Resistant Salmonella causes 6,200 illnesses a year in US

Posted on December 18, 2016 by Douglas Powell

Chris Dall of the Center for Infectious Disease Research Policy reports the U.S. Centers for Disease Control and Prevention (CDC) has published new estimates of the incidence of antibiotic-resistant Salmonella infections in the United States, putting the burden at about 6,200 cases annually.

In a report in Emerging Infectious Diseases, CDC researchers estimate the overall incidence of resistant salmonella infections as roughly 2 for 100,000 persons per year from 2004 to 2012They also determined that clinically important resistance was linked to four specific Salmonella serotyopes: Enteritidis, Newport, Typhimurium, and Heidelberg.

Nontyphoidal Salmonella causes an estimated 1.2 million foodborne illnesses and about 450 deaths each year, according to the CDC. While most people who get Salmonella infections recover within a week and do not require antibiotics, more severe infections are generally treated with either ampicillin, ceftriaxone, or ciprofloxacin. Resistance to these drugs can result in increased hospitalization, invasive illnesses, and death.

The new estimates are based on data from the US Census Bureau and from two surveillance systems the CDC uses to track Salmonella and drug-resistant Salmonella: The National Antimicrobial Resistance Monitoring System (NARMS) and the Laboratory-based Enteric Disease Surveillance (LEDS) system. NARMS monitors resistance in Salmonella by testing isolates from infected individuals and determining the percentage of isolates that show resistance. LEDS collects Salmonella surveillance data, including serotypes, from state and territorial public health labs.

The researchers defined three mutually exclusive categories of resistance for the study: ampicillin-only resistance, ceftriaxone/ampicillin resistance, and ciprofloxacin nonsusceptibility.

According to the LEDS data, there were 369,254 culture-confirmed Salmonella infections from 2004 through 2012. Four primary serotypes—Enteritidis, Typhimurium, Newport, and Heidelberg—accounted for 52% of all fully serotyped isolates. NARMS tested 19,410 isolates from 2004 through 2012, and overall resistance was detected in 2,320 isolates. Ampicillin-only resistance was the most common resistance pattern detected, followed by ceftriaxone/ampicillin resistance and ciprofloxacin nonsusceptibility.

Using these data, the researchers determined that from 2004 to 20012 there were approximately 6,200 resistant culture-confirmed infections annually. Overall incidence was 1.93/100,000 person-years for any clinically important resistance, 1.07 for ampicillin-only resistance, .51 for ceftriaxone/ampicillin resistance, and .35 for ciprofloxacin nonsusceptibility.

The authors note that while Enteritidis, Typhimurium, Newport, and Heidelberg account for only half of all culture-confirmed Salmonella infections, the four serotypes accounted for 73% of the Salmonella infections that involved clinically important resistance.

The predominance of these four serotypes, they write, reflects their ability to persist in food animals, be transmitted through the food system, and cause illness. It also suggests that strategies to reduce Salmonella infections caused by these four serotypes could have an impact on the incidence of resistant infections overall.

“The 4 major serotypes that have been driving the incidence of resistant infections should continue to be high priorities in combating resistance,” the authors write.

The report also notes that two of these serotypes—Typhimurium and Newport—have been associated with outbreaks of drug-resistant Salmonella infections linked to contaminated meat, which highlights the need for NARMS to continue monitoring emerging resistance patterns by serotype.

The authors caution, however, that while this estimate of resistant Salmonella infection incidence will help define the magnitude of the problem and guide prevention efforts, it might be telling only part of the story. That’s because it relies on culture-confirmed infections only.

The CDC has estimated that for every culture-confirmed case of Salmonella, there may as many as 29 undetected cases. That could put the annual US incidence as high as 180,000 cases.

E. coli O26, HUS and dairy

Posted on December 9, 2016 by Douglas Powell

In their recent article in Eurosurveillance, Germinario et al. describe a community-wide outbreak of Shiga toxin 2-producing Escherichia coli (STEC) O26:H11 infections associated with haemolytic uraemic syndrome (HUS) and involving 20 children between 11 and 78 months of age in southern Italy during the summer 2013 [1]. The investigation identified an association between STEC infection and consumption of dairy products from two local milk-processing establishments. We underline striking similarities to a recent multi-country STEC O26 outbreak in Romania and Italy and discuss the challenges that STEC infections and their surveillance pose at the European level.

In March 2016, Peron et al. published, also in Eurosurveillance, early findings of the investigation of a community-wide STEC infection outbreak in southern Romania [2]. As at 29 February 2016, 15 HUS cases with onset of symptoms after 24 January 2016, all but one in children less than two years of age, had been identified, three of whom had died. Aetiological confirmation was retrospectively performed through serological diagnosis and six cases were confirmed with STEC O26 infection. Shortly after this publication, and following the identification of the first epidemiologically-linked case in central Italy, the European Centre for Disease Prevention and Control (ECDC) and the European Food Safety Authority (EFSA) published a joint Rapid Outbreak Assessment [3]. The Italian and Romanian epidemiological, microbiological and environmental investigations implicated products from a milk-processing establishment in southern Romania as a possible source of infection. The dairy plant exported milk products to at least four European Union (EU) countries. The plant was closed in March 2016 and the implicated food products recalled or withdrawn from the retail market.

Pulsed Field Gel Electrophoresis (PFGE) and whole genome sequencing (WGS) analyses did not establish a microbiological link between the Italian (2013) and the Romanian/Italian (2016) outbreaks (personal communication, Stefano Morabito, October 2016). However, the epidemiological similarities between the two community-wide outbreaks associated with HUS and STEC O26 infections, mostly affecting young children and implicating dairy products, are notable. While raw milk and unpasteurised dairy products are well known potential sources of STEC infection, milk products, as highlighted by Germinaro et al. [1], have been rarely implicated in community-wide STEC outbreaks in the past, emphasising an emerging risk of STEC O26 infection associated with milk products.

Reporting of STEC O26 infections has been steadily increasing in the EU since 2007, partly due to improved diagnostics of non-O157 sero-pathotypes [4]. The attention to non-O157 STEC sero-pathotypes rose considerably after the severe STEC O104 outbreak that took place in Germany and France in 2011 during which almost 4,000 cases and more than 50 deaths were reported [5]. In light of the recently published outbreaks related to dairy products and the simultaneous increased reporting of isolations of STEC O26 from milk and milk products in the EU/European Economic Area (EEA) [6], strengthening STEC surveillance in humans and food and enhancing HUS surveillance in children less than five years of age is warranted. Paediatric nephrologists should be sensitised to this effect

Community-wide outbreaks of haemolytic uraemic syndrome associated with Shiga-toxin producing Escherichia coli O26 in Italy and Romania: A new challenge for the European Union

Eurosurveillance, Volume 21, Issue 49, 08 December 2016, DOI: http://dx.doi.org/10.2807/1560-7917.ES.2016.21.49.30420

E Severi, F Vial, E Peron, O Mardh, T Niskanen, J Takkinen

http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=22664

Data says so: Australia does have a raw egg problem

Posted on December 6, 2016 by Douglas Powell

Statistics show that the consumption of foods containing raw or minimally cooked eggs is currently the single largest source of foodborne Salmonella outbreaks in Australia.

I based a large part of my research career on verifying the soundbite, ‘we have released guidelines’ or, ‘we follow all recommendations’ by arranging to have students see what actually goes on.

In October 2014, the New South Wales Food Authority released Food Safety Guidelines for the Preparation of Raw Egg Products (the Guidelines). Despite this, outbreaks continued to take place, particularly where business hygiene and temperature control issues were apparent. In addition, businesses and councils approached the Food Authority for advice on desserts containing raw eggs and other unusual raw egg dishes. As a result, the Guidelines were recently updated and give specific reference to Standard 3.2.2, Division 3, clause 7 of the Australia New Zealand Food Standards Code to ensure that only safe and suitable food is processed.

To reduce the risk of foodborne illness outbreaks caused by Salmonella, retail businesses are advised to avoid selling food containing raw or minimally cooked eggs. The Guidelines give food businesses that do sell food containing raw egg specific safety steps for its preparation and clear guidance and advice on what they must do to meet food safety regulations. The revised Food Safety Guidelines for the Preparation of Raw Egg Products is available at www. foodauthority.nsw.gov.au/_Documents/ retail/raw_egg_guidelines.pdf.

Or as the Australian Food Safety Information Council now says, buy, don’t make aioli or mayonnaise.

This is nice but of no use to consumers at a restaurant who order fish and chips with a side of mayo or aioli. I’ve already begun an ad hoc investigation – because I don’t want my family to get sick – and can say that out of the 15 times I’ve asked over the past few years – is the aioli or mayo made at the restaurant or bought commercially – the server invariably returns and proclaims, We only use raw eggs in our aioli or mayo.

Wrong answer.

Only once, so far, has an owner or chef said, we know of the risk, we only use the bought stuff. And they’re ex-pat Canadians.

Giv’r, eh.

A table of Australian egg outbreaks is available at https://barfblog.com/wp-content/uploads/2015/10/raw-egg-related-outbreaks-australia-10-9-15.xlsx

Raw is risky: Searching for answers behind Vibrio-in-raw-oyster outbreaks

Posted on December 4, 2016 by Douglas Powell

Michael Casey of The Charlotte Observer reports that for the past 25 years, researcher Stephen Jones has tried to understand the threat that bacteria may pose to oysters in New Hampshire’s Great Bay estuary. He often couldn’t get funding to study the problem. But that is beginning to change as scientists notice “something is going on.”

Scientists are recognizing that a waterborne disease sickening tens of thousands of people each year is associated with warmer waters of the Gulf of Mexico moving northward, partly due to climate change. The problem is extremely rare in New Hampshire and neighboring Maine, but scientists have seen cases elsewhere in New England and expect it to become a bigger problem.

Cases of human illness have been piling up since Sept. in Florida, Massachusetts and Western Canada.

“We have this situation in the northern part of the United States and other cooler climates where people haven’t thought this had been a problem,” said Jones, of the Northeast Center for Vibrio Disease and Ecology at the University of New Hampshire. “In the last 10 or 20 years, it’s become very apparent that there is something going on.”

In a paper in the science journal PLOS One, Jones and other scientists reported their findings that illnesses from vibrio bacteria have jumped significantly in New England — from five cases in 2000 to 147 in 2013. Disease-causing bacteria can contaminate oysters, leading to infections such as diarrhea, vomiting and abdominal pain.

Jones and his colleague, Cheryl Whistler, concluded that warmer waters in the Great Bay, higher salinity and the presence of chlorophyll all contributed to higher concentrations of one of the more common vibrio species that makes people sick — vibrio parahaemolyticus. The researchers are hoping their findings will serve as the foundation of an early warning system for the region’s booming oyster industry.

Currently, all experts can do is monitor the waters and rapidly cool harvested oyster to halt bacteria growth.

An August report in the Proceedings of the National Academy of Sciences found that warming waters were linked to waterborne food poisoning, especially from eating raw oysters.

“There is similar reporting in Alaska where it has been found that increased cases have been occurring where it has not been reported before because of the temperature rise,” said the study’s lead author, Rita Colwell, of the University of Maryland.

The industry has welcomed Jones and Whistler’s work, noting that outbreaks like the one that occurred last month in Massachusetts need to be avoided. Nearly 75 people were sickened.

“When you are involved with a recall because people have gotten sick, you are a losing tremendous amount of money and a tremendous amount of credibility,” said Tom Howell, president of Spinney Creek Shellfish Inc., in Eliot, Maine, which harvests oysters from the Great Bay. A predictive model would allow the industry to move more aggressively to avoid an outbreak, he said.

But Howell and Chris Nash, New Hampshire’s shellfish program manager, said that day could be far off.

“We are still learning what seems to trigger these pathogenic strains to multiply … We don’t have that knowledge yet and it may be that we never do,” Nash said. “We are talking about biological organisms … They react to their environment different, the same way humans do.”

Marketing food safety: Denmark, schnapps and Salmonella

Posted on December 4, 2016 by Douglas Powell

I’ve been a long-time proponent that those farmers, processors and retailers that are really good at microbial food safety should be able to market such evidence directly to consumers.

This has nothing to do with food safety being a non-competitive issue, or whatever else industry types claim: It has everything to do with providing a market-based incentive for those in the farm-to-fork food safety system to brag about what they do.

There are good actors, there are bad actors: if trade associations were really concerned about their customers barfing, they’d stop saying everyone cares about food safety and support efforts to make such information readily available at retail.

But such microbiologically-safe claims are only valid with publicly available data: And there’s no such thing as no risk – or no Salmonella.

As that foodborne Salmonella infections in Denmark reached a historic low, some Danish processors are, according to Steve Sayer of Meatingplace.com, claiming on labels their chicken is Salmonalla-free.

Right, is a retail package containing raw skinless/boneless chicken that was recently purchased in Denmark (DK) Europe.

The labeling on the package is claiming to Danish consumers (where there’s an orange drawing of a chicken within a round circle): “Dansk Salmonelllafri Kylling,” when translated means – “Danish salmonella-free chicken.”

The DK packer is Rose Packing that claims their chicken is “salmonella free” on their website.

The long and winding road that the Danes labored to lowering salmonella within their hatcheries, layer hens, broiler chickens and eggs are impressive.

In 2015 a total of 925 salmonella infections were reported among Danes, which is equivalent to 16.2 infected cases per 100,000 inhabitants. This is the lowest number of salmonella infections since 1988, which is the first year from which researchers at the National Food Institute have used data to map the sources of foodborne salmonella infections.

2015 is also the first year since the introduction of the salmonella source account that Danish eggs have not caused illness. There have also been no registered cases of infection due to Danish chicken meat, which has been the case in four of the previous five years.

“The good results regarding Danish eggs and poultry are very encouraging. However, salmonella still constitutes a risk. Therefore it is important to maintain the preventive measures that researchers, governments and industry have jointly implemented over the years to ensure that salmonella is kept out of Danish products,” Senior Scientific Officer Birgitte Helwigh from the National Food Institute says.

Campylobacter continued to be the cause of most of the registered foodborne infections in Denmark in 2015 with 4,348 cases of illness. This represents a 15% increase from 2014 and is the highest number of cases ever recorded.

Improvements in the reporting system and changes in diagnostic methods mean that more cases of illness are registered than in the past. Therefore it is unclear whether more people actually got a campylobacter infection in 2015 compared to previous years.

In 2015, only 39 foodborne disease outbreaks have been registered. This is the lowest number of outbreaks since a nationwide database for food and waterborne disease outbreaks was established almost ten years ago. A total of 1,233 people have become sick in connection with the 39 outbreaks.

As in previous year norovirus was the leading cause of outbreaks (42%).

FDA says 1 percent of US cucumbers carry Salmonella

Posted on November 27, 2016 by Douglas Powell

One in a hundred cucumbers carries Salmonella, according to new data from the U.S. Food and Drug Administration — and for fresh hot peppers that number rises to three per hundred.

Both the vegetables were targeted by the agency’s proactive testing because of their role in previous outbreaks. Because cucumbers are often eaten raw, bacteria on them are more likely to make it into food; raw cucumbers have been blamed in five outbreaks of illness from 1996 to 2014.

Hot peppers, such as jalapeño and serrano peppers, on the other hand, are often cooked but can be a “stealth component” of multi-ingredient dishes, the FDA said. In 2008, hot peppers were implicated in an outbreak that caused 1,500 illnesses, 308 hospitalizations, and two deaths.

The FDA’s proactive sampling program began testing for disease-causing microbes in certain foods in 2014 to learn more about the prevalence of disease-causing bacteria and to help the agency identify patterns that may help predict and prevent future contamination.

The latest findings, released lastThursday, included results from 1,050 cucumber samples and 1,130 hot pepper samples. Eventually 1,600 of each will be sampled.

Of the cucumber samples, 15 tested positive for salmonella. None tested positive for E. coli. Of the hot pepper samples, 35 tested positive for salmonella, and one tested positive for a strain of Shiga toxin-producing E. coli that was determined to be incapable of causing severe illness.

The samples were collected at ports, packing houses, manufacturers, and distributors across the US.

The agency may take enforcement action, such as a recall, on foods that test positive.

“This testing is still underway and no conclusions can be drawn at this time,” according to the FDA.

In 2014, the FDA started a sampling program for a variety of commodities to learn more about the prevalence of disease-causing bacteria on the commodities.

The microbiological sampling assignments were designed to collect a statistically determined number of samples of certain commodities over 12 to 18 months and test them for certain types of bacteria that can cause foodborne illnesses.

Beware jailhouse nachos

Posted on November 20, 2016 by Douglas Powell

The U.S. Centers for Disease Control reports on October 12, 2015, a county health department notified the Wyoming Department of Health of an outbreak of gastrointestinal illness among residents and staff members at a local correctional facility.

The majority of ill persons reported onset of symptoms within 1–3 hours after eating lunch served at the facility cafeteria at noon on October 11. Residents and staff members reported that tortilla chips served at the lunch tasted and smelled like chemicals. The Wyoming Department of Health and county health department personnel conducted case-control studies to identify the outbreak source.

Consuming lunch at the facility on October 11 was highly associated with illness; multivariate logistic regression analysis found that tortilla chips were the only food item associated with illness. Hexanal and peroxide, markers for rancidity, were detected in tortilla chips and composite food samples from the lunch. No infectious agent was detected in human stool specimens or food samples. Extensive testing of lunch items did not identify any unusual chemical. Epidemiologic and laboratory evidence implicated rancid tortilla chips as the most likely source of illness.

This outbreak serves as a reminder to consider alternative food testing methods during outbreaks of unusual gastrointestinal illness when typical foodborne pathogens are not identified. For interpretation of alternative food testing results, samples of each type of food not suspected to be contaminated are needed to serve as controls.

Gastrointestinal illness associated with rancid tortilla chips at a correctional facility — Wyoming, 2015

CDC MMWR

Tiffany Lupcho et al.

https://www.cdc.gov/mmwr/volumes/65/wr/mm6542a4.htm?s_cid=mm6542a4_e

Blame the media: Crypto reporting in England

Posted on October 19, 2016 by Douglas Powell

During August 2015, a boil water notice (BWN) was issued across parts of North West England following the detection of Cryptosporidium oocysts in the public water supply.

Using prospective syndromic surveillance, we detected statistically significant increases in the presentation of cases of gastroenteritis and diarrhea to general practitioner services and related calls to the national health telephone advice service in those areas affected by the BWN.

In the affected areas, average in-hours general practitioner consultations for gastroenteritis increased by 24.8% (from 13.49 to 16.84) during the BWN period; average diarrhea consultations increased by 28.5% (from 8.33 to 10.71). Local public health investigations revealed no laboratory reported cases confirmed as being associated with the water supply. These findings suggest that the increases reported by syndromic surveillance of cases of gastroenteritis and diarrhea likely resulted from changes in healthcare seeking behaviour driven by the intense local and national media coverage of the potential health risks during the event.

This study has further highlighted the potential for media-driven bias in syndromic surveillance, and the challenges in disentangling true increases in community infection from those driven by media reporting.

The potential impact of media reporting in syndromic surveillance: An example using a possible Cryptosporidium exposure in north west England, August to September 2015

Euro Surveill. 2016;21(41):pii=30368. DOI: http://dx.doi.org/10.2807/1560-7917.ES.2016.21.41.30368

AJ Elliot, HE Hughes, J Astbury, G Nixon, K Brierley, R Vivancos, T Inns, V Decraene, K Platt, I Lake, SJ O’Brien, GE Smith

http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=22610

Foodborne (1973-2013) and waterborne (1971-2013) disease outbreaks – United States

Posted on October 13, 2016 by Douglas Powell

This isn’t the detailed overview, but the annual overall snapshot of food and waterborne illness in the U.S.

My favorite part has always been the second figure. To avoid foodborne illness, move to Texas. That hasn’t changed since 1973.

All it means is, cowboys and girls don’t look too hard.

It’s just a little barfing – get over it

Foodborne Disease Outbreaks

During 1973–2013, the U.S. Centers for Disease Control (CDC) received reports of 30,251 foodborne disease outbreaks with 742,945 outbreak-associated illnesses from the 50 states, Puerto Rico, the District of Columbia, and freely associated states/territories. An average of 738 (range: 298–1,404) outbreaks were reported each year.

The average annual number of foodborne disease outbreaks reported to CDC increased in 1998 in comparison to previous years, coinciding with the transition to an electronic reporting system, and decreased in 2009 in comparison to 1998–2008 coinciding with the transition to reporting through NORS (FDOSS and WBDOSS share an enhanced reporting platform, the National Outbreak Reporting System (NORS) (http://www.cdc.gov/nors). NORS also collects information on disease outbreaks with modes of transmission other than food and water, including person-to-person contact, animal contact, and environmental contamination.)

In 2013, a total of 792 single-state exposure outbreaks were reported with 11,786 illnesses by 47 states and Puerto Rico (Table) (Figure 2); an additional 26 multistate outbreaks (i.e., exposure to the implicated food occurred in more than one state) with 1,530 associated illnesses also were reported. CDC periodically publishes more detailed annual summaries describing the implicated foods, etiologic agents, settings, and points of contamination associated with foodborne disease outbreaks (http://www.cdc.gov/foodsafety/fdoss/data/annual-summaries/index.html).

Waterborne Disease Outbreaks

During 1971–2013, CDC received reports of 1,957 waterborne disease outbreaks with 642,782 outbreak-associated illnesses from 50 states and six freely associated states/territories. An average of 46 waterborne outbreaks was reported each year (Figure 1). In 2013, a total of 55 outbreaks causing at least 2,824 illnesses occurred in 21 states. No multistate outbreaks were reported; waterborne disease outbreak data for 2013 are preliminary (Table) (Figure 3). CDC periodically publishes more detailed summaries of waterborne disease outbreaks associated with recreational water and of waterborne disease outbreaks associated with drinking water (http://www.cdc.gov/healthywater/surveillance/surveillance-reports.html).

Reported outbreaks represent only a small fraction of all foodborne and waterborne illnesses that occur each year and the outbreak data reported here are subject to limitations. Outbreaks caused by certain pathogens or vehicles might be more likely to be recognized, investigated, or reported. Some illnesses reported as sporadic (i.e., not outbreak-associated) are likely not recognized as being part of a reported outbreak or might be part of an undetected outbreak. In addition, all outbreak-related illnesses might not be identified during an investigation, smaller outbreaks might not come to the attention of public health authorities, and some outbreaks might not be investigated or reported to CDC.

Reporting practices for foodborne and waterborne disease outbreaks vary among states and territories, which might have differing definitions or interpretations of which events are reportable and unique laws related to disease outbreak reporting. Thus, variations in reporting rates by state or territory might reflect variations in levels of effort and funding for foodborne and waterborne disease outbreak investigation, rather than true differences in outbreak incidence rates by state. NORS maintains a dynamic database; this report includes data available on May 1, 2015, for foodborne disease outbreaks and May 4, 2015, for waterborne disease outbreaks; data published in this Summary might differ from those published earlier or later.

Foodborne disease outbreaks are defined as two or more cases of a similar illness resulting from ingestion of a common food. Waterborne disease outbreaks are defined as two or more cases of a similar illness linked epidemiologically by time and location to exposure to water or water-associated chemicals volatized into the air.

Is there anybody out there? Physicians and handwashing

Posted on October 3, 2016 by Douglas Powell

Our objectives were to evaluate the utility of electronic hand hygiene counting devices in outpatient settings and the impact of results feedback on physicians’ hand hygiene behaviors.

We installed 130 electronic hand hygiene counting devices in our redesigned outpatient department. We remotely monitored physicians’ hand hygiene practices during outpatient examinations and calculated the adherence rate as follows: number of hand hygiene counts divided by the number of outpatients examined multiplied by 100. Physician individual adherence rates were also classified into 4 categories.

Results

Two hundred and eighty physicians from 28 clinical departments were monitored for 3 months. The overall hand hygiene adherence rate was 10.7% at baseline, which improved significantly after feedback to 18.2% in the third month. Of the clinical departments, 78.6% demonstrated significant improvement in hand hygiene compliance. The change in the percentage of physicians in each category before and after feedback were as follows: very low (84.3% to 72.1%), low (8.6% to 14.3%), moderate (2.9% to 8.9%), and high (4.3% to 4.6%), from the first to third month, respectively. Based on category assessment, 17.1% of physicians were classified as responders.

Conclusions

Physicians’ adherence to hand hygiene practices during outpatient examinations was successfully monitored remotely using electronic counting devices. Audit and feedback of adherence data may have a positive impact on physicians’ hand hygiene compliance.

Utility of electronic hand hygiene counting devices for measuring physicians’ handwashing

American Journal of Infection Control, DOI: http://dx.doi.org/10.1016/j.ajic.2016.08.002

A Arai, M Tanabe, A Nakamura, D Yamasaki, Y Muraki, T Kaneko, A Kadowaki, M Ito

http://www.sciencedirect.com/science/article/pii/S0196655316307532

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