abstract: # Objective
  .
  To examine whether business improvement districts (BID) contributed to greater than expected declines in the incidence of violent crimes in affected neighbourhoods.
  .
  # Method
  .
  A Bayesian hierarchical model was used to assess the changes in the incidence of violent crimes between 1994 and 2005 and the implementation of 30 BID in Los Angeles neighbourhoods.
  .
  # Results
  .
  The implementation of BID was associated with a 12% reduction in the incidence of robbery (95% posterior probability interval −2 to 24) and an 8% reduction in the total incidence of violent crimes (95% posterior probability interval −5 to 21). The strength of the effect of BID on robbery crimes varied by location.
  .
  # Conclusion
  .
  These findings indicate that the implementation of BID can reduce the incidence of violent crimes likely to result in injury to individuals. The findings also indicate that the establishment of a BID by itself is not a panacea, and highlight the importance of targeting BID efforts to crime prevention interventions that reduce violence exposure associated with criminal behaviours.
author: John MacDonald; Daniela Golinelli; Robert J Stokes; Ricky Bluthenthal**Correspondence to** Dr John M MacDonald, Department of Criminology, University of Pennsylvania, McNeil Building, Suite 483 3718 Locust Walk, Philadelphia, PA 19104-6286, USA; <firstname.lastname@example.com>
date: 2010-06-29
institute: 1University of Pennsylvania, Philadelphia, Pennsylvania, USA; 2RAND Corporation, Santa Monica, California, USA; 3Drexel University, Philadelphia, Pennsylvania, USA
references:
title: The effect of business improvement districts on the incidence of violent crimes

Research indicates the importance of community-level attributes for explaining the incidence of interpersonal violence and crime in neighbourhoods, but there are few examples of effective community-level violence prevention interventions.1–3 Several studies suggest that implementation of the community economic development model of the business improvement district (BID) reduces crime in affected neighbourhoods.4 5 The BID model relies on special assessments levied on commercial properties located within designated business areas to augment services typically provided by public agencies, including sanitation, public safety, place marketing and planning efforts.6 Although managed and operated by private sector non-profit organisations, the majority of BID are public entities, chartered and regulated by local governments.7 The services delivered through BID assessment schemes, however, do not typically replace current public services. BID services typically are directed towards sanitation and security of common public space areas such as sidewalks (and not interior spaces), analogous to the common area service arrangements seen in home owners' associations.8 BID often focus their budgets on providing private security to their business locales and surrounding neighbourhoods, as a basic level of enhancement to publicly funded police services.9

One of the more rigorous evaluations of BID by Brooks5 indicated that their adoption in areas of Los Angeles was associated with a significant drop in the number of serious crimes reported to the police between 1990 and 2002, controlling for time stable differences between areas and in comparison with neighbourhoods that proposed BID but did not end up adopting them. Given that the adoption of a BID in Los Angeles requires extensive support from business and property owners (eg, at least 15% of the business owners or 50% of the property owners must sign supporting petitions) and a laborious process of legal and legislative oversight, the simple proposed adoption of a BID may not provide a strong comparison group.10 11 The actual process of BID adoption is, by itself, a signal of commitment from business merchants and landowners to promote economic development through various community change activities. Even after taking into account time stable area differences in the average volume of crime, poverty rates and other neighbourhood features, it is difficult to reconcile whether establishing a BID is independent from other facets of community change that may presage drops in crime. A detailed analysis of budget data and observations of neighbourhoods in Los Angeles where BID are situated, for example, showed that their priorities of spending were correlated with observable indicators of neighbourhood physical decay and surrounding economic conditions.12 Therefore, using the BID area before BID implementation may be a more appropriate comparison group.

We rely on a pre–post intervention design to assess the effects of BID on the incidence of violent crimes. We use the year of implementation to reflect the exposure to the BID intervention and examine the pre–post changes in the incidence of violent crimes in affected neighbourhoods, controlling for overall time trends.

# Methods

## Design

We examined BID effects by modelling the pre–post changes in the incidence or rate of violent crimes from 1994 to 2005 for all neighbourhood areas exposed to BID. Between 1996 and 2003, a total of 30 separate BID were implemented in Los Angeles. The unit of analysis is any of the 30 neighbourhood areas that eventually adopted a BID in Los Angeles during the period of observation. Table 1 reports the number of BID areas that became fully operational at any given year. We consider a BID fully operational if its implementation occurred for the entire calendar year. The formulation of BID in Los Angeles requires a formalised and uniform planning and adoption stage that is structured by law. Details are provided elsewhere.12 For all the areas that eventually adopted a BID in Los Angeles, there are at least 2 years' worth of data during which no BID (pre) was operational and, similarly, at least 2 years of data during which all the BID were fully operational (post). We make use of this type of interrupted time series to estimate the average BID effect on the rate of violent crimes.

BID by year of observation in Los Angeles

Year
No of BID started
BID area

1994
–

1995
–

1996
2
Wilshire Centre

Fashion District

1997
2
Hollywood Entertainment I

San Pedro

1998
6
Los Feliz Village

Larchmont Village

Downtown Centre

Figueroa Corridor

Century Corridor

Greater Lincoln Heights

1999
11
Granada Hills

Canoga Park

Van Nuys Boulevard Auto Row

Tarzana

Studio City

Hollywood Media

Westwood Village

Historic Core (Downtown)

Toy District

Downtown Industrial

Jefferson Park

2000
2
Chatsworth

Sherman Oaks

2001
4
Encino

Los Angeles Chinatown

Wilmington

Lincoln Heights Industrial

2002
2
Northridge

Highland Park

2003
1
Reseda

2004
0
–

2005
0
–

Source: Los Angeles City Clerk's Office.

BID, business improvement district.

## Data

The data consist of the yearly counts of officially recorded violent felony crimes (homicide, rape, robbery and aggravated assault) by the Los Angeles Police Department that were aggregated from police reporting districts to corresponding BID areas. If a reporting district is present in a BID this district is counted as receiving the BID intervention. A total of 179 reporting districts are present in the 30 BID neighbourhood areas. We focus primarily on the counts of robbery, because this crime is less susceptible to underreporting by the police, is more likely than other crimes to occur in public settings between strangers and just over 30% of people who are robbed experience an injury.13–15 Nearly one out of five robberies nationally result in a serious injury that requires medical treatment, such as a gunshot wound, knife/stab/slash wound, broken bones or teeth, internal injury and/or loss of consciousness.16 17 The estimated social costs of an average robbery are high, with an average cost of US\$39 287 (in 2005 dollars) if one includes monetary costs associated with medical and emergency services, lost productivity, mental health and general quality of life.18 By focussing our analysis primarily on violent crimes, and in particular robbery, we are offering a closer look at the effective role that BID expend on crime prevention efforts that attempt to improve the social control of public space areas through environmental design modifications and spending on private security. We do not examine property crime offences because they are less likely to be reported to the police, many occur in private settings (eg, larceny/theft) and are not 'street crimes' directly subject to BID efforts to enhance social control in public spaces.

## Time trends

Table 2 presents a summary of the average frequency of robbery and all violent crimes for areas exposed to BID compared with non-BID areas that incorporate the rest of Los Angeles. The simple linear trend of these data indicates that BID areas experienced greater, on average, yearly reductions in the incidence of robbery and violence than non-BID areas. For example, the average yearly reduction in robbery was 1.9 in BID areas, compared with 1.2 in non-BID areas. The log of the average robbery counts indicates a 7% reduction in BID areas compared with a 5.7% reduction in non-BID areas. During the 12-year period, however, the average yearly count of reported violent offences dropped by 58% for Los Angeles as a whole, suggesting that it is important to take into account this secular trend in assessing the effects of BID on violent crimes.

Average crimes, by year in BID and non-BID reporting districts

| Year         | Non-BID areas (n=893) |            | BID areas (n=179) |            |
|--------------|-----------------------|------------|-------------------|------------|
|              | Robbery               | Violent    | Robbery           | Violent    |
|              | M (median)            | M (median) | M (median)        | M (median) |
| 1994         | 25.88 (17)            | 64.27 (42) | 41.6 (35)         | 86.53 (66) |
| 1995         | 24.01 (16)            | 60.89 (41) | 41.56 (35)        | 89.75 (74) |
| 1996         | 21.06 (13)            | 54.70 (35) | 34.3 (29)         | 77.35 (61) |
| 1997         | 16.85 (11)            | 49.14 (33) | 29.37 (24)        | 70.52 (57) |
| 1998         | 13.06 (8)             | 42.99 (28) | 22.34 (17)        | 59.77 (51) |
| 1999         | 11.82 (7)             | 40.58 (26) | 19.98 (16)        | 56.46 (46) |
| 2000         | 12.90 (8)             | 43.63 (26) | 21.66 (18)        | 60.26 (51) |
| 2001         | 15.43 (10)            | 49.38 (31) | 26.20 (21)        | 68.74 (55) |
| 2002         | 14.05 (8)             | 44.56 (26) | 24.83 (20)        | 62.94 (54) |
| 2003         | 13.60 (8)             | 42.24 (26) | 23.92 (19)        | 60.21 (51) |
| 2004         | 11.81 (7)             | 36.65 (22) | 19.43 (15)        | 49.12 (44) |
| 2005         | 11.49 (7)             | 26.49 (15) | 18.06 (14)        | 37.91 (34) |
| Average      | 16.00 (9)             | 46.29 (28) | 26.94 (10)        | 64.96 (52) |
| Linear trend | −1.2                  | −2.5       | −1.9              | −3.6       |

Each column presents the average (M) and median (50th percentile) values for the number of incidents in business improvement district (BID) and non-BID areas.

## Statistical model

We used a Bayesian hierarchical model to assess the pre–post effects of BID adoption in areas that were exposed to BID. We estimate the BID effect in each individual area and the average BID effect across all areas. We model the number of reported robberies and violent crimes with a Poisson distribution with mean (*λ~it~*) for each of the 30 BID areas (*i*) over a 12-year (*t*) time period. We include a random effect parameter for areas to scale the time trend for the volume of crimes in each BID area, and to account for time invariant differences across the 30 BID areas. We account for the overall 12-year crime time trend in Los Angeles with a natural cubic spline.19 As the yearly incidence of violent crimes for Los Angeles as a whole was declining over the 12-year study period, it is important to account for the secular trend in the model so as not to overestimate the BID effect. The population at risk of violent crimes in each BID area is unknown, representing a mix of residents and non-residents (eg, shoppers). We bypass the problem of having to estimate the population at risk of violent crimes by comparing every BID area with itself. Under the assumption that the population at risk does not change over time, we propose a model that has as the main parameter of interest for area *i* the ratio (*K~i~*) of the crime rate if a BID was adopted divided by the crime rate that the trends predict would have happened if the BID had not been adopted. If *K~i~* is less than 1, this indicates that the presence of a BID in area (*i*) is associated with a reduction in the incidence of violent crimes for that area. We use a Bayesian hierarchical model to assess individual effects across each BID area (*i*) and to approximate the average overall BID effect (*μ~K~*) across all 30 areas.20 Full technical details on the model and specification of priors are available elsewhere.12

The yearly violent crime trends for a sample of 12 of the 30 BID areas are displayed in figure 1 and show the timing of each of the BID interventions (denoted by a vertical line). Figure 1 provides a visual sense for the fact that the Bayesian hierarchical model is estimating an interrupted time series for each unique BID area and then pooling the effect across all areas. The Poisson model implies the counterfactual that the rate of violent crimes in an area after the BID becomes fully operational is proportional to what the rate would have been in that area had the BID not been implemented.

# Results

Table 3 reports the overall BID effect for the incidence of robbery and violent crimes in terms of the percentage reductions (posterior mean) associated with the adoption of BID and the 95% posterior probability intervals. Table 3 also reports the posterior probability of observing an overall BID effect on reducing the incidence of robbery and violent crimes (P(*μ~K~*\<1), where *μ~K~* represents the overall effect across the 30 BID areas. We find that the posterior probability of a BID effect is 0.96. In other words, there is strong evidence that BID reduced the robbery rate. The estimated percentage reduction: obtained as one minus the posterior mean (*μ~K~*) indicates a 12% average reduction (95% posterior probability interval −2 to 24) in the incidence of robbery associated with the implementation of BID. For the total incidence of violence BID effects are in the same direction, but the statistical evidence is not as strong (P(*μ~K~* \<1)=0.91), and indicates an 8% average reduction (95% posterior probability interval −5 to 21) in the total incidence of violence associated with the adoption of BID.

Estimated percentage reduction in reported violent crimes from BID

| Outcomes | Posterior mean* | 95% Posterior probability interval | Posterior probability BID effect (P(μ~*K*~ \<1)) |
|----|----|----|----|
| Robbery | 12 | (−2,24) | 0.96 |
| Violent | 8 | (−5,21) | 0.91 |

Posterior mean reflects the percentage reduction as calculated by (1−*μ~K~*)×100.

BID, business improvement district.

Given that the observed probability of an overall BID effect was strongest for robbery, table 4 reports the BID area-specific effects for official reports of robbery in terms of percentage reductions in robberies (*1–K~i~)*. The individual BID area results for robbery show that for 14 of the 30 areas the posterior probability of observing a BID effect is 0.90 or higher. In terms of effect sizes for these 14 areas, the robbery rate is reduced by a high of 27% in the Century Corridor BID to a low of 14% in the Downtown Industrial BID. For another two BID areas, the observed posterior probability is more than 0.80, which still provides evidence for the presence of a BID effect in the expected direction. The BID effects appear to be most pronounced for the incidence of robbery, which one would expect is likely to be affected by environmental features of the neighbourhoods, such as hiring private security officers, which are the focus of BID efforts to control public space areas. Overall, there seems to be evidence in the data that the BID in Los Angeles had an effect in reducing the incidence of reported robberies.

Area-specific estimates of BID effects on robbery

| BID name | Posterior mean (1–*K~i~*) | BID effect (p=*K~i~*\<1) | 95% Posterior CI |
|----|----|----|----|
| Granada Hills | 18 | 0.93 | −6, 37 |
| Chatsworth | 5 | 0.65 | −20, 25 |
| Northridge | 18 | 0.94 | −5, 36 |
| Reseda | 15 | 0.90 | −9, 33 |
| Canoga Park | 3 | 0.60 | −24, 25 |
| Van Nuys | 26 | 0.99 | 7, 41 |
| Tarzana | −10 | 0.25 | −44, 16 |
| Encino | 11 | 0.76 | −22, 35 |
| Sherman Oaks | 10 | 0.76 | −18, 31 |
| Studio City | 9 | 0.76 | −20, 31 |
| Los Feliz Village | 21 | 0.98 | 1, 39 |
| Highland Park | 11 | 0.83 | −14, 30 |
| Hollywood Entertainment | 9 | 0.80 | −16, 28 |
| Hollywood Media | 15 | 0.95 | −5, 32 |
| Larchmont Village | 34 | 0.99 | 5, 53 |
| Wilshire Centre | 4 | 0.63 | −25, 26 |
| Los Angeles Chinatown | 21 | 0.98 | 0, 38 |
| Westwood Village | 21 | 0.97 | −1, 39 |
| Downtown Centre | 7 | 0.74 | −17, 25 |
| Historic Core | 1 | 0.55 | −21, 21 |
| Toy District | 8 | 0.77 | −16, 27 |
| Fashion District | −24 | 0.05 | −63, 5 |
| Downtown Industrial | 14 | 0.90 | –8, 31 |
| Figueroa Corridor | 20 | 0.96 | −2, 36 |
| Jefferson Park | 17 | 0.95 | −4, 33 |
| Century Corridor | 27 | 1.00 | 8, 43 |
| Wilmington | –7 | 0.28 | −34, 14 |
| San Pedro | 8 | 0.75 | −18, 29 |
| Lincoln Heights | 11 | 0.77 | −20, 34 |
| Greater Lincoln Heights | 25 | 1.00 | 6, 41 |

*K~i~*=ratio of robbery crimes (post-business improvement district (BID)/pre-BID). Bold indicates a BID with a probability of a BID effect of ≥0.90.

Given the size of the BID effects appear to be most pronounced for robbery, this raises the question of how much BID spending occurs in relation to social costs saved by reducing robberies. Multiplying our estimated 12% (annual) reduction to the average incidence of robberies (*M*=160.7) associated with BID implementation to the estimated social costs (US\$39 287 in 2005 dollars)18 of an average robbery shows a marginal cost saving of approximately US\$757 611 (in 2005 dollars) (annually). Given that the average annual budget of the 30 BID in Los Angeles was approximately US\$736 670 (in 2005 dollars),12 this suggests that a sizeable social cost–benefit of BID implementation can be attributed to the reductions in robbery alone.

## Additional tests

We also conducted several additional tests on our measures of violent crime and the methods for approximating BID effects. Homicides, for example, are the most accurately reported violent crimes, but we did not discuss the yearly trends in homicide because the counts are so low. The average number of homicides per year in neighbourhoods associated with BID is less than one, and the median (50th percentile) is zero. The point estimates from replicating our model for homicide counts varies widely, and the probability of detecting a BID effect is low (P(μ~K~\<1)=0.43)), suggesting that BID have no appreciable effect on homicide. In particular, the homicide model indicates a 5% increase associated with BID adoption but with a large CI (95% posterior probability interval −50 to 29), resulting from low counts and imprecision in our estimate. A combined estimate of the count of robbery and homicide together was statistically identical to that of robbery alone, suggesting that the BID adoption effect observed is driven by the rate of robberies.

We also constructed alternative model specifications in line with previous work that Brooks5 used on an analysis of the effects of BID on reported serious crimes in Los Angeles during earlier years. We compared the estimated effect of BID implementation on robberies and all reported violent crimes using all police reporting districts in Los Angeles as the unit of analysis, including those that do not intersect BID areas. We then included a dummy variable denoting the timing of BID, adjacent neighbourhoods to BID as control variables, and fixed-effect terms (dummy variables) for each individual reporting district, year, and their interactions (reporting district\*year). Our results from these specifications were sensitive to the parameterisation of the outcomes. If we relied on ordinary least squares regression we found a statistically significant BID effect in reducing the mean incidence of robberies (b=−4.63; p\<0.001) and all violent crimes (b=−7.33; p\<0.001) by approximately 16% and 11%, respectively. However, if we relied on a Poisson regression model the results were substantially lower and were only marginally significant for robberies (b=−0.02; p=0.07) and total violence (b=−0.01; p=0.09), reducing the respective incidence by 3% and 2%. We think this sensitivity test provides further justification for our use of a simpler model that estimates only the BID effects for those areas that eventually adopted BID, rather than assigning BID effects to the entire city of Los Angeles.

## Limitations

The Bayesian hierarchical model provides an estimate of the effect of BID on the incidence of robbery and violent crimes in areas that were exposed to BID. Like all models this approach has several limitations. First, the model assumes that the population at risk of violence does not change once a BID starts. It is, however, possible that the establishment of a BID could change the population at risk of violent crimes in a number of ways. If, for example, there is a substantial increase in the number of shoppers or new residents because a BID was implemented then even a substantial decline in the incidence of violence would be offset by an increase in the denominator for the population at risk. Such an increase in the population at risk of violence would lead one to conclude that the adoption of the BID did not have an effect in reducing violence. Assuming that the population at risk coincides with the residential population in an area would be incorrect, as it is almost certain that successfully implemented BID attract a larger number of people for commerce to areas.

Second, the model assumes that the level to which violent crimes are reported to the police does not change systematically with the adoption of a BID. If, however, the adoption of a BID implies an increase in local merchants' and residents' willingness to report crimes to the police and an increased response from the police to combat crime, then the violent crime reports may actually increase as a function of the implementation of a BID. If this were the case, the adopted model would suggest that adopting a BID has the effect of increasing the incidence of violent crimes. Given that the findings suggest an overall effect of BID on reducing the robbery rate and marginal effects for all violent crimes, we have some confidence in these results.

In addition, if one assumes that BID areas have unique features in terms of the businesses that operate and the communities that encourage their establishment, constructing a group of comparison areas that are matched to the BID areas with respect to certain demographic features of area residents would represent a less conservative test of the effects of BID. We think that the areas that will eventually adopt a BID are the best comparison group for those areas that have already adopted a BID, as there are clearly features of BID areas that are unique in their ability to get a majority of landowners and merchants interested in their adoption. At the same time, our analysis offers no prescription for the various mechanisms by which BID impact robbery rates. BID adopt a variety of tactics, such as mobilising the police, hiring private security officers, street cleaning and environmental redesign to increase a sense of cleanliness and safety of BID areas. Unfortunately, the tactics adopted by each BID area are complex and not easy to approximate in a statistical model.

# Discussion and conclusions

The results from this study suggest that BID reduce the rate of robbery crimes in affected Los Angeles neighbourhoods. The overall effect of BID on robberies is consistent with the efforts that many of these Los Angeles BID expend on improving the physical appearance of their areas to make them more attractive to commercial business and less attractive to potential offenders (eg, painting over graffiti, increased street lighting, closed-circuit television, or CCTV, cameras). The size of the BID effect on robberies varies across the 30 BID areas and appears to indicate a greater than expected reduction in robberies in those located in neighbourhoods that have undergone significant patterns of economic development or invested heavily in crime prevention. For example, BID area-specific effects were apparent in Jefferson Park and Figueroa Corridor, which are situated close to the University of Southern California, in areas of notable gentrification and economic development. Hollywood Media and Larchmont also exhibited BID-area-specific effects on the incidence of robberies and are situated in neighbourhoods undergoing gentrification. BID effects are present in Century Corridor, Figueroa Corridor and Hollywood Media, all of which invest heavily in crime prevention through hiring private security officers and other activities. 10–12 Los Angeles BID spend a considerable share of their resources hiring private security or public ambassadors who focus on keeping streetscapes clean and safe, thereby increasing the level of social control in public spaces. Approximately 13 of the 30 BID in Los Angeles spend more than US\$200 000 a year (2005 dollars) on such 'clean' and 'safe' efforts. These strategies are closely linked to research and theory on crime prevention through environmental design to reduce opportunities for crime and violence and, in particular, robbery.21–23

Given the limited budgets and staff of many BID, it is of no surprise that the mere presence of a BID is not uniformly associated with a reduced incidence of violence. Some BID spend as much as half their annual budgets on crime prevention and environmental redesign or beautification efforts. BID crime prevention activities may also garner additional resources from the police, as the police now have an active 'partner' in a community. Other established Los Angeles BID have relatively small budgets and focus their efforts primarily on place promotion in an effort to foster improved commercial activity for their constituent businesses.12 While the protocol for establishing a BID in Los Angeles is uniform and codified into law,12 the dosage of tactics to improve neighbourhood environments varies between BID areas. Relying on a conservative estimate of pre–post changes in reported violent crimes for only those areas that adopted BID we found significant overall effects on robbery, with some BID areas exhibiting greater effects than others. We cannot say whether spending on private security or economic development efforts caused these reductions or are merely correlated with them. This study relied on observational data, which limits our ability to infer as to whether the correlations observed are causally related. We attempted to remove the potential selection effects of establishing a BID by estimating pre–post effects on reported violent crimes for only those areas that eventually adopted a BID. In the absence of an experimental design in which BID are randomly assigned to neighbourhoods we do not know whether BID activities actually caused the declines in robbery rates.

The efforts spent by BID in Los Angeles on economic development activities and social control efforts that focus on crime prevention, beautification and advocating for more public safety and sanitation services to many blighted sections of Los Angeles12 are associated with a reduction in the incidence of robberies. This information can assist in designing and testing the feasibility of BID as a community-level violence prevention intervention.

###### What is already known on this subject

-   The incidence of violence is associated with neighbourhood environments.

-   BID focus on public safety.

-   Community economic development models may help reduce crime.

###### What this study adds

-   The first systematic look at the effects of BID on violent crimes.

-   Rigorous methodology for assessing the effects of BID on violent crimes.

# References


abstract: Pollination improves the yield of most crop species and contributes to one-third of global crop production, but comprehensive benefits including crop quality are still unknown. Hence, pollination is underestimated by international policies, which is particularly alarming in times of agricultural intensification and diminishing pollination services. In this study, exclusion experiments with strawberries showed bee pollination to improve fruit quality, quantity and market value compared with wind and self-pollination. Bee-pollinated fruits were heavier, had less malformations and reached higher commercial grades. They had increased redness and reduced sugar–acid–ratios and were firmer, thus improving the commercially important shelf life. Longer shelf life reduced fruit loss by at least 11%. This is accounting for 0.32 billion US\$ of the 1.44 billion US\$ provided by bee pollination to the total value of 2.90 billion US\$ made with strawberry selling in the European Union 2009. The fruit quality and yield effects are driven by the pollination-mediated production of hormonal growth regulators, which occur in several pollination-dependent crops. Thus, our comprehensive findings should be transferable to a wide range of crops and demonstrate bee pollination to be a hitherto underestimated but vital and economically important determinant of fruit quality.
author: Björn K. Klatt; Andrea Holzschuh; Catrin Westphal; Yann Clough; Inga Smit; Elke Pawelzik; Teja Tscharntkee-mail: <firstname.lastname@example.com>
date: 2014-01-22
institute: 1Agroecology, Department of Crop Sciences, University of Göttingen, Grisebachstrasse 6, 37077 Göttingen, Germany; 2Centre for Environmental and Climate Research, University of Lund, Sölvegatan 37, 22362 Lund, Sweden; 3Department of Animal Ecology and Tropical Biology (Zoology III), Biocenter, Am Hubland, University of Würzburg, 97074 Würzburg, Germany; 4Quality of Plant Products, Department of Crop Sciences, Carl-Sprengel-Weg 1, 37075 Göttingen, Germany
references:
title: Bee pollination improves crop quality, shelf life and commercial value

# Introduction

Agricultural production forms one of the most important economic sectors \[1\]. The quantity of most crop species is increased by pollination \[2,3\], which is a highly important, but also seriously endangered \[4\] ecosystem service. More than 75% of the 115 leading crop species worldwide are dependent on or at least benefit from animal pollination, whereas wind and self-pollination are sufficient for only 28 crop species \[2\]. Thereby, animal pollination contributes to an estimated 35% of global crop production \[2\]. It is mostly pollination-dependent crops such as fruits that contribute to a healthy human diet by providing particularly high amounts of essential nutrients such as vitamins, antioxidants and fibre \[5,6\]. Berries especially have been found to benefit human health and are increasingly used for therapies against chronic diseases and even cancer \[5\]. First attempts for sustaining pollination and other ecosystem services have been aligned in a strategic plan of the Convention on Biological Diversity in Nagoya in 2010. However, recent decisions, such as the new Common Agricultural Policy of the European Union (EU), still endanger ecosystem services by promoting high-intensity agricultural management. Thus, the value of pollination and other ecosystem services is still underestimated or even disregarded in national and international policies. In this study, we expand our knowledge of the underestimated benefits of bee pollination by experimentally quantifying its impacts on crop quantity, quality, shelf life and market value. This should contribute to a better understanding of its monetary and social importance, thereby enhancing a sustainable implementation in future policies. We used strawberries (*Fragaria x ananassa* DUCH.), a crop whose worldwide cultivation is on the increase \[1\], as a model system.

Strawberry plants flower in several successive flowering periods within a season, with flowers becoming smaller over time \[7\]. Varieties are self-compatible in most cases, and stigmas become receptive before the anthers of the same flower release pollen, so that allogamy is favoured. Bee pollination increases strawberry weight and shape. Effects depend on varieties \[8,9\], presumably owing to differences in pollinator attraction \[10\] and their dependence on cross-pollination \[7\]. Recent findings about metabolic processes in strawberries support the idea that pollination may also impact shelf life \[11–14\]. Owing to high fruit sensitivity to fungal infections and mechanical injuries, strawberry fruits have a short shelf life \[12\]. More than 90% of fruits can become non-marketable after only 4 days in storage \[15\]. Several studies addressed the potential elongation of the shelf life of strawberries with modified storage procedures \[15–19\], which highlights how economically important this problem is. Crop features allowing longer storage and thereby, reducing post-harvest losses in supermarkets and households are of major interest worldwide \[20\], but have so far not been analysed in terms of pollination. Shelf life and pathogenic susceptibility of strawberries are mostly related to fruit firmness \[15\], but surface colour and sugar–acid–ratios are also involved \[15–19\]. Fruit colour further determines consumers perception and influences their purchasing behaviour \[19\], but has never been related to animal pollination. In addition, only few studies report a relation of pollination to firmness \[21–23\] and sugar contents \[22,24–27\] of fruits. Hence, comprehensive economic gains of bee pollination are largely unknown and in particular, the potential effect on commercially important parameters of the overall fruit quality has not yet been explored.

We set up a field experiment with nine commercially important strawberry varieties and assessed the influence of self, wind and bee pollination on strawberry fruits using exclusion treatments. We expected that: (i) bee-pollinated fruits would have higher numbers of fertilized achenes, the true 'nut' fruits of the strawberry, owing to higher pollination success compared with wind- and self-pollination; (ii) bee pollination would therefore lead to fruits with higher commercial value compared with wind- and self-pollinated fruits, owing to less malformations improving commercial grades and higher fruit weight; as well as (iii) higher firmness and longer shelf life; and (iv) bee-pollinated fruits should have a more intense red colour and lower sugar–acid–ratios, thus improving the post-harvest quality of strawberries.

# Methods

## Experimental set-up

In 2008, we planted nine commercially important strawberry varieties of *Fragaria x ananassa* DUCH. (Darselect, Elsanta, Florence, Honeoye, Korona, Lambada, Salsa, Symphony, Yamaska) on an experimental field. The field was subdivided in 12 plots, and nine rows per plot planted with 18 plants of a single variety per row. All varieties were present in all plots. The sequence of the rows within the plots was randomized. The field was surrounded by two further rows of strawberries to weaken edge effects. Five honeybee hives (*Apis mellifera* L.) and approximately 300 trap nests dominated by *Osmia bicornis* L., have been established for several years close to the field to ensure stable pollination services. Experiments were conducted in 2009 in the first yield year using exclusion treatments on two plants per variety and plot. Following the consecutive flowering periods of strawberries \[7\], all buds of a plant were covered with Osmolux bags (Pantek, Montesson, France) to allow only self-pollination (self-pollination treatment), gauze bags (mesh width 0.25 mm) to allow self- and wind pollination (wind pollination treatment) or remained uncovered to allow additional insect pollination (bee pollination treatment), respectively. Osmolux bags are semipermeable for water and steam, so that microclimate differences between bagged and unbagged flowers were kept at a minimum. Gauze bags do not create an atmosphere closed from outside the bags and thus have no influence on microclimate. Bags were removed directly after fruit set, when petals began to wither and fall off the flower, and the first approach of a fruit was visible, about 7 days after flower opening. At least 50 fruits per variety and treatment were harvested at maturity. All analyses except the titratable acid content were conducted on the same day of harvesting to avoid influence on post-harvest quality owing to water loss and metabolic procedures.

We collected insect pollinators under favourable weather conditions (*T* \> 17°C; low cloud cover; wind speed less than 4 m s^−1^) in 2010, using standardized transect walks. Four strawberry varieties (Honeoye, Elsanta, Korona, Lambada) were selected based on their flowering time, so that all other varieties were flowering at the same time as at least one of these four varieties. Thus, pollinators were collected across the entire flowering season of the commercial strawberry field. Each transect consisted of one row of strawberries per plot of each of the selected varieties. On each of 4 days, four different plots of the experimental field were randomly selected and insects pollinating strawberry flowers were collected using sweep nets on each of the four selected varieties. Each transect was visited for 10 min. Pollinators were identified to species level, and data were pooled across all varieties.

## Commercial value

### Weight and commercial grades

We calculated the commercial value of each fruit based on fruit weight (BA2001 S, Sartorius, Göttingen, Germany) and the market value of strawberry fruits, which is based on the availability of fruits on the market and commercial grades. Fruits were sorted into commercial grades, owing to aberrations in shape (deformations), colour (areas with yellow or green colour) and size (fruit diameter), following the official trade guidelines \[28\]. B.K.K. was trained by experienced strawberry growers and colleagues on how to apply the EU trade guidelines. Fruits with no or only slight deformations, with minimal areas of yellow or green colour which did not affect their general appearance, and with a minimum diameter of 18 mm, were sorted into grade extra/one. Fruits showing distinct deformations and larger areas with yellow or green colour, but that had a minimum diameter of 18 mm were classified as grade two. Non-marketable fruits had strong deformations, large areas of yellow or green colour or were of a diameter smaller than 18 mm. Aberrations in colour usually occurred in combination with fruit deformations and were thus not treated separately. Following the above-mentioned Commission's regulation, grades extra and one can be treated separately, but are used combined in practice. We calculated proportions of fruits for each commercial grade and pollination treatment across all varieties (figure 2*b*) and also separately for each variety (see the electronic supplementary material, S2).

We obtained the commercial value of each fruit by multiplying its weight with its market value per gram \[29\]. The latter was assessed based on harvest time and commercial grades. Harvest time influences the market value of strawberry fruits owing to the availability of fruits on the market: the more fruits that are available, the lower the market value. Thus, fruits that are sorted into lower commercial grades have lower market values. Finally, we extrapolated commercial value to 1000 fruits for a better relationship to market situations.

### Firmness and shelf life

We bisected fruits and measured firmness at the centre of each half according to Sanz *et al.* \[17\] with the following modifications: we fitted the texture analyser (TxT2, Stable Micro System, Surrey, UK) with a 5 mm diameter probe and a 25 kg compression cell, and used a maximum penetration of 4 mm.

## Post-harvest quality

Colourimetric analysis was applied according to Caner *et al.* \[19\] at two opposite sides of the centre of each fruit in the Lab-colour space using a portable colourimeter (CR-310 Chromameter, Konica Minolta, Badhoevedorp, The Netherlands). The total soluble solids are strongly correlated to the total sugar content of a solution and were measured using a handheld refractometer (HRH30, Krüss, Hamburg, Germany). Measurements for each fruit were conducted twice and repeated when the values differed by more than 0.2 Brix. Fruits were freeze-dried (Epsilon 2-40, Christ, Osterode, Germany), and all samples from the same plant were pooled and milled. To account for an average water content of 82%, which was analysed on a sample of 250 fruits, 0.18 g of each freeze-dried sample was diluted in 20 ml distilled water and titrated according to Caner *et al.* \[19\].

## Pollination success

We used at least eight fruits from each variety and treatment to analyse the number of fertilized achenes per fruit, which represent pollination success. Each fruit was blended in 100 ml distilled water for two minutes (Speedy Pro GVA 1, Krups, Offenbach, Germany). Fertilized achenes are heavier than water and sink to the bottom, whereas aborted achenes are lighter and accumulate at the water surface. Fertilized achenes were counted (Contador, Pfeuffer, Kitzingen, Germany) after drying for 48 h at 85°C.

## Statistical analysis

In the case of repeated measurements per fruit, we calculated mean values for fruit characteristics. We fitted linear mixed-effects models with random effects allowing treatment slopes and intercepts to vary among varieties \[30\], using R \[31\]. To account for space and time errors and unbalance in the data, the random part was completed by two further terms: the interaction of plot, variety and plant, whereas flowering period was included as a crossed random effect. Response variables were commercial value per fruit, fruit weight, firmness, surface colour values (red colour, brightness, yellow colour) and number of fertilized achenes. In the models with sugar–acid–ratio as response variable, only plot and variety were used to complete the random part, because sugar–acid–ratios were calculated based on arithmetic means per plant.

Bee, wind and self-pollination treatments were used as fixed effect levels. To test whether pollination treatments differed and whether there was a main effect of all pollination treatments across all varieties, a model with unpooled treatment levels (full model), models with successively pooled treatment levels and a model without treatment as fixed effect were compared \[30\] using second order Akaike's information criterion (AICc) and likelihood \[32\]. This allowed us to test whether all treatments, specific treatment levels only, or none of the treatments had an effect on the response variables. The latter case was taken to indicate that treatment effects were specific to the variety and without a shared common effect between varieties. Residuals were inspected for constant variance, and transformations were used to account for non-normality and heterogeneity, where necessary. Main effect values and parameter estimates were extracted from the model and used for plotting after back transformation.

Pearson's chi-squared analysis was used to calculate differences between pollination treatments in the number of fruits for each commercial grade. Differences were shown in proportions for better illustration (figure 1*b*).

# Results

## Commercial value

### Weight and commercial grades

Strawberry flowers were mainly visited by bees (98.5%). Wild bees were most abundant (64.6%), whereas *A. mellifera* L. (33.9%) and non-bee pollinators (flies: 1.6%) were found less often (table 1). The solitary wild bee *O. bicornis* L. (52.0%) was the most abundant pollinator, whereas other wild bee species accounted for less than 5% of the bee community.

Pollinators visiting strawberry flowers on the experimental field. (To identify the main pollinators of strawberry flowers on the experimental field, four varieties were randomly selected and insects visiting strawberry flowers were collected. Sweep netting was conducted for 10 minutes on four transects that were randomly selected on each of four different days in 2010. Strawberries were mainly pollinated by solitary wild bees with *O. bicornis* L. being the most frequent species, while honeybees (*Apis mellifera* L.) and non-bee pollinators were less abundant.)

| species                      | abundance | proportion | functional group |
|:-----------------------------|-----------|------------|:-----------------|
| *Osmia bicornis* L.          | 66        | 52.0       | wild bee         |
| *Apis mellifera* L.          | 43        | 33.9       | honeybee         |
| *Bombus terrestris* L.       | 5         | 3.9        | wild bee         |
| *Andrena flavipes* Panz.     | 3         | 2.4        | wild bee         |
| *Merodon equestris* F.       | 2         | 1.6        | fly              |
| *Andrena gravida* Imhoff     | 2         | 1.6        | wild bee         |
| *Bombus hypnorum* L.         | 1         | 0.8        | wild bee         |
| *Bombus lapidarius* L.       | 1         | 0.8        | wild bee         |
| *Bombus lucorum* L.          | 1         | 0.8        | wild bee         |
| *Bombus pascuorum* Scop.     | 1         | 0.8        | wild bee         |
| *Bombus pratorum* L.         | 1         | 0.8        | wild bee         |
| *Andrena chrysosceles* Kirb. | 1         | 0.8        | wild bee         |
| total wild bees              | 82        | 64.6       | —                |
| total honeybees              | 43        | 33.9       | —                |
| total non-bees (flies)       | 2         | 1.6        | —                |

Bee pollination resulted in strawberry fruits with the highest commercial value (figure 1*a*). On average, bee pollination increased the commercial value per fruit by 38.6% compared with wind pollination and by 54.3% compared with self-pollination. Fruits resulting from wind pollination had a 25.5% higher market value than self-pollinated fruits. Pollination treatments were stronger than differences between varieties and thus had a main effect across all varieties (see table 2 for AICc and likelihood values). Our results suggest that altogether, bee pollination contributed 1.12 billion US\$ to a total of 2.90 billion US\$ made with commercial selling of 1.5 million tonnes of strawberries in the EU in 2009 \[1\]—but so far without consideration of the monetary value provided by enhanced shelf life (see below). Price and marketability of strawberries depend on commercial grades of fruit quality (shape, size and colour) \[28\]. Malformations, in particular, are a common problem affecting strawberry price and marketability \[33\]. Our experiment showed that pollination treatments significantly differed in the number of fruits for each commercial grade (**χ**~4~^2^ = 60.504; *p* \< 0.001, *n* = 1895). Bee pollination reduced malformations and thus enhanced marketability in all varieties except the variety Symphony (figure 1*b*; see the electronic supplementary material, S2 for variety values). The highest proportion of bee pollinated fruits was assigned to the best grade extra/one, whereas non-marketable fruits formed the smallest fraction. By contrast, wind and self-pollination led to high proportions of non-marketable fruits. When compared with wind and self-pollination, bee pollination not only improved fruit shape, but also fruit weight (figure 1*c*). Bee-pollinated fruits were on average 11.0% heavier than wind-pollinated and 30.3% heavier than self-pollinated fruits. Pollination treatments were stronger than differences between varieties and thus had a main effect across all varieties (see table 2 for AICc and likelihood values).

Delta AICc values and likelihood resulting from model comparisons. (AICc = 0 indicates the model with the highest explanatory power. Lower delta AICc and higher likelihood indicate better explanatory power of a model. Likelihood was calculated for models with delta AICc of less than seven \[32\]. Best explaining models are highlighted in italics. Sample sizes are given in brackets behind fruit parameters. None, no treatment level pooled; sans, model without fixed effect.)

| fruit parameter | pooled levels |  |  |  |  |
|:---|:---|:---|:---|:---|:---|
|  | none | bee = wind | wind = self | bee = self | sans |
| commercial value (*n* = 1892) |  |  |  |  |  |
| * *AICc | *0* | 4.512 | 0.173 | 3.527 | 2.501 |
| * *likelihood | *0.403* | 0.042 | 0.370 | 0.069 | 0.115 |
| fruit weight (*n* = 1895) |  |  |  |  |  |
| * *AICc | *0* | 4.162 | 3.507 | 4.872 | 3.137 |
| * *likelihood | *0.627* | 0.078 | 0.109 | 0.055 | 0.131 |
| shelf life (*n* = 1268) |  |  |  |  |  |
| * *AICc | *0* | 0.347 | 1.791 | 7.218 | 5.273 |
| * *likelihood | *0.431* | 0.362 | 0.174 | — | 0.031 |
| red colour (*n* = 1279) |  |  |  |  |  |
| * *AICc | 1.428 | 1.608 | *0* | 2.021 | 0.323 |
| * *likelihood | 0.155 | 0.142 | *0.317* | 0.115 | 0.270 |
| sugar–acid–ratio (*n* = 345) |  |  |  |  |  |
| * *AICc | 2.128 | 3.244 | *0* | 1.247 | 1.147 |
| * *likelihood | 0.131 | 0.075 | *0.378* | 0.203 | 0.213 |
| pollination success (*n* = 356) |  |  |  |  |  |
| * *AICc | *0* | 4.267 | 9.192 | 8.704 | 7.290 |
| * *likelihood | *0.894* | 0.106 | — | — | — |

### Shelf life

Bee pollination strongly impacted the shelf life of strawberries by improving their firmness (figure 2*a*). The firmness values of each treatment and variety were related to shelf life, measured as the number of days until 50% of fruits had been lost owing to surface and fungal decay (see the electronic supplementary material, S3). Higher firmness resulting from bee pollination potentially elongated the shelf life of strawberry fruits by about 12 h compared with wind pollination, and by more than 26 h compared with self-pollination. After 4 days in storage, only 29.4% of the wind-pollinated fruits and none self-pollinated fruit were still marketable, whereas, at the same time, 40.4% of the bee-pollinated fruits remained in a marketable condition. Thus, bee pollination accounted for a decrease of at least 11.0% in fruit losses during storage. These findings suggest that the value for bee pollination calculated in §3a(i) has to be increased to accommodate this impact on the shelf life of strawberries. Hence, pollination benefits on the shelf life of strawberries potentially added another 0.32 billion US\$ to the commercial value of strawberry pollination (without shelf-life effects: 1.12 billion US\$). In total, bee pollination contributed 1.44 billion US\$ to a total of 2.90 billion US\$ made with the commercialization of 1.5 million tonnes of strawberries in the EU in 2009 \[1\]. Pollination treatments had a main influence on shelf life across all varieties (see table 2 for AICc and likelihood values). Varieties producing fruits with high firmness benefitted most from bee pollination.

## Post-harvest quality

In most varieties, bee-pollinated fruits had a more intense red colour compared with fruits resulting from wind and self-pollination (figure 2*b*). Self-pollinated fruits of the varieties Lambada and Symphony showed the most intense red colour in the self-pollination treatment. The bee pollination treatment differed from the two other pollination treatments across all varieties, whereas strong variety differences imped a difference between wind and self-pollination treatments (see table 2 for AICc and likelihood values). The brightness of bee- and wind-pollinated fruits was similar and highly correlated to yellow colour intensity (see the electronic supplementary material, S4 and S5). Both colour properties did not differ between bee and wind pollination, but self-pollinated fruits were darker and had less intense red colour. Thus, bee pollination resulted in bright fruits with a more intense red colour than wind pollination fruits, whereas self-pollinated fruits were darker and less red (figure 2*b* and the electronic supplementary material, S4).

Senescence of strawberries is not only related to losses in firmness and colour changes, but also to increasing sugar–acid–ratios. Bee-pollinated fruits generally had a lower sugar–acid–ratio compared with wind- and self-pollinated fruits across all varieties (figure 2*c*), but fruits of the varieties Elsanta and Symphony had a higher sugar–acid–ratio with bee pollination. The difference between wind and self-pollination remained variety-dependent (see table 2 for AICc and likelihood values), whereas the sugar–acid–ratio of fruits resulting from bee pollination differed from both other treatments across all varieties.

## Pollination success

Pollination success was related to the number of fertilized achenes dependent on pollination treatments. Bee pollination was much more efficient than wind and self-pollination, resulting in a higher number of fertilized achenes per fruit across all varieties (figure 3; see table 2 for AICc and likelihood values). Bee pollination on average increased the number of fertilized achenes by about 26.8% compared with wind pollination and about 61.7% compared with self-pollination. Wind-pollinated fruits had a 47.7% higher number of fertilized achenes than fruits resulting from self-pollination. This confirms our findings to be true effects of bee pollination.

# Discussion

We found bee pollination, which was mainly conducted by solitary wild bees, to play a key role for several features of the quantity and quality of strawberry fruits. Bee pollinated fruits showed less malformations, greater fruit weight and longer shelf life, resulting in higher commercial value as well as improved post-harvest quality by more intensive red colour and lower sugar–acid–ratios than fruits resulting from wind and self-pollination.

The mechanism behind the benefits of strawberry pollination by bees is based on the fertilization of the true 'nut' fruits of the strawberry, the achenes \[11–14\]. During their visits, bees allocate pollen homogeneously on the receptacles, increasing the number of fertilized achenes per fruit \[34\]. While unfertilized achenes resulting from insufficient pollination have no physiological functionality, fertilized achenes produce the plant hormone auxin \[35\], which mediates the accumulation of gibberellic acid \[14\]. Together, these plant hormones induce fruit growth by improving cell progeny and size, thereby enhancing the weight of strawberry fruits \[12\]. This further improves fruit quality and thereby commercial grades \[12\] by preventing malformations, which are caused by areas of unfertilized and thus physiologically inactive achenes \[33\].

How can pollination induce a longer shelf life in strawberries? The shelf life of strawberries and other fruits is mostly dependent on their firmness \[15,33\], which is also functionally based on fertilized achenes \[33\] and thus dependent on successful pollination. Auxin and gibberellic acid delay fruit-softening and thereby enhance firmness and shelf life, by limiting the expression of several fruit-softening proteins, the so-called expansins \[11\]. Higher levels of both plant hormones also increase the post-harvest quality of strawberries. Although auxin alone reduces the accumulation of anthocyanins \[11\], high levels of both auxin and gibberellic acid can, in conjunction, increase anthocyanin accumulation \[12\]. In contrast to firmness and colour changes, sugar–acid–ratios of strawberries are not directly affected by auxin and gibberellic acid \[12\]. But higher firmness of fruits is associated with more stable cell walls which might reduce respiration, which is known to limit metabolic processes affecting sugar and acid contents during storage \[19\]. Indirect positive effects of pollination are therefore probable.

Plant hormones that can influence the quality of fruits and vegetables are known to occur not only in strawberries, but also in several other crops \[36\] that require animal pollination \[7\]. Crops such as coffee \[37\] and blueberry \[38\] benefit from animal pollination in terms of fruit set and fruit size; and it has been shown elsewhere that fruit shape can benefit from increased animal pollination \[7\]. This indicates that our findings may be transferable to a high variety of crops and that animal pollination may largely contribute to crop quality. However, only few studies have focused to date on effects of pollination other than the effects on crop yield and fruit set. It has been shown that the sugar content of loquats \[24,26\], vine cactus \[25\] and oriental melon \[22\] as well as the firmness of oriental melon \[22\] and cucumber \[23\] can be increased by animal pollination. Contrasting results are available for the tomato, whereas Al-Attal *et al.* \[21\] showed that pollination increased the firmness of tomatoes in greenhouses, but pollination had no effect on the firmness of cherry tomatoes under field conditions \[27\]. Oilseed rape is another important crop whose quality benefits from insect pollination by higher oil content and lower chlorophyll content \[39\]. These results support the assumption of a general impact of pollination on multiple aspects of crop quality. However, such comprehensive findings about the benefits of pollination on crop quality, yield and commercial value as in our study, which can be mechanistically well linked to formerly reported physiological processes, have never, to our knowledge, been reported before.

Our results showed strawberries to be almost exclusively visited by bees, with solitary wild bees being most abundant. This contrasts with earlier findings, where honeybees were the most common pollinators of strawberries and other crops \[7\] and further shows that the wild bee pollination can be important for crop production, if wild bees are abundant close to crop fields. Wild bee pollinators have already been shown to be effective crop pollinators \[40\], including strawberries \[41\]. Additional experiments are required to assess the current abundance of wild bee pollinators and thus their importance for strawberry production on commercial strawberry fields under conventional management conditions.

In our study, we used an innovative approach to the calculation of the commercial value of pollination by considering not only overall yield \[2,3\] but also crop quality in terms of trade classes, shelf life and changing market values. Shelf life is a major factor determining the commercial value of pollination. Globally, between one-third and a half of all fruits and vegetables are lost due to mechanical damage and deterioration during handling, transport and storage directly after harvest, or wasted at retailer and consumer levels \[42\]. This illustrates the commercial and social importance of crop shelf life and the far-reaching impact of pollination deficits.

Of course, our calculations may still underestimate the commercial value of bee pollination as they are not considering commercial pollination benefits related to colour, sugar–acid–ratio and other taste components.

# Conclusion

In conclusion, our results showed that crop pollination is of higher economic importance than hitherto thought. Plant hormones, the production of which is mediated by pollination, occur in several other pollination-dependent fruits and vegetables \[36\]. This highlights the major importance of animal pollination for crop quality in other crops in addition to strawberries. Quality improvements of crops can greatly affect marketability and contribute to reducing food loss and waste. In the industrialized countries, 30–50% of all crops are thrown away at retail and consumer levels \[20,42\]. Under the current scenario of rapid human population increase and global food demand \[43\], achieving high quality and quantity of crops is a pressing issue. Our study suggests that comprehensive analyses of the benefits of pollination for animal-dependent crops, which comprise 70% of all major crop species \[2\], may clearly increase estimates of the economic value of this ecosystem service. Pollination appears to be economically much more important than previously recognized and needs better support through adequate agricultural management and policy.

## Acknowledgements

We thank, K. M. Krewenka, J. Fründ, C. Scherber, M. von Fragstein, G. Everwand, B. Scheid, K. Klatt and H. P.-G. Klatt for comments on the manuscript and N. Blüthgen, D. Kleijn and L. Garibaldi for reviewing the manuscript prior to submission. We thank the members, students and technicians of the agroecology group for their field assistance.

## Funding statement

This work has been supported by the German Research Foundation (DFG) and the SAPES research environment. Data can be accessed on request from the Agroecology at Göttingen University (see <http://www.uni-goettingen.de/en/74726.html> for contact details) and 3TU.Datacentrum (see <http://datacentrum.3tu.nl/en/home/>).

# References


abstract: # Introduction
  .
  National Health Service hospitals and government agencies are increasingly using mortality rates to monitor the quality of inpatient care. Mortality and Morbidity (M&M) meetings, established to review deaths as part of professional learning, have the potential to provide hospital boards with the assurance that patients are not dying as a consequence of unsafe clinical practices. This paper examines whether and how these meetings can contribute to the governance of patient safety.
  .
  # Methods
  .
  To understand the arrangement and role of M&M meetings in an English hospital, non-participant observations of meetings (n=9) and semistructured interviews with meeting chairs (n=19) were carried out. Following this, a structured mortality review process was codesigned and introduced into three clinical specialties over 12 months. A qualitative approach of observations (n=30) and interviews (n=40) was used to examine the impact on meetings and on frontline clinicians, managers and board members.
  .
  # Findings
  .
  The initial study of M&M meetings showed a considerable variation in the way deaths were reviewed and a lack of integration of these meetings into the hospital's governance framework. The introduction of the standardised mortality review process strengthened these processes. Clinicians supported its inclusion into M&M meetings and managers and board members saw that a standardised trust-wide process offered greater levels of assurance.
  .
  # Conclusion
  .
  M&M meetings already exist in many healthcare organisations and provide a governance resource that is underutilised. They can improve accountability of mortality data and support quality improvement without compromising professional learning, especially when facilitated by a standardised mortality review process.
author: Juliet Higginson; Rhiannon Walters; Naomi Fulop**Correspondence to** Professor Naomi Fulop, Department of Applied Health Research, University College London, 1-19 Torrington Place, London WC1E 7HB, UK; <firstname.lastname@example.com>
date: 2012-05-03
institute: NIHR King's Patient Safety and Service Quality Research Centre, King's College London, London, UK
references:
title: Mortality and morbidity meetings: an untapped resource for improving the governance of patient safety?

# Introduction

In recent years, there has been an increasing international interest in using mortality rates to monitor the quality of hospital care.1 2 Concern about patient safety and scrutiny of mortality rates intensified in the UK with the extensive coverage of investigations into National Health Service (NHS) hospital failures and the Dr Foster report with its patient safety rating for NHS trusts.3 4 As a consequence, boards of healthcare organisations now require assurance that the care they provide is safe and that patients are not dying through failure of their services. Many trusts include mortality rates in their performance scorecards or dashboards and actively engage with national patient safety improvement initiatives, such as Patient Safety First and Safer Patient Initiative, to reduce mortality rates.5 6

A forum that has traditionally reviewed in-hospital deaths is the long-standing Mortality and Morbidity (M&M) meeting established by surgeons to further professional education. In regularly reviewing deaths and complications, these meetings have the potential to provide accountability and the necessary improvement measures required for patient safety as well as professional learning. How effective they are in fulfilling these additional roles remains unexplored.

In many countries, M&M meetings are embedded within the medical curriculum for doctors in training.7 Junior doctors present cases to other doctors for reflection on diagnostic or treatment decision-making, and in return they receive clinicopathological wisdom and learn presentation skills. In the past, the brief discussions between the clinicians about the causes of death were thought to be effective peer review and an adequate means of changing practice.8 9 Little attention was paid to analysing the causes of deaths for quality improvement.10 11 Studies have shown that for M&M meetings to facilitate improvement and be more than a forum for peer review, they need to be structured and systematic in reviewing and discussing deaths, directing discussions towards improving system and process variations.12–14 Studies recommended that to support this, junior doctors' training should include more focus on systematic process change and less on medical error in M&M meetings.15–17

Historically, M&M meetings have been led and attended only by the medical profession and have remained autonomous, with knowledge not being available or shared with other professions or across the wider hospital governance framework. This 'silo' working has led to a lack of organisational learning and accountability.18 Increasingly hospitals are beginning to integrate M&M meetings into their governance processes, by making them mandatory and more accountable for reviewing deaths and taking corrective action should adverse events arise.19–21 To support this, the US Agency for Healthcare Research and Quality has produced web-based guidance for case analysis.22

Traditionally, adverse outcomes discussed at M&M meetings have been attributed to individual competence in treating patients rather than the system or process failures involved with the care.11 23 Although both contribute to errors, the focus on individuals has led clinicians to fear embarrassment and loss of reputation, making them reluctant to speak openly about errors at meetings.24 25 This defensive behaviour is thought to be counterproductive to eliminating adverse events and assuring safe care.26 27

In light of this evidence we wanted to see whether and how M&M meetings in an English teaching hospital could facilitate quality improvement, be accountable and provide assurance within the organisation's governance processes. Using a structured mortality review process as a facilitating mechanism, we wanted to assess what impact this would have on the original focus of the meetings and on professional learning; to explore how hospital staff viewed the changes; and evaluate the potential that a different format of M&M meeting could offer the organisation.

# Methods

## Setting

The participating organisation was an English NHS teaching hospital offering specialist tertiary services in addition to general and surgical care. The study was carried out in close collaboration with the hospital to inform and support other strategies for reducing mortality rates. The single case study allowed us to study both horizontally (ie, across divisions) and vertically (up and down the managerial and professional hierarchies) within the organisation and this approach allowed us to make analytic generalisations rather than statistical ones.28

## Initial assessment

During 2009, we studied the characteristics and processes of all the hospital M&M meetings and their position within the governance framework using non-participant observations at meetings (n=9) and semistructured interviews with meeting chairs and governance managers (n=19). The results showed considerable variation in meeting structure, format and case presentations, confirming the findings from previous studies. We found that the responsibility for managing these meetings was devolved to clinical groups and as a consequence they had developed independently and in individual ways. There was no formal reporting structure from these meetings into the wider hospital governance to inform or assure the board that deaths were not occurring as a result of unsafe care.

Following this we codeveloped a standardised mortality review form and database with hospital staff, based on recommendations in the literature and drawing on the method of examining death used by the National Confidential Enquiry into Patient Outcome and Death and the Scottish Audit of Surgical Mortality.29–32 The review form focused on whether the death was avoidable; on issues arising from the care of the patient; and on whether these could have contributed to the patient's death. It recorded where actions were necessary to address any problems; whether an adverse incident report was needed; and who was going to take any actions forward (Mortality review form: Appendix 1, web only). We developed and piloted the review form and database which were then introduced into three clinical specialties selected purposively for their patient cohort. This process was carried out from January to December 2010 during which time we studied whether and how this standardised mortality review process supported M&M meetings to contribute to wider governance processes.

## Participants

Five care groups across two divisions agreed to participate in the study. Three care groups agreed to adopt a standardised mortality review process, two from a general medical division and one from a specialist division. One group in each division agreed to be a study control and not implement the review process but participate in the evaluation process. The two clinical divisions were selected to participate because they regularly experienced high numbers of deaths albeit for contrasting reasons. Patients admitted to the general medical division had a range of complex medical problems and multiple comorbidities, were often frail and elderly and had numerous possible causes of death. In contrast, patients admitted into the second division, which offered specialist tertiary services, had a narrower range of specialty-specific causes of death, such as acute or end-stage organ failure.

## Data collection

We used qualitative methods, interviews and observations to understand how and whether the standard mortality review process was or was not used, and how and whether it supported M&M meetings in contributing to governance.

Forty semistructured interviews were carried out by the researcher (JH), including frontline staff (n=32) and at senior executive level (n=8). (Interview schedule: Appendix 2, web only). Participants were recruited with the aim of acquiring a broad sample across professional and occupational groups (Sampling matrix: Appendix 3, web only). Interviews were carried out with Chairs of M&M meetings (n=5) as well as a range of consultants (n=6), junior doctors (n=6), nursing staff (n=7) who attended the meetings, and some who were not invited, to capture a wide range of experiences and views. Managers and senior clinicians (n=8), senior executives and board members (n=8) were selected because of their governance role.

Interviewees were provided with study details when they were invited to participate and were assured of anonymity and confidentiality. Consent to participating and being recorded was obtained at the start of the interview. Interviews lasted approximately 45 min. Frontline staff interviewees were asked to identify the role and format of M&M meetings; the importance of quality improvement in making care safer; views about the introduction of the review form and process; and the governance of M&M meeting outcomes and accountability. Senior executives were asked what patient safety data they currently received; the role that M&M meetings played in providing that data; and how they perceived the potential for a standardised process for reviewing deaths in the hospital governance of patient safety.

In addition to the interviews, we used non-participant observations at M&M (n=26) and governance (n=4) meetings to provide background and context to the interviewees' comments. Consent for these was obtained prior to commencing the data collection.

## Data analysis

Observations were organised in Microsoft Excel. Data from interviews were dual coded (JH and RW), generating inductive and deductive themes, which were agreed with a third researcher (NF) who read a sample of transcripts. Data were organised and analysed using NVivo 9 software.

# Findings

Two of the three specialties implemented the review process throughout the study. The remaining specialty helped with the development of the process but refrained from testing the final version. We present our findings under the following three main headings: how M&M meetings contributed to the governance of patient safety within the hospital; how M&M meetings provided a resource for learning and accountability; and what impact the standardised review process had on both activities.

# The contribution of M&M meetings to the governance of mortality data

During the study, changes occurred in the governance of mortality data at both trust and divisional levels of the organisation as shown in figure 1. The left hand side of the figure outlines the prestudy governance processes for mortality data within the general medical division and hospital and shows no upward reporting from divisions to the hospital board and only informal cascading of information down to frontline staff. The right hand side shows the changes to governance introduced during the course of the study.

A monthly high-level trust safety committee was established to monitor externally published risk adjusted mortality rates, investigate outliers identified by the national regulator (the Care Quality Commission) and receive 6-monthly divisional reports from M&M meetings. It provided quarterly reports and assurance to a quality subcommittee of the board. M&M meetings within each division began reporting quarterly to the divisional risk and governance committee, using outcome measures produced from the standardised review process. Improvement measures determined by the M&M meetings were communicated to the frontline staff through newly established ward-based specialty governance and clinical management meetings. This strengthening of divisional and hospital governance arrangements may have been shaped in part by participation in, and feedback from, the study and a greater awareness of the potential of M&M meetings to contribute to governance.

All interviewees agreed that senior executives and board members should be accountable for the safety of patient care, especially when 'things went wrong', and that reporting outcomes from M&M meetings to a trust committee necessary. Illustrative interview quotes are shown in box 1.

###### The contribution of Mortality and Morbidity meetings to the governance of mortality data

'Obviously, it's very important for the trust to know what's going on mortality-wise across the entire trust. And actually I don't think you can have meetings that are about such a significant area of care without that going to a higher group of people. It's all very well to say yes well we've got mortality meetings in all of the divisions and they're all going fine, but how does anybody know? … Because at the end of the day they're going to be the ones who are answering the phone when the press sort of ring up and say ah we hear that your standardised mortality ratio is through the roof!' (Consultant).

'I think that information from these meetings can provide assurance that we don't have excess deaths. It helps us to pre-empt problems perhaps before we are alerted. By looking at morbidity cases we can also try to avoid problems before they lead to a fatality.' (Chair, Safety Monitoring Committee).

'I think that it's really important to … know that we have learned from the experience, and so how you capture that and reassure management that we won't make the same mistake again is really important….' (Board member).

M&M participants viewed reporting to this Safety Monitoring Committee as acceptable provided that the environment was non-judgemental and understanding of the case mix of their patients. Some clinicians and managers appreciated the committee's focus on data while others wished for an opportunity to share learning from other specialties, escalate unresolved issues and receive support for change. This was contrary to the views of two senior executives who thought the role of the committee was to monitor mortality rates, and that it was the divisions' responsibility to address quality and safety issues.

# M&M meetings as a resource for learning, improvement and accountability

Observations of M&M meetings during January to December 2010 showed considerable variation in the structure, organisation and the process of reviewing deaths as shown in tables 1 and 2. Responsibility for the meetings was devolved to the specialties which had led them to be non-standard and autonomous.

Summary of the structure and format of Mortality and Morbidity meetings

| Meeting characteristics | General medical division |  |  | Specialist division |  |
|----|----|----|----|----|----|
|  | Test group 1 | Test group 2 | Control 1 | Test group 3 | Control 2 |
| Frequency | Weekly | Monthly | Monthly | Monthly and then weekly | Not formalised |
| Timing | Working hours | Lunchtime | Lunchtime | Lunchtime | Working hours |
| Length | 20–30 min | 1 h | 1 h | 3 h then 1 h | 1 h |
| Venue | Departmental seminar room | Lecture theatre in medical school | Hospital committee room | Departmental seminar room | Departmental seminar room |
| Reason for organisation | Part of a management meeting | Part of a grand round programme | Capacity and semiformal setting | Local and easily accessible | Part of the professional development programme |
| Attendees | Consultants, a junior doctor representative, clinical director, senior nurses, managers | Consultants, junior doctors, senior nurse, governance managers | Consultants, junior doctors | Consultants, junior doctors, clinical director, nurses | Consultants, junior doctors, clinical director nurses, pharmacists and dietician |
| Number of attendees | 12 | 15–35 | 18–20 | 24–41 | 25 |

Summary of the review processes carried out by Mortality and Morbidity (M&M) meetings

|  | General medical division |  |  | Specialist division |  |
|----|----|----|----|----|----|
|  | Test group 1 | Test group 2 | Control 1 | Test group 3 | Control 2 |
| Source of mortality data for meetings | Departmental database | Inpatient episode data | Inpatient discharge data | Inpatient episode data | Departmental database |
| How meetings informed | M&M coordinators extracted cases from database | Hospital intelligence unit notified M&M coordinators | Software programme designed by M&M co-chair | Hospital intelligence unit notified M&M coordinators | M&M coordinators extracted cases from database |
| Numbers of cases reviewed | 1–6 | 10–42 | 8–15 | 2–7 | 5–6 |
| Criteria for selection | All deaths | All deaths | All deaths | All deaths | 'Interesting' cases |
| Review process | Standardised mortality review | Standardised mortality review | Departmental structured process | No formalised structure | No formalised structure |
| Meeting records | Standardised mortality review and minutes | Standardised mortality process | Excel spreadsheet | Minutes | Minutes |
| Issues identified and recorded | Yes | Yes | Yes | Yes | Yes |
| Actions specified | Yes | Yes | Yes | Yes | Yes |
| Actions assigned | Yes | Yes | No | No | No |
| Actions followed up at next meeting | No | No | Yes | No | No |
| Record circulated | Minutes yes | No | Yes | Available for viewing but not circulated | Available at next meeting |

## Meeting frequency

Clinical staff found weekly meetings helpful as the cases were still fresh in their minds and the small number allowed time for indepth discussion. However, the chair of a meeting that met monthly suggested that weekly meetings were less 'special' and would lose their impact.

## Venue

To encourage attendance, meetings were held at lunchtime or during working hours as part of the department's education programme. One specialty held their M&M review as part of a larger management meeting that considered adverse incidents, complaints and other 'bad bits' of the service. Incorporating mortality reviews had the benefit of integrating and addressing all risk issues together, especially as it had 'all the right people round the table' to achieve changes. It reduced the number of meetings that clinicians with managerial responsibilities had to attend but had the disadvantage of not being open to all clinical staff.

The various ways in which M&M meetings reviewed deaths is summarised in table 2. One control group M&M meeting had already identified a need for a structured approach to their meetings and developed its own system for categorising deaths. However, this system did not identify the specific failures in care or action needed to address them.

## Case presentations

Generally, junior doctors were tasked with reviewing deaths prior to meetings and presenting a summary of each case at the meetings. In one instance, 40 cases were presented in an hour and was 'mind-numbingly boring' according to one clinician. There was no time for indepth discussions making the review a tick box ceremony with errors liable to be 'swept under the table'. As peer review was also important to clinicians, many felt that all deaths should be presented to a wide audience. Achieving a balance between scrutinising all deaths by more than one person, and selecting and discussing avoidable deaths in depth, appeared to be challenging.

## Participation and culture

Both doctors and nurses reported that it was important to know which cases were going to be discussed at meetings. They wanted to familiarise themselves with the relevant case details to 'defend' any course of action that they had, or had not taken and for nurses especially, to give them the confidence to participate. All interviewees stressed that M&M meetings should be blame-free to facilitate improvement and accountability, although some were not sure that this was true of their meetings. One control group had made a deliberate decision to develop a safe and non-critical environment before considering any other aspect of the meeting.

## Accountability

All the participants saw learning and improvement in care as the purpose of M&M meetings and an essential part of the clinical activity. Many saw them as having an additional governance role as shown in box 2. There were no reports that the educational and learning role of the M&M meeting was compromised by a greater focus on accountability.

###### Mortality and Morbidity (M&M) meetings as a resource for learning and accountability

'I think the potential for them (M&M meetings) is absolutely massive. I think if we have a culture of openness and discussing these cases that are very difficult in a very frank robust way, and junior doctors and hopefully other staff come to that and see that discussion, take (learning) away with them, then I think that's very powerful. And I think that if we're able to look at trends and patterns, then you can also use that to influence policy or practice within the division and within our wards and within our daily work.' (Consultant).

'In terms of reporting, I think … the Trust should know exactly what is happening just as we should as clinicians' (Chair, M&M meeting).

'Everything should be transparent; what you are doing well and what can be improved. If there are failings in the system it should be readily available for board members.' (Junior doctor).

'I think the big driver (for M&M meetings) would be about improving patient outcomes…and linking it to the governance agenda, patient safety and patient experience and that would be how I, and ward managers, should be engaged in the process.' (Nurse).

'I guess if I look back I kind of wonder how on earth we thought we had assurance of any description before we started having robust M&Ms. I guess the reality is we didn't question too hard and had we questioned we'd have said no we didn't have any assurance. So they have a very important role.' (Senior manager).

# The impact of the standardised mortality review process

## Improved structure to meetings

Case reviewers liked how the standardised process directed the line of questioning and made it easier to extract the relevant information from case notes. Some thought it was helpful as a teaching aid for junior doctors. It highlighted and captured areas of concern and helped to focus and structure the meeting: 'helps stop the rambling'. Many thought this was what was needed in their meetings, as described in box 3.

###### The impact of the standardised process on Mortality and Morbidity meetings

'I think they've become much more structured, and again that's been partly helped by the fact that we have a form that actually provides a framework. I think without that things become very woolly; people can kind of get bogged down in looking at the micro aspects of morbidity and mortality, and not necessarily the bigger picture.' (Manager).

## Improved case review

The review process brought standardisation to the examination of deaths and provided a framework that could be applied to patient deaths in different circumstances. It also provided an assurance that all deaths were reviewed in the same way, a fact that board members viewed positively. It gave the meetings more significance and made them 'official', reported one person, 'not just a paper exercise'. To maintain transparency in meetings clinicians suggested that the review form should be completed openly in the meeting.

## Improved records

The electronic record of the standardised mortality review facilitated easier reporting and the identification of themes of issues over time. Clinicians spoke of its capacity to formalise 'organisational memory', those issues that arose infrequently and were only remembered by long-standing members of staff. Actions needed and assigned were more formally recorded, and in doing so improved the likelihood of corrective measures being undertaken. Equally important was the paper trail it provided of how problems were addressed and practice had changed.

## Improved reporting and governance

Chairs and managers of the participating groups were especially positive about the support the process offered in producing performance reports for the trust Safety Monitoring Committee. M&M meeting outcomes—the number of avoidable deaths, contributory factors and actions taken to address any quality issues—were included in their twice-yearly report and were later developed into a standard reporting template by the committee.

One of the intervention groups in the general medical division identified a continuing problem with care which was identified through a more structured mortality review and addressed through an improved governance structure. This is outlined in box 4.

###### An example of a change in practice in the division with improved governance

At a monthly departmental Mortality and Morbidity (M&M) meeting, all 22 deaths from the previous month were presented. These cases had been reviewed by two junior doctors in consultation with the M&M meeting chair. The junior doctors presented a summary of each case on a single PowerPoint slide, describing clinical details and causes of death. In four of the 22 cases, where the patients were not expected to die, the meeting chair led a greater examination and discussion. In one of these cases, an acutely ill patient admitted to a medical ward had not received the appropriate timely specialist input despite a referral having been made. The M&M meeting agreed that this omission constituted poor clinical care which potentially contributed to the death. 'Process issues and communication' were attributed to the lack of response to the referral. The case was also reviewed in the corresponding specialist M&M meeting.

### Action

1.  Specialty consultant invited to the next M&M meeting for an open discussion.

2.  Referral guidelines to be produced jointly by the two departments.

### Problem repeated

1.  Failure to get prompt specialist input on a further occasion.

### Action

1.  Chair raised the issue at a quarterly divisional M&M meeting: clinical director advised specialist divisions of the need for compliance with new referral guidance.

2.  Chair reported problem in his 6-monthly feedback to the trust Safety Monitoring Committee for hospital-wide compliance with the referral guidance.

## Standardised process

Many clinicians, and especially board members, saw the benefit of having a standardised process across the hospital to provide reassurance that all deaths were being reviewed in the same way. The majority of those interviewed wanted to see the review process extended to all hospital M&M meetings. Some participants of the control group M&M meetings, who had no experience of using the process, felt that if it was rigorously completed, the data would provide 'clear performance metrics which could be hugely valuable to the organisation'.

## Concerns

There were a few less-positive comments from staff who had not experienced the review process first-hand. The specialty that decided not to continue testing the study review felt it would not advance their own process and might limit the openness of the discussion, thus jeopardising the 'fragile culture' of their meeting.

Some meeting participants expressed concern that completing the review might become the focus of the meeting rather than it being an aid to direct discussion. Extra administrative support might also be needed. Others suggested that specialties might wish to add specialty-specific questions to the core template. Overall, the concerns were outweighed by support for the process.

# Discussion

M&M meetings are an established part of medical education and have existed for decades as forums for doctors to review and present cases for biomedical exploration. Their potential for quality improvement depends on them being more structured and reviewing deaths in a more systematic way. Changes to the curriculum of junior doctors' professional education have done much to promote this.24 33 34 Studies have also shown how specialty or departmental M&M meetings have improved quality by adopting structured reviews.14 23 35 Our findings build on these and show how M&M meetings can be integrated across the whole hospital and contribute to the accountability for deaths and governance of patient safety. Meetings that adopt a standardised and systematic review process can focus on systems and process failures; provide a record of meeting outcomes and follow-up actions taken to address failures; and facilitate the reporting of meeting outcomes and assurance to the board.

We had anticipated that there might be greater resistance from clinicians, who would want to maintain their autonomy and not want to codify and share sensitive data.36 37 Our findings show considerable support from them for both the standardised review process and the wider governance role of M&M meetings. There may be several reasons for a greater acceptance than expected. Health professionals are expected to take responsibility for governance of their own clinical practice and are increasingly aware that hospitals are being monitored for the quality of their care.38 Many are being co-opted into managerial roles such as clinical directors, medical directors and chairs of governance committees and are accountable for the governance of quality and safety data.36 39 This additional managerial responsibility encourages clinicians to value systems that make the provision of governance data easier.

The standard review process was generally accepted because it met with clinicians' requirements to capture the tacit nature of case context and complexity.18 26 Unlike many checklists it was adapted to their particular contextual needs which gave them ownership.40 Close collaboration during its development also helped to increase engagement and was seen less as a top-down imposition.41 42 Health professionals welcomed the focus on systems and process failures and away from individual competence, while senior executives and board members appreciated the standardisation and safety monitoring that the process supported.43 Suggestions for an M&M meeting review process that facilitates both learning and assurance, based on our findings, are listed in box 5.

###### Suggestions for using Mortality and Morbidity (M&M) meetings for governance of patient safety

-   Invite all types of health professionals to M&M meetings and notify them in advance which cases are to be reviewed and discussed.

-   Employ a short, standardised review process that highlights avoidable deaths and contributory factors, allowing for staff involvement in the design and flexibility for specialty-specific questions as necessary.

-   Allow adequate time for case discussions using the review questions as an aid.

-   Encourage a focus on systems and process variations and not individual competence.

-   Carry out the review openly, summarising actions at the end of the meeting and tracking them at the following one.

-   Record meeting outcomes electronically to facilitate audit and performance data.

-   Integrate M&M meetings into the wider governance structure and monitor meeting outcomes for shared learning and assurance.

Although this is a single case study, personal communications with medical directors of four other NHS trusts championing patient safety helped place our findings into context. As with our case study, responsibility for M&M meetings in these hospitals had previously been devolved to clinicians and provided no assurance that deaths were being reviewed in a systematic and rigorous way. Outcomes from meetings were neither standardised nor integrated into the hospital governance. In the smaller hospitals, there was an increased focus on reviewing and following up deaths but this was carried out by individual senior clinicians. However, the larger hospitals were beginning to see the need for a more effective way of reviewing larger numbers of deaths and the important role that M&M meetings could play, and were introducing standard trust-wide review processes.

# Conclusion

M&M meetings have the potential to contribute to the governance of patient safety. They exist in many healthcare organisations and are a governance resource that is generally underutilised. They can improve the accountability of mortality data and support quality improvement without compromising professional learning, especially when facilitated by a standardised mortality review process.44

The research team would like to thank all the hospital staff who contributed to the research, and members of the PSSQ team for their helpful comments on earlier drafts of the paper.

# References