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Uncertainty in most probable number calculations for microbiological assays

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1084 MCBRIDE ET AL.: JOURNAL OF AOAC INTERNATIONAL VOL. 86, NO. 5, 2003

SPECIAL GUEST EDITOR SECTION

Uncertainty in Most Probable Number Calculations for


Microbiological Assays
GRAHAM B. MCBRIDE
National Institute of Water and Atmospheric Research, PO Box 11-115, Hamilton, New Zealand
JUDITH L. MCWHIRTER and MATTHEW H. DALGETY
University of Waikato, Department of Statistics, Hamilton, New Zealand

Microbiological assays commonly use incubations ultiple tube incubation techniques have been in use
of multiple tubes in a dilution series, and microor-
ganism concentration is read as a most probable
number (MPN) in standard tables for the observed
M for many decades and continue today with an in-
creasing variety of setups (i.e., number of dilution
series and numbers of tubes in each series). The essence of
pattern of positive tubes. Published MPN tables the technique concerns the pattern of positive results ob-
differ, sometimes substantially, because of use of tained after incubation of the tubes. These are routinely
approximate MPN calculation procedures, differ- translated into a concentration of microbes via a table of
ent rounding conventions in the results, and dif- most probable number (MPN) values, where MPN is de-
ferent methods of calculating confidence or credi-
fined as the mode of the distribution of all possible concen-
ble intervals. We conclude that the first 2 issues
trations that could have given rise to that pattern. The for-
can now be resolved by using recently developed
mal development of these procedures was first set down
exact MPN calculation methods and by reporting
during the First World War (1–3), with continuing develop-
rounding conventions in standard tables. The
third issue is not amenable to complete resolu- ments thereafter (4, 5). Those tables may now also contain
tion, especially if credible interval (as opposed to confidence limits (typically for 95% intervals and some-
confidence interval) limits are desired—as we times also for 99% intervals) as measures of uncertainty in
think they most often are. In that case, Bayesian the MPN result (6, 7).
statistics are called for and the analyst must pro- It may come as a surprise that differences remain among
vide a distribution of concentration that was pre- published standard tables, despite the longevity of the de-
sumed to be true before the assay was performed. velopment of MPN theory. For example, consider a pattern
This is mathematically combined with the assay of 5-5-2 positive tubes in a setup with 5 tubes in each of
data, resulting in a posterior concentration distri- 3 series of decimal dilutions. Two standard works have the
bution. These distributions may then be used to equivalent MPN (per 100 mL water) as 500 (6) and as
quantify the uncertainty in the MPN estimate, and 540 (7). In these 2 cases the 95% confidence limits are
the best approach is to use the highest posterior stated as the intervals 200–2000 and 220–2000, respec-
density regions of these distributions. If based on tively. Other examples are cited below. There are 3 causes
diffuse prior information (positing that, prior to an for these differences: Most of the methods used to date for
assay being performed, all positive concentra- calculation of MPNs are approximate, and it is seldom clear
tions are equally likely), then established proce- exactly what approximations form the basis of particular ta-
dures might be used to calculate the limits and bles; different and unstated rounding conventions appear to
publish them in standard tables. In the event that have been used (e.g., rounding 540 to 500, as noted above);
this prior assumption is held to be not satisfac- and quite different approaches have been used to develop
tory, we show results for an empirical Bayes pro- the confidence intervals and limits (and some are not actu-
cedure, with a Poisson prior distribution, giving ally confidence limits at all).
credible interval widths much narrower than in We suggest that the first 2 causes can now simply be ad-
the other cases examined. dressed and resolved by using exact MPN methods (8, 9) and
by authorities adopting the convention of stating the rounding
criteria adopted in preparing their tables. Therefore, readers
are at least aware that the differences in MPN among tables
may be attributable to rounding conventions. For the third is-
Guest edited as a special report on “Uncertainty of Measurement in sue, we survey the types of intervals being used and their im-
Chemical and Microbiological Testing” by John L. Love. plications for the width of the interval reported. It is noted that
Corresponding author’s e-mail: g.mcbride@niwa.co.nz.
the intervals commonly reported are based on 2 quite different
MCBRIDE ET AL.: JOURNAL OF AOAC INTERNATIONAL VOL. 86, NO. 5, 2003 1085

statistical paradigms: classical and Bayesian, and a conscious ing in “Sterne-type intervals” (16) and other lognormal ap-
choice has to be made between them. proximations (4, 5, 17). It has been held that Woodward’s is
the most accurate of these methods, especially when accom-
METHODS panied by necessary corrections (16). More recently the U.S.
Food and Drug Administration (FDA) has endorsed a nar-
Calculation of Exact MPN Values
rower set of confidence intervals—those published in 1983 by
Procedures for exact calculation of MPN values, using oc- de Man (15) as discussed below.
cupancy theory, were first described in the 1980s (8, 9), by us- However, a substantive and seldom-addressed issue with
ing results of occupancy theory documented by de Moivre in respect to the interpretation of confidence intervals remains.
1718 (10). Essentially this theory allows the calculation of a That is, because these intervals are based on concepts of rela-
probability that a particular tube among a set of replicates will tive frequency, the 95% (or 99%) probability they invoke re-
contain at least one bacterium (as shown by a positive re- fers to the proportion of time that the interval would contain
sponse after incubation) if a number of bacteria are distributed the true value, were repeated assays to be performed. But
at random among those tubes. By properly accounting for all commonly only one assay (or a limited number) is performed,
the possible combinations over a wide range of possible num- and the analyst wishes to claim 95% probability that the sam-
bers of bacteria (n), we can obtain the probability of a particu- ple assayed had a microbial concentration in the numerical
lar pattern occurring for each possible value of n. From the re- range given by the confidence limits for the observed pattern
sulting bar graph of these occurrence probabilities versus n we of positive results. In that case the frequency interpretation has
can then read both the MPN (i.e., the value of n for the highest no meaning (21) and one is actually making a Bayesian state-
bar, divided by the total volume in the test’s setup) and its oc- ment, that is, a probability statement about the concentration
currence probability. This is a relatively straightforward task given the pattern of positives obtained in the test. Further-
in computer programming (11). An example of such exact re- more, Bayesian probability calculations can proceed only if
sults is given in Table 1, along with approximate MPN values one invokes (even unwittingly) a “prior probability distribu-
reported by various authors, including the simple and popular tion,” that is, the analyst’s view as to the distribution of con-
method reported by Thomas (12). For reasons of compactness centration prior to performing the test. This is used, along with
the table refers to series with only 3 replicates per decimal di- the data via a likelihood function, to calculate the posterior
lution (setups with 5 replicates are rather more common). probability distribution, mimicking the learning process of
Approximations for more complex setups, using tables for updating previous views in the light of new information.
subseries, also give rise to inaccuracies. For example, consider The specification of prior probability is a matter of some
a setup consisting of 5 ´ 100, 5 ´ 10, 5 ´ 1, and 5 ´ 0.1 mL. If a contention, because it appears to introduce subjectivity. Yet, if
5-5-1-0 set of positive tubes is obtained, a common conven- probability limits are desired for a particular result, one must
tion (13) is to use a 3-series table to read the value for a 5-1-0 invoke a prior distribution. In that regard we note the views
pattern (in a 5 ´ 10, 5 ´ 1, 5 ´ 0.1 mL series), or a 5-5-1 pattern of 2 experienced environmental professionals: “It is interest-
(in a 5 ´ 100, 5 ´ 10, 5 ´ 1 mL series), and to take the value as ing that most researchers are taught statistics from a classical
the correct result. In fact this procedure is an approximation to perspective, yet confidence intervals are often interpreted in a
the correct result because it ignores the volume of sample dis- Bayesian sense. When the Bayesian interpretation is adopted,
carded. For example, the exact MPN for the 5-5-1-0 pattern is the analyst should realize that this implies a subjective inter-
32.76 per 100 mL (i.e., 182 bacteria in the total volume of pretation for probability, and this should be specified in the
555.5 mL), whereas the 5-5-1 pattern gives an MPN of analysis … the prior probability distribution must be stipu-
34.59 per 100 mL and the 5-1-0 pattern gives an MPN of lated if the Bayesian interpretation for confidence intervals is
30.63 per 100 mL. adopted…” (22). Such intervals are more properly called
“credible intervals” (23).
Calculation of Confidence and Credible Intervals
In fact, early MPN theory was developed in a Bayesian
Although early theoretical developments focused on calcu- framework (1–3), in which a diffuse uniform prior was
lation of the MPN value (1–3), attention has since focused on adopted, which stated that any positive concentration value is
quantifying some measure of uncertainty about that value. equally likely (the manner in which this analysis leads to cred-
Routinely, one uses confidence intervals, in which probabili- ible intervals was not pursued because of its computational
ties of various MPNs are computed for a range of assumed complexity). More recently, the development of intervals put
true concentrations; unlikely MPNs then fall into the tail of the forward by de Man (14) is equivalent to a Bayesian approach
distribution of those probabilities and so define the confidence using a diffuse prior (16, 24), as the author later acknowl-
limits. This is the relative frequency approach—the probabili- edged (15). Technically these are “likelihood intervals” (25),
ties refer to a proportion of outcomes under a particular hy- but in the MPN context they are equivalent to a credible inter-
pothesis (the assumed concentrations). An example is Wood- val with a diffuse prior. Interestingly, these results appear in
ward’s much-quoted paper (13) describing the use of an many recent standard tables such as those found in standard
MPN-ordering procedure (as explained in ref. 16), results for methods for food and for water (6, 7). Users of these tables are
which have been used in standard works (19, 20). Different in fact using Bayesian intervals correctly. Whether that use is
sets of intervals have been calculated by using pattern-order- appropriate depends entirely on how reasonable the adopted
1086 MCBRIDE ET AL.: JOURNAL OF AOAC INTERNATIONAL VOL. 86, NO. 5, 2003

Table 1. MPN values reported from the literature, and accompanying occurrence probabilities for a 3 ´ 10, 3 ´ 1, and
3 ´ 0.1 mL setup

MPN (per 100 mL) reported by reference number


a
Pattern (2) (3)b (12) (13) (14) (15) (16) (17) (18) Exact (11)c Pd

0-1-0 3 3.05 3.05 3.0 3 3.0 3.01 3 3 3.00 0.090


1-0-0 4 3.57 3.59 3.6 4 3.6 3.57 4 4 3.00 0.901
1-0-1 7 7.23 7.20 7.2 7 7.2 7.23 7 7 6.01 0.016
1-1-0 7 7.36 7.34 7.3 7 7.4 7.36 7 7 6.01 0.162
2-0-0 9 9.18 9.50 9.1 9 9.2 9.18 9 9 6.01 0.541
1-2-0 12 11.38 11.26 11 11 11 11.38 11 11 9.01 0.015
2-0-1 14 14.33 14.31 14 14 14 14.33 14 14 12.01 0.018
2-1-0 15 14.69 14.82 15 15 15 14.68 15 15 12.01 0.184
2-2-0 20 21.06 20.62 21 21 21 21.07 21 21 18.02 0.033
3-0-0 25 23.12 28.62 23 23 23 23.12 23 23 21.02 0.398
3-0-1 40 38.50 38.75 39 40 38 38.50 39 39 36.04 0.034
3-1-0 45 42.73 45.71 43 40 43 42.73 43 43 39.04 0.400
3-1-1 75 74.89 58.42 75 70 75 74.89 75 75 72.07 0.069
3-2-0 95 93.28 75.99 93 90 93 93.28 93 93 90.09 0.339
3-1-2 115 115.21 71.75 120 — 120 115.22 115 120 114.15 0.007
3-2-1 150 149.36 94.92 150 150 150 149.36 149 150 147.15 0.129
3-2-2 200 214.66 115.66 210 210 210 214.66 215 210 213.21 0.025
3-3-0 250 239.79 189.83 240 200 240 239.79 240 240 237.24 0.370
3-3-1 450 462.18 271.24 460 500 460 462.18 462 460 459.46 0.430
3-3-2 1100 1098.95 438.40 1100 1100 1100 1098.95 1099 1100 1096.10 0.446

a
Only some patterns are shown in the table. Those omitted generally have lower occurrence probabilities, and so can be considered as
improbable MPNs.
b
Calculated by the authors using software with Newton-Raphson root-finding to solve the MPN equation of Greenwood and Yule (3; p. 54).
c
Rounding to 2 decimal places was adopted to facilitate comparison with other results.
d
P is the occurrence probability for the given pattern (assuming the MPN is the true concentration), using the exact theory (11).

prior distribution is. At least in some cases one can argue that sults that are overconfident (26), i.e., his intervals are too
it is not. For example, the diffuse prior posits that the ana- short. This is because such methods use the data twice (in the
lyst’s view prior to the data being collected was that all con- prior distribution and in the data likelihood function). This
centrations are equally likely. This prior implies that a water naïvety can be addressed by explicitly incorporating posterior
body is more likely to be grossly contaminated than it is to be uncertainty about the Poisson parameter (26); this is a fruitful
healthy (with a much larger range of concentrations imply- research area.
ing contamination), even when historical sampling has rou- We also note that some have proposed the use of the Most
tinely demonstrated a healthy state. One can adopt other Probable Range to quantify uncertainty, being the range of
more informative priors or adopt the Empirical Bayes ap- values with occurrence probabilities at least 95% of that for
proach (26), in which the data are used to guide the choice the MPN (9), though its arbitrariness and difficulty of inter-
and parameter(s) of the prior distribution. One such approach pretation have been noted (29). This term has also been used
is to adopt a Poisson prior, based on the notion that microbes to refer to equi-tailed credible intervals (28), for which per-
are distributed following a Poisson random process in the haps a better term is MCR (Most Credible Range).
sampled environment (27), and using the calculated MPN as
the mean of that distribution. A detailed description can be Results and Discussion
found in Dalgety (28).
Table 2 gives selected confidence and credible intervals for Table 1 shows that the exact and approximate methods are
the same pattern of positives shown in Table 1, including this in reasonable agreement, except that the Thomas approxima-
Empirical Bayes interval. It should be noted that Dalgety’s ap- tion (12) tends to return values that are considerably too low,
proach is a naïve Empirical Bayes method and so produces re- especially when many tubes are positive. The exact values
MCBRIDE ET AL.: JOURNAL OF AOAC INTERNATIONAL VOL. 86, NO. 5, 2003 1087

Table 2. Published confidence and credible intervals (per 100 mL) for a 3 ´ 10, 3 ´ 1, and 3 ´ 0.1 mL setup

95% Confidence intervals 95% Credible intervals

Pattern (13) (15) (14)a (18)a (18)b (28)a

0-1-0 0.085–13 0.1–10 <1.0–17 0.7–17 0.1–15 3–6


1-0-0 0.085–20 0.2–17 <1.0–21 0.9–21 0.1–18 3–6
1-0-1 0.87–21 1.2–17 2–27 2.2–27 1.1–24 6–12
1-1-0 0.88–23 1.3–20 2–28 2.2–28 1.1–24 6–12
2-0-0 1.0–36 1.5–35 2–38 2.9–38 1.3–33 6–12
1-2-0 2.7–36 4–35 4–35 4.1–35 2.6–31 9–15
2-0-1 2.7–37 4–35 5–48 5.2–48 3.1–43 9–21
2-1-0 2.8–44 4–38 5–50 5.3–50 3.2–44 9–21
2-2-0 3.5–47 5–40 8–62 8.5–63 5.8–56 12–30
3-0-0 3.5–120 5–94 <10–130 8.7–130 3.8–108 9–33
3-0-1 6.9–130 9–104 10–180 15–180 8.1–150 18–57
3-1-0 7.1–210 9–181 10–210 17–210 8.4–180 18–60
3-1-1 14–230 17–199 20–280 28–280 16–250 42–102
3-2-0 15–380 18–360 30–380 33–390 18–340 57–123
3-1-2 30–380 30–360 40–350 44–350 29–320 78–150
3-2-1 30–440 30–380 50–500 56–510 34–450 105–189
3-2-2 35–470 30–400 80–640 86–640 59–580 162–264
3-3-0 36–1300 40–990 <100–1400 91–1400 40–1170 183–291
3-3-1 71–2400 90–1980 100–2400 180–2400 88–2070 384–534
3-3-2 150–4800 200–4000 300–4800 380–4800 190–4130 981–1212

a
Central credible interval (with an area of 0.025 in each tail of the posterior distribution).
b
Noncentral HPDR (shortest interval with total tail area of 0.05 in the posterior distribution).

tend also to be a little lower than the remaining approxima- as delimiting the highest posterior density region (HPDR).
tions. Note that the Thomas approximate MPN for the 3-2-0 Such regions have the added attraction that the probability
pattern is higher than that for the 3-1-2 pattern, in contrast to density at any point inside the interval is greater than at any
all the other methods shown. outside point (23). Because the posterior MPN distribution is
Table 2 shows that the two 95% confidence interval results skewed to the right, both of the HPDR limits are always to the
displayed are reasonably similar in their widths and limits. left of their central credible interval counterparts. As the re-
However, because of their particular method of construction, sults show, they are indeed always shorter than the first 2 cred-
the intervals of de Man (15) are always shorter than those of ible intervals shown in the table. Our implementation of the
Woodward (13). If confidence intervals are to be used it there- Greenwood and Yule theory (3) shows, as expected, that it
fore seems appropriate to endorse the intervals presented by gives almost identical answers to those in Beliaeff and
de Man (15), especially as they have been incorporated into Mary (18) for these 2 intervals. In the HPDR case it also
the FDA (2001) Bacteriological Analytical Manual agrees with results calculated from equivalent procedures re-
(http://vm.cfsan.fda.gov/~ebam/bam-a2.html). We note that a ported by Roussanov et al. (30).
previous endorsement of Woodward’s confidence inter- The last column shows the Poisson Empirical Bayes credi-
vals (16) was made before de Man’s paper was published. ble interval (28), which is much shorter than the others, re-
The first 95% credible interval shown in Table 2, that of de flecting the strong influence of the Poisson prior distribution
Man (14), is widely used. As expected it is very similar to the on the results. We note that others (26) have adopted similar
second interval shown, developed by using a diffuse assumptions. For this interval the central and HPDR intervals
prior (18). These intervals are designed to have an area of are very similar, because the posterior distribution with a Pois-
0.025 in each tail of their posterior distributions. The third son prior tends to be quite symmetrical.
credible interval, the noncentral case (18), has been obtained Finally, there is a question about what MPN estimate
by using a diffuse prior but requiring only that the total tail should be reported with credible intervals. It could be argued
area is 0.05. These are guaranteed to be the shortest intervals that when a Bayesian credible interval approach is used, the
satisfying this criterion; for that reason they may be described MPN should be read as the median or mean of the posterior
1088 MCBRIDE ET AL.: JOURNAL OF AOAC INTERNATIONAL VOL. 86, NO. 5, 2003

distribution. Our view is that it is better to use the exact value (3) Greenwood, M., Jr, & Yule, G.U. (1917) J. Hyg. 16, 36–54
obtained from occupancy theory because it is exact and be- (4) Eisenhart, C., & Wilson, P.W. (1943) Bacteriol. Rev. 7, 57–137
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(6) APHA (1998) Standard Methods for the Examination of Wa-
Conclusions ter and Waste Water, 20th Ed., American Public Health
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The practice of developing standard tables from various ap- (7) APHA (2001) Compendium of Methods for the Microbiologi-
proximate procedures should now be abandoned because the cal Examination of Foods, 4th Ed., American Public Health
result can be calculated exactly. The promulgation of a com- Association, Washington, DC
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32) therefore seems inappropriate. Rounding conventions used 381–388
in standard tables should always be stated. We do not recom- (9) Tillett, H.E. (1987) Epidemiol. Infect. 99, 471–476
mend a particular convention here, other than to note that (10) David, F.N., & Barton, D.E. (1962) Combinatorial Choice,
rounding a figure of 540 MPN/100 mL to 500 MPN/100 mL (as Griffin, London, UK
noted earlier) seems excessive; the exact integer value in that (11) McBride, G.B. (2003) Preparing Exact MPN Tables Using
case is actually 541 MPN/100 mL (11). Occupancy Theory and Accompanying Measures of Uncer-
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In contrast, there is no exact way to calculate measures of
uncertainty about the MPN value. Most importantly, one must (12) Thomas, H.A. (1942) J. Am. Water Works Assoc. 34,
572–576
decide between the use of classical confidence intervals and
(13) Woodward, R.L. (1957) J. Am. Wat. Works Assoc. 49,
Bayesian credible intervals. If the former is appropriate (i.e.,
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(14) de Man, J.C. (1977) Eur. J. Appl. Microbiol. 4, 307–316
formance in the long run), then the intervals presented by de
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Man (15) should be used. If the Bayesian approach is to be
taken (i.e., the analyst wants to make statements about the cur- (16) Loyer, M.W., & Hamilton, M.A. (1984) Biometrics 40,
907–916
rent result), we recommend the use of noncentral intervals
(17) Best, D.J. (1990) Int. J. Food Microbiol. 11, 159–166
(i.e., HPDR), as given for 2 common setups by Beliaeff and
Mary (18). We favor use of the HPDR, rather than equi-tailed (18) Beliaeff, B., & Mary, J.Y. (1993) Water Res. 27, 799–805
intervals, because they are the narrowest of all possible credi- (19) APHA (1975) Standard Methods for the Examination of Wa-
ter and Wastewater, 14th Ed., American Public Health
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Association, Washington, DC
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(20) WHO (1984) Guidelines for Drinking-Water Quality, Vol. 1,
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Annex 2, World Health Organization, Geneva, Switzerland
can be applied to any other (11). But note that this approach
(21) Casella, G., & Berger, R.L. (1990) Statistical Inference,
assumes as its necessary prior distribution that all concentra-
Wadsworth & Brooks/Cole, Pacific Grove, CA
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(22) Reckhow, K.H., & Chapra, S.C. (1983) Engineering Ap-
data the analyst held that a water body was more likely to be proaches for Lake Management, Volume 1: Data Analysis
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Acknowledgments Bayes Methods for Data Analysis, Chapman & Hall, CRC
Press, Boca Raton, FL
Partial funding was obtained from the New Zealand Foun- (27) Broman, K., Speed, T., & Tigges, M. (1998) Stat. Sci. 13, 4–8
dation for Research, Science and Technology (contracts (28) Dalgety, M.H. (1999) Establishing a Most Probable Range
C01819 and C01X0215), and the Ministry of Health. Our mi- Using Existing Most Probable Number Estimation Tech-
crobiologist colleagues Chris Francis and Desmond Till and niques, BSc(Hons) Project Report 0655.420, Department of
Andrew Ball reviewed the manuscript; Andrew Ball also Statistics, University of Waikato, Hamilton, New Zealand
tested the software. (29) Beliaeff, B. (1995) Water Res. 29, 1215
(30) Roussanov, B., Hawkins, D.M., & Tatini, S.R. (1996) Food
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