With regards to commercially available ice based drinks such as “slush puppy” the group reached consensus to avoid these due to unknown source of ice production, storage conditions and potential risk of contamination from the machine dispenser.
Ice cream is used as a quick high calorie snack for many of our patients. There is inadequate research available to give evidence based guidance; therefore the recommendations are based on group consensus. When considering the manufacturing process it was felt that ice cream is unlikely to present a significant risk, provided it has been stored at the correct temperature, had not previously thawed, was individually wrapped and from a reputable source. This excludes ice cream sold from mobile vans including ice cream from soft serve machines that may harbour unacceptable levels of bacteria.
There is no evidence that ingested Lactobacilli and bifidobacteria are any greater infection risk than commensal strains, e.g. those found in the mouth, ileum and colon (14). Reported infections from specific probiotics are mainly limited to Saccharomyces boulardii/ cerevisiae, the soil organism B Subtilis and lactobacillus rhamnosus LGG (15;16). In some cases of bacteraemia, the methods for matching the particular strain of bacteria to that consumed has been criticised. Lactobacillus and Bifidobacteria identification verified by DNA based approaches at species level is required but this is rarely carried out routinely (17).
There is a growing body of evidence that probiotics are safe in other immunocompromised groups e.g. HIV and neonates (14;16) (18) (19) and there may be benefits to the haematology patient in terms of graft versus host disease (20) gastrointestinal health or immune function (21). However disruption of the intestinal epithelial barrier during cancer treatment could theoretically lead to translocation of Lactobacilli or bifidobacteria. Other risk factors for the pathogenicity of probiotics have also been suggested i.e. immune compromise, presence of a central venous catheter or jejunal administration of the probiotic (15;16). One or more of these risk factors may be present in a neutropenic patient.
Therefore, the recommendations to avoid probiotic cultures if patients are immunosuppressed have not changed. This approach is endorsed by the product manufacturers themselves. The advice is based on uncertainty rather than robust evidence of harm and these recommendations will require on-going review as further evidence becomes available.
All yogurts are made using the live bacterial starter cultures Lactobacillus delbrueckii subsp. bulgaricus and/ or Streptococcus thermophilus. Historically patients with a low neutrophil count have been advised to avoid yogurt containing live cultures and choose pasteurised products. However, the majority of yogurts are not pasteurised post production. Often where the term pasteurised is found on a yogurt label it relates to the milk used. Hence immunocompromised individuals already (unwittingly) consume live yogurt cultures.
Unlike probiotic bacteria, starter cultures cannot survive in the human stomach and are not normal human commensals. These cultures have been used safely since the early 1900s to produce yogurt and are considered by the food industry as non-pathogenic. A literature review in 2004 found no reports linking lactic acid bacteria from fermented milk to infection in humans (22). Therefore previous advice, which considered live yogurt with probiotic cultures, has been revised. Live yogurt is not potentially harmful and no restriction is necessary. This represents a significant change to neutropenic dietary advice and will greatly improve choice for this patient group.
Of note is the lack of legislation surrounding product labelling of live cultures or probiotics. Hence there is a risk some yogurts may contain unlabelled probiotic bacteria (17). However it is unlikely that significant numbers of probiotic bacteria would be added to a product unless that product was to be marketed for its probiotic content/ benefits. Therefore unless a product specifically makes reference to its probiotic content then no restriction is necessary. Due to the lack of clear definition of the term “bio” it was felt prudent to avoid these products also.
The microbes of concern in honey are primarily yeasts and spore-forming bacteria. Bacterial spores, particularly those in the Bacillus genus are regularly found in honey. Although the antibacterial property of honey discourages growth or persistence of many microorganisms it is recommended that the following types of honey are avoided when following a neutropenic diet: raw honey, unpasteurised honey, strained honey, fresh honey comb. Honey that is labelled as pasteurised has undergone heat treatment to destroy the yeast cells. Filtered honey is heated and strained to remove fine particles such as pollen, dust, and nectar which can contaminate the honey. The neutropenic diet therefore allows pasteurised and filtered honey to be consumed. It is recommended that where possible single serving or small jars of pasteurised or filtered honey should be used as there is a potential for large jars to become contaminated with microorganisms from the normal environment and from food handlers and/or equipment being used (23).
Nuts and dried fruit
Salmonella and Escherichia coli have been linked to the consumption of nuts. Peanuts, almonds, pistachios, pecans, pine nuts, macadamias, hazelnuts, Brazil nuts, and walnuts have all been involved in product recalls due to salmonella. Recent evidence of unacceptable levels of Salmonella spp in ready to eat nuts supports the avoidance of “raw” nuts (24).
The most common method for reducing pathogens in nuts is the application of heat (25). Therefore if the nut has undergone a process of heating such as roasting then these can be consumed when neutropenic. It is recommended that raw and unshelled nuts/nut products should not be consumed. Similarly cooked and processed dried fruit is not considered high risk, allowing consumption of products such as flap jacks, cereal bars, fruit cakes or scones.
Vegetable and Fruit Smoothies
The guidelines have now clarified that the packaging on any commercially bought juice or smoothie should state that it has undergone pasteurisation or heat treatment. Homemade smoothies can be made from washed and peeled fruit allowed from the original list or from tinned or frozen fruit and vegetables.
Previous advice to avoid ready to eat smoked fish during neutropenia was based on potential risk for contamination with listeria moncytogenes. However a recent Food Standards Agency survey found only 3 samples that breached the legal limit in 3000 samples of ready to eat smoked fish at point of sale in 1000 outlets (26). As a result the group felt that ready to eat smoked fish from a vacuum packet was safe to eat where neutrophil counts > 0.5 provided it was consumed within 24 hours of opening. This is in line with the FSA advice to other vulnerable groups i.e. pregnant women, where ready to eat smoked fish is not restricted (27). Due to uncertainty surrounding risk from low levels of bacteria the group have continued to recommend avoidance of ready to eat smoked fish where neutrophils < 0.5.